Taking the Bite Out of Rabies: The Evolution of Rabies Management in Canada 9781487519827

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TAKING THE BITE OUT OF

RABIES

The Evolution of Rabies Management in Canada

Involved in rabies research for much of their working careers, editors David J. Gregory and Rowland R. Tinline explore Canada’s unique contributions to rabies management in Taking the Bite Out of Rabies. By placing the major players in rabies management from provincial and federal agencies, universities, and research institutions in historical context, Gregory and Tinline trace Canada’s largely successful efforts to control rabies. Concerned about the loss of institutional memory that tends to follow success, Gregory and Tinline view this book as a crucial way to collate, verify, and preserve records for future understanding and research. The book maps the history of rabies across Canada and explores the science, organization, research, and development behind Canada’s public health and wildlife vaccination programs. It also discusses how ongoing changes in agency mandates, the environment, and the evolution of the rabies virus affect present and future prevention and control efforts. david j. gregory was the Chief of Poultry and Zoonotic Diseases at the Canadian Food and Inspection Agency and, following his retirement, carried out consultancies for Health Canada, the Canadian Executive Services Overseas in Russia, and the Inter-American ­Institute for Cooperation on Agriculture in Trinidad and Tobago. rowland r. tinline is Emeritus Professor in the Department of Geography at Queen’s University and was director of the Queen’s GIS Laboratory.

TAKING THE BITE OUT OF

RABIES

The Evolution of Rabies Management in Canada

Edited by David J. Gregory and Rowland R. Tinline

UNIVERSITY OF TORONTO PRESS Toronto Buffalo London

© University of Toronto Press 2020 Toronto Buffalo London utorontopress.com Printed in the U.S.A. ISBN 978-1-4875-0428-1 (cloth) ISBN 978-1-4875-1983-4 (EPUB) ISBN 978-1-4875-1982-7 (PDF)

Library and Archives Canada Cataloguing in Publication Title: Taking the bite out of rabies : the evolution of rabies management in Canada / edited by   David J. Gregory and Rowland R. Tinline. Names: Gregory, David J., 1938– editor. | Tinline, Rowland R., 1940– editor. Description: Includes bibliographical references. Identifiers: Canadiana (print) 20190224630 | Canadiana (ebook) 20190224665 |   ISBN 9781487504281 (cloth) | ISBN 9781487519834 (EPUB) | ISBN 9781487519827 (PDF) Subjects: LCSH: Rabies – Canada – History. | LCSH: Rabies – Vaccination – Canada. Classification: LCC RA644.R3 T35 2020 | 616.95/300971 – dc23 This book has been published with the help of a grant from the Ontario Ministry of Natural Resources and Forestry. This book has been published with the help of a grant from Dr Charles MacInnes. This book has been published with the help of a grant from Sanofi Canada. This book has been published with the help of a grant from Artemis Technologies, Inc. University of Toronto Press acknowledges the financial assistance to its publishing program of the Canada Council for the Arts and the Ontario Arts Council, an agency of the Government of Ontario.

For David Our colleague and co-editor, David Gregory, passed away on 22 April 2020 after several months of battling with liver cancer. Bravely, with great determination, he worked through the final editing and proofing of this book despite increasing fatigue, limited mobility, and much pain. David was passionate about celebrating and preserving the legacy of the many Canadians who had, for over a century, developed innovative methods for rabies research, management, and control. Sadly he was not able to see the published edition after working for many years on this project. We the authors, co-editor, and friends are honoured to dedicate this book to David as a testament to his drive and perseverance, without which this book would not have happened.

Contents

Acknowledgments Introduction

xi

xiii

20

38

Hugh Whitney

Catherine Filejski, David J. Gregory, Christopher J. Rutty

Paul Varughese

Overview 73 6 British Columbia

3 Human Rabies in Canada

b) HUMAN RABIES

65

PART 3: A HISTORY OF RABIES MANAGEMENT IN THE PROVINCES AND TERRITORIES

David J. Gregory, Rowland R. Tinline



5 Health Canada and Rabies

5

Christine Fehlner-Gardiner, Pamela Hamill, Alexander I. Wandeler

a) THE MYTH OF THE DUKE OF RICHMOND

57

David J. Gregory

Overview 3

2 Domestic and Wildlife Rabies Incidence in Canada

Overview 55 4 The Federal Department of Agriculture

PART 1: THE BASICS OF RABIES IN CANADA

1 A Rabies Primer

PART 2: THE ROLE OF FEDERAL AGENCIES IN RABIES MANAGEMENT

41

77

David J. Gregory, Rowland R. Tinline, Eleni Galanis, Ken Cooper

7 Alberta

92

Margo J. Pybus

8 Saskatchewan Byrnne Rothwell

102

Contents

9 Manitoba

b) BAIT DEVELOPMENT

111



Tim Pasma

10 Ontario



Rowland R. Tinline, Rick Rosatte

11 Quebec

19 The Development of Aerial Baiting

179

PART 5: DATA COLLECTION AND DIAGNOSTIC METHODS

195

14 Canada’s North

Overview 331

a) YUKON 211

20 Laboratory Development and Standard Basic Diagnostic Methods for Rabies in Canada

Mary Vanderkop, David J. Gregory, Philip Merchant

219

333

Allan Webster, David J. Gregory

Kami Kandola, Brett Elkin

21 Passive Surveillance

c) NUNAVUT 232

344

Frances Muldoon, David J. Gregory, Rowland R. Tinline

Darcia Kostiuk, Peter Workman, Stephen Atkinson d) NUNAVIK 241

311

Peter Bachmann, Lucy J. Brown, Neil R. Ayers

David J. Gregory, Rowland R. Tinline

b) NORTHWEST TERRITORIES

299

M. Kimberly Knowles, Susan Nadin-Davis, Christine Fehlner-Gardiner, G. Allen Casey

James Goltz, Jacqueline Badcock, Rowland R. Tinline

13 Newfoundland and Labrador

291

Artemis Technologies Inc.

18 Testing Rabies Vaccines at Ottawa Laboratory Fallowfield (formerly the Animal Diseases Research Institute)

157

Denise Bélanger, Pierre Canac-Marquis, Ariane Massé, Rowland R. Tinline

12 Maritime Provinces: Nova Scotia, Prince Edward Island, and New Brunswick

Kenneth Lawson, Charles MacInnes

c) BAIT PRODUCTION

125

287

22 Collection and Transport of Specimens

David J. Gregory, Manon Simard

359

David J. Gregory, Graeme Stott

PART 4: THE DEVELOPMENT OF VACCINES AND DELIVERY SYSTEMS

23 Genetic Methods for Rabies Diagnosis and Rabies Virus Typing Techniques

Overview 253

Susan Nadin-Davis, Alexander I. Wandeler

15 Rabies Vaccines in Canada a) HUMAN VACCINES

24 Ancillary Approaches

255

a) ENHANCED SURVEILLANCE IN QUEBEC

Paul Varughese

b) DOMESTIC ANIMAL VACCINES

266



Christopher J. Rutty

16 Regulation of Vaccines in Canada



276

Erin E. Rees Peter Bachmann, Rowland R. Tinline

c) DIRECT RAPID IMMUNOHISTOCHEMICAL TEST FOR THE DETECTION OF RABIES ANTIGEN

281

a) ORAL VACCINES

376

b) BIOMARKERS 384

Carolyn Cooper, Tara da Costa, Oksana Yarosh

17 Oral Vaccine Development in Canada

365

Peter Bachmann, Kim Bennett, Tore Buchanan, Andrew Silver

James B. Campbell, Ludvik Prevec viii

393

Contents

d) TECHNOLOGICAL ADVANCES IMPACTING RABIES VIRUS RESEARCH

32 Rabies and Practice in Public Health in Ontario

402

Susan Nadin-Davis

527

Ian Gemmill

33 Communication Strategies PART 6: THE ECOLOGY AND EPIZOOTIOLOGY OF WILDLIFE RABIES

a) FEDERAL LEVEL

b) PROVINCIAL LEVEL – ONTARIO

Overview 405 25 The Impact of Raccoon Ecology on the Epizootiology of Raccoon Rabies



26 Fox Rabies



PART 8: SPECIAL INTEREST GROUPS 424

Overview 575

Peter Bachmann

b) ECOLOGY OF RABIES IN THE ARCTIC FOX (VULPES LAGOPUS) 453

35 Trapper Participation in Rabies Control in Canada

Audrey Simon, Denise Belanger, Dominique Berteaux, Karsten Hueffer, Erin E. Rees, Patrick A. Leighton

27 Bat Rabies in Canada

577

Beverly Stevenson

36 First Nations People and Rabies

591

Henry Lickers, Michael T. Francis Jr.

466

37 Inuit and Rabies

M. Brock Fenton, Alan C. Jackson, Paul A. Faure

28 Striped Skunks and Rabies: Ecology and Epizootiology

555

David J. Gregory, Beverly Stevenson

Rick Rosatte a) RED FOX (VULPES VULPES) AND RABIES

544

Beverly Stevenson

34 Costs of Rabies Management

407

538

David J. Gregory

599

David J. Gregory, Susan Nadin-Davis, Maanasa Raghavan

480

Margo J. Pybus

29 Recent Advances in the Epizootiology of Wildlife Rabies

PART 9: CONTRIBUTIONS TO RABIES MANAGEMENT

489

Susan Nadin-Davis

30 Understanding Host Dynamics: Applications of Molecular Ecology

Overview 613 38 The Role of the US Department of Agriculture, Wildlife Services in Wildlife Rabies Management

509

Cathy I. Cullingham

615

Dennis Slate, Richard Chipman

PART 7: PREVENTION AND MANAGEMENT OF RABIES IN CANADA

39 Assessing Canada’s Contributions to Rabies Management and Control

Overview 517 31 Prevention and Management in Domestic Animals

Rowland R. Tinline, David J. Gregory

Colour plates follow page 330

519

David J. Gregory

ix

631

Acknowledgments

The idea of a book on rabies evolved from a meeting after a rabies conference in Guelph, Ontario, in 2005. Two colleagues, Dr Rowland Tinline and Dr David Gregory, were concerned that the information derived over the years from the development of Canada’s successful rabies research and management programs was being shredded or lost in various archives and that the experience of persons responsible for this program would be forgotten as they retired or died. They resolved to write a book, a memoir perhaps, to preserve the record of this work as a resource for future managers and researchers and to honour those Canadians whose contributions made it possible. As authors and editors, both Drs Tinline and Gregory had been involved with rabies for years. Dr Gregory had worked for the Canadian Food Inspection Agency (CFIA) for a number of years, both as a field veterinarian at the district level first, and then heading the rabies program when he arrived in Ottawa in 1982. These experiences provided a background to the regulatory content of the book, as well as the many contacts providing information and authorship for the book. Dr Tinline, a professor of geography and ­Director of the Geographic Information Systems (GIS) Lab at Queen’s University, had been a research contractor with the Ontario Ministry of Natural Resources and Forestry (OMNRF) from the early 1970s to his retirement in 2005. He was involved with the analysis of rabies incidence and spread and the development of simulation models and information systems integral to the operation and planning of the wildlife rabies vaccination program of OMNRF. Both were members of the Rabies Advisory Committee for many years. The tables, maps, and graphs throughout the book

would not have been possible without the expertise of Dr Tinline. Dr Gregory used the carrot and stick to keep the authors on a timeline – sometimes with limited success. Resolved to write the book, the two sought to obtain data on submissions and positive rabies cases from the CFIA. An agreement with CFIA to provide rabies data to the authors was signed 8 January 2007, by the two editors/authors and Andrew Adams, director, Ontario Laboratories Network for CFIA. This agreement gave the authors and editors access to stored paper records from 1925 to 1984 and digital submission data from 1985 to 2017. With the ongoing cooperation of CFIA, especially Dr Christine Fehlner-Gardiner, they were able to check, correct, and assemble these data as a digital database that is the source of many of the maps, tables, and graphs in this book. The book could not have been completed without the positive, enthusiastic support and help of many authors, editors, and friends. They were essential to the success of the book by writing, editing, and provoking new interpretations of past events. Those contributors are cited as authors at the beginning of each chapter, acknowledged at the end of many chapters, or included in many of the references quoted. The authors’ access to the history of rabies depended a great deal on the wonderful cooperation received from Canadian libraries and their dedicated staff, who helped research data from many sources. Lynne Thacker and Dorothy Drew from the libraries of Agriculture and Agri-Food Canada head this list for their patience in recovering requested references; Julia McIntosh and Michelle Guitard of Library and Archives Canada for their help in uncovering indemnity payments, clinicals, and vaccination records;

Acknowledgments

the libraries at the CFIA laboratories in Lethbridge and Ottawa for the pictures of past Agriculture Canada laboratories, as well as Dr Bert Stevenson, Sackville Laboratory director, and Rhianna Edwards of the Mount Allison University Archives for photographs of the Sackville Laboratory; Midge Landals of the Alberta Veterinary Medical Association for a copy of the thesis “Sylvatic Rabies and Its Control in Alberta” by Dr Edwin Erb Ballantyne; Dr Christopher Rutty, Health Heritage Research Services for data from Connaught Laboratory Archives, as well as tireless research of the newspaper archives in Toronto; Notman Photographic Archives, McCord Museum, in Montreal for archived photographs of past veterinarians; Leona Kober, Archives and Documentation, Avatage Cultural Institute, Quebec, for translated scripts of Inuit stories; Andrée Marie Delisle, access to information manager in Ottawa, Ontario, for her direction in successfully making numerous requests for government information; Dean Middleton of Public Health Ontario for providing much of the post-exposure prophylaxis (PEP) information for Ontario; and Jean Peart of Health Canada for her insights on health issues. Much of the travel to and research carried out at the libraries was supported by a generous grant of $5000 from the Ontario Wildlife Federation. This grant was solicited by John Lee and administered by the West Parry Sound Health Centre. A deep debt of gratitude goes to Chris Davies, Dennis Donovan, and Tore Buchanan of the Ontario Ministry of Natural Resources and Forestry (OMNRF) for their continuing support of the book. Additionally, and unconditionally, program and data support was provided by four members of their staff, Beverly Stevenson and Peter Bachmann (now retired), and two retired members, Charles MacInnes and David Johnston. Charles MacInnes’s experience and knowledge gained through years as director of the Rabies Research Unit in OMNRF proved to be an invaluable resource in editing many of the chapters. David Johnston, the first biologist to be hired by OMNRF to specifically work on rabies, was our memory archive for details about early research efforts and innovations that made aerial vaccine baiting a reality. Thanks, as well, to

Steve Smith, former chair of the Rabies Advisory Committee, whose advocacy was instrumental in operationalizing the wildlife rabies control program in Ontario. We cannot forget friends and colleagues from CFIA who provided data, information, and wisdom and direction for the book without question. This list includes Brian Evans, Penny Greenwood, Carolyn Inch, Jim Clark, Paul Langan, Nina Szpakowski, Elliot Salsberg, Doug Hayes, Michel ­Beauregard, Ross Singleton, Randall Morley, and David Orr. While mention has been made of the important part played by colleagues at the Ottawa Laboratory, just as important was the part played by Josephine Kush of the Lethbridge Laboratory in bringing together rabies data from western Canada, including survey data, which made life so much easier for the authors. If any colleague has been forgotten in the preceding list, it was not done on purpose and can be attributed to the editors’ fading memories and tangled neurons. The book could not have been published without the continued advice and support from the staff and associates of the University of Toronto Press. Our thanks go to Lynn Fisher, Vice President, Book Publishing, for getting the book on track, Leah Connor, Associate Managing Editor, for her patient guidance of the final production process, and Suzanne Rancourt, Manager of Acquisitions who, together with Ani Deyirmenjian, Production Manager, oversaw cover design and image production. Special thanks to Dawn Hunter, our copy editor from “Mark My Words,” for her careful and insightful improvements to the text and for her special skill in catching those little errors that seem to pop up no matter how much we reviewed our work. Publication does not come without cost. Our thanks to Artemis Technologies, Guelph; Sanofi Pasteur, Toronto; Dr Charles MacInnes (OMNRF – retired) and the Ontario Ministry of Natural Resources and Forestry for their very generous donations in support of the publication of this book. Last but not least are all those people from various walks of life and institutions who went before, and whose vision, energy, foresight, and contributions made Canada’s rabies management program a success nationally and internationally.

xii

Introduction

Rabies is a worldwide problem in mammals both domestic and wild. It is a viral disease that spreads between individuals, primarily in saliva, via bite contact. In humans, it is almost 100% fatal and the “mad dog” remains the main source of infection around the world. Since the late 1940s, however, the ecology of rabies in North America and Europe has changed markedly through a combination of viral shifts, control initiatives, and environmental changes. In those areas, human cases of rabies have decreased; wildlife have become the main source of infection; and innovative control methods have demonstrated that it is possible to eliminate the disease in the treated areas and significantly reduce spread between regions. Research has revealed much about the nature of the virus and has led to the development of improved vaccines for human and animal use and methods of delivering those vaccines orally to wildlife through aerial baiting. Canada has been very successful throughout this period in controlling rabies and is a world-recognized leader in research and development of technologies, policies, and methods that have improved our understanding of the disease and its control. The major objective of this book is to inform the public, the research community, governments, and agencies involved with rabies about Canada’s rabies control and management efforts over time. Our goal is to provide a reference text that allows the reader to understand the contemporary rabies scene in Canada and how this scene evolved, and to appreciate that, although Canada has had success in managing rabies, the ecology of rabies will continue to evolve, and success in the future will depend on continued vigilance and research by those tasked

with rabies surveillance and control. The text will also outline some of the lessons that can be drawn from the Canadian experience that could benefit other jurisdictions. The book began as a discussion between the co-authors/ editors at a rabies conference in Guelph, Ontario, in 2005. They realized that many people, particularly those from the early history of rabies management, had passed away or retired. Further, the corporate memory base was being eroded as important information on rabies was being shredded or stored in various locations without cataloguing. Those trends were accelerating because, as rabies cases declined, government priorities were changing. Resources were being reduced and programs were being off-loaded. We felt that these changing priorities, coupled with the deteriorating collective memory, would make it increasingly difficult for future generations to build on the past contributions to rabies management. Hence, an important goal of the book was to record those contributions and document data relevant to Canada’s story. We have done this by selecting authors who are, or have been, involved in rabies management and research in Canada. Further, where possible, the acknowledgments and references in the various chapters cite other involved Canadians. Finally, we have included tables, graphs, and illustrations to provide a statistical and photographic record of the rabies story in Canada. The book is divided into nine parts so that the reader can approach the story of rabies in Canada from a range of perspectives and needs without reading the book from cover to cover. For example, for the reader wanting to appreciate what is currently known about the virus and the

Introduction

history of rabies incidence in Canada, Part 1 provides a comprehensive overview of these topics. Subsequent parts of the book detail the agencies, the policies, the control methods, and the research and development that have led to the implementation of successful control methods. The organization of those parts revolves around three major themes. First, Canada is a federal state and responsibility for rabies is shared between the federal and provincial or territorial governments. Over the years the federal government has provided the regulations for dealing with rabies and until 2014 was responsible for the collection of suspect specimens and their diagnosis. It retains a leadership role in coordinating control efforts in the provinces and territories. The provincial and territorial governments have ultimate responsibility for rabies management and control, a responsibility that increased dramatically over the past 65 years. This division of labour is reflected throughout the book. Part 2 of the book outlines the work of the two federal agencies, the Department of Agriculture (now called the Canadian Food Inspection Agency) and Health Canada (now the Public Health Agency of Canada) in rabies surveillance, diagnosis, and prevention. Part 3 documents the detailed history of rabies incidence and control in each province and territory. Part 3 also recognizes that the geography of provincial and territorial jurisdictions has changed over time. The current geography was set as recently as 1999 with declaration of Nunavut as Canada’s latest (and largest) territorial government, and the data in those chapters reflect those geographies. The second major organizational theme is chronological. Until 1925 rabies reporting in Canada was not required and, therefore, discussions of rabies incidence and control in this book rely on government and newspaper reports up to 1925. Although human vaccination was used before then, 1925 is a watershed in terms of the emphasis on reporting, prevention, and control. Between 1926 and 1950 rabies incidence in Canada was scattered and occasional and was primarily in dogs and cats and linked to importations of infected animals. Control was typically by quarantine and population control. By the late 1940s and especially in the 1950s, the situation in Canada changed rapidly as invasions of what was later shown to be the arctic fox strain of the virus swept south through the wild canid populations (coyote and fox) in southern Canada, and then remained endemic in Ontario and Quebec. Rabies had become a wildlife disease and much of the rest of the book deals with how it was handled within the provinces and territories (Part 3), especially after 1950; how new vaccines were developed, regulated, and delivered to humans and animals (Part 4);

and how the new threat was handled at the federal level in terms of data collection and improvements in diagnostic methods (Part 5). Finally, one of the most important breakthroughs in understanding rabies was that, rather than there being just one virus strain, there were many and the virus was co-evolving with the specific species at risk. For instance, the arctic fox strain of the virus was the culprit in the spread of rabies from the Arctic to southern Canada in the 1950s. It remained endemic in southern areas until it was controlled via the methods described, for the most part, in Part 2 of this book. Rabies incidence in Canada demonstrates four spatial patterns of rabies incidence associated with specific virus strains. Bat strains have, primarily been associated with British Columbia, although bat strains are increasingly reported across southern Canada. The skunk variant has been endemic in the Canadian prairies since the late 1950s, the result of an invasion from bordering prairie states in the United States. The raccoon variant moved north along the eastern seaboard of the United States, reached southeastern Ontario in 1999, and subsequently reached southwestern Quebec and southern New Brunswick. Those invasions were stopped; intensive control ­efforts remain in place along the vulnerable borders between those provinces and their neighbouring states. Currently Ontario is battling another invasion around Hamilton. Rabies persists in the arctic fox population in the north and remains a threat to southern Canada. To understand those patterns, Part 6 details the ecology and epizootiology of rabies in raccoon, fox (red and arctic), bat, and skunk populations in Canada. It also describes the ­development of the genetic methods used to type the rabies virus and to understand the dynamics of the co-evolution of the virus and its interaction with various hosts. The last three parts of the book deal with topics that are taken for granted or have rarely been treated in the public discussions dealing with rabies. Part 7 deals with the prevention and management of rabies in Canada. It provides a behind-the-scene look at how various agencies at the federal and provincial or territorial levels have cooperated to inform the public about rabies and how those agencies have handled rabies reporting and treatment, especially about human incidence. Chapter 34 goes further to examine some of the actual costs of rabies management and control and, surprisingly, demonstrates that on a per capita basis, Canadians pay well under one dollar per person per year for all management and control programs. Part 8 deals with the role of special interest groups in rabies control and incidence – a topic that has seldom been

xiv

Introduction

common threads or themes running through them seen from different perspectives (i.e., economic, health, safety, management, technical, institutional, or scientific). The data on rabies cases in these chapters have been provided courtesy of the Canadian Food Inspection Agency (CFIA), which originally provided data to 2014. Three subsequent events have required us to update our data to the end of 2017. First, given the size and breadth of topics in the book, the review process took much longer than expected. Subsequently, a number of changes were required to reflect ongoing events, especially the outbreak of raccoon variant rabies in the Hamilton, Ontario, area in 2015. Second, in 2014, the CFIA withdrew from its responsibilities to collect and transport rabies specimens to its laboratories if the species were not human or domestic animal contacts with wildlife with proven or suspected rabies. All other specimen collections came under the mandate of provincial and territorial agencies, although all positive cases from those investigations had to be sent to one of the two existing CFIA laboratories for confirmation. The impact of these changes is discussed throughout the book. Finally, both the reviewers and the authors agreed that the data and associated graphs and tables should be updated to the end of 2017. Chapter 39, the final chapter of this book, reviews Canada’s success in rabies management. The chapter also strikes a cautionary note. Despite the demonstrated success of various control programs, concerns remain that the continuing evolution of the rabies virus, changes in vector ecology, changing agency mandates and budgets, and the possibility of an accidental long-distance transport of a rabid animal will lead to a major rabies event. The raccoon rabies variant outbreak in Hamilton that began in late 2015 confirmed those suspicions and raised others. The authors firmly believe there will be other major rabies events and suggest directions for Canada to pursue to deal effectively with future outbreaks.

examined in the press or in research publications about rabies. Chapters 35 and 36 outline the contributions to rabies control and research by trappers and Indigenous peoples. Chapter 37 discusses how the migrations of northern peoples and their evolving use of dogs appear to be associated with the spread and evolution of the arctic fox strain of the virus and, perhaps, the persistence of rabies in the north. Part 9 documents Canada’s successes in rabies control and management. It also points out concerns that affect Canada’s ability to deal with future rabies threats and how those concerns need to be addressed. Part 9 also deals with the role of our immediate neighbour to the south in rabies control. Rabies knows no borders, and international cooperation between Canada and the United States has played an important role in rabies control in both countries. To this end, Chapter 38 is the only chapter in the book whose authors are not directly associated with Canadian institutions. Those authors, Dennis Slate and Richard Chipman, are the former and current managers, respectively, of the National Rabies Management Program of Wildlife Services within the United States Department of Agriculture, the major agency directing control and research efforts in the United States. The other authors in this book are researchers and managers who have played, or are playing, important roles in dealing with rabies and its management in Canada. We hope this collective approach delivers a comprehensive story about rabies in Canada in a scientifically credible and readable fashion. As well, we have tried to link events through time and, where possible, provide an explanation of the thinking behind decisions taken and how lessons might be drawn from the Canadian experience. Authors were encouraged to tell the “people” stories behind rabies and its management. Because authors and agencies often have been involved in several aspects of rabies research and management, the events in chapters often overlap and have

xv

PART 1

The Basics of Rabies in Canada

Overview Part 1 is an overview of the biology, history, and geography of rabies in Canada and provides a framework for understanding the paths taken by agencies and researchers in the fight to prevent and manage rabies in Canada. Chapter 1 documents our growing understanding of how the rabies virus spreads, how it develops within the host, and how the host reacts to infection. This story is interwoven with the development of human and animal vaccines and the increasing role played by molecular methods in the study of rabies. The story of work on the virus and management methods is closely linked to the history and geography of rabies incidence in Canada. Hence, Chapter 2 examines rabies incidence in animals, which, because of the nature of reporting in Canada, is broken into two time frames: pre-1925 and post-1925. Chapter 3 documents human incidence in Canada, beginning with the story of the Duke of Richmond and moving through the subsequent history of human cases until 2012. In Canada, rabies reporting was driven by the need to investigate circumstances of potential rabid contacts between human and animal populations, so our view of the patterns in animal rabies has been filtered through the emphasis on reporting human cases.

1 A Rabies Primer Christine Fehlner-Gardiner,1 Pamela Hamill,2 and Alexander I. Wandeler3 1

Canadian Food Inspection Agency Centre of Expertise for Rabies, Ottawa, Ontario, Canada 2 BioReliance, Ltd., Stirling, Scotland 3 Canadian Food Inspection Agency Centre of Expertise for Rabies (Retired), Ottawa, Ontario, Canada

Rabies Virus

Structure and Morphology

Classification

GENOME

Rabies virus (RABV) belongs to the Rhabdovirus family and, more specifically, is the type species of the Lyssavirus genus. Lyssaviruses are further grouped into 16 distinct species based on similarities in nucleotide sequences (ICTV Reports, 2019), all of which can cause rabies-like illness in infected mammals. In common with other lyssaviruses, RABV possesses a ribonucleic acid (RNA) genome and a distinctive bullet-shaped virion surrounded by an envelope. Nucleotide sequence variation in different regions of the RABV genome can be used to discriminate between different strains and variants of RABV, which may be geographically r­estricted and are associated with specific host reservoirs. Sequence analysis is also used as a tool to investigate the evolution of RABV variants and their movement through geographical regions, which will be discussed in detail in Chapter 29.

RABV has a relatively small and simple genomic structure of single-stranded, negative-sense RNA consisting of only five genes that encode the five viral proteins, all of which are incorporated into the rabies virion and play both structural and functional roles in the life cycle (Figure 1.1). VIRION

In common with other lyssaviruses, the RABV RNA genome is tightly associated with the viral nucleoprotein (N). Encapsidation of the viral genome by the N protein is essential for virus replication, and the RNA-N complex is termed the ribonucleoprotein (RNP). The viral polymerase enzyme (L) and phosphoprotein (P) are also closely associated with the RNP complex; collectively, the N, L, and P proteins constitute the capsid, the protein shell of the virus. The capsid is in turn associated with the matrix (M) protein, which forms a layer between the viral capsid and the outer envelope, a lipid membrane derived from the host cell

Figure 1.1: Rabies virus genome. Source: authors.

The Basics of Rabies in Canada

Figure 1.2: Schematic representation of a rabies virus. Source: authors.

that surrounds the entire virion. The RABV glycoprotein (G) is a transmembrane protein that extends outward from the surface of the viral envelope but also interacts via its cytoplasmic domain with the M protein. A cartoon representation of the RABV particle is shown in Figure 1.2.

UNCOATING

Attachment of the virus particle triggers internalization by endocytosis into cytoplasmic vesicles. The details of this process are also not well characterized; however, rabies virions are found inside clathrin-coated and uncoated vesicles (Superti et al., 1984). The viral envelope then fuses with the vesicle membrane so that the viral capsid is released into the cell cytoplasm, which is essential for replication. Fusion only occurs following a decrease in the pH of the vesicle and is solely dependent on the viral G protein.

Rabies Virus in Cells Rabies Virus Replication An overview of the replicative infective strategy of RABV is provided here based on the known multifunctional roles of the RABV proteins in the virus life cycle and by analogy with other rhabdoviruses, recently reviewed in Guo et al. (2019). Since many aspects of RABV replication are still not fully understood, additional functions of the five proteins in the virus life cycle and how they interact with host cell proteins are likely to be elucidated as research progresses.

REPLICATION

Once the naked capsid is released into the cytosol, viral replication can begin. It is thought that this occurs in inclusion bodies throughout the cytoplasm of infected cells known as Negri bodies. These structures are often used as diagnostic markers for rabies since they are typically found in rabies-infected neuronal cells and contain a concentration of RABV protein that can be detected by anti-RABV antibodies. The first step in replication requires the production of positive-sense viral messenger RNA (mRNA) that can then be transcribed for de novo viral protein synthesis. Once in the cytosol, the RABV RNP complex must undergo a structural change, since the condensed form of the RNP complex is unsuitable as a template for RNA synthesis. After conversion to a relaxed form, the viral polymerase, also present in the uncoated viral capsid, transcribes the RNA into leader RNA (uncapped, unpolyadenylated) and positive-sense mRNAs encoding the viral proteins, which are synthesized in the cytoplasm on free ribosomes. Transcription proceeds in a 3'–5' direction, with the polymerase disengaging from the template at conserved stop signal sequences and restarting at transcription start signals for each gene. Since commencement of transcription following stop signals may not always be successful, generally lower levels of transcription occur for genes

ATTACHMENT/ENTRY

The first step in RABV infection is attachment to the host cell. This involves specific interaction between the viral G protein and receptors on the cell surface. The receptor(s) used by RABV are not well understood. Although several in vitro studies have identified putative candidate cell surface receptors (Lentz et al., 1982; Lentz et al., 1983; Thoulouze et al., 1998; Tuffereau et al., 1998), so far none of these receptors have been verified as being required for viral replication in animal studies (Tuffereau et al., 2007). A recent study identified metabotropic glutamate receptor subtype 2 as a receptor for RABV both in vitro and in vivo (Wang et al., 2018). In addition to specific cell receptors, other cell surface molecules, such as carbohydrates (Conti et al., 1986) and lipids (Wunner et al., 1984), have been proposed as being involved in RABV attachment (reviewed in Lafon, 2005).

6

A Rabies Primer

closer to the 5' end of the genome, resulting in an intrinsic regulation of mRNA production and hence the protein expression levels of the different RABV proteins. After sufficient quantities of viral protein have been made, a switch occurs from the production of viral mRNAs to genome replication, which involves the generation of fulllength positive-sense copies to act as templates for synthesis of new genomes to be incorporated into progeny virus. The precise mechanism by which this switch occurs is not fully understood, but it is thought that the relative ratios of leader RNA and N dictate the switch. When sufficient quantities of leader RNA have been made, it is encapsidated by N, in a process also involving the P protein, which appears to impart selectivity on N to bind viral RNA. This is inferred by studies showing that, in the absence of the P protein, N binds equally well to viral and cellular RNA (Liu et al., 2004). Encapsidation of the leader RNA is thought to result in synthesis of full-length genome copies rather than mRNAs corresponding to each gene.

in continuous cell culture was first achieved almost 40 years ago using baby hamster kidney cells, line 21 (BHK21) (Larghi et al., 1975); chick embryo–related (CER) cells; and neuroblastoma cells (Smith et al., 1978). The landmark findings that RABV can be cultured in both continuous cell lines and in primary cells has facilitated the development of cell-based infectivity tests (Rudd et al., 1980; Webster, 1987; see Chapter 20) and enabled in vitro research to investigate pathogenesis and host cell responses to infection. Cellbased diagnostic assays in which cell lines are inoculated with tissue from suspect rabid animals are as, or more, sensitive than the previously used mouse inoculation test (Koprowski, 1966) and allow the detection of viral antigen by immunofluorescent staining approximately four days post-inoculation.

Rabies Virus in Organisms Entry Sites

ASSEMBLY/EGRESS

Following protein synthesis and genome replication, encapsidation of viral genomic RNA by N occurs as the first stage in packaging of the genome and assembly of new viral particles. The N and P proteins together specifically interact with viral genome copies to form the RNP, along with the polymerase protein. Once the M protein has also formed a layer around the RNP complex, the virion is ready to bud and be released from the infected cell. The M protein has been shown to have a critical role in condensing and targeting the RNP to the plasma membrane and incorporation of the G protein into budding virions (Finke et al., 2010; Mebatsion et al., 1999; Okumura & Harty, 2011). The G protein, which must be glycosylated, traffics through the endoplasmic reticulum and Golgi apparatus and translocates to the cell plasma membrane (Wojczyk et al., 1998). Assembled viral capsids then migrate to the plasma membrane to regions containing G protein, where they interact and bud from the cell, releasing progeny virus enveloped in host cell plasma membrane. A summary of the structural and functional roles of the RABV proteins are provided in Table 1.1, along with the relevance of each protein to rabies prophylaxis, diagnosis, and treatment.

RABV is most commonly transmitted to a susceptible host through a bite from an infected animal; however, infection can result from contamination of open wounds or mucous membranes with viremic saliva. Virus transmission by the oral route has been demonstrated experimentally in some species (Bijlenga & Joubert, 1974; Black & Lawson, 1973; Charlton & Casey, 1979a, 1979c; Lawson et al., 1987), and the discovery of vaccine-induced cases in wildlife and domestic animals following oral vaccination programs using live, attenuated vaccines further support that transmission through the oral route is possible (Fehlner-Gardiner et al., 2008; Wandeler, 2000). Infection of tissues within the oral cavity is required as the virus is readily inactivated by the high pH in the stomach. Aerosol transmission of rabies to animals has been demonstrated experimentally (Constantine, 1962; Johnson et al., 2006), and laboratory-acquired infections have been documented after exposure to aerosols (Tillotson et al., 1977; Winkler et al., 1973). In the 1950s two cases of human rabies in individuals exploring a Texas cave harbouring millions of bats suggested that aerosol transmission is possible in natural settings (Constantine, 1967), although subsequent investigations suggested that more common routes of transmission were more likely (Gibbons, 2002). Human rabies cases have also been reported following organ transplantation (Hellenbrand et al., 2005; Houff et al., 1979; Srinivasan et al., 2005) and butchering of dogs for consumption (Kureishi et al., 1992; Wallerstein, 1999; Wertheim et al.,

Rabies Virus in Cell Culture Although RABV displays a tropism for neuronal cells during a natural infection in vivo, in culture it can grow in a variety of cells. Isolation of RABV from infected tissue

7

The Basics of Rabies in Canada

Table 1.1  Rabies virus protein roles and functions; relevance to rabies virus prophylaxis, diagnosis, and treatment. Protein

Structural/Functional role

Significance for rabies prophylaxis, diagnosis, and treatment

Nucleoprotein (N)

Encapsidates the viral RNA genome to form the ribonucleoprotein (RNP) complex, the condensed form required for packaging of progeny viral genomes

Important antigen for generation of anti-rabies antibodies used in rabies diagnostic tests Gold-standard diagnostic tests such as fluorescent antibody test (FAT) employ antibodies directed against RNP to detect rabies virus Gene encoding N can be used as a target for polymerase chain reaction (PCR) reactions to detect rabies virus in molecular diagnostic tests

Polymerase (L)

Phosphoprotein (P)

Forms part of the viral nucleocapsid, along with N and P

Target for antibodies against the RNP complex used in rabies diagnostic tests

Multiple enzymatic activities, including the viral RNA polymerase function required for the transcription of mRNAs for viral protein expression and synthesis of full-length copies of the genome

Gene encoding L can be used as a target for PCR reactions to detect rabies virus in molecular diagnostic tests.

Forms part of the viral nucleocapsid, along with N and L

Target for antibodies against the RNP complex used in rabies diagnostic tests

Is a non-catalytic subunit of the viral polymerase complex

Gene encoding P can be used as a target for PCR reactions to detect rabies virus in molecular diagnostic tests.

Is thought to act as a co-factor for specific binding between N and the viral genome Matrix (M)

Forms bridge between the viral RNP and the G protein in the viral envelope Plays critical role in recruitment of rabies RNP complexes to sites of budding of progeny virus from infected cells

Gene encoding M can be used as a target for PCR reactions to detect rabies virus in molecular diagnostic tests.

Involved in the regulation of viral transcription and replication: high concentrations may inhibit RNA synthesis and promote condensation of the RNP into helical form found in virions Glycoprotein (G)

Is the outermost viral protein in the rabies virion; interacts with the matrix protein, spans the viral envelope, and extends from the surface of the virion

Antigenic determinant of rabies virus strains

Is responsible for attachment to host cell; pH-dependent fusion with host cell vesicular membrane

Immunogenic target of rabies vaccines, since antibodies reactive against G can neutralize rabies virus and prevent infection; anti-G antibodies measured in serological assays used to determine post-vaccination immunity against virus (neutralization assays such as rabies fluorescent focus inhibition test)

Target for rabies immunoglobulin treatment (RIG): antibodies in immune sera neutralize G and prevent viral spread at the wound site

Source: authors.

the incubation period is generally between one and three months following exposure, but much shorter and much longer incubation periods have been documented (Fishbein, 1991; Smith et al., 1991). Variable incubation periods are also characteristic of rabies in animals, from several days to months, though periods of 3 to 12 weeks are common for domestic animals (Beran, 1994). The length of the incubation period can vary depending on the species, size of inoculum, site of entry, severity of bite wound, and

2009). Nonetheless, RABV transmission by bite accounts for the vast majority of rabies cases in both humans and animals (Warrell & Warrell, 2004).

Incubation, Progression to, and Spread within the Central Nervous System RABV infection is characterized by a variable incubation period during which the host is asymptomatic. In humans 8

A Rabies Primer

immune status of the host (Wandeler, 1987). Replication within muscle fibres can occur (Charlton & Casey, 1979b; Murphy et al., 1973; Murphy & Bauer, 1974) and may affect the length of the incubation period; indeed, in experimental infections of skunks, the virus could be detected in muscle tissue for as long as two months following inoculation (Charlton et al., 1996). However, replication in muscle is not a requirement for infection. Studies using the fixed RABV challenge virus standard-11 in rodent and primate models demonstrated that the virus could directly infect motor endplates following intramuscular inoculation at high titre (reviewed in Ugolini, 2011). As early as the late nineteenth century, it was known that rabies infection involved the nervous system (see references in Baer et al., 1965); however, it was still postulated that virus dissemination could occur via blood or lymph. The role of peripheral nerves in the progression of virus from the site of inoculation to the central nervous system (CNS) was nicely demonstrated by protection from disease in various animal species (rodents, dogs, and foxes) that underwent amputation or surgical removal of the sciatic and saphenous nerves following footpad inoculation (Baer et al., 1968; Baer et al., 1965; Dean et al., 1963). The virus transits from the periphery to the CNS via retrograde transport from the axon terminus to the neuronal cell body in the spinal cord, where robust viral replication occurs (Tsiang, 1993). Once within the spinal cord, the virus propagates between connected neurons exclusively by unidirectional transneuronal transfer, with fast axonal transport to the brain occurring at a rate of between 50 and 100 mm/day (Ugolini, 2008). Within the brain, RABV replicates predominantly within neuronal cells; however, infection of astrocytes and oligodendrocytes has been observed (Jackson et al., 2000, and its references).

Hemachudha, 2010), contact with urine or blood is not considered a rabies exposure (World Health Organization [WHO], 2005). Anterograde spread of virus from the CNS to extraneuronal organs is likely mediated by passive diffusion rather than by active transport mechanisms (Ugolini, 2011). Centrifugal spread of the virus to extraneuronal tissue is clearly important for disease transmission in natural settings via saliva and also as observed in human organ transplantation cases and those associated with the butchering of infected animals. From a diagnostic standpoint, the appearance of the virus in saliva, skin, and eyes can be exploited for ante-mortem testing in suspected human cases (Dacheux et al., 2010).

Excretion with Saliva Of most relevance for disease transmission is virus replication within the salivary glands and its excretion in saliva. Although it is unlikely for the virus to be found in the salivary glands before replication in the brain, experimental infections in dogs, cats, ferrets, and foxes showed that the virus could be detected in the saliva of some animals several days before the onset of clinical signs (Fekadu & S­ haddock, 1984; Fekadu et al., 1982; Niezgoda et al., 1998; Sikes, 1962; Vaughn et al., 1963; Vaughn Jr et al., 1965). These observations form the basis of the common recommendation for a 10-day observation period for biting dogs and cats that appear healthy at the time of the incident (Brown, 2011). However, virus excretion in saliva is not observed in all rabies cases, can be intermittent, and can vary in magnitude among species. For example, a survey of rabid wildlife from Switzerland found that while the brains of foxes, badgers, and stone martens had similar virus titres, a higher proportion of rabid foxes and badgers had detectable virus in their salivary glands and had median titres two orders of magnitude higher than did stone martens (Wandeler et al., 1974). Thus, while the presence of virus in saliva is diagnostic for rabies, its absence is not. For this reason, it is recommended for human diagnosis that serially collected saliva samples be analysed for the highest sensitivity (Dacheux et al., 2008).

Centrifugal Spread and Replication in Peripheral Organs Following replication to high titre in the CNS, RABV spreads centrifugally to peripheral tissues. Although RABV is often found within peripheral nerves, extraneuronal replication can also be observed (Wandeler, 1987). Within both humans and animals, virus, viral antigen, and viral RNA can be found to varying extents in salivary glands, skin, cornea, nasal mucosa, tongue, pancreas, intestines, adrenal glands, and other tissues (Beauregard & Casey, 1969; Charlton et al., 1984; Constantine et al., 1972; Dierks et al., 1969; Fekadu & Shaddock, 1984; Hamir et al., 1992; Jackson et al., 1999; Jogai et al., 2002). Although in one study viral RNA was detectable in the urine of human patients (Dacheux et al., 2008; Wacharapluesadee &

Clinical Presentation As with the incubation period for rabies, the clinical presentation can be quite variable. The morbidity period can vary with species but in general lasts from four to seven days. Longer morbidity periods have been observed in humans who have received intensive supportive care in 9

The Basics of Rabies in Canada

hospital (Jackson et al., 2003). The asymptomatic incubation period is followed by a period of prodromal symptoms that may include malaise, anorexia, fever, fatigue, and nausea (Jackson, 2000). These prodromal symptoms may be followed by pain, numbness, or tingling at the site of the bite wound; agitation; and difficulty swallowing. An acute neurologic period follows, which in general may be characterized as either encephalitic (also known as “furious rabies”) or paralytic (also known as “dumb rabies”). Furious rabies tends to have a shorter morbidity period than the paralytic form (Hemachudha et al., 2005) and is characterized in humans by extreme agitation and restlessness, hydrophobia, and aerophobia (reviewed in Jackson, 2007; see Chapter 5). Periods of delirium and lucidity may be intermittent. The paralytic form of rabies is characterized by ascending flaccid paralysis from the site of the bite and lacks the dramatic hallmarks of the furious form. For this reason it is not always recognized by clinicians as rabies, although approximately 20% of human cases exhibit this presentation (Jackson, 2000). Patients eventually succumb to coma and death caused by autonomic dysfunction and resulting organ failure (Jackson, 2007). Behaviours such as activity during the day for nocturnal animals, loss of fear of humans, and abnormal vocalizations are characteristic of rabies in animals (reviewed in Hanlon et al., 2007). Those with the furious form of rabies exhibit extreme agitation and aggressive behaviours, including attacking other animals and even stationary objects. These behavioural changes can facilitate the transmission of the virus to a new host. Dumb rabies in animals manifests as paralysis, often starting in the hind limbs; lethargy; and depression. In both forms, hypersalivation and the inability to swallow can result in the characteristic foaming at the mouth. As with human disease, death results from multi-organ failure (Hanlon et al., 2007).

cell-mediated (T-cell) and humoral or antibody-mediated (B-cell) responses, which can directly inactivate the virus by neutralization, opsonisation, or complement-mediated lysis in the case of antibody responses, or which can result in the destruction of virus-infected cells by cytolytic or apoptotic mechanisms, as well as production of cytokines, mediated by activated T cells. RABV has evolved a number of strategies to evade both the innate and the adaptive immune responses of the host; these have been reviewed in detail (Lafon, 2011). As examples of these mechanisms, the RABV G protein promotes the survival of infected neurons by interfering with apoptotic and survival signalling pathways (Prehaud et al., 2010), and the P protein inhibits transcriptional activation of interferon genes and interferon signalling pathways (Rieder & Conzelmann, 2011; Wiltzer et al., 2012). Sequestration of TLR-3 into Negri bodies within infected cells decreases TLR-3’s ability to promote neuronal apoptosis and inhibition of axonal growth (Ménager et al., 2009). Maintenance of the integrity of infected neurons minimizes the inflammatory response within the CNS; a number of studies have demonstrated an inverse correlation between RABV strain pathogenicity and the level of the induced inflammatory response, although the specific mechanisms involved have not been elucidated (Bahloul et al., 2003; Hicks et al., 2009; Laothamatas et al., 2008; Wang et al., 2005). At the same time, RABV infection upregulates neuronal expression of molecules that trigger cell death pathways in activated migratory T-cells that, in the absence of this effect, would be expected to clear the infection from CNS tissue (Lafon, 2011). Last, infection of cells within an immune-privileged site decreases the opportunity for B-cell activation and subsequent production of protective antibody (Hooper et al., 2011). Indeed, while vaccination can result in robust humoral and cell-mediated immune responses that protect against virulent challenge (see the next section, “Vaccination against Rabies and Protective Mechanisms”), natural infection does not appear to induce a vigorous immune response. In human infection, production of a virus-neutralizing antibody is generally not seen until late in infection (Jackson, 2000) and frequently seroconversion is not detectable (reviewed in Johnson et al., 2010). Despite these immune-evasive mechanisms and the high mortality rate of rabies, results of sero-surveys in various wildlife species, particularly in bats, have suggested that recovery from rabies resulting from natural infection may be possible (Dimitrov et al., 2007; East et al., 2001; Jackson et al., 2008; Turmelle, Kunz, et al., 2010). Similarly, studies on human populations have found seropositive individuals in the Arctic, with potential repeated exposures to

Immune Response to Natural Infections Viral infections in general induce both innate and adaptive immune responses that contribute to viral clearance. Innate responses involve the activation of pattern recognition receptors, such as the toll-like receptors (TLR) and retinoic acid-inducible gene I (RIG-1), by components unique to viruses, such as double-stranded RNA or single-stranded RNA with a 5'-triphosphate as found in the RABV genome. Activation of these receptors initiates intracellular signalling cascades resulting in the production of pro-­inflammatory cytokines, including interferons, thus promoting an anti-viral state. Adaptive immunity is characterized by

10

A Rabies Primer

infected foxes through trapping (Follmann et al., 1994; Orr et al., 1988), and in Amazonia, with exposures to vampire bats (Gilbert et al., 2012), in the absence of vaccination or reported disease. However, the question still remains whether the seropositive animals and humans observed in these studies survived clinical lyssavirus infection or were exposed to the virus (resulting in antibody production) without development of clinical disease. Several cases of human recovery from clinical rabies without vaccination have been documented (Centers for Disease Control & Prevention, 2010; Wiedeman et al., 2012; Willoughby et al., 2005), suggesting it is possible under certain circumstances.

by deficiencies in the application of the treatment (e.g., no RIG given, vaccine regimen not completed) or in the vaccines themselves (e.g., vaccine of inadequate potency). Passive immunization likely contributes to protection from disease by neutralization of the virus at the site of inoculation. Similarly, mechanisms of protection resulting from post-exposure vaccination may include neutralization of extracellular virus, complement-mediated lysis of infected cells, and antibody-dependent cytoxicity (Schumacher, 1989). As well, cellular immune responses, particularly those of T helper cells, also likely play a role in protection (Celis et al., 1986; Ertl et al., 1989; Wiktor, 1978; Wiktor et al., 1977). However, given that the CNS is an immunologically privileged site, these mechanisms of protection may not be adequate to clear the infection once the virus has reached the CNS. Indeed, once symptoms are evident (i.e., the virus has reached the brain), vaccination is ineffective (WHO, 2005).

Vaccination against Rabies and Protective Mechanisms For both human and animal vaccines, the principle protective antigen is the glycoprotein as this is the only viral protein against which neutralizing antibodies are raised (Cox et al., 1977), levels of which are considered a correlate of protection (Moore & Hanlon, 2010). However, it has been demonstrated that laboratory animals were protected from virulent challenge following immunization with RNP or purified recombinant N protein (Dietzschold, 1987; Fu et al., 1991) and that some neutralizing antibody-positive raccoons orally immunized with recombinant vaccines that encoded only the G gene succumbed following challenge (Rupprecht et al., 1988; Brown et al., 2012). These data support that other viral proteins have a role in inducing a protective immune response, likely through the activation of other immune effector mechanisms that complement or augment the production of neutralizing antibodies (Dietzschold et al., 1989).

ANIMALS

As with human rabies vaccines, animal vaccines produced in cell culture are recommended to replace the use of nerve-tissue vaccines and live-attenuated rabies vaccines for parenteral immunization (World Organisation for Animal Health [OIE], 2008). Mass vaccination campaigns targeting dogs have been successful for the reduction of both dog rabies cases and associated human cases transmitted by dogs (Schneider et al., 2007). As is described in detail in later chapters, oral vaccination (ORV) programs using live-attenuated and recombinant vaccines in baits, in conjunction with trap-vaccinate-release (parenteral vaccination with killed vaccines) and limited population reduction, have been very successful in Canada for the control of rabies in foxes (Chapter 26), raccoons (Chapter 25), and skunks (Chapter 28). Similarly, ORV has been efficacious in controlling rabies in grey foxes and coyotes in Texas (Sidwa et al., 2005; Slate et al., 2009) and in red foxes and raccoon dogs in Europe (reviewed in Vitasek, 2004). Use of oral vaccines for immunization of domestic dogs that are inaccessible for parenteral vaccination (e.g., some feral dog populations) is also under investigation (Cliquet et al., 2007; Faber et al., 2009; WHO, 2007; Gibson et al., 2019).

HUMANS

Although rabies has the highest mortality rate of any zoonotic disease (approaching 100% once clinical symptoms appear), the disease is completely preventable with appropriate and timely treatment following an exposure to a rabid animal. This treatment includes proper wound cleaning, passive immunization by administration of rabies immunoglobulin (RIG), and active immunization through parenteral administration of inactivated vaccine prepared in either purified duck embryos or cell-culture (WHO, 2005). Nerve-tissue vaccines are no longer recommended because of the possibility of severe adverse events and inferior potency (WHO, 2005). Various intramuscular and intradermal regimens have been shown to be effective. True vaccine failures are rare and can usually be explained

Rabies Virus in Host Populations Lyssaviruses have two main reservoirs. Different carnivores, including domestic dogs, are the principal hosts for the classical rabies virus (Rabies virus, formerly; genotype 1)

11

The Basics of Rabies in Canada

in Asia, Africa, Europe, and in the Americas. Bats are recognized as hosts of lyssaviruses in Australia, Africa, Europe, and in the Americas. Our understanding of the epidemiology of rabies in North America changed considerably during the twentieth century. Up to the 1930s rabies was thought to be almost exclusively propagated by domestic dogs. Interestingly, the first convincing information on rabies in wildlife came mostly from the Arctic (Elton, 1931). With dog rabies declining, rabies in wild Carnivora became more and more recognized, with increasing awareness of an expanding fox rabies epizootic advancing from the North (Tabel et al., 1974; see Chapter 10) and the identification of the disease in skunks in the American Midwest (Charlton et al., 1991) and in raccoons in Florida (Winkler, 1991). The discovery of rabies in bats first in the United States and then in Canada led to much speculation about the role of Chiroptera in sustaining rabies in wild Carnivora (Fischman & Young, 1976). Other hypotheses speculated about the role of some bat species migrating south during winter and bringing rabies back to the species hibernating in northern locations (Pybus, 1986; Rosatte, 1985). Though attractive, these speculations were largely proven false when newly developed techniques for virus variant identification demonstrated that each of the important rabies vector species propagated their own distinct virus variants (Baer & Smith, 1991; Nadin-Davis et al., 2001). This demonstrates the danger of accepting hypotheses not sufficiently tested for their relevance to real life. Unfortunately, epidemiological hypotheses are frequently complicated or even impossible to test. Null hypotheses are tricky to formulate and even more difficult to falsify. Aside from these more academic issues, there is also the problem of the validity of data. Though we now understand the epidemiology of rabies much better than a few decades ago, we still have to be vigilant when interpreting field data. The material submitted to a diagnostic laboratory is highly biased since it is influenced not only by the disease prevalence in nature but also by the density of humans in the area, by their inclination to notice and submit suspect animals of a particular species, and by submission policies and guidelines that restrict submissions to specimens that have a history of human or domestic animal contact (Chapter 21).

its principal hosts is always characterized by high hostspecific pathogenicity and high levels of virus excretion with saliva. This concept was reinforced by observations on the European fox rabies epizootic. Jean Blancou (1988) and his team at the Laboratoire d’études et de recherches sur la rage et la pathologie des animaux sauvages in Nancy, France, established the susceptibility and the rate and magnitude of virus excretion for many European species. They found that the red fox has indeed the highest susceptibility to the European fox virus. Rabid foxes also excrete more virus in their saliva than do most other rabid animals infected with the European fox virus. From these observations the French team developed the concept of viral biotypes. A biotype is a virus variant adapted to a principal host species by especially high pathogenicity for this species, a high rate of excretion, and low immunogenicity (Blancou, 1988). In addition, the high efficiency of transmission and the high lethality does not generate any substantial herd immunity (Wandeler et al., 1974). We might be tempted to view RABV as perfectly adapted to persist in large populations of species with high intrinsic growth rates that are capable of recovering rapidly after an epizootic wave has reduced the population density to a level at which the reproductive rate of the disease (disease transmission) falls below unity. This appears to fit well with the observation that the Carnivora serving as principal hosts all have similar life history traits and population characteristics. Red foxes, jackals, domestic dogs, striped skunks, and raccoons all are opportunistic, medium-sized species with a wide distribution and contiguous populations of relatively high density. They all also have high reproductive rates that permit rapid population recovery. The statement above may be incorrect for the situation in the Arctic. The epidemiology of arctic rabies is poorly understood. It is commonly believed that the disease is maintained in populations of arctic foxes. Sometimes the participation of red foxes is assumed. A possible role of domestic dogs is generally not considered (Chapter 37). It is also frequently alleged that arctic rabies is the source of fox rabies epidemics in agricultural areas of temperate climate zones. If all these assumptions are correct, then there must be mechanisms that permit the disease to persist in these patchily distributed hosts that experience dramatic fluctuations in population density. The periodicity of rabies in red fox populations in agricultural and urbanized areas is well described and might be interpreted to be the result of density-dependent transmission: initial high population densities are reduced by a high disease-induced mortality, with a rapid recovery thereafter to restart the cycle (Anderson et

Rabies in Wild Carnivora The pioneering work of Keith Sikes (1962) and Parker & Wilsnack (1966) on the high susceptibility of foxes and skunks to RABV propagated by these species in North America led to speculation that RABV adaptation to

12

A Rabies Primer

al., 1981; see Chapter 26). It is uncertain if similar mechanisms are the cause of disease cycles in northern areas. We may assume that the frequency with which the two Canadian rabies laboratories receive submissions from the Arctic reflects the undulating incidence of the disease in foxes. However, populations of arctic and red foxes in Arctic and subarctic habitats fluctuate in density, mostly as a consequence of varying prey (rodents, lagomorphs) availability (Englund, 1970; Tannerfeldt & Angerbjörn, 1996). The number of animals submitted for diagnosis may reflect disease-independent population cycles. Chapter 26b on arctic foxes provides further discussion on the persistence of rabies in the Arctic.

time is indicated by its widespread occurrence across the continent from the tropics to subarctic regions, its occurrence in almost all species of bats (Constantine, 1979), and most importantly its genetic polymorphism (Nadin-Davis et al., 2001; Smith, 1988). Most North American bat species propagate their own specific RABV variants. This could be interpreted as ecological compartmentalization or as adaptive radiation of RABV within the bat community. Both processes likely take more time than just a few decades to evolve to the stage observed today.

Rabies Virus in Host Communities

Bat Rabies

It is essential for rabies survival that the virus is transmitted by an infected host during a period of virus excretion to enough, but not too many, other susceptible individuals. For this to occur, lyssavirus strains must adapt to the physiological traits and population biology of their hosts (Bacon, 1985a; Wandeler, 1991). They must have a host-specific pathogenicity and pathogenesis. The length of the incubation period, duration and magnitude of virus excretion, and duration and signs of clinical illness must correlate with the principal host’s population dynamics, its behavioural traits, and its social use of space. The frequency of infectious contacts is not simply a result of population density. It is the result of a complex set of interactions that occur between a susceptible animal reacting to a conspecific, possibly familiar, individual that is behaving abnormally. We attempt to explain the epidemiological patterns of fox rabies by the very high transmissibility (high susceptibility and high rate of excretion) and high lethality of this disease. Also, use of such disease characteristics and parameters of fox population biology and ecology in theoretical models can result in plausible outcomes (see Bacon, 1985b; Harris & White, 2004). However, this type of association between a parasite and its host is fairly uncommon. We might expect to observe other blueprints for RABV survival in other host species. This is fairly obvious for species with completely different life history traits, such as bats, but important digressions can also be found in Carnivora. All principal hosts transmit the disease to other species, which are sometimes highly susceptible, but whose population biology and behaviour are not conducive to maintaining an epizootic. Genome sequencing confirms that most cases that we had interpreted as spillover are indeed victims of exposure to a principal rabies host species. The prevalence of spillover cases in other species is a result not only of their susceptibility but also of behavioural peculiarities

The zoological order Chiroptera (bats) comprises over one thousand species worldwide. They occur on all continents except Antarctica. Four families with 46 species have been reported in the United States, while in Canada 20 species (Chapter 27) belonging to two families have been reported (van Zyll de Jong, 1985). The non-colonial (solitary) tree bats of the genera Lasionycteris and Lasiurus migrate south in winter. Species that remain all year in areas with temperate climates hibernate, often in large colonies in hibernation roosts (also called hibernacula). Some bats migrate over long distances to overwinter in specific hibernacula. Microchiroptera have evolved a complicated echolocation system that permits them to navigate without any visual clues and allows insectivorous species to detect and locate their prey. Though the majority of the North American bats are aerial insectivores, some collect insects from the ground or from vegetation, while others are generalists. The Americas are the only continents where bats harbour lyssavirus RABV. That vampire bats transmit a lethal disease to terrestrial mammals and humans was already noted by the sixteenth-century Spanish colonists of Central America (Acha & Arambulo, 1985). That this disease was indeed rabies was recognized early this century (Carini, 1911; Haupt & Rehaag, 1925). That not only vampire bats, but also frugivorous bats (Artibeus and other species) could be infected by rabies was already recognized at that time. But it was not until 1953 that the first bat (Lasiurus intermedius) north of Mexico was diagnosed rabid (Scatterday, 1954; Venters et al., 1954). Within a decade bat rabies was found in almost all the US states and in Canada. There is no doubt that the recent emergence of bat rabies is an artefact because of its sudden recognition in the media. That rabies existed in insectivorous bat populations for a long

13

The Basics of Rabies in Canada

that may make them more prone to exposure from infectious contacts. The colonization of a new host species is facilitated in particular locations where habitat conditions

lead to a population structure that allows the propagation of a virus variant usually associated with another principal host.

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New England Journal of Medicine, 352, 1103–1111. https://doi.org/10.1056 /NEJMoa043018 Superti, F., Derer, M., & Tsiang, H. (1984). Mechanism of rabies virus entry into CER cells. Journal of General Virology, 65(Pt. 4), 781–789. https://doi.org/10.1099/0022-1317-65-4-781 Tabel, H., Corner, A. H., Webster, W. A., & Casey, C. A. (1974). History and epizootiology of rabies in Canada. Canadian Veterinary Journal, 15, 271–281. Tannerfeldt, M., & Angerbjörn, A. (1996). Life history strategies in a fluctuating environment: Establishment and reproductive success in the arctic fox. Ecogeography, 19(3), 209–220. https://doi.org/10.1111/j.1600-0587.1996.tb00229.x Thoulouze, M. I., Lafage, M., Schachner, M., Hartmann, U., Cremer, H., & Lafon, M. (1998). The neural cell adhesion molecule is a receptor for rabies virus. Journal of Virology, 72, 7181–7190. Tillotson, J. R., Axelrod, D., & Lyman, D. O. (1977). Rabies in a laboratory worker—New York. Morbidity and Mortality Weekly Report, 26, 183–184. Tsiang, H. (1993). Pathophysiology of rabies virus infection of the nervous system. Advances in Virus Research, 42, 375–412. https://doi .org/10.1016/S0065-3527(08)60090-1 Tuffereau, C., Benejean, J., Blondel, D., Kieffer, B., & Flamand, A. (1998). Low-affinity nerve-growth factor receptor (P75NTR) can serve as a receptor for rabies virus. EMBO Journal, 17(24), 7250–7259. https://doi.org/10.1093/emboj/17.24.7250 Tuffereau, C., Schmidt, K., Langevin, C., Lafay, F., Dechant G., & Koltzenburg, M. (2007). The rabies virus glycoprotein receptor P75NTR is not essential for rabies virus infection. Journal of Virology, 81(24), 13622–13630. https://doi.org/10.1128/JVI.02368-06 Turmelle, A. S., Kunz, T. H., & Sorenson, M. D. (2010). A tale of two genomes: contrasting patterns of phylogeographic structure in a widely distributed bat. Molecular Ecology, 20(2), 357–375. https://doi.org/10.1111/j.1365-294X.2010.04947.x Ugolini, G. (2008). Use of rabies virus as a transneuronal tracer of neuronal connections: Implications for the understanding of rabies pathogenesis. Developments in Biologicals (Basel), 131, 493–506. https://doi.org/10.1016/B978-0-12-387040-7.00010-X Ugolini, G. (2011). Rabies virus as a transneuronal tracer of neuronal connections. Advances in Virus Research, 79, 165–202. https://doi .org/10.1016/B978-0-12-387040-7.00010-X van Zyll de Jong, C. G. (1985). Handbook of Canadian mammals 2: Bats. Ottawa, ON: National Museums of Canada. Vaughn, J. B., Gerhardt, P., & Paterson, J. C. (1963). Excretion of street rabies virus in saliva of cats. Journal of the American Medical Association, 184(9), 705–708. https://doi.org/10.1001/jama.1963.73700220001013

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A Rabies Primer Vaughn Jr, J. B., Gerhardt, P., & Newell, K. W. (1965). Excretion of street rabies virus in the saliva of dogs. Journal of the American Medical Association, 193(5), 363–368. https://doi.org/10.1001/jama.1965.03090050039010 Venters, H. D., Hoffert, W. R., Scatterday, J. E., & Hardy, A. V. (1954). Rabies in bats in Florida. American Journal of Public Health, 44(2), 182–185. https://doi.org/10.2105/AJPH.44.2.182 Vitasek, J. (2004). A review of rabies elimination in Europe. Veterinarni Medicina, 49(5), 171–185. https://doi.org /10.17221/5692-VETMED Wacharapluesadee, S., & Hemachudha, T. (2010). Ante- and post-mortem diagnosis of rabies using nucleic acid-amplification tests. Expert Review of Molecular Diagnostics, 10(2), 207–218. https://doi.org/10.1586/erm.09.85 Wallerstein, C. (1999). Rabies cases increase in the Philippines. BMJ (Clinical research ed.), 318(7194), 1306. https://doi.org/10.1136 /bmj.318.7194.1306-a, https://doi.org/10.1136/bmj.318.7194.1306 Wandeler, A. I. (1987). Rabies virus. In M. C. Horzinek (Ed.), Virus infections of vertebrates (pp. 458–461). Amsterdam, The Netherlands: Elsevier. Wandeler, A. I. (1991). Carnivore rabies: Ecological and evolutionary aspects. Hystrix, 3, 121–135. https://doi.org/10.4404 /hystrix-3.1-3949 Wandeler, A. I. (2000). Oral immunization against rabies: Afterthoughts and foresight. Schweizer Archiv fur Tierheilkunde, 142, 455–462. Wandeler, A., Wachendörfer, G., Förster, U., Krekel, H., Schale, W., Müller, J., & Steck, F. (1974). Rabies in wild carnivores in Central Europe. I. Epidemiological studies. II. Virological and serological examinations. III. Ecology and biology of the red fox in relation to control operations. Zentralblatt für Veterinarmedizin Reihe B, 21(10), 735–773. https://doi.org/10.1111/j.1439-0450.1974.tb00478.x Wang, J., Wang, Z., Liu, R., Shuai, L., Wang, X., Luo, J., … Bu, Z. (2018). Metabotropic glutamate receptor subtype 2 is a cellular receptor for rabies virus. PLoS Pathogens, 14(7), e1007189. https://doi.org/10.1371/journal.ppat.1007189 Wang, Z. W., Sarmento, L., Wang, Y., Li, X.-Q., Dhingra, V., Tseggai, T., ... Fu, Z. F. (2005). Attenuated rabies virus activates, while pathogenic rabies virus evades, the host innate immune responses in the central nervous system. Journal of Virology, 79(19), 12554– 12565. https://doi.org/10.1128/JVI.79.19.12554-12565.2005 Warrell, M. J., & Warrell, D. A. (2004). Rabies and other Lyssavirus diseases. Lancet, 363(9413), 959–969. https://doi.org/10.1016 /S0140-6736(04)15792-9 Webster, W. A. (1987). A tissue culture infection test in routine rabies diagnosis. Canadian Journal of Veterinary Research, 51, 367–369. Wertheim, H. F. L., Nguyen, T. Q., Nguyen, K. A. T., De Jong, M. D., Taylor, W. R. J., Le, T. V., ... Nguyen, H. D. (2009). Furious Rabies after an atypical exposure. PLoS Medicine, 6(3), e1000044. https://doi.org/10.1371/journal.pmed.1000044 Wiedeman, J., Plant, J., Glaser, C., Messenger, S., Wadford, D., Sherriff, H., ... Petersen, B. W. (2012). Recovery of a patient from clinical rabies—California, 2011. Morbidity and Mortality Weekly Report, 61, 61–65. Wiktor, T. J. (1978). Cell-mediated immunity and postexposure protection from rabies by inactivated vaccines of tissue culture origin. Developments in Biological Standardization, 40, 255–264. Wiktor, T. J., Doherty, P. C., & Koprowski, H. (1977). In vitro evidence of cell-mediated immunity after exposure of mice to both live and inactivated rabies virus. Proceedings of the National Academy of Sciences USA, 74(1), 334–338. https://doi.org/10.1073 /pnas.74.1.334 Willoughby, R. E., Tieves, K. S., Hoffman, G. M., Ghanayem, N. S., Amlie-Lefond, C. M., Schwabe, M. J., Chusid, M. J., & Rupprecht, C. E. (2005). Survival after treatment of rabies with induction of coma. New England Journal of Medicine, 352(24), 2508–2514. https:// doi.org/10.1056/NEJMoa050382 Wiltzer, L., Larrous, F., Oksayan, S., Ito, N., Marsh, G. A., Wang, L. F., ... Moseley, G. W. (2012). Conservation of a unique mechanism of immune evasion across the Lyssavirus genus. Journal of Virology, 86(18): 10194–10199. https://doi.org/10.1128/JVI.01249-12 Winkler, W. G. (1991). Raccoon rabies. In G. M. Baer (Ed.), The natural history of rabies (pp. 325–340). Boca Raton, FL: CRC Press. Winkler, W. G., Fashinell, T. R., & Leffingwell, L. (1973). Airborne rabies transmission in a laboratory worker. Journal of the American Medical Association, 226(10), 1219–1221. https://doi.org/10.1001/jama.226.10.1219 Wojczyk, B. S., Stwora-Wojczyk, M., Shakin-Eshleman, S., Wunner, W. H., & Spitalnik, S. L. (1998). The role of site-specific N-glycosylation in secretion of soluble forms of rabies virus glycoprotein. Glycobiology, 8(2), 121–130. https://doi.org/10.1093 /glycob/8.2.121 World Health Organization. (2005). WHO expert consultation on rabies. Geneva, Switzerland: Author. World Health Organization. (2007). Guidance for research on oral rabies vaccines and field application of oral vaccination of dogs against rabies. Geneva, Switzerland: Author. World Organisation for Animal Health. (2008). Manual of diagnostic tests and vaccines for terrestrial animals. Paris, France: Author. Wunner, W. H., Reagan, K. J., & Koprowski, H. (1984). Characterization of saturable binding sites for rabies virus. Journal of Virology, 50, 691–697.

19

2 Domestic and Wildlife Rabies Incidence in Canada David J. Gregory1 and Rowland R. Tinline2 1

Canadian Food Inspection Agency (Retired), Ottawa, Ontario, Canada Professor Emeritus, Geography, Queen’s University, Kingston, Ontario, Canada

2

Introduction Rabies has been a disease of man, terrestrial animals, and bats for a very long time. Steele and Fernardez (1991) note that Democritus was thought to be the first to describe canine rabies in 500 BCE and that Aristotle, writing in the fourth century BCE, noted that “dogs suffer from the madness. This causes them to become very irritable and all animals they bite become diseased” (Baer, 1991, p. 416). Steele and Fernandez further noted that Roman writers described the infectious material as a poison for which the Latin was virus. Since then rabies or rabies-like diseases have been described throughout the Middle East, Europe, and Asia. Accounts of rabies in North America come from the Arctic in early colonial times. The arctic peoples have his­ torical, oral accounts of “crazy foxes or arctic dog disease” (Walker & Elkin, 2005, p. 1) that could transmit their disease to Inuit and their sled dogs (K. Kandola, M.  Etan, J.  Walker,  & N. Mair, personal communication, 2004; see Chapter 14b). Old records of the Moravian missions in Labrador described pandemics of “a serious disease of dogs” as being a source of loss and suffering along the coasts (Elton, 1931, p. 680) affecting dogs, foxes, wolves, and caribou. Epidemics of fox rabies had been reported on the east coast of Canada since the late eighteenth century (Hart et al., 1946) and in reports from the Atlantic coast of the United States (see next section). Rabies was described as originating in hot weather (Hodgkins, 1897), but another explanation for the cause of rabies is given in the Klondike Nugget in 1901:

The origin of rabies, now so prevalent among dogs both in Dawson and upon the outlying creeks is still an unexplained mystery. Various theories have been advanced, none of which, however, have proven entirely satisfactory. The suggestion has been made that the disease has come about as a result of the fact that many dogs are forced to go without water for considerable lengths of time. Stray animals, and their number has been by no means few in Dawson during the present winter, are compelled very frequently to eat snow as a substitute for water. These dogs appear to be among the first affected by the rabies which fact has led to the theory noted above. In the absence of a better explanation we shall have to give some credence to the snow theory. (“Cause of Rabies,” 1901, p. 4)

Until recently, little was known about the origins of rabies in North America. Recent debate centres on whether North America had indigenous rabies, whether the disease arrived from Asia across the Bering Land Bridge during the last Ice Age (see Chapter 37), or whether it was introduced by early European settlers in the seventeenth to eighteenth centuries. In the last decade, however, Susan Nadin-Davis, Alex Wandeler, and their colleagues have used viral typing tools (see Chapter 23) to demonstrate the existence of several distinct viral strains across Canada and their association with specific reservoir hosts. They describe three distinct viral lineages with different evolutionary origins circulating in North America: arctic/arctic-like, cosmopolitan, and American indigenous. The arctic branch of the arctic/arctic-like lineages is believed to have originated in Asia and then spread north into

Domestic and Wildlife Rabies Incidence in Canada

State. In 1797, the disease appeared in Rhode Island as an epizootic disease of dogs and cattle. The disease then reappeared in 1810 in the eastern United States and Ohio as an epizootic of dogs, foxes, and wolves. Rabies was widely reported across the United States after the Civil War (1861– 1865) and had crossed the Great Plains by the 1830s and California by 1850s (Smithcors, 1958). Since then the disease has remained enzootic across the entire United States. Early epizootics of rabies in Canada had several things in common: they were most often “canine in origin, the origins of outbreaks were probably dogs imported from the United States” (Tabel et al., 1974; Report of the Veterinary Director General, 1906), and the disease was poorly understood and often treated by some very crude methods. It is also likely that the disease was often not suspected and consequently not reported. The earliest reports of rabies in Canada came by word of mouth, the local newspapers or, more consistently, in the annual reports of the veterinary director general (VDG) for the Dominion of Canada, from 1902 to 1942. These reports often described attacks on humans by dogs, and then the dispatch of those dogs and any of their contact animals, and with rigid controls of dogs by the Department of Agriculture in Canada. The first human death noted in Canada was Charles Gigueres, who died following the bite of a dog in Quebec in August 1814. On 14 March 1816, Jean Maheu was bitten by a large dog in Quebec and died in November 1816. In May 1817 Madame Bruneau was bitten by a cat and died of rabies probably in Quebec (Blaisdell, 1992; see Chapter 3b). Perhaps the most famous death from rabies in early Canada was that of the Duke of Richmond, who was bitten by his pet fox and died in Richmond (near Ottawa, Ontario) in 1919. Chapter 3a explores the “Myth of the Duke of Richmond.” The article “Hydrophobia” (1819) appeared in the Kingston Chronicle of 18 June 1819, referring to rabid dogs in the Kingston area biting children and chasing cows. Further reports of rabies did not appear until 19 February 1865 when Mrs Cruickshank died of hydrophobia at Elora, Ontario (Connon, 1930/1974). The Daily Globe for 3 March 1868 (“Exterminating the Canine Race,” 1868) described an outbreak of canine rabies around Ingersoll and Woodstock. The Daily Globe reported on 29 September 1877 that a King Charles Spaniel with hydrophobia was dispatched with an axe in Toronto. On 24 July 1897, the Evening Star, Toronto quoted a report given by Dr MacKenzie on rabies outbreaks in Ontario over the past seven years (“Rats, Sewers,” 1897). In the article, Dr MacKenzie stated that nine outbreaks had occurred during that period in which 10 to 12 people had been bitten by dogs, one death had occurred in Dundalk in

Siberia before moving east across the Canadian Arctic, where the arctic fox became its primary reservoir (Walker & Elkin, 2005). The Arctic branch currently circulating in circumpolar regions is a relatively recent offshoot of this lineage and is divided into four main clades or groups of viruses, all of which have been identified in North America: Arctic-1 viruses, early offshoots of the original Arctic progenitor circulating in red foxes in Ontario; Arctic-2 viruses present in Alaska and also in Siberia; Arctic-3 viruses circulating throughout the circumpolar regions; and Arctic-4 viruses found circulating exclusively in Alaska (Kuzmin et al., 2008; Nadin-Davis et al., 2012). The red fox (Vulpes fulva) is native to Canada while the European red fox (Vulpes vulpes) was introduced by the colonists from Europe for sport (Voigt, 1987). Confusion existed as to the range boundaries of these species, with records of Vulpes vulpes discovered in Pennsylvania as early as 1770 and becoming more abundant in the twentieth century, perhaps providing a highly rabies-susceptible population in the late 1950s (Voigt, 1987). The distinct viral lineage termed Cosmopolitan is thought to have arrived with the colonists. It comprises a number of variants, including the north central skunk variant that became established in the northern plains of the United States. Reports of skunk rabies were common from the Great Plains in the1830s and California in the 1850s; early settlers referred to rabid skunks as “hydrophobia cats” or “phobey cats” (Baer, 1991, pp. 10, 11). Subsequently, skunk rabies spread northwards into Canada. A third distinct strain and the most divergent of all classical rabies viruses is the American indigenous lineage. It includes all North American bat rabies virus variants, as well as the raccoon and south central skunk viruses. It is likely that bats (Chiroptera) are the original hosts of this lineage, with host switching to terrestrial reservoir hosts (Nadin-Davis et al., 2001; Nadin-Davis et al., 2002).

Rabies Incidence before 1925 Early Reports of Rabies in North America Dog rabies was reported in the historical archives of Virginia in 1753. Other reports note rabies in North Carolina in 1762, in the Boston region by 1768, and in all New England states by1785 (Hart et al., 1946). Although recognized as a disease of dogs at that time, there were repeated outbreaks in wild animals. Epizootic fox rabies was reported in Massachusetts in 1812, in Alabama in 1890, and in Alaska in 1915. In 1789, a man died of rabies after skinning a rabid cow in New York

21

The Basics of Rabies in Canada

1896, and all those bitten were sent for treatment at New York’s Pasteur Center. The municipality had paid for the treatments. Dr MacKenzie called for “definite action to prevent the spread of rabies.”

quarantine in 1907 in two counties, Welland and Lincoln counties (Report of the Veterinary Director General, 1911, p. 15), and 64 other premises in Ontario; 94 in Qu’Appelle, Saskatchewan; and 5 in Red Deer, Alberta, under quarantine in his annual report ending 31 March 1909 (Report of the Veterinary Director General, 1909, p. 10). On 20 May 1909, the Toronto Daily Star reported Hamilton to be “a dog-less town” (“Hamilton to Be,” 1909, p. 9). No dogs were allowed at large, and owners had killed 25 dogs in a single day. The paper also reported on 6 August 1909 that a boy who was attacked in Brantford was sent for treatment and 19 dogs were destroyed on investigation (“Special to the Star,” 1909, p. 3). On 7 February 1910, the Toronto Daily Star reported that “all dogs must be chained up” in Western Ontario, by order of the minister of agriculture and Dr Rutherford, veterinary director general, with a fine of $200 for offenders (“All Dogs,” 1909, p. 8). It reported 206 premises under quarantine; 42 persons bitten and sent to New York State for treatment; and 63 cattle, 1 horse, 6 sheep, and 30 swine dying of rabies. On 12 February 1910, the Star reported a rabid cow in Welland (“Cow Had Rabies,” 1910, p. 5); on 21 February 1910 a muzzling order in Toronto resulted in a run on muzzles for dogs (“Market Cleared,” 1910, p. 12). Several dogs were destroyed; and on 23 April 1910, nine cows had died of rabies in Chatham, Ontario (“Rabies Near Chatham,” 1910, p. 8). The annual report of the VDG for 31 March 1909 (Report of the Veterinary Director General, 1909, p. 10), reported a rabies outbreak in Red Deer, Alberta resulting from a dog shipped from Hamilton, Ontario. In November 1909, another dog shipped from Ontario resulted in an outbreak in Minnedosa, Manitoba, affecting several dogs, eight cattle, three pigs, and one horse, with nine premises placed under quarantine. For the next few years, the VDG reported rabies outbreaks by the number of premises under quarantine, instead of by the number of animals. By 31 March 1910 the VDG (Report of the Veterinary Director General, 1910) reported 303 premises in Ontario, 1 in Assiniboia, Saskatchewan, and 4 in Red Deer, Alberta, under quarantine in his report (Table 2.1). The number of premises under quarantine in Ontario then dropped to 286 (Report of the Veterinary Director General, 1912) and 112 for 31 March 1913 (Report of the Veterinary Director General, 1913). In 1913, an outbreak of rabies occurred in Medicine Hat, Alberta (Report of the Veterinary Director General, 1913, p. 13), resulting in 32 premises being quarantined in the northeast and 8 premises in the southeast. An outbreak in Victoria, British Columbia, in 1914 resulted in 1 cow

Rabies from 1901 to 1925 In 1901 there were further reports of rabies in Ontario and in Yukon (“Mad Dogs Make Trouble in Yukon,” 1901). The Yukon situation is described in Chapter 14a. The Toronto Daily Star, on 14 August 1901 reported rabies “raging” in Pelham Township in Welland County (“Rabies Raging,” 1901, p. 3). Dog attacks led to a number of dogs being destroyed, as well as one horse and two cows. There were no further reports until March 1905, when a clinical diagnosis of rabies in two dogs from North Dakota was made in North Portal, Saskatchewan. The two dogs, along with all local strays, were destroyed and other owned dogs were muzzled and quarantined (Report of the Veterinary Director General, 1906). These actions appear to have been normal procedures for the Department in its follow-up. In July 1905, two dogs from Oxbow, Saskatchewan, were found to be rabid and were destroyed. The origin however, was not determined. In June 1905, a young boy was bitten by a dog in Ontario and taken to the Pasteur Center in New York for treatment. That case led to rabies being declared a reportable disease on 9 August 1905 by virtue of the Contagious Diseases Act, 1903 (see Chapter 4). Under these new regulations, investigations were conducted when people had been bitten, quarantine orders were issued, and veterinary inspectors were instructed to cooperate with city officials and local boards of health (Report of the Veterinary Director General, 1906). By 1907 there were rabies outbreaks in both eastern and western Canada. The outbreaks in the west occurred at Shoal Lake, Manitoba, and Moosomin, Saskatchewan, and were thought to have originated from dogs belonging to US settlers. The outbreak in the east resulted from a stray US dog crossing the Bridge at Queenston, Ontario, and biting several other dogs before returning to the US side. That outbreak persisted for several years and spread as far as Windsor, Parry Sound, and Peterborough (Tabel et al., 1974). On 26 June 1908, the Toronto Daily Star reported two dogs destroyed in Paris, Ontario (“To Muzzle Dogs,” 1908, p. 9). Then, on 31 August 1908, that newspaper reported that rabies had infected several animals in Cayuga, Ontario, two weeks earlier and that a farm where a colt and three steers had died of rabies was under quarantine (“Steers Died,” 1908, p. 3). The farmer, too, had also received treatment in New York. Dr Rutherford reported 18 premises under

22

Domestic and Wildlife Rabies Incidence in Canada

the shores of Hudson and James Bay. In 1812 the company merged with the North West Company to form a trading enterprise with posts across the continent and the north (Goldi Productions, 2007). Although the posts came and went, the post records included daily journals, district reports and district fur returns (Archives of Manitoba), which often described disease in foxes, and dogs. In 1926 Charles Elton (1931) conducted a survey of existing Hudson’s Bay Company Post records (see Chapters 14b, 14c, and 14d), asking for any information relating to outbreaks of rabies in those areas and for descriptions on these outbreaks, especially when they occurred, symptoms (if any), and the species affected. The respondents described a variable disease scene affecting the fox population about every four years and spreading to their sled dogs. The incubation of the disease was often short – four days – and the animal fearless and often vicious. Other respondents described a “distemper-like” disease, perhaps a “dumb” form of rabies. Canadian Inuit have historical oral accounts of “crazy foxes” that could transmit their disease to them and their sled dogs (Elton, 1931). The reports came from many of the posts located around Baffin Island, Hudson Strait, Hudson Bay, and Ungava Bay and included records of the Moravian missionaries in1859 of a disease affecting dogs in Hopedale (Labrador) and Ungava Bay (now part of Nunavik). Some respondents were sure that the disease was rabies; others suggested that it was a distemper-like disease. The outbreaks reported to Elton (1931) occurred between 1900 and 1926, the year of his survey. Those reports are discussed in more detail in Chapters 13, 14c, and 14d. Reports before 1925 focused on domestic and stray dogs as the primary vectors for rabies transmission in North America south of the 60th parallel, with spillover in domestic livestock. Further, the origins of domestic animal rabies seemed to be the United States. Recent phylogeographic evidence suggests that some North American rabies outbreaks in dogs originated in parts of Asia (Bourhy et al., 2008; see Chapter 37). In the north, the disease affected dogs and wildlife carnivores alike, and the virus is likely to have been one of the arctic fox strains currently circulating in the circumpolar regions of the world (Nadin-Davis et al., 2012).

Table 2.1  Summary of premises quarantined in Ontario, 1907 to 1911. Year

Premises quarantined

Counties

1907 1908 1909 1910 1911

18 42 146 308 146

2 6 11 25 23

Sources: compiled from Report of the Veterinary Director General, 1908, 1909, 1910, 1911.

and 38  dogs confirmed as rabid (Tabel et al., 1974). This resulted in 43 quarantines placed: 29 in Nanaimo, 13 in Vancouver, and 1 in Victoria. In the same year, 2 premises, in Qu’Appelle and Regina (Saskatchewan), and 56 premises in seven counties of Ontario were also under quarantine (Report of the Veterinary Director General, 1915, p. 12). By 1916, 69 premises in 11 counties in Ontario were still under quarantine (Report of the Veterinary Director General, 1916, p. 6). The report for 1917 placed 1 premise in Calgary and 51 premises in Ontario in 17 counties under quarantine (Report of the Veterinary Director General, 1917, p. 7). For 1918 the VDG reported quarantines on 1 premise in Yale, British Columbia, 1 in east Edmonton, Alberta, and 52 in Ontario, in 17 counties (Report of the Veterinary Director General, 1918, p. 11). No reports of rabies were received in 1919, but 15 premises were under quarantine in seven counties of Ontario for the year 1920 (Report of the Veterinary Director General, 1920, p. 11). In 1921 and 1922, rabies was reported by the number of animals under quarantine instead of the number of premises. In 1921, 51 animals were under quarantine: 1 each in Nova Scotia, Manitoba, and British Columbia; 3 in Quebec; and 45 in Ontario (Report of the Veterinary Director General, 1921, p. 12). In 1922, 50 animals were under quarantine: 1 in British Columbia and 49 in Ontario (Report of the Veterinary Director General, 1922, p. 12). No cases were reported in 1923 or 1924. In 1925 an outbreak was reported in the Low District of Quebec (Report of the Veterinary Director General, 1926, p. 5).

Rabies in the North

Rabies Incidence after 1925

Consolidated information on rabies for the northern half of Canada, what we are loosely defining as Yukon, the North West Territories, Nunavut, Nouveau Quebec, and Labrador, is scarce. Perhaps the best source of information is the trading post records of the Hudson’s Bay Company, a company established by royal charter in 1670 to trade in furs around

Considerations In 1919 a federal Order in Council provided for the collection and publication of information bearing on public

23

The Basics of Rabies in Canada

health. Canada-wide reports on rabies began in 1926 when Quebec also joined this system. Until the end of 2013, the Department of Agriculture (later known as Agriculture Canada, AgCAN; and now the Canadian Food Inspection Agency, CFIA) collected and disseminated rabies incidence data for all of Canada. In 2014 provinces and territories became responsible for the collection of specimens and sending them to CFIA for testing (see Chapter 21). Despite this change, the system remains, in our opinion, one of the most comprehensive and consistent rabies reporting systems in the world. Chapter 21 discusses some problems with this dataset but, at the annual and county (census division) levels of aggregation, we are reasonably confident that the data are a good representation of human/ animal contact with rabies in Canada. Further, as analyses of rabies incidence across provinces and territories (see Part 3) indicate, the system devised for collecting and testing rabies specimens associated with actual or potential human contact also provides a good indication of rabies incidence in wildlife. Hence the rabies reporting system in Canada allows us to examine the spatial and temporal trends in rabies incidence in this country with some confidence.

Northwest Territories and were the precursor to the southward invasion of rabies in the 1950s, discussed in the section “The Invasion of Arctic Fox Rabies into Southern Canada.” The other outbreaks were typically linked to dogs brought in by visitors or hunters from the United States (Tabel et al., 1974). There were two major outbreaks in this period, one beginning north of Hull, Quebec, in 1926 (Report of the Veterinary Director General, 1926) and spreading into eastern Ontario and the eastern townships of Quebec, and the other beginning in Essex County in southwestern Ontario in 1942 and spreading to two adjacent counties. The 1926 Hull outbreak had 498 cases and died out in 1934. The 1942 outbreak ended in 1946 with 128 diagnosed cases. Combined, these outbreaks accounted for 95% of all diagnosed cases from 1926 to 1950. After 1950, rabies incidence in Canada increased dramatically (Figure 2.1 and Table 2.3). Rabies incidence in dogs after 1950, however, was only 5.1% of the total reported cases in Canada (Table 2.4). Terrestrial wildlife species dominated incidence, especially in foxes and skunks (66.2% of all diagnosed cases). Further, as subsequent chapters point out, foxes and skunks and, more recently, raccoons were the primary rabies vectors. Recent work on viral typing (see Chapter 23) indicates that the viruses involved with these cases (except bats) were, depending on location, arctic fox, skunk, and raccoon strains rather than dog rabies. If and when dog rabies disappeared remains unknown. We surmise that since the spatial and temporal patterns of incidence since 1950 were associated with wildlife vectors and since there were wide spread efforts to vaccinate pets (see Chapters 32 and 34), dog rabies disappeared sometime in the 1950s.

Characteristics of Rabies Incidence, 1926–2017 Over the past century, rabies in Canada has had several distinct characteristics: the dominant presence and then apparent disappearance of what is generally called dog rabies and the persistence of wildlife rabies in the Arctic; the invasions of fox and skunk strains of rabies into southern Canada; the invasion of the raccoon strain of rabies into eastern Ontario, southern Quebec, and New Brunswick; the development of successful control programs to combat those invasions; the dominance of rabies in bats in British Columbia and recent increases in incidence in bats in other parts of Canada; and the growing understanding of the relationship between rabies virus and regional physiography. These characteristics are discussed in the following sections.

RABIES IN NORTHERN CANADA

There were persistent reports of “arctic dog disease” before and throughout the 1920s to 1940s in northern Canada that were probably linked to enzootic rabies in arctic foxes (and Table 2.2  Diagnosed rabies cases in Canada, 1926–1950.

“DOG” RABIES

The section “Rabies from 1901 to 1925” in this chapter points out that before 1926 rabies outbreaks in southern Canada were scattered across the country and linked to dogs. That pattern of isolated outbreaks continued until 1950. Table 2.2 shows that between 1926 and 1950, 488 of 660 diagnosed cases (68%) were in dogs and that 473 of those were concentrated in Ontario and Quebec. Most of the remaining cases were in livestock, with only three cases in wildlife. Those three cases occurred in 1947 in the

 

ON

QC

NT

AB

PE

SK

Total

Dog Cow Sheep Cat Pig Horse Wolf Fox Total

329 64 21 18 7 3 0 0 442

144 31 18 3 2 1 0 0 199

7 0 0 0 0 0 2 1 10

6 0 1 0 0 0 0 0 7

1 0 0 0 0 0 0 0 1

1 0 0 0 0 0 0 0 1

488 95 40 21 9 4 2 1 660

Source: compiled from CFIA data.

24

Domestic and Wildlife Rabies Incidence in Canada

Figure 2.1: Diagnosed rabies cases in Canada, 1926–2017. Source: created from CFIA data.

Table 2.3  Diagnosed rabies cases in Canada, 1951–2017. Prov/Terr

Total

Fox

Live

Skunk

Dom

Bat

Raccoon

Wild

Other

AB BC MB NB NL NS NT NU ON PE QC SK YK  Total   % Total

920 527 4,069 448 142 14 353 450 56,009 5 6,616 5,157 6 74,716  

26 5 57 196 115 3 254 335 25,275 3 3,282 21 3 29,575 39.6

78 2 513 82 3 2 0 0 11,191 0 1,602 395 0 13,868 18.6

318 4 3,224 27 0 0 0 0 11,429 0 372 4,200 0 19,574 26.2

95 7 205 29 12 2 81 96 5,310 1 890 254 3 6,985 9.3

316 502 36 23 1 7 0 0 1,502 1 210 260 0 2,858 3.8

0 0 8 87 0 0 0 0 763 0 153 7 0 1,018 1.4

75 2 9 0 11 0 13 17 408 0 86 7 0 628 0.8

12 5 17 4 0 0 5 2 131 0 21 13 0 210 0.3

Live = livestock, Dom = cat and dog, Wild = wolf and coyote, Rac = raccoon, Other = various terrestrial wildlife (squirrels, etc.). Source: compiled from CFIA data.

25

The Basics of Rabies in Canada

Table 2.4  Diagnosed rabies cases by province and territory, 1951–2017 Year

Total

BC

AB

SK

MB

ON

QC

NB

NS

1951 1952 1953 1954 1955 1956 1957 1958 1959 1960 1961 1962 1963 1964 1965 1966 1967 1968 1969 1970 1971 1972 1973 1974 1975 1976 1977 1978 1979 1980 1981 1982 1983 1984 1985 1986 1987 1988 1989 1990 1991 1992 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011

4 44 134 73 154 204 654 2,550 700 287 1,057 956 1,137 1,402 1,323 1,272 1,408 2,179 2,126 1,447 2,115 1,990 1,957 1,676 2,119 1,624 1,565 1,688 1,662 1,708 2,035 2,445 2,127 1,699 2,336 3,872 2,769 2,281 2,202 2,318 2,078 2,260 1,892 857 443 293 235 371 500 664 439 342 265 254 248 229 274 235 145 123 115

0 0 9 0 1 0 2 2 0 2 0 0 1 2 3 3 4 3 5 5 12 10 3 4 17 9 9 1 5 10 8 7 9 7 12 9 7 14 11 7 5 12 11 9 14 8 9 12 14 12 20 11 18 17 18 11 15 14 9 5 7

0 19 89 51 41 12 0 1 0 0 0 0 0 0 1 1 0 0 0 17 22 16 39 26 25 39 18 5 15 66 34 51 40 13 12 7 47 28 18 42 13 11 13 2 3 2 8 6 3 3 4 6 4 3 1 5 1 1 2 3 0

0 2 5 10 0 0 0 1 0 0 0 0 4 24 31 45 51 85 48 61 53 66 268 127 117 162 212 119 100 120 229 128 136 185 231 435 610 193 66 55 49 76 109 24 28 21 16 76 140 171 46 27 24 25 24 33 17 33 24 21 34

0 1 3 5 3 4 1 2 29 18 83 119 199 38 50 56 25 82 57 24 63 76 98 60 84 92 114 60 48 53 170 124 51 54 48 74 54 37 41 62 92 137 84 77 37 24 57 172 227 237 53 47 49 78 73 65 39 50 32 40 21

0 0 2 2 103 142 325 2,493 638 227 862 790 870 1,148 1,021 1,002 1,048 1,730 1,719 1,187 1,777 1,480 1,318 1,229 1,722 1,273 1,162 1,357 1,407 1,416 1,557 2,107 1,860 1,382 1,984 3,273 2,007 1,832 1,905 1,634 1,238 1,305 1,254 611 328 158 97 81 100 187 212 202 126 106 96 82 106 79 49 39 26

0 0 8 2 1 36 326 50 26 40 111 46 56 184 210 77 231 243 243 115 143 292 215 198 146 33 37 94 84 37 10 13 26 49 31 57 35 133 136 493 642 685 387 116 22 62 38 14 10 22 17 24 22 12 21 15 81 40 16 7 17

0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 85 39 33 50 28 44 33 10 0 1 2 1 0 0 0 0 0 0 1 0 0 0 0 0 0 0 1 0 0 1 0 4 0 0 13 51 3 1 1 1 0 1 0 0 1 0

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 1 2 0 0 1 0 1 0 0 0 0 0 2 0 0 2 0 0 0 2 0 0 1 0

PE

NL

YK

NT

NU

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 1 0 0

0 0 0 0 1 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 5 2 0 0 0 0 0 20 2 0 1 14 1 0 1 18 0 0 0 1 11 4 19 7 4 0 0 0 0 0 0

0 1 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 2 0 0 1 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

4 21 18 1 2 6 0 0 7 0 0 1 5 0 6 2 7 1 1 8 1 13 3 27 2 0 1 50 2 2 5 5 1 7 7 1 1 6 8 3 5 2 2 2 2 0 4 3 1 11 12 6 0 0 3 8 6 4 7 1 6

0 0 0 2 2 4 0 1 0 0 0 0 2 5 0 1 3 2 3 0 0 4 2 5 4 13 11 2 1 4 17 8 4 1 11 15 7 18 13 22 33 16 28 15 7 0 2 7 5 5 13 12 0 4 7 10 6 14 5 5 4

(Continued)

26

Domestic and Wildlife Rabies Incidence in Canada

Year 2012 2013 2014 2015 2016 2017  Total   % Total

Total

BC

AB

SK

MB

ON

QC

NB

NS

PE

NL

YK

NT

NU

142 115 95 155 403 245 74,716

10 4 10 10 18 11 527 0.7

2 4 4 4 10 7 920 1.2

24 13 21 27 53 22 5,157 6.9

25 28 15 18 16 14 4,069 5.4

29 28 18 24 288 149 56,009 75.0

18 15 8 18 6 14 6,616 8.9

1 1 2 24 3 11 448 0.6

1 0 0 0 0 0 14 0.0

0 0 0 0 0 0 5 0.0

16 0 1 12 0 0 142 0.2

0 0 0 0 0 0 6 0.0

6 12 6 1 4 4 353 0.5

10 10 10 17 5 13 450 0.6

Source: compiled from CFIA data.

the rarer wolves), particularly when these animals were involved with sled dogs (Tabel et al., 1974). In 1947 rabies was officially diagnosed in the Northwest Territories in cases reported in Aklavik (wolf and dog), Baker Lake (fox, wolf, dog), and Frobisher Bay (dog). These widely separated locations confirmed the extent of the disease in the north and its existence in wildlife, which has persisted to the present (Tables 2.3 and 2.4). Although rabies was not diagnosed again in the Northwest Territories until 1951, there were reports of crazy foxes and wolves fighting with sled dogs in the intervening years in the MacKenzie Delta (Plummer, 1954; Tabel et al., 1974). By the end of 1951, rabies was confirmed near the borders of northern Alberta, Manitoba, and Quebec. Since then, with few exceptions (1957, 1960, 1961, 1996, and 2003) rabies has been diagnosed annually in four northern areas: Northwest Territories, Nunavut, Yukon, and northern Quebec (see Table 2.4). Incidence in the territories has been dominated by arctic and red foxes (72%), with most of the other cases in dogs (23%). It appears that almost 65% of fox incidence is arctic fox and that the persistence in the north is related to the biology of the arctic fox. Chapter 26 explores the reasons for this persistence and the interaction between arctic foxes and the northward expansion of the red fox.

in Saskatchewan and five years later in Alberta. The intensive control efforts undertaken by Alberta (see ­Chapter 7) probably hastened the end of this outbreak. Rabies spread south through Ontario and Quebec, reaching the southern borders by the late 1950s, and then spread along the St Lawrence Lowlands into New Brunswick in the mid-1960s where it died out a decade later. Rabies driven by incidence in foxes remained at high levels in Ontario and Quebec until 1989, and then began to decline rapidly in Ontario. Within one or two years, there was a similar decline in Quebec. From 1958 to 1989 annual incidence averaged over 1440 cases per year in Ontario and 100 cases per year in Quebec. By 1999 there were only 100 cases in Ontario and 10 in Quebec. That decline was the result of Ontario’s wildlife oral vaccination programs that began in 1989 (see Chapter 10). We suspect that rabies would not have persisted in Quebec without incursions from Ontario. Hence, the decline in Quebec was related to control efforts along the Ontario-Quebec border (see Chapter 11). In both provinces the temporal pattern of incidence in skunks tracked incidence in foxes but lagged by several months. As well, the virus associated with skunks was the arctic fox strain (see Chapter 29). We believe, therefore, that foxes were the primary vector in both provinces. Hence, even though early wildlife vaccination efforts were less successful in targeting skunks than foxes (see Chapter 17), incidence in skunks in Ontario and Quebec declined as rabies in foxes was successfully controlled. Why did rabies persist in the fox populations in southern Ontario for 50 years? Tinline and MacInnes (2004) argue that environmental conditions favourable for red fox populations and the landscape was partitioned into relatively large units of similar physiography separated by physical or land use barriers (see Chapter 30). This loosely connected set of units permitted the fox population in any one unit to rebound after an outbreak setting the stage for another outbreak several years later as virus circulating between adjacent units made its return. While it appears that the arctic fox strain of rabies has been controlled in southern Ontario and Quebec and has

THE INVASION OF ARCTIC FOX RABIES INTO SOUTHERN CANADA

In the 1950s rabies moved rapidly south into Alberta, Saskatchewan, Manitoba, and Quebec causing a huge spike in reported cases (Table 2.4, Figure 2.1). Figure 2.2 (based on the work of Tabel et al., 1974) shows the probable routes of the spread southward. Given the wide spread distribution of rabies in the Arctic before 1950, the southern spread of the disease was an Arctic-wide phenomenon. The primary vectors were arctic and red foxes, especially in Manitoba, Ontario, and Quebec. In Alberta, coyotes were the major vector. Their wide distribution drove the disease rapidly to the south end of the province and subsequently into northern and central Saskatchewan. Rabies died out three years later

27

The Basics of Rabies in Canada

Figure 2.2: Invasions of rabies into southern Canada, 1947–2015. The map is a revision and update by the authors based on an earlier map drawn by Tabel et al. (1974). The arctic fox movements on Baffin Island on the 1974 map were speculations based on reports from the Hudson’s Bay Company. The dates on the map represent cases diagnosed by CFIA. The fox movements on the map represent both arctic fox and red fox cases as early CFIA records often did not distinguish fox species associated with a diagnosis. Source: CFIA. Map based on Natural Resources Canada public data.

Saskatchewan but died out in Alberta by 1993 (Figure 2.4). Manitoba and Saskatchewan have used vaccination programs for domestic animals (Chapters 8 and 9) but have not introduced wildlife rabies control programs. Alberta, on the other hand, introduced vector elimination programs during the initial fox/coyote invasion in the 1950s and then refocused those efforts in the 1970s to keep rabies in skunks out of the province (see Chapter 7). The control programs concentrated on potential threats along the Alberta-Saskatchewan border and the border with US states, where the skunk strain of rabies remains enzootic. It is not clear whether rabies in Manitoba and Saskatchewan can persist without reintroductions from

disappeared from the southern prairie provinces, pockets of infection remain in arctic and red foxes in the northern territories (Figure 2.3). Incursions of fox rabies in 2012 into northern Manitoba, northern Quebec, and Labrador make clear that the threat of a major southward invasion of arctic fox rabies remains. SKUNK RABIES IN THE PRAIRIES

Figure 2.2 shows the invasion of the skunk rabies strain into southern Manitoba from the United States in 1958. By 1963 skunk rabies had spread west into Saskatchewan and, by 1971, into Alberta. Since then rabies has persisted in Manitoba and

28

Domestic and Wildlife Rabies Incidence in Canada

Figure 2.3: Fox rabies cases, 2003–2012. Incidence data are at the county/region/district level as defined by the census divisions of ­Statistics Canada. Source: created from CFIA data.

the bordering US states. Figure 2.5 shows the distribution of rabies in skunks in Canada over the past decade and emphasizes the continuing concentration of cases in Saskatchewan and Manitoba. Note, however, the absence of cases in Alberta, a situation most likely due to that province’s continuing control efforts. Cases in Ontario and Quebec were spillovers from cases in other species in which the arctic fox or the raccoon strain of the virus was circulating.

in Ontario (see Chapter 10), Quebec (see Chapter 11), and New Brunswick (see Chapter 12). Despite the small numbers, the raccoon rabies strain represents the third major invasion of wildlife rabies into Canada. Figure 2.6 shows the annual incidence of raccoon rabies in the three provinces where the invasion occurred. Note the discontinuity in cases in 1996–1998. Before then, it appears that rabies in raccoons was a spillover from epizootics in those provinces that were driven by rabies in foxes and involved the arctic fox strain. In 1999, however, the northward expansion of the mid-Atlantic strain of rabies (raccoon strain) through northeastern United States (see Chapter 37) breached the St Lawrence River near Prescott in southeastern Ontario. By 2000 the mid-Atlantic strain had entered

RACCOON RABIES IN CANADA

The positive cases of rabies in raccoons represent only about 1% of the total of all cases diagnosed since the first case in Canada in 1956. While cases in raccoons (Table 2.3) have only appeared in five provinces, they are concentrated

29

The Basics of Rabies in Canada

Figure 2.4: Diagnosed rabies cases in skunks in Canada’s prairie ­provinces, 1957–2017. Source: created from CFIA data.

Figure 2.5: Diagnosed rabies cases in skunks, 2003–2012. Source: created from CFIA data.

30

Domestic and Wildlife Rabies Incidence in Canada

Figure 2.6: Diagnosed cases of rabies in raccoons in Ontario, Quebec, and New Brunswick, 1956–2017. Source: created from CFIA data.

southeastern New Brunswick and by 2006 had reached the Eastern Townships of Quebec. The remarkable feature of those epizootics was that all three were quickly contained and eradicated via wildlife vaccination programs. In 2015 raccoon rabies re-entered southeastern New Brunswick from the neighbouring state of Maine. This outbreak also appears to have been contained by 2016. Also in 2015, raccoon rabies was discovered near Hamilton, Ontario, some 65 kilometres from the Niagara River vaccine barrier along the border between Ontario and New York. That outbreak grew rapidly in 2016 around Hamilton and the Niagara Peninsula. At the time of writing, despite rapid and massive control efforts, the outbreak has been slowed but not arrested. Interestingly, recent advances in virus typing have shown that the virus in the current outbreak is genetically related to the virus strain found in southeastern New York, rather than the strain immediately across the border along the Niagara River in the United States. This suggests that the outbreak was caused by long distance translocation of a raccoon(s) from southeastern New York (S. Nadin-Davis, personal communication, 14 December 2016). The details of these descendants of the successful fox rabies control programs in Ontario are discussed in the chapters dealing with Ontario, Quebec, and New Brunswick. Chapter 10 (Ontario) further discusses why control efforts have not succeeded as dramatically since 2016 as in the past

and what this implies for the future control efforts, since rabies in raccoons remains enzootic in the bordering states of New York, Vermont, New Hampshire, and Maine and presents a continuing threat for reintroduction. BAT RABIES IN CANADA

Rabies in bats represents only 3.7% of diagnosed cases in Canada (Table 2.3). Despite those small numbers, the incidence in bats has several distinctive features. First, British Columbia (see Chapter 6) is unique in that cases in bats have dominated incidence representing 95% (491/516) of all cases in that province (Table 2.3). The first diagnosed case of rabies in a bat occurred in 1957 in BC. Since then, with the exception of 1960 and 1961, rabies in bats in BC has increased slowly, levelling off in 1971 and averaging about 10 cases per year. Further, unlike other provinces, cases in BC have not been associated with the arctic fox, skunk, or raccoon strains of virus that have dominated incidence in the other provinces and territories. Second, bat rabies cases are primarily in southern Canada. Several species of bats have been submitted for testing from the northern territories, but no case of rabies has been diagnosed. There have been few positive cases in the Maritimes. Incidence in bats is concentrated in Ontario, Quebec, Saskatchewan, Alberta, and British Columbia. Together those provinces account for almost 98% of all

31

The Basics of Rabies in Canada

Figure 2.7: Diagnosed cases of rabies in bats in Ontario, British Columbia, Saskatchewan, Alberta, and Quebec, 1957–2017. Source: created from CFIA data.

diagnosed cases in bats. Interestingly, Manitoba, the province lying between Ontario and Saskatchewan, reported far fewer cases (36) than either of its neighbours (Ontario: 1482 cases, Saskatchewan: 253 cases). Chapter 9 discusses this discrepancy. Third, the annual patterns of incidence in the dominant provinces (Figure 2.7) show some interesting features. In both Ontario and Quebec, bat rabies cases spiked shortly after raccoon rabies invaded those provinces. We speculate that the intense publicity surrounding this invasion increased public awareness and led to an increase in submissions. Rabies in bats spiked in Alberta shortly after the province was invaded by skunk rabies from Saskatchewan. The correspondence is interesting, but we do not have knowledge of the virus strains in those bats to make a causal link between incidence in skunks and bats. Perhaps our previous speculation about increased publicity leading to more submissions applies in this case. In absolute terms, the number of rabies cases in bats has been relatively consistent across Canada since 2000 and has usually been higher and has tended to dominate incidence in other species (Figure 2.8).

Figure 2.8 also demonstrates the dominance of rabies in dogs, cats, and livestock until the 1950s; the invasion, persistence, and control of fox rabies from the late 1940s to the late 1990s; the invasion of skunk rabies in the 1960s in the prairies, the spillover into skunk populations following fox and raccoon rabies incursions into eastern Canada; the invasions of raccoon rabies in the current century; and the increase in the relative importance of rabies in bats in the last two decades. Fourth, some 18 species of bats have been diagnosed with rabies in Canada (Table 2.5). Across the country the big brown bat (Eptesicus fuscus) is the most commonly diagnosed. It often roosts in attics, barns, and old houses, and under eaves and shutters, so there is a good chance of contact with humans. The two other commonly reported bats are the little brown bat (Myotis lucifugus) and the silver-haired bat (Lasionycterus noctivagans). Like the big brown bat, the little brown bat often roosts in buildings where contact with humans is more likely. The silver-haired bat more often roosts in tree cavities or bark crevices. Of the six cases of human deaths caused by rabid bats, two cases have been associated with the silver-haired bat (see Chapter 3b).

32

Domestic and Wildlife Rabies Incidence in Canada

Figure 2.8: Percentage of total rabies incidence in Canada by species by year, 1947–2017. Before 1947 there were no reported cases in wildlife – all cases were in domestic animals (livestock, dogs, and a few cats). Source: created from CFIA data.

Finally, as Figure 2.9 shows, rabies cases in bats occur across the breadth of Canada even though the absolute numbers are low. The virus strains involved are varied and it is not clear what, if any, the relationship is between rabies in bats and rabies in terrestrial mammals.

Table 2.5  Diagnosed rabies in bat species in Canada, 1957–2017. Common and species name

Total % Total

Big brown bat, Eptesicus fuscus Silver-haired bat, Lasionycterus noctivagans Little brown bat, Myotis lucifugus Hoary bat, Lasiurus cinereus Long-eared bat, Myotis evotis California bat, Myotis californicus Yuma bat, Myotis yumanensis Long-legged bat, Myotis Volans Keen’s bat, Myotis keenii Eastern red bat, Lasiurus borealis Northern long-eared bat, Myotis septentrionalis Western small-footed bat, Myotis ciliolabrum Eastern pipistrille bat, Perimyotis subflavus Fringed bat, Myotis thysanodes Western big-eared bat, Corynorhinus townsendii Spotted bat, Euderma maculatum Unnamed  Total

1742 61.0 174 6.1 133 4.7 73 2.6 40 1.4 30 1.0 22 0.8 11 0.4 10 0.3 14 0.5 7 0.2 4 0.1 3 0.1 3 0.1 2 0.1 1 0.0 589 20.6 2858  

RABIES AND GEOGRAPHY

Figure 2.10 shows the overall distribution of rabies cases in Canada for 2003 to 2012. The number of cases has dropped substantially from previous highs, but there was rabies in most areas except Yukon and the northern prairies. The current spatial distribution of rabies reflects Canada’s climate and physiography, the distribution of rabies along Canada’s southern border, and recent control efforts. Southern British Columbia, for example, is relatively isolated from incursions of arctic fox rabies from the north and skunk rabies from the east. Rabies in bats in British Columbia is concentrated in valleys of the coastal and interior ranges, which offer a favourable environment for a large number of species of bats. Rabies in skunks in Canada is an extension of the enzootic of skunk rabies on the US prairies, and the northward extent of it is limited to the northern extent of the prairie

Note: One of the two cases listed as Western big-eared bat was coded as Townsend’s big-eared bat. Source: compiled from CFIA data.

33

The Basics of Rabies in Canada

Figure 2.9:  The distribution of diagnosed rabies cases in bats, 2003–2012. Source: created from CFIA data.

ecotone. Arctic fox rabies persists in the tundra of Canada’s north, with occasional spread southward through the bordering taiga regions and the boreal forests that cover the majority of the Canadian Shield. The most recent invasion moved through northern Quebec into Labrador and then onto the northern peninsula of Newfoundland. Over the past decade the last remnants of the arctic fox invasion of the 1950s that reached the mixed-wood plains of southern Ontario and Quebec have been eliminated by the ongoing control programs in those provinces. The barrier of the Great Lakes helped contain the original invasion and made it easier to concentrate focus on control efforts. Yukon has remained remarkably free of rabies over the years, shielded by mountain ranges along its eastern and western boundaries from incursions of arctic fox rabies.

Incursions of raccoon rabies into southern Ontario, southern New Brunswick, and southwestern Quebec reflected the northern extension of the raccoon strain of the virus along the eastern seaboard of the United States, up through the ridge and valley topography of the Appalachians, into Quebec and New Brunswick, and around the Adirondacks into Ontario. To date, further expansion has been checked by intensive control efforts in those areas.

Discussion Since 1926 Canada has had a comprehensive and uniform system of collecting, diagnosing, and reporting rabies. This has made it possible to document, with some confidence,

34

Domestic and Wildlife Rabies Incidence in Canada

Figure 2.10: The distribution of all rabies cases in Canada, 2003–2012. The dominant virus strain(s) in each area of concentration are shown. Source: created from CFIA data.

mammals in southern Canada has renewed attention to the long standing incidence of bat rabies across the country. Although annual levels are low, typically around 60 cases per year, contact with rabid bats has been the leading cause of human deaths from rabies in recent years (see Chapter 3b). Arctic Canada remains an enigma. Anecdotal evidence suggests rabies has persisted in arctic foxes for centuries and southern Canada can expect future invasions. The history of rabies also depends on the developments in viral technology that have identified major virus strains and sub-strains associated with specific host species. Those developments are discussed in terms of diagnostic methods in Part 5; the ecology of the vector species in Part 6; and the evolution of rabies control programs in chapters 10, 11, and 12 (Ontario, Quebec, and the Maritimes).

major changes in the temporal and spatial distribution of rabies and provide detailed evidence that control programs undertaken in various provinces have been effective. In 1926 there were 99 reported cases diagnosed in Canada, primarily in dogs. In 2017 there were 245 cases in Canada: mostly bats, raccoons, skunks, and foxes. In southern Canada rabies has changed from being a disease associated with domestic animals to a disease largely seen in wildlife. At its peak in 1986, there were 3873 positives in Canada, the majority of which were foxes and skunks with spillovers into pets and livestock. Control programs have almost eliminated wildlife rabies from most southern provinces, except for skunk rabies in Manitoba and Saskatchewan and the recent invasions of raccoon rabies from neighbouring US states. The success in controlling rabies in terrestrial

35

The Basics of Rabies in Canada

References All dogs must be chained up. (1910, February 7). Toronto Daily Star, p. 5. Baer, G. M. (Ed.). (1991). The natural history of rabies (2nd ed.). Boca Raton, FL: CRC Press. Bourhy, H., Reynes, J.-M., Dunham, E. J., Dacheux, L., Larrous, F., Huong, V. T. Q., ... Holmes, E. C. (2008). The origin and phylogeography of dog rabies virus. Journal of General Virology, 89(11), 2673–2681. https://doi.org/10.1099/vir.0.2008/003913-0 Blaisdell, J. D. (1992). Rabies and the governor-general of Canada. Veterinary History, 7(1), 19–26. Cause of rabies – Eating snow. (1901, February 17). Semi-Weekly Klondike Nugget, p. 4, col. 1. Connon, J. (1974). Elora: The early history of Elora and vicinity. Waterloo, ON: Wilfrid Laurier University Press. (Original work published in 1930). Cow had rabies. (1910, February 12). Toronto Daily Star, p. 5. Elton, C. (1931). Epidemics among sledge dogs in the Canadian Arctic and their relation to disease in the arctic fox. Canadian Journal of Research, 5(6), 673–692. https://doi.org/10.1139/cjr31-106 Exterminating the canine race. (1868, March 3). Daily Globe, Toronto. Goldi Productions. (2007). The Hudson’s Bay Company and the North West Company. Retrieved from http://firstpeoplesofcanada .com/fp_furtrade/fp_furtrade3.html Hamilton to be a dog-less town. (1909, May 20). Toronto Daily Star, p. 1. Hart, G. H., Bethke, R. M., Hardenbergh, J. G., Mitchell, C. A., Hagan, W. A., Hastings, C. C., & Petersen, W. E. (1946). Rabies and its control. Journal of American Veterinary Medical Association, 108, 293–302. Hodgins, J. S. (1897). The veterinary science: The anatomy, diseases and treatment of domestic animals, also containing a full description of medicines and receipts (18th ed.). London, ON: Veterinary Science Company, Ontario Veterinary Correspondence School. Hydrophobia. (1819, June 18). Kingston Chronicle, p. 3. Kuzmin, I. V., Hughes, G. J., Botvinkin, A. D., Gribencha, S. G., & Rupprecht C. E. (2008). Arctic and Arctic-like rabies viruses: Distribution, phylogeny and evolutionary history. Epidemiology and Infection, 136(4), 509–519. https://doi.org/10.1017/S095026880700903X Mad dog. (1877, September 29). The Daily Globe, p. 5. Mad dogs make trouble in Yukon: Epidemic of rabies assumes serious proportions in Dawson, Yukon. (1901, March 9). Toronto Daily Star, p. 11. Market cleaned of muzzles. (1910, February 21). Toronto Daily Star, p. 12. Nadin-Davis, S. A., Huang, W., Armstrong, J., Casey, G. A., Bahloul, C., Tordo, N., & Wandeler, A. I. (2001). Antigenic and genetic divergence of rabies viruses from bat species indigenous to Canada, Virus Research, 74(1–2), 139–156. https://doi.org/10.1016/ S0168-1702(00)00259-8 Nadin-Davis, S. A., Abdel-Malik, M., Armstrong, J., & Wandeler, A. I. (2002). Lyssavirus P gene characterization provides insights into the phylogeny of the gene and identifies structural similarities and diversity within the encoded phosphoprotein. Virology, 298(2), 286–305. https://doi.org/10.1006/viro.2002.1492 Nadin-Davis, S. A., Sheen, M., & Wandeler, A.I. (2012). Recent emergence of the Arctic rabies virus lineage. Virus Research, 163(1), 352–362. https://doi.org/10.1016/j.virusres.2011.10.026 Plummer, P. J. G. (1954). Rabies in Canada, with special reference to wildlife reservoirs. Bulletin of the World Health Organization, 10, 767–774. Rabies near Chatham. (1910, April 23). Toronto Daily Star, p. 8. Rabies raging in Welland district. (1901, August 14). Toronto Daily Star, p. 3. Rats, sewers and mad dogs – A report on rabies in Ontario. (1897). The Evening Star, Toronto. Report of the veterinary director general for the year ending March 31, 1906. (1906). Ottawa, ON: Department of Agriculture. Available from Library and Archives Canada, https://bac-lac.on.worldcat.org/oclc/29657040 Report of the veterinary director general for the year ending March 31, 1908. (1908). Ottawa, ON: Department of Agriculture. Available from Library and Archives Canada, https://bac-lac.on.worldcat.org/oclc/29657040 Report of the veterinary director general for the year ending March 31, 1909. (1909). Ottawa, ON: Department of Agriculture. Available from Library and Archives Canada, https://bac-lac.on.worldcat.org/oclc/29657040 Report of the veterinary director general for the year ending March 31, 1910. (1910). Ottawa, ON: Department of Agriculture. Available from Library and Archives Canada, https://bac-lac.on.worldcat.org/oclc/29657040 Report of the veterinary director general for the year ending March 31, 1911. (1911). Ottawa, ON: Department of Agriculture. Available from Library and Archives Canada, https://bac-lac.on.worldcat.org/oclc/29657040 Report of the veterinary director general for the year ending March 31, 1912. (1912). Ottawa, ON: Department of Agriculture. Available from Library and Archives Canada, https://bac-lac.on.worldcat.org/oclc/29657040

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Domestic and Wildlife Rabies Incidence in Canada Report of the veterinary director general for the year ending March 31, 1913. (1913). Ottawa, ON: Department of Agriculture. Available from Library and Archives Canada, https://bac-lac.on.worldcat.org/oclc/29657040 Report of the veterinary director general for the year ending March 31, 1915. (1915). Ottawa, ON: Department of Agriculture. Available from Library and Archives Canada, https://bac-lac.on.worldcat.org/oclc/29657040 Report of the veterinary director general for the year ending March 31, 1916. (1916). Ottawa, ON: Department of Agriculture. Available from Library and Archives Canada, https://bac-lac.on.worldcat.org/oclc/29657040 Report of the veterinary director general for the year ending March 31, 1917. (1917). Ottawa, ON: Department of Agriculture. Available from Library and Archives Canada, https://bac-lac.on.worldcat.org/oclc/29657040 Report of the veterinary director general for the year ending March 31, 1918. (1918). Ottawa, ON: Department of Agriculture. Available from Library and Archives Canada, https://bac-lac.on.worldcat.org/oclc/29657040 Report of the veterinary director general for the year ending March 31, 1920. (1920). Ottawa, ON: Department of Agriculture. Available from Library and Archives Canada, https://bac-lac.on.worldcat.org/oclc/29657040 Report of the veterinary director general for the year ending March 31, 1921. (1921). Ottawa, ON: Department of Agriculture. Available from Library and Archives Canada, https://bac-lac.on.worldcat.org/oclc/29657040 Report of the veterinary director general for the year ending March 31, 1922. (1922). Ottawa, ON: Department of Agriculture. Available from Library and Archives Canada, https://bac-lac.on.worldcat.org/oclc/29657040 Report of the veterinary director general for the year ending March 31, 1926. (1926). Ottawa, ON: Department of Agriculture. Available from Library and Archives Canada, https://bac-lac.on.worldcat.org/oclc/29657040 Smithcors, J. F. (1958). Outbreaks in America. Veterinary Medicine, 435. Special to the Star. (1909, August 6). Toronto Daily Star, p. 8. Steele, J. H., & Fernandez, P. J. (1991). History of rabies and global aspects. In George M. Baer (Ed.), The natural history of rabies (2nd ed., pp. 1–26). Boca Raton, FL: CRC Press. Steers died from rabies. (1908, August 31). Toronto Daily Star, p. 3. Tabel, H., Corner, A. H., Webster, W. A., & Casey, C. A. (1974). History and epizootiology of rabies in Canada. Canadian Veterinary Journal, 15(10), 271–281. Retrieved from https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1696688/ Tinline, R. R., & MacInnes, C. D. (2004). Ecogeographic patterns of rabies in Southern Ontario based on time series analysis. Journal of Wildlife Disease, 40(2), 212–221. https://doi.org/10.7589/0090-3558-40.2.212 To muzzle dogs for two months. (1908, June 26). Toronto Daily Star, p. 9. Voigt, D. R. (1987). Red fox. In M. Novak, J. A. Baker, M. E. Obbard, & B. Malloch (Eds.), Wild fur-bearer management and conservation in North America (pp. 379–392). North Bay, ON: Ontario Trappers Association. Walker, J., & Elkin, B. (2005). Rabies in the Northwest Territories, Part 1: A historical overview of rabies in NWT. Epi-North, 17, 1–3.

37

3a Human Rabies in Canada THE MYTH OF THE DUKE OF RICHMOND

Hugh Whitney Chief Veterinary Officer (Retired), St John’s, Newfoundland and Labrador, Canada

The story of Charles Lennox, the Fourth Duke of Richmond and governor-in-chief of British North America from 1818 to 1819 (see Figure 3a.1), is passably well known to those interested in the colonial history of Canada and of the history of rabies in this country. The story suggests that the life, and too short rule, of an illustrious English nobleman (Christie, 1820), after a distinguished military and political career (Jackson, 1994), was tragically ended by the bite of a pet fox while the duke was on a tour of duty through Lower and Upper Canada. The bite resulted in his untimely death from rabies while visiting the hamlet of Richmond (Upper Canada) (Tabel et al., 1974). Popular (McElroy, 1990) and scientific (Cameron, 2007) articles have repeated the story with little questioning of the “facts,” incredible as they may be, including the duke jumping over an almost two-metre fence. Most articles limit their sources to the accounts of two of Richmond’s officers, Lieutenant Colonel Francis Cockburn (deputy quartermaster general to the forces) and Major George Bowles (military secretary), or just repeat the conclusions of others. No questioning is made of the legitimacy of these documents, nor the pressures upon, or motivations of, these officers. Little reference is made to any other sources that may have existed at the time or subsequently. These documents, though little is available on their origin, appear to be official accounts produced after the events in question. However, they are not raw documents produced as daily journals but appear more to have been written after the fact, with many hands involved in their writing. In the study of historical documents, we are cautioned to question the writing of the document as much as its content.

For example, the manuscript most often referred to (“Particulars of the Death,” MS 2021) also exists in two other forms (“Account of the Last Days,” MS 1986 and Goodwood Archives, MS 2250) each one in a different hand and with slightly different wording, with the final one (MS 2021) being the most polished. MS 1986 and MS 2250 appear to be earlier drafts of Major George Bowles’s account. Added to this is the knowledge that under Bathurst, colonial officers were advised to keep two sets of documents: one that was official and one that was private (McLachlan, 1969), with the understanding being that the details provided in each would differ. James Stephen, an English lawyer, MP, and abolitionist, advised Earl Grey in 1850 that “commentators on colonial or any other history who confine themselves to official documents are as sure to go wrong as if they entirely overlooked them” (McLachlan, 1969, p. 477). The truth is likely more ignoble than noble. Richmond was a known alcoholic with his health compromised by years of drinking; his wife was a heavy gambler. In spite of being given the position of lord lieutenant of Ireland from 1807 to 1813 by his brother-in-law, Lord Bathurst, Richmond’s habits left him poorer upon departure than when he arrived (Miller, 2005). At the time of the Battle of Waterloo (1815) he was intentionally sidelined from any active position (Foulkes, 2006). Indeed, he never gained any experience in active military service: “The duke has had no opportunity to show his talents as a soldier, having been employed in civil life” (“Westminster Abbey,” 1819, p. 373). His position in Canada was also provided by Lord Bathurst (then secretary of state for war and the colonies) as a last attempt to recover some family wealth, a fact readily recognized

The Myth of the Duke of Richmond

Figure 3a.1: Left, Monument in Richmond, Ontario, dedicated to Charles Lennox, the Duke of Richmond and Lennox; right, “His Grace Chas. Duke of Richmond.” It is interesting to examine the various portraits of Richmond throughout his life as there is no consistent image of what he looked like. At times the suggestion is of a tall man with an athletic build and at others, of a fairly thin, short man. Source: Left, David Gregory; right, C. Schroeder (1819).

by Canadian politicians of the day, such as Louis-Joseph Papineau.1 Descriptions of him before he left were of a broken man (Greig, 1923). Upon arriving in Canada, Lord Dalhousie, then lieutenant governor of Nova Scotia, was furious over the choice and considered resigning. Upon meeting Richmond, he too commented on his broken health (Whitelaw, 1978). Richmond was reportedly bitten on the hand by a pet fox in Sorel (Fort William Henry) on 28 June 1819, when he tried to separate the fox from playing with his dog. Contrary to expectations if the fox had been rabid, the dog, Blücher,2 survived for many years afterwards. Reports suggest alternatively that it was a bite or lick, which occurred on Richmond’s face, chin, hand, or heel, and that it could have been a dog in Quebec City or the fox in Sorel. He reportedly then died in the house of the Chapman family in Richmond on 28 August 1819 after suffering from symptoms comparable to rabies. However, a few days earlier

he reportedly drank heavily with the local soldiers and the whispered comments of the community were that it was alcohol that killed him, not the fox (Armour, ca. 1900). It is entirely reasonable to consider that the official account was a cover-up for a sad end to an abused life. His two officers were his “muscle,” Cockburn3 and Secretary Bowles, both representatives of the Crown and both with ample reason and authority to provide a convenient alternative cause of death and to assure that the dependent locals were kept silent – a silence that could only be tolerated by passing the story down orally through the community.4 The discipline of historical writing demands that documents be questioned and alternative explanations sought. Though the duke may have died of rabies, he more likely died after a life of excess. A more complete rendering of this story is available (Whitney, 2013, 2017).

Notes 1 “S’en vint ici pour réparer les débris de sa fortune” (Lamonde, 1997). 2 Speculation on the reason for naming the dog Blücher is also of interest. Field Marshall Gebhard Lebrecht von Blücher was the commander at the Battle of Waterloo. The duke’s wife lost £30,000 in gambling to the field marshall.

39

The Basics of Rabies in Canada 3 Cockburn had been sent to the community of Richmond in advance of the duke’s arrival to settle some messy financial issues poorly handled by the local administrator. After the duke’s death he had to advise the local Presbyterian minister that now that an Anglican minister was available, there would be no need for him to occupy the church. In Lord Dalhousie’s journals (Whitelaw, 1978, p. 130), he describes Cockburn as a “pompous, bullying sort of a fellow, not liked by any of the party.” 4 An 1899 document suggests that the Chapman family, owners of the barn and house where the duke died, passed down the oral history through their family that the Duke died of delirium tremens not rabies (Gardiner, 1899).

References Account of the last days of the life of the 4th Duke of Richmond, found among the papers of General S. Browne. Goodwood Archives (Manuscript 1986). West Sussex Records Office, Chichester, England. Armour, M. G. (ca. 1900). A few notes about: The forming of a military settlement at Perth and surrounding country [undated manuscript from the Perth Historical and Antiquarian Society]. Retrieved from http://lcgsresourcelibrary.com/mostly/M-MSET.HTM Cameron, I. (2007). Grace in extremis. Canadian Medical Association Journal, 176(6), 819–820. https://doi.org/10.1503/cmaj.045218 Christie, R. (1820). Memoirs of the administration of the government of Lower-Canada by Sir John Coape Sherbrooke, the late Duke of Richmond, James Monk, Esquire, and Sir Peregrine Maitland. Quebec: New Printing-Office. Monographs Collection (CIHM/ICMH microfiche series no. 43593, FC 02 0203). Canadian Institute for Historical Microreproductions, Ottawa, Ontario, Canada. Retrieved from http://online.canadiana.ca/view/oocihm.43593 Foulkes, N. (2006). Dancing into battle: A social history of the Battle of Waterloo. London, England: Weidenfeld & Nicolson. Gardiner, H. F. (1899). Nothing but Names. Toronto: George F. Morang and Company. Goodwood Archives (Manuscript 2250). West Sussex Records Office, Chichester, England. Greig, J. (1923). The Farington diary (Vol. VIII). London, England: Hutchinson and Co. Jackson, A. C. (1994). The fatal neurological illness of the Fourth Duke of Richmond in Canada: Rabies. Annals of the Royal College of Physicians and Surgeons of Canada, 27(1), 40–41. Lamonde, Y. (1997). Conscience coloniale et conscience internationale dans les écrits publics de Louis–Joseph Papineau (1815–1839). Revue d’histoire de l’Amérique française, 51(1), 3–37. https://doi.org/10.7202/305621ar McElroy, G. E. (1990, June–July). The strange death of the Duke of Richmond. The Beaver, 70(3), 21–26. McLachlan, N. D. (1969). Bathurst at the colonial office, 1812–27: A reconnaissance. Australian Historical Studies, 13(52), 477–502. https://doi.org/10.1080/10314616908595394 Miller, D. (2005). The Duchess of Richmond’s ball – June 15, 1815. Staplehurst, England: Spellmount Publishers. Particulars of the Death of Charles, 4th Duke of Richmond. Colonel Cockburn’s Accounts. Major Bowles’s Account. Goodwood Archives (Manuscript 2021, MG 24 A 14). National Archives of Canada, Ottawa, Ontario. Schroeder, C. (1819). His Grace Chas. Duke of Richmond, Lennox and Aubigne K.G. [Photo]. Gift of Mr. David Ross McCord, McCord Museum (M2970). McGill University, Montreal, Quebec, Canada. Tabel, H., Corner. A. H., Webster, W. A., & Casey, C. A. (1974). History and epizootiology of rabies in Canada. Canadian Veterinary Journal, 15(10), 271–281. Westminster Abbey: Or, Records of very eminent and remarkable persons recently departed. (1819). The Monthly Magazine, or British Register, Vol. XLVIII, part II for 1819. London, England: J. and C. Adlard. Whitelaw, M. (1978). The Dalhousie journals (Vol. 1). Ottawa, Ontario: Oberon Press. Whitney, H. (2013). What evil felled the duke? A re-examination of the death of the 4th Duke of Richmond. Ontario History, 105(1), 47–72. https://doi.org/10.7202/1050746ar Whitney, H. (2017). What evil felled the duke? A follow-up. Ontario History, 119(2), 290.

40

3b Human Rabies in Canada HUMAN RABIES

Catherine Filejski,1 David J. Gregory,2 and Christopher J. Rutty3 1

Canadian Animal Health Institute, Guelph, Ontario, Canada Canadian Food Inspection Agency (Retired), Ottawa, Ontario, Canada 3 Health Heritage Research Services, Toronto, Ontario, Canada

2

Introduction Business Statement for Federal Rabies Program: “To reduce human exposure to rabies.” – Executive Report, Mini-Review of the Federal Rabies Program, Ottawa, 14 August 1989. p. 4

Rabies is found on all continents, except for Australia and Antarctica, and is nearly always fatal in all mammal species. While rabies is not present in Australia, in the 1990s, Australian bat lyssavirus, which is closely related to rabies and causes an infection with symptoms similar to that of rabies, was first identified circulating in Australian bat populations. While all mammals are susceptible to rabies infection, bats and wild carnivores act as the main reservoirs of the disease in North America and expose domestic animals and humans to the virus. It is estimated that more than 50,000 people die every year from the disease globally, mostly in Asia and Africa (World Health Organization [WHO], 2013). Estimates in Africa are 24,000 deaths per year, mostly in children (“Africa – Rabies Deaths,” 2013). Dogs are the source of the vast majority of human rabies cases in these countries. An estimate by the World Health Organization (WHO) suggests that about half the world’s population (3 billion people) lives in countries where contact with rabies in dogs is a possible risk (“Rabies, a Deadly Viral Disease,” 2013). Human mortality data are often used as an estimate to measure the global impact of rabies (Centers for Disease Control and Prevention [CDC], 2014a). Vaccines to prevent human rabies have been

available for more than 100 years. However, most human deaths occur in countries with inadequate public health resources and limited access to preventative treatment (CDC, 2014b). These countries have few diagnostic facilities and little rabies surveillance. In comparison with Africa and Asia, reported human deaths from rabies in Canada and the United States are rare, likely as a result of the successful management of rabies in dogs. A total of 100 or more deaths were attributed to rabies in the United States in the nineteenth and twentieth centuries, while 23 deaths due to rabies were reported from 2008–2017 (CDC, 2017). The total number of human rabies deaths in Canada from the nineteenth century to the present is estimated to be fewer than 50 (Figure 3b.1). The success of these two countries in rabies prevention and control can be attributed to ongoing dog population management and control, and rabies vaccination programs in both domesticated animals and wildlife, which have reduced the risk of human exposure to terrestrial strains of rabies, and the use of rabies post-exposure prophylaxis in exposed individuals. Despite the often repeated story that His Grace, Charles Lennox, the fourth duke of Richmond and Lennox and the fifth governor general of Canada died of rabies in 1819, there is ample evidence to suggest that this was not the case (see Chapter 3a). However, as Blaisdell (1992) points out in his article “Rabies and the Governor-General of Canada,” even if the duke had died of rabies, he would not have been the first reported such case in Canada. He would also most certainly not be the last. An exhaustive study of Canadian newspaper archives, historical records, and medical journals reveals a trail of human cases that begins in the

The Basics of Rabies in Canada

Figure 3b.1: Human deaths in Canada by decades, 1810 to 2010. The numbers represent contacts through dogs and the letters represent contact through other animals (C = cat, S = skunk, B = bat, shaded = imported, W = wolf). Source: authors.

early nineteenth century, and leads up to the present day (Figure 3b.1). This chapter provides an overview of these cases and brings together what is known about some of these cases from both archival and published sources. Varying amounts of information on the earliest human rabies cases on record in Canada are found in newspaper articles, journals, and a few early North American medical journals. Despite the fact that a general widespread acceptance of the germ theory of disease would only develop later in the nineteenth century, the idea that humans could contract rabies after being bitten by a rabid animal (most often a dog at that time) was widely understood in the early nineteenth century. The determination of rabies as the cause of death in human cases before the development of laboratory diagnostic techniques by 1910 (see Chapter 20) was consistently based on a combination of a history of an animal bite and the development of symptoms of hydrophobia. Before Louis Pasteur’s discovery of a rabies vaccine in 1885, treatment options following a bite from an animal known or suspected to be rabid were extremely limited and often crude. The development of postexposure prophylaxis treatments in general is discussed in more detail in Chapters 15a and 32. The cases of human rabies reported and investigated by the authors are outlined in chronological order below.

generated considerable public interest. The first of these was the case of nine-year-old Charles Giguères, who died in 1814. An inquest into the boy’s death was called by the coroner for the district of Quebec on 3 August 1814, and the results of the inquest were published in the Québec Gazette (“Mad Dogs,” 1814). The coroner’s office in Quebec had been established in 1764 to hold inquiries into violent or sudden deaths from unknown or suspicious causes. Inquests were called for deaths that were not clearly the result of natural causes. In the nineteenth century, these inquests involved the presentation of evidence to a coroner’s jury, usually made up of 12 “honest (without a criminal record) and objective men” from the community, whose responsibility was determining the cause of death (Lessard & Tésio, 2008, p. 436). The verdict would in turn constitute the basis of the coroner’s report. The medical testimony heard by coroner’s juries in this period was often exclusively that of the attending physician in the case (Johnston, 1893). Verdicts of death by “Visitation of God” (i.e., an act of God) in this period frequently served as an indication that no autopsy had been performed (Johnston, 1893, p. 4) but also implied that the circumstances of the death were not suspicious and did not require further criminal or judicial actions (Lessard & Tésio, 2008). Evidence presented to the coroner’s jury in the 1814 case included the following facts (“Mad Dogs,” 1814): on 21 June 1814, Charles Giguères had been playing with two other children at his father’s house on St Foi Road in the parish of Quebec when a dog belonging to a neighbour and family relation came to the house, which happened quite regularly. However, in this instance, as Charles went to pet the dog, it suddenly bit him under the lower right jaw. The bite wound healed slowly over the following three weeks, after which the boy appeared in good health until 30 July 1814, when

Human Rabies Cases Before Pasteur: 1800–1885 Case 1 (1814)  The earliest documented human cases of rabies in Canada were all reported from Quebec in the early nineteenth century (Blaisdell, 1992, p. 19; see Chapter 2) and 42

Human Rabies

unable to swallow her saliva, which “issued from her mouth in a viscid and stringy state.” She died after a series of particularly violent convulsions (Blaisdell, 1992, p. 19). Case 4 (1819)  The story of His Grace, Charles Lennox, the fourth duke of Richmond and Lennox, and fifth governor general of Canada who died in 1819, is recounted in Chapter 3a. With the uncertainty as to whether his death was from alcohol or the bite of his pet dog or a fox, the authors have not included his death in Figure 3b.1. Case 5 (1839)  The story of William Clancy and his death from rabies in 1839 was recorded in surviving medical records transcribed and published in the Medical Services Journal in May 1967. The story was related by Dr George Douglas, who had witnessed this case of “Lysa” while visiting his brother Dr James Douglas who worked at the Marine and Emigrant Hospital in Quebec City. William Clancy, a 40-year-old servant, had been bitten by a house dog on the left cheek six weeks before his death. The bite left an irregular wound an inch long, which was treated by the surgeon by rubbing argent nitrate into it. The dog was confined after the biting incident and died six days later, exhibiting signs of rabies. Clancy continued in good health until 18 December, when he started having difficulty breathing and an uneasy feeling in his chest and throat. By the next morning, he had fasciculations in the muscles of his chest, throat, and upper extremities. He exhibited nausea and vomiting, but initially was able to swallow fluids with great difficulty, and was given a large dose of a cathartic of calomel and carminatives. By the afternoon, he was unable to swallow at all because of spasms in his trunk and neck. The scar on his left cheek was now red and inflamed, but not painful. He had ongoing nausea and vomiting, and his spasmodic attacks progressed in duration and frequency, apparently in response to stimuli such as the light of a candle, a current of air, or anything with a shiny surface. Three hours before his death he became very aggressive, attempting to bite the attendants. He died at 3 a.m., 20 December 1839, within 36 hours of the onset of his symptoms. At the time of death, his mental powers seemed unimpaired with the exception of short intervals during which he appeared incoherent. He had been treated with a steam in the form of a vapour bath, and shortly before dying had been given a “homeopathic dose,” perhaps belladonna (Mitchell, 1967, p. 811). Case 6 (1860)  An address by Dr J. McCrea of Campbellford, Ontario, to the 1883 meeting of the Newcastle and Trent, and Quinte and Cataraqui Medical Association described a human rabies case near the village of Hastings, Ontario, in June of 1860. No details were provided other than that the patient had died within five days of the onset of symptoms (McCrea, 1883, pp. 231–232).

he began to complain of an earache on the right side. On 31 July his symptoms worsened to include pain “in every part of his body and general indisposition.” By 1 August he was “seized with the unusual symptoms of hydrophobia” and Mr Lloyd, the surgeon of the artillery, was called to tend to him. The surgeon tried all available treatments, including mercurial applications and bleeding the little boy copiously, but was of the opinion that nothing could be done to save his patient, and the symptoms continued to worsen. Charles Giguères died at about three o’clock on 2 August 1814, four days after the onset of symptoms. The jury from the coroner’s inquest returned the following verdict: “He died by the visitation of God, of hydrophobia” (“Hydrophobia,” 1816). The formal recognition of rabies as the cause of death by the inquest jury precipitated the implementation of a number of precautionary measures within Quebec City to prevent further deaths from rabies. Case 2 (1816)  Despite these measures, another human case of rabies in Quebec City was documented in 1816. The victim was 13-year-old Jean Maheu, and another coroner’s inquest was requested by one of the attending physicians to ascertain and record “all the circumstances attendant upon the sickness, and death of the patient” (“Hydrophobia,” 1816). Jean Maheu had been brought home by his friends on 15 January 1816 after being bitten by a large dog. He had three large, deep wounds (two on the upper part and one on the lower part) of his left thigh, one of which just missed the femoral artery, as well as a smaller wound just above the left ankle. His wounds were treated by a Dr Blanchet and his nephew Jean Blanchet, and healed over without any complications within three weeks. The boy then continued in good health until 10 March 1816, when he began to have trouble sleeping. By the following day, he was complaining of “violent pains in his loins and both his legs.” On 12 March he was experiencing frequent convulsions and difficulty swallowing, and Dr Blanchet and his nephew were called to attend him again. By 13 March the symptoms were becoming more pronounced, and Dr Blanchet bled the boy copiously both in the morning and in the evening, and ordered him placed in a warm bath. Mr Blanchet returned to see his patient at two o’clock in the morning of 14 March, when he found him in strong convulsions and foaming at the mouth, and was unable to do anything for the boy. Jean Maheu died three hours later, at 5 o’clock in the morning on 14 March. Case 3 (1817)  Madame Bruneau, the wife of a member of the Ordinance Department, was bitten by a cat in November 1816. Her wound was initially washed and dressed and healed. The wound became itchy and inflamed in May 1817, and soon afterward she came down with symptoms that included being unable to look at herself in a mirror and eventually being 43

The Basics of Rabies in Canada

Case 7 (1862)  In 1862, James Cain, a labourer living on the farm owned by W. W. Bowman, Elmira, Woolwich township, Ontario, was bitten on the cheek by a strange dog as he ascended the steps to his house. Mr Cain grabbed the dog by the neck and held him while his wife stunned the dog with a stick. Mr Cain then killed the dog with an axe. The wound healed rapidly but he felt a tingling sensation on Saturday, 1 March. Dr Bowlby of Berlin (now Kitchener) visited the man and offered him a cup of tea, which precipitated attacks of hydrophobia. Mr Cain died on Monday, 3 March 1862 (“Death from Hydrophobia,” 1862, p.188). Case 8 (1865)  John Connon in his book, Elora: The Early History of Elora and Vicinity, reported on the death of Mrs Cruickshank by hydrophobia. Her husband had died by drowning while fishing in 29 June 1853 and “sadder still was the death of Mrs Cruickshank, from hydrophobia on February 19, 1865” (p. 40).

died of paralytic rabies in 14 days, the second in 21 days (Provincial Board of Health, 1897). Case 13 (1901)  On 2 May 1901, a newspaper article reported “the first case of death from hydrophobia” in Dawson, Yukon, during an outbreak of rabies in dogs. Aaron Ewing, a miner on Hunter Creek, was bitten by a dog six weeks prior to the development of symptoms, which then progressed rapidly following their onset. A post-mortem examination confirmed it to be “a clear case of hydrophobia” (“Hydrophobia at Dawson,” 1901, p. 5). Case 14 (1905)  The following story was told by Dr Edward Hasell of the Provincial Royal Jubilee Hospital, Victoria, British Columbia, in a letter to Dr Charles Higgins of Ottawa after Dr Hasell observed the following case of human rabies. A man living in Whitehorse, Yukon, was attacked by a tame wolf chained at the police station (Figure 3b.1). The man was bitten on his fingers and other parts of his body. The wounds were cauterized and healed in a couple of days. Eight weeks later, he returned to Victoria, where he lived. Three days before admission to hospital, he became nervous, experienced tingling in his hands, could not control his hands, and was unable to sleep. He was admitted to hospital under Dr Frank Hall’s care on 31 December 1904. He had hiccups, was drooling saliva, appeared to be almost suffocating, and sudden noise or movements sent him into convulsions. His condition worsened despite treatments administered to relax him and he died the next day, 1 January 1905 (Loir, 1906). Case 15 (1910)  On 2 May 1910 a 10-year-old boy from Hamilton developed rabies as a result of a bite from a pet dog, which had occurred six weeks earlier (“Editorial,” 1910). The case was confirmed by Dr Amyot, based on the identification of Negri bodies in the brain of the child (Hodgetts, 1910, p. 241). Case 16 (1912)  In 1912 a dog bit two men in Port Arthur, Ontario. This resulted in the death of one of the men sometime later. The other could not pay for the expense of going to Toronto for treatment, but apparently survived nevertheless (“Editorial,” 1912, p. 7). Case 17 (1913)  Alexandra May Kenn, the four-yearold daughter of Jon Kenn of St Thomas, died of hydrophobia in the early hours of 17 January 1913. The girl had been bitten by a stray dog invited into her house by the mother. The dog appeared normal to the parents and was sent away, no treatment being thought necessary by the authorities. The girl became ill a week before her death, but showed few signs of convulsions, although eight doctors stated she had rabies. A nine-year-old boy, Karl Wimbush, was bitten an hour later near the Kenn house, apparently by the same

From Pasteur to Mandatory Reporting of Rabies Cases: 1885–1925 Case 9 (1891)  A newspaper article from 18 November 1891 reported that a four-year-old, the son of a farmer named William Dooley, near Gatineau, died of hydrophobia after being bitten by a rabid dog. The boy showed symptoms of hydrophobia within a few days of the biting incident and died in convulsions (“Died of Hydrophobia,” 1891, p. 5) Case 10 (1892)  A reference in a newspaper article from March 1892 notes that two girls with the surname Hawley, resident in Chandos, Peterborough County, were suffering from hydrophobia, with one expected to die shortly (“Editorial,” 1892, p. 1). Case 11 (1896)  A seven-year-old boy, the stepson of J. Fenner, a butcher in Arkona, died of hydrophobia on 6 February 1896. He had been bitten by a mad dog six weeks earlier. The same dog was known to have bitten several other dogs. A proclamation was issued for the villages of Arkona and Thedford and the Township Bosanquet, warning residents to muzzle their dogs or risk having their animal shot (“Dies from Hydrophobia,” 1896). Case 12 (1897)  On 1 June 1897, the Ontario Provincial Board of Health received word from Dr J. W. Smith of Dundas that a young boy named James McKenzie had died of hydrophobia (Provincial Board of Health, 1897). James and his brother had been bitten by a dog about 10 days earlier, and his brother was sent to the Pasteur Institute in New York for treatment, but James was not (“Editorial,” 1897). Rabies was confirmed both by microscopic study and animal inoculation. One of the inoculated animals 44

Human Rabies

dog. The boy’s parents sought treatment for him in Toronto, and he appears to have survived (“Editorial,” 1913, p. 18). Case 18 (1914)  A young girl (F.F.S.), four years of age,  was admitted to the Toronto Hospital for Sick Child­ ren  on 24 January 1914. She was suffering from nervousness and fits or spasms. On admission her condition did not seem critical, but with a history of a dog bite injury six weeks ­before admission, rabies was suspected. The dog in question had been captured and quarantined for 10 days, but had shown no signs of disease and had been released. The girl was therefore not treated at the time of the biting incident and was only admitted to the hospital after developing some vague symptoms. Her condition worsened and she died on 26 February 1914. A histological finding of Negri bodies and the subsequent death of animals inoculated with the child’s cortex, cerebellum, and basal ganglia confirmed the diagnosis of rabies (Fitzgerald, 1914, p. 246). Case 19 (1916)  William Gray died of hydrophobia on 24 May 1916 at the Toronto General Hospital following a bite from a dog. The physicians who attended him after the biting incident had advised him to receive the Pasteur treatment. Mr Gray declined the treatment and allowed the wound to heal. Sometime later he became ill and was diagnosed with hydrophobia by Dr Hamilton. Drs Bell, McCullough, and Fitzgerald of the Provincial Health Department confirmed the diagnosis: “It was too late to do anything except to give the patient relief,” said Dr Hamilton, who emphasized the importance of undergoing the Pasteur treatment (“Dies from Hydrophobia,” 1916, p. 9).

in Quebec. The outbreak was purportedly started by two dogs brought in from the United States during the lumber season of 1925. Starting 29 January 1926, two persons from Gatineau and three from Ottawa were receiving the Pasteur treatment (“Quarantine,” 1926). By 6 March 1926 two people were receiving Pasteur treatment at the Royal Victoria Hospital in Montreal (“Steps Taken,” 1926). By 14 July 1926 a further 147 people were undergoing Pasteur treatment at the same hospital (“Epidemic of Rabies,” 1926). The first death from hydrophobia related to this outbreak was reported by Notre Dame Hospital in the case of six-year-old Roger Pisonnault, resident at Ange Gardien, Rouville County. The boy had been bitten by a dog on 2 October 1926 on his nose, right eye, and leg. He was treated locally but when his condition worsened he was moved to hospital where he died on 19 October (“Died from Hydrophobia,” 1926, p. 5; “Victim of Hydrophobia,” 1926). Case 22 (1927)  The existence of a second case of human rabies due to this epidemic in Montreal is supported by a statement made on 28 February 1927, by the Hon. W. R. Motherwell, minister of agriculture, in the House of Commons indicating that “one hundred and forty cases of human rabies were being treated at the present time, and from the disease two deaths had so far resulted” (“140 Cases,” 1927, p. 2). Case 23 (1927)  Francois Ouelette of Perkins Mills, Quebec, died in a cell in the Hull jail, where he had been taken on 12 November 1927, after he became violent in the Sacred Heart Hospital. He was a victim of hydrophobia, and medical attention given to him through the night failed to offset the ravages of the disease. An inquest was to be held. He had been bitten by a mad dog some six weeks before his death (“Mad Dog’s Bite Blamed,” 1927). Case 24 (1927)  Mrs George Scharf of West Templeton, Quebec, died of hydrophobia on 20 November 1927. She had been bitten six weeks earlier when she tried to take a dish of food away from her dog. She did not consider the bite serious, and it was some time before she sought medical attention (“Rabies Contracted,” 1927). Case 25 (1928)  William Wilkinson, a 13-year-old resident of Windsor, was bitten by a cat on 16 June 1928, after he provoked the cat. The boy received the Pasteur treatment for rabies and his wound healed uneventfully, although the brain of the cat tested positive for rabies (“Pasteur Treatment,” 1928). It is believed that this same cat bit Lorraine Goyeau, causing her death on 25 July 1928. Goyeau had been clawed in the face by the cat and the wounds healed well. She was rushed to Hotel Dieu, where she died in convulsions four days later. Both the cat’s brain and the girl’s brain tested positive for Negri bodies (“Pasteur Treatment,” 1928). The rabid cat had

From Mandatory Reporting of Rabies Cases to Human Diagnosis by Agriculture Canada: 1925–1950 Case 20 (1925)  While it was not possible to verify the source of this case, the Saskatchewan Ministry of Heath, with access to historical information (V. Mann, personal communication, 2015), reported two human rabies deaths occurring in Saskatchewan, one in 1925 and one in 1970 (Case 35 below). This information aligns with the Public Health Agency of Canada’s notifiable diseases information for Saskatchewan. Rabies was added to Saskatchewan’s notifiable disease list in 1927. The original records to validate this 1925 case were archived years ago and not included in the notifiable disease computer database system. The cause of the incident has been attributed to a dog exposure in Figure 3b.1, as cases due to wildlife and bat exposures were not diagnosed or recorded until later. Case 21 (1926)  Newspaper accounts from 1926 describe a number of dog bite incidents in Ontario and more 45

The Basics of Rabies in Canada

also bitten Jeanette Jackson, who received the Pasteur treatment and recovered (“Pasteur Treatment,” 1928). The cat was thought to have been attacked by rabid dogs in the area, many of whom belonged to residents of Detroit coming to Windsor on a daily basis or owning summer cottages on the Canadian side of Lake Erie. In the first five months of 1928, 302 dogs in Detroit had been diagnosed with rabies (Adams, 1928). Case 26 (1929)  Rita Vaillancourt, eight years old, died of rabies at the Royal Victoria Hospital in Montreal at six o’clock in the evening, 5 July 1929. She had been bitten by a dog several weeks earlier, but her condition had only developed the day before her death. She had first been taken to Ste Justine Hospital, but when it was believed that she had rabies, she was moved to Royal Victoria Hospital, which had a special department for the disease (“Rabies Possible,” 1929). Case 27 (1929)  A post-mortem examination carried out at Queen’s Park by the Ontario Department of Health in October 1929 confirmed that the death of a little boy with the surname Villeneuve, in Wendover, Ontario, was due to rabies. The boy had been bitten on the face by a stray dog while playing, and the dog subsequently disappeared (“Godfrey Criticism,” 1929). This was reported to be the second death from rabies in the province that year, although the authors have not been able to locate any reports or information on the first case referenced in the newspaper articles. Case 28 (1931)  Richard Pellow, aged three years, of Chapleau, Ontario, died of suspected rabies. He had been bitten on the cheek by a husky dog 11 days earlier and taken to Chapleau Hospital where he was treated but apparently not given the Pasteur treatment. A few days later he became ill and eventually was transferred to the Hospital for Sick Children in Toronto. He died on 17 April 1931 (“Bitten by Husky,” 1931). Case 29 (1933)  In 1983, a list of human rabies cases reported in Canada from 1924 to 1982, published in the federal department of Health and Welfare’s Canada Diseases Weekly Report, included a case in Quebec in 1933 (Varughese, 1983). However, the authors have been unable to find any other reports containing information about this case. Case 30 (1944)  An 11-year-old boy, L.M. was admitted to hospital on 29 August 1944 and died four days later. He had been bitten on 5 July on his right thigh by a strange dog. The wound required sutures and healed uneventfully. However, on 22 August, the boy noticed pain in his right leg, which became intense by 25 August. He developed delirium and hallucinations by 28 August (Breault, 1944, p. 172) and was admitted to Hotel Dieu Hospital in Windsor on 29 August. His condition deteriorated rapidly with the development of high fever, hydrophobia, logorrhea, and clonic convulsions.

He became aggressive and died in severe convulsions on 2 September 1944. Typical inclusion Negri bodies were found in his hippocampus and cerebellum (Breault, 1944).

From Diagnosis of Human Rabies Cases by Agriculture Canada to Present: 1950–2012 Case 31 (1959)  Richard Knight, a seven-year-old boy from Port Perry, Ontario, died of rabies on 6 November 1959. He had been bitten by a baby skunk five weeks before seeking medical attention. He received treatment at the Port Perry and Oshawa Hospitals before being transferred to Toronto’s Hospital for Sick Children on 31 October 1959. He had not received the Pasteur treatment as the boy could not or would not say how he received the bites on his fingers. It was subsequently discovered that his playmates had had to pry open the skunk’s mouth to get the boy’s fingers loose (“Believe Rabid Skunk,” 1959). On admission to hospital, his temperature was elevated, he exhibited disorientation and excessive limb movement, and had a shrill cry. He became comatose the following day, developing a vacant stare and dilated pupils. Two days after admission, he became more deeply unconscious. There were no signs of hydrophobia throughout the course of his illness, and the boy was able to swallow saliva but unable to swallow any fluids administered to him orally. He died early on the third day. Tissue smears of the hippocampus demonstrated Negri bodies with Seller’s stain, indicative of rabies (McLean et al., 1960). Case 32 (1959)  In December of 1959, Barry Montgomery Spence Kilborn, of Peterborough, Ontario, died of rabies. He had been bitten on the arm by a puppy he had, which itself had previously been bitten by a skunk. He was admitted to hospital and died on 17 December 1959. His wife and son received anti-rabies shots in Parry Sound. Rabies was confirmed as the cause of death on the basis of post-mortem testing in February of 1960 (“Blame Death on Rabies,” 1960, p. 8). Case 33 (1964)  A 14-year-old girl from Fort Huntingdon, Quebec, was bitten on the face by a skunk while sleeping on or about 15 February 1964. The girl’s father rushed to her aid when she awoke screaming, grabbed the skunk, and threw it out the window. The father was bitten by the skunk on the hand. No attention was paid to the incident at the time and no physician was called to see the child. On 3 March the girl became ill and was taken to the local hospital by her mother. Her condition worsened at the local hospital, and she was transferred to the Montreal Children’s Hospital where a clinical diagnosis of rabies was made, and the girl bit one of the nurses. The patient died on 15 March 1964. The clinical diagnosis was confirmed through

46

Human Rabies

received 14 daily inoculations of the Semple rabies vaccine distributed by the Ontario Department of Health. Approximately 80 days following the attack by the rabid cat, the girl became sick and showed signs of encephalitis, which progressed to death. Examination of the child’s brain confirmed the presence of Negri bodies (Bell, 1967). Case 35 (1970)  A 15-year-old boy (R.G.) from Meadow Lake, Saskatchewan, became ill on 19 September 1970, exhibiting signs of paresis of the lower limbs. This was followed by salivation and dysphagia. When his condition worsened, he was admitted to the University Hospital in Saskatoon on 22 September, and he died on 29 September 1970 (Dempster et al., 1972). A post-mortem diagnosis of rabies in this case was made on the basis of laboratory results obtained three weeks after the boy’s death, which included the confirmation of rabies antigen present in a specimen of his brain, and the identification of Negri bodies in mouse brain studies. A field investigation into events leading to the boy’s death initially indicated contact with a dog and cat that had died of a distemper-like illness. However, as the evidence for rabies in these animals was not convincing, additional questioning of the boy’s parents uncovered that the boy had been bitten on 1 September 1970 by a bat that had flown into his room, which he killed. This event had been forgotten at the time of the initial investigation, but was recounted by his father after the boy’s death (Dempster et al., 1972; Davidson, 1970). Case 36 (1977)  A 63-year-old man from Parrsboro, Nova Scotia, was admitted to the Victoria General Hospital in Halifax on 9 August 1977, suffering from an undiagnosed neurological condition. On admission he was agitated, unable to make precise movements with his left arm, and had pain in the fingers of the arm. While in the hospital, he became more agitated and disoriented. In his final 12 hours, he was moved to a separate room because of uncontrolled agitation, which did not respond to sedation. Lapsing into a coma, he died on 11 August 1977 (King et al., 1978). Subsequent investigation revealed that the man had been bitten on the left hand by a bat while attempting to remove it from his residence, about a year before his death. The man had not travelled outside the province in the previous year, and his dog was clinically normal. Tissue sections taken at autopsy were re-examined in November and the diagnosis of rabies confirmed by the Health of Animals Laboratory in Ottawa (“Zoonoses – Rabies,” 1978). Case 37 (1984)  On 9 August 1984, a 43-year-old male missionary sought medical attention in Quebec City for numbness in his arm. He had recently returned from the

Figure 3b.2: Picture of Donna Featherstone.

Permission to use the photograph was given to David Johnston by Donna’s mother, Dawnean Featherstone.

laboratory tests on the brain. Rabies post-exposure prophylaxis was administered to the father, mother, and nurse (Foley, 1964). A thorough description of this case appears in the McGill Medical Journal (Chaffey & Binney, 1964). Case 34 (1967)  A four-year-old girl, Donna Darlene Featherstone (Figure 3b.2), from Richmond, Ontario, died of rabies on 13 January 1967. While playing with a cat at her home on 21 October 1966, she was suddenly attacked by the cat, which bit and scratched her face. The mother and two other individuals were also scratched and bitten by the cat on the wrist and forearm (“Ottawa Girl,” 1967; “Three More Lives,” 1967). The cat was euthanized and the head submitted to the Animal Disease Research Institute of the Department of Agriculture in Ottawa for examination. The next day, a report was issued indicating that Negri bodies had been found in the brain and the cat was rabid. In accordance with the World Health Organization’s recommendations (WHO, 1966), post-exposure prophylaxis was started for the girl and the other three exposed individuals, beginning on 22 October 1966. All exposed individuals

47

The Basics of Rabies in Canada

Dominican Republic, where he had been bitten by a dog on 16 July 1984. The brain of the dog had been removed for testing, but had been subsequently lost. The patient had received 10 doses of an unknown type of rabies vaccine subcutaneously starting on the day of the incident. Based on information obtained from the physician involved, the vaccine administered may have been expired and the patient received no immune globulin (Picard, 1984). The patient was admitted to hospital in Quebec City on 9 August. A diagnosis of rabies encephalitis was made, the patient was revaccinated with human diploid cell vaccine, and he was given rabies immune globulin. The fasciculations present in the patient’s right scapula, shoulder, and arm at the time of admission to the hospital then extended to the left hemithorax. His condition grew rapidly worse, and by 11 August, the fasciculations extended over his whole body, although the patient was still conscious. By 14 August his brain electroencephalogram showed severe anomalies, later progressing to no brain activity at all. The patient died on 17 August; specific fluorescent antibody staining of autopsy brain tissue was positive for rabies (Picard, 1984). The virus was isolated from brain tissue in neuroblastoma cells and characterized with a panel of 43 anti-­nucleocapsid and 40 anti-glycoprotein monoclonal antibodies. The patterns obtained were different from those found in Canadian wildlife and domestic animals. However, because little information was available about rabies isolates from the Caribbean or Central and South America at that time, the isolate could not be characterized (Webster et al., 1985). Case 38 (1985)  A 25-year-old male student at the University of British Columbia died of rabies on 26 November 1985. He had been working as a cook at a Forest Service camp in Smythe, Alberta, during the third week of July 1985, when he was scratched or bitten on the face by a bat that flew into his tent. At that time, he received no post-exposure prophylaxis. At the end of August, he left the camp and went hiking near Nelson, BC, and returned to Vancouver on 2 September. He experienced neck pain, swollen lymph nodes, a high fever, and sweating on 25 October. Four days later he experienced convulsions and hydrophobia. He was hospitalized on 31 October and received human rabies immune globulin and human diploid cell rabies vaccine but was comatose. Subsequently, a brain biopsy confirmed rabies on the basis of a fluorescent antibody test. Rabies virus was also isolated from the brain tissue and saliva. All of the student’s household and hospital contacts received rabies post-exposure prophylaxis (Varughese, 1985; Webster et al., 1987).

Case 39 (2000)  A nine-year-old boy and his brother came into contact with a bat on 28 August 2000, while sleeping in a rural cottage in Quebec. The brother had seen the bat in the bathroom the same evening and reported it to the father, who collected and disposed of the bat with his hands. A small puncture wound was observed by the boy on his left arm, which he showed to his mother. On 22 September 2000 the boy was feverish and complained of pain in his left arm. He was admitted to a Montreal hospital on 27 September and by the next day developed tremors and myoclonic jerks in both arms, was agitated, and had hydrophobia, acrophobia, dysarthria, and visual hallucinations. His condition worsened the following day with the onset of hypersalivation, tremors, and feelings of suffocation. A diagnosis of rabies was considered, and he was transferred to a children’s hospital. A diagnosis of rabies was confirmed ante-mortem by direct immunofluorescent staining of a skin biopsy and by polymerase chain reaction product analysis from several submitted specimens. Rabies immune globulin and vaccine were administered, but the boy’s clinical status deteriorated and he died on 6 October 2000 (Turgeon et al., 2000). Virus isolation from post-mortem samples was not possible since brain tissue was not available. Rabies virus was isolated from saliva and was determined to be similar to a rabies variant circulating in silver-haired bat (Lasionycteris noctivagans) populations (Elmgren et al., 2002). Case 40 (2003)  A 52-year-old man from the Vancouver region of British Columbia with a two-day history of left upper arm weakness was examined at a local hospital on 6 January 2003. He was sent home but returned the next day with a progression of his symptoms to both arms. He was admitted to hospital and when his breathing became affected, he was sedated and intubated before admission to the intensive care unit (ICU). The patient’s condition deteriorated over the next seven days, with the initial working diagnosis being atypical Guillain-Barré syndrome (GBS). Administration of intravenous immune globulin, the treatment of choice for GBS, resulted in no improvement. He was transferred to a tertiary care hospital ICU on 16 January under the care of the neuromuscular disease unit. A tracheotomy was performed on 18 January. His condition worsened, terminating in brain death. Life support was withdrawn on 30 January 2003. The patient’s history was unremarkable, although his wife recalled her husband mentioning that he been around bats in old abandoned cabins in British Columbia. A tentative diagnosis of rabies was made on the basis of Negri bodies identified on histopathologic slides of the patient’s brain tissue. Further tests at the Centre of Expertise for Rabies 48

Human Rabies

in Ottawa, using direct fluorescent antibody and reverse transcriptase-polymerase chain (RT-PCR) reaction testing were strongly positive for rabies. Subsequent monoclonal antibody and RT-PCR tests identified the virus strain as a variant associated with Myotis bats, with the little brown bat as the most likely species (Parker et al., 2003). Case 41 (2007)  A 73-year-old man was bitten by a bat on his left shoulder while sleeping at home in rural Alberta during August of 2006. He killed and disposed of the bat but did not seek medical attention. He had no previous history of rabies vaccination and became ill on 14 February 2007, complaining of left shoulder pain. The pain progressed to include left hand weakness. He sought care at the local emergency department over the following three days and was given analgesics. The patient was admitted to the local hospital on 21 February 2007, with signs of general weakness, anorexia, dysphagia, and irritability. Two days after admission the patient had left arm muscle spasms and difficulty breathing. His condition worsened and he was transferred to a tertiary care hospital on 23 February, with a diagnosis of aspiration pneumonia and sepsis. The history of the previous bat bite was not reported at this time. His condition continued to worsen but it was not until 26 February that the patient’s family recalled the bat incident some six months earlier. A nuchal skin biopsy specimen and a saliva sample were submitted to the Canadian Food Inspection Agency’s Rabies Laboratory in Ottawa, where a diagnosis of rabies was confirmed on 1 March 2007. Viral antigen and viral RNA were detected by direct fluorescent antibody test and reverse transcription polymerase chain reaction, respectively. The patient died on 26 April 2007, after nine weeks in the intensive care unit, from encephalitis caused by a rabies virus strain variant associated with silver-haired bats (L. noctivagans) (Johnstone et al., 2008). Case 42 (2012)  A 41-year-old man had been working in the Dominican Republic as a bartender for four months and had also travelled to Haiti. While on the island, he became ill and had been to the resort clinic three times in the month before leaving the Dominican Republic for Toronto in April. His condition worsened, progressing to dysphagia, hydrophobia, cibophobia (fear of food) and anemophobia (fear of air), and he returned to Toronto by plane on 9 April. On arrival, he was behaving erratically and was taken to a Toronto hospital by the police, exhibiting symptoms consistent with rabies. He cited a 10-day history of increasing neck and shoulder pain, arm tingling and numbness, headache, anxiety, and hydrophobia. His symptoms worsened by 11 April, and on 12 April specimens from a nuchal skin biopsy, saliva, and cerebrospinal fluid were submitted for

analysis by the Centre of Expertise for Rabies in Ottawa. The skin biopsy was positive to the fluorescent antibody test, confirming that the patient had rabies. He was transferred to the neurological intensive care unit at Toronto Western Hospital. Further studies using phylogenetic analysis determined that the rabies virus was the Hispaniola dog/mongoose strain, a variant not found in Canada (Fehlner-Gardiner, 2013). He died in early May of 2012 (“Rabies Diagnosed,” 2012), 30 days after the onset of initial symptoms. Neither the patient nor the family could remember any potential exposures to animals. After the confirmation of rabies, the hospital assessed the risk to potential contacts, and five close contacts received post-exposure prophylaxis. Fifteen hospital staff were considered for post-exposure prophylaxis, and 12 chose to receive prophylaxis with both rabies immune globulin and vaccine, one chose to receive vaccine alone, and two refused all post-exposure prophylaxis (Public Health Ontario, 2012).

Discussion While the authors have made every effort to locate reports of cases in newspaper articles, journals, annual reports, and books, the information in this chapter likely still does not represent a complete and exhaustive list of Canadian cases given the lack of a centralized reporting of rabies prior to 1925, when it became mandatory in Canada to report cases of certain diseases, such as rabies. Furthermore, reported human cases could not always be confirmed. Examples of reported cases where specific information could not be located include the 1925 case in Saskatchewan, several cases appearing in federal reported case lists for Quebec in 1929, and the Quebec case in 1933. The lack of information about these cases could be attributed to changes in diagnosis or an inability to find the archived reports. In addition, changes in case definitions or case criteria could also affect whether a case was included in official case counts or not, such as a 1964 case involving an Alberta man who contracted rabies in Arizona and died there (Varughese, 1983). The case is included in some federal case counts, but then subsequently disappears from later case counts. It is worth noting that human rabies case numbers for Canada reported by several authors differ from those reported in this chapter, perhaps because of reporting errors or difficulties in accessing or verifying archived data. For example, one author found 24 cases of human deaths between 1924 and 2010, and 10 cases between 1924 and 1929 (Varughese, 1983; see Chapter 5). However, in perusing archived newspaper 49

The Basics of Rabies in Canada

reports, the authors of this chapter found 25 cases and 10 cases in the same time frames. Between 1925 and 1967, another author reported 19 cases (Singleton, 1969) while the authors of this chapter found 18. The cases of human deaths from rabies discussed in the previous section were presented in chronological order and were grouped in time periods representing important events in the evolution of rabies management in Canada, which, in turn, influenced rabies reporting and rabies incidence. Hence the following discussion follows the same structure.

the movement of dogs from the United States (see Chapter 2) into Ontario, Quebec, and Saskatchewan. In 1895, the cost for a minimum treatment of 15 days at the Pasteur Institute in New York is reported to have been $200 with an additional $50 charged for board (“Reports of Societies,” 1895). In 1897, the estimated cost for Canadians receiving treatment in New York was $5,000 to $6,000 (“Don’t Shoot,” 1898). This probably was an overall figure as the estimate given in 1899 was again $250 per patient (“Will Go to New York,” 1899). In later years, reports cite the following numbers of Ontarians going to New York for treatment: one case in 1906, none in 1907, six in 1908, twenty-two in 1909, and fifteen in the first two weeks of 1910 (“15 Cases,” 1910); a second report for 1910 states 40 patients were treated at the Toronto General Hospital in March 1910 (“Care of the Sick,” 1910) and 61 persons treated in June 1910 (Amyot, 1910), presumably with vaccine imported from New York as a Canadian vaccine was not yet available. Two events in this period vastly improved the management of human rabies cases in Canada: first, the ability to diagnose rabies, and second, the availability of the Pasteur treatment in Canada. From 1909 onwards, rabies could be diagnosed in both humans and animals at the federal laboratory located in Ottawa (see Chapter 20) and at the Ontario Provincial Laboratory located at Queen’s Park, University of Toronto. Diagnostic tests included the identification of Negri bodies in brain tissue and animal inoculation with suspensions of brain material. The federal and provincial laboratories continued to share responsibilities for human and animal rabies diagnoses until 1950 when Agriculture Canada took over human rabies diagnoses from the province (C. Rutty & C. Fehlner-Gardiner, personal communication, 2012). The ability to diagnose rabies was complemented by an improved ability to prevent the onset of clinical rabies in Canada when a supply of Pasteur rabies vaccine produced in Canada became available in 1913. The Ontario Provincial Laboratory, under Dr J. G. Fitzgerald and William Fenton, began producing the vaccine in 1913, with the process then taken over by Connaught Laboratory in 1914 (C. Rutty, personal communication, 2012).

1800–1885 Without a doubt, canine rabies posed a serious threat to human health before the Pasteur treatment became available in 1885 in Europe, and by the early 1890s in the United States. Of 45 cases of human death attributed to rabies in Canada, 32 can be reported as caused by dog bites in the period from the 1800s to 1950, and most of these were the result of exposures to rabid dogs before 1930. This was the result of several factors: the disease was poorly understood, often going unsuspected or entirely unreported; effective options for the prevention of the onset of clinical rabies were not available until the development of Pasteur’s vaccine in 1885; diagnostic tests were not available until the early twentieth century, with diagnosis prior to this being based on a history of a human exposure to a “mad dog”; and outbreaks of rabies were often considered to originate from south of the border, linked to the arrival of miners, hunters, and vacationers from the United States (see Chapter 2; Adams, 1928). With the proximity of Ontario, Quebec, and Saskatchewan to areas of the United States where canine rabies was circulating, these provinces were often the focal points of outbreaks in Canada.

1885–1925 The availability of the Pasteur treatment after 1885 provided hope for some victims of exposures to rabid dogs. Prior to 1913, when Canada started to produce its own rabies vaccine, patients had to travel to the United States for post-exposure prophylaxis, usually at one of the Pasteur Institutes located in New York, Chicago, or at the State University of Michigan (Loir, 1906), and most often at their own expense. In this period, there were numerous outbreaks in Ontario (Provincial Board of Health, 1897; Veterinary Director General’s annual reports, see Chapter 2). Human deaths were still primarily caused by exposures to canine rabies and usually blamed on

1925–1950 The year 1925 saw the implementation of mandatory reporting of certain diseases in Canada and the beginning of annual disease case reports by both federal and provincial departments. From the early nineteenth century, hydrophobia had been the original term of choice to describe the disease but with the advent of standardized disease reporting,

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Human Rabies

this was replaced with the term rabies. In the period between 1925 and 1950, there were a number of human rabies deaths resulting from exposures to rabid dogs. The majority of these occurred during canine rabies outbreaks, which occurred in Quebec and Ontario between 1925 and 1933. In 1927, debates in the House of Commons included discussions of efforts to control rabies outbreaks in dogs. On 28 February 1927, the federal minister of agriculture argued that “the steps being taken in Montreal to enforce the muzzling order against dogs was the only way to eradicate the disease rabies.” Given the number of human exposures and deaths due to the outbreak at that time, he continued: “It was therefore incumbent upon the department to carry out the muzzling order as rigidly as possible” (“140 Cases,” The Globe, 1927, p. 2). In fact, considerable efforts were taken to control the Quebec rabies outbreak. During a meeting in Montreal of the Society for the Prevention of Cruelty to Animals on 8 July 1927, officers stated that some 13,000 dogs had been killed at the Society’s pounds as a result of the outbreak. The outbreak had lasted one year, but had been brought under control (“Over 13,000 Dogs,” The Globe, 1927). In addition, the obligatory muzzling order (“140 Cases,” The Globe, 1927, p. 2) was to remain in effect to prevent a recurrence of the outbreak. In Ontario, the Department of Health had long blamed rabies outbreaks on dogs imported from the United States and had lobbied Agriculture Canada to place an embargo on the dogs. Just across the border from Ontario, in Detroit, Michigan, 265 cases of rabid dogs had been reported in 1927, and 302 cases in 1928 (Adams, 1928), resulting in the death of as many as 10 humans from the bites of rabid dogs. “Surely,” said Dr Godfrey speaking of Case 27, “the authorities at Ottawa will now climb down off their high horse, and do something to prevent further occurrences of this kind” (“Godfrey Criticism,” 1929, p. 3). Yet a subsequent outbreak of canine rabies in Ontario between 1941 and 1946 resulted in one further human death in this period. It should be noted that prior to 1983, national summaries of cases of human rabies in Canada also included a report of a human death due to rabies in Alberta in 1931, but inquiries with the provincial government of Alberta led to the discovery that this report was the result of a coding error in reporting the cause of death (Varughese, 1983), and this case was excluded from subsequent national summaries.

The Veterinary Director General’s annual reports reported cattle, horses, and pigs being placed in quarantine as a result of the rabies outbreak in dogs (Report of the Veterinary Director General, 1909). Larger cities such as Windsor, situated closer to the US border, had by-laws in place to control dogs, sheep, cows, and horses (but not cats) at that time (“Pasteur Treatment,” 1928). With the arrival of rabies diagnoses in wildlife by Plummer (1954), it became evident that rabies was in fact a disease of many wild and domestic species. By the early 1950s, vaccination of domestic animals became possible, and Agriculture Canada embarked on a program of vaccination, especially targeting dogs and cats (see Chapter 35). This interrupted the transmission of rabies from wildlife to dogs to humans; but while protecting the dogs against rabies, it did not prevent other animals from becoming vectors and attacking humans. This was demonstrated in 1959 (Case 31), 1960 (Case 32), and 1964 (Case 33), when exposures to rabid skunks resulted in human deaths from rabies. In 1966, the death of Donna Featherstone (Case 34) was caused by exposure to a rabid cat, which may have become infected as a result of exposure to either a rabid dog or a rabid skunk. It was Donna’s death that finally spurred the Ontario government to initiate a program to control rabies in wildlife. Following a forceful speech by Lieutenant Colonel W. Erskine Johnston, the member of the provincial parliament for Carleton County, the Ontario legislature agreed to “increase funding for rabies control through bounties, and to actively search for new methods to control rabies in wildlife” (Government of Ontario, 1967). This resulted in the immediate transfer of $18,000 to the Department of Lands and Forests, Research Branch, Lab Studies Unit, located in Maple, from the Ontario government. Within a month, the first wildlife rabies control program in Ontario was on the ground in Carleton County around Richmond where Donna had died and where a rabies epizootic was still underway (D. Johnston, personal communication, 6 November 2013). With the exception of two imported human rabies cases in 1984 and 2012, both from the Dominican Republic, the remaining human rabies deaths in Canada since 1967 have been due to exposures to rabid bats, with the first of these occurring in 1977. A comparison of human rabies deaths in the United States and Canada during the period from 1995 to 2011 is revealing. The cases from the United States represent three groups: transplant or donor cases (5 cases), domestically acquired cases (35 cases), and imported cases (11 cases). Imported cases are those where an American

1950–2012 As early as 1910, there had been an awareness of rabies in domestic animals other than dogs and cats in Canada.

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The Basics of Rabies in Canada

patient was infected outside the country and came home for treatment and died. The vast majority of domestically acquired cases were the result of infection with a bat strain of rabies, 18 being from the Eastern pipistrelle/silver-haired bat group (Pipistrellus subflavus/ L. noctivagans), 11 from the Brazilian free-tailed bat (Tadarida brasiliensis), and one each of big brown bat (Eptisicus fuscus), Myotis species, and vampire bat (Desmodus rotundus). All imported cases were from dog bites in different countries (CDC, 2014a). By comparison, Canada had four reported human deaths from rabies in the same time period: three from bats and one, an imported case, in a man likely exposed to a rabid dog in the Dominican Republic (Case 42). The dog virus was typed and found to be a Hispaniola dog/mongoose variant, while the three bat cases included two silver-haired variants and one Myotis species variant, probably from a little brown bat (see Chapter 29; S. Nadin-Davis, personal communication, 2014). Compared with the number of human deaths in Africa and Asia from rabies, those occurring in the United States and Canada are worlds apart. This vast discrepancy in case numbers is certainly the result of a number of contributing factors: successful pet population control programs, rabies vaccination programs in animals and humans, efficient diagnostics, and government resources. But decidedly lower human rabies case numbers in Canada in the 21st century as compared to the United States can be harder to explain. One significant confounding factor in any such comparisons is population size and density. Canada’s population is approximately one-tenth that of the United States, with only a few regions of the country approaching population densities comparable to those found in the United States. Fewer people generally mean fewer domestic animals, including pets, and fewer opportunities to come into contact with rabid wildlife. A paper by Wallace et al. (2014) raises an interesting point with respect to the role that cross-species transmission of the rabies virus from reservoir species such as raccoons and bats to other, non-reservoir species, which appears to accelerate under certain conditions, may play in increasing the risk of human and domestic animal exposures to rabies. Paradoxically, despite the success of US rabies prevention and control programs over the past century, this cross-species transmission risk appears to be increasing in some regions of the United States, and may signal a similar trend in Canada. Applying the lens of cross-species rabies virus transmission to the Canadian context from a historical perspective, since viral variant typing was not routinely

undertaken until the 1980s, the actual sources of human exposures to rabies prior to this period can only be hypothesized. If it is assumed that only canine rabies variants were present in terrestrial species between 1816 and 1928, then the cats that attacked Madame Bruneau (Case 3) and Lorraine Goyeau (Case 25) were likely infected with a canine variant and represented cases of cross-species transmission. The report for Lorraine Goyeau states that someone had seen rabid dogs attacking the cat, thus providing support for the hypothesis that the canine variant was responsible for this case. However, bat variant viruses were almost certainly also circulating at that time and could also have been an alternative source of infection. After pet vaccines became available in the 1950s, canine rabies variants disappeared from Canada, but rabies in wildlife assumed greater prominence in the south of the country as a result of an incursion of the arctic fox rabies variant carried by red foxes. The deaths of Richard Knight in 1959 (Case 31), Barry Montgomery in 1960 (Case 32), and an unnamed girl in 1964 (Case 33) were probably the result of exposures to skunks infected with the arctic fox variant. Certainly, the puppy that bit Montgomery was most likely infected when it was attacked by a skunk. Similarly, in 1967 Donna Featherstone was attacked by her cat (Case 34). Since canine rabies had disappeared from Canada by that point, it is highly likely that Donna died from either the arctic fox rabies virus variant or a bat variant. As Wallace et al. (2014) point out in their paper, when a new rabies virus variant such as the northeastern raccoon strain first becomes established in a region, cross-species transmission rates to dogs and cats increase. While foxes, raccoons, skunks, and bats are responsible for the continuing circulation of rabies virus in the United States, Ontario’s wildlife oral vaccination program has resulted in a drastic reduction in rabies in foxes, although two main wildlife reservoirs, bats and skunks, remain. In addition, Canada has recently acquired a third wildlife rabies reservoir through both the natural spread and anthropogenic translocation of raccoon rabies from the US to Canada, which have occurred with some frequency in the past two decades. While a host shift of the rabies virus to a non-reservoir species is rare, such shifts can and do happen and may lead to new challenges for Canada’s rabies management programs, possibly once again threatening the health and safety of Canadians and their domestic pets with new sources for exposures to rabies.

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Human Rabies

References Africa – Rabies deaths linked to cost of vaccine. (2013, October 10). The New York Times. Retrieved from https://www.nytimes .com/2013/10/11/world/africa/rabies-deaths-linked-to-cost-of-vaccine.html Adams, F. (1928). Rabies in Essex County, Ontario. The Canadian Journal of Public Health, 19(9), 421–425. Amyot, A. J. (1910). Rabies. Paper presented at the Pathological Section of the Canadian Medical Association, University of Toronto, June 2, 1910. Believe rabid skunk caused boy’s death. (1959, November 6). The Globe, 1959. Bell, J. S. (1967). Rabies – Ontario. Epidemiological Bulletin, 11(2), 7. Bitten by husky, Chapleau child dies in hospital. (1931, April 17). The Globe, p. 13. Blaisdell, J. D. (1992). Rabies and the governor-general of Canada. Veterinary History, 7(1), 19–26. Blame death on rabies. (1960, February 20). The Toronto Daily Star, p. 8 Breault, H. J. (1944). Hydrophobia. The Ontario Medical Review, 11(5), 170–177. Care of the sick after they leave hospital. (1910, April 7). Toronto Daily Star, p. 8. Centers for Disease Control and Prevention. (2014a). Rabies around the world: Cost of rabies prevention. Retrieved from http://www .cdc.gov/rabies/location/world/index.html Centers for Disease Control and Prevention. (2014b). Human rabies – Human rabies surveillance. Retrieved from http://www.cdc.gov /rabies/location/usa/surveillance/human_rabies.html Centers for Disease Control and Prevention. (2017). Human rabies. Retrieved from https://www.cdc.gov/rabies/location/usa /surveillance/human_rabies.html Chaffey, P., & Binney, J. (1964). Rabies, a case presentation and discussion. McGill Medical Journal, 33(1), 27–37. Connon, J. (1974). Elora: The early history of Elora and vicinity. Waterloo, ON: Wilfrid Laurier University Press. (Original work published in 1930) Davidson, W. G. (1970). A fatal case of rabies in a boy bitten by a bat – Saskatchewan. Epidemiological Bulletin, 14(12), 95. Death from hydrophobia. (1862). British American Journal, 3(6), 188–189. Dempster, G., Grodums, E. I., Bayatpour, M., & Zbitnew, A. (1972). A human case of unsuspected rabies in Saskatchewan diagnosed by virus isolation. Canadian Journal of Public Health, 63(3), 215–218. Died from hydrophobia. (1926, October 20). The Montreal Gazette, p. 5. Died of hydrophobia. (1891, November 18). The Globe, p. 2. Dies from hydrophobia. (1896, March 9). The Globe, p. 7. Dies from hydrophobia, month after dog bite. (1916, January 24). The Globe, p. 9. Don’t shoot the dog. (1898, March 15). The Globe, p. 12. Editorial. (1892, March 30). The Globe, p. 1. Editorial. (1897, June 5). The Globe, p. 1. Editorial. (1910, March 2). The Globe, p. 6. Editorial. (1912, January 5). The Globe, p. 7. Editorial. (1913, January 18). The Globe, p. 18. Elmgren, L. D., Nadin-Davis, S. A., Muldoon, F. T., & Wandeler, A. L. (2002). Diagnosis and analysis of a recent case of human rabies in Canada. The Canadian Journal of Infectious Diseases, 139(2), 129–133. http://doi.org/10.1155/2002/235073 Epidemic of rabies serious in Montreal. (1926, July 15). The Globe, p. 2. Fehlner-Gardiner, C. (2013, October). Rabies in Canada – 2012. Presentation to the annual Rabies in the Americas meeting in Toronto, Ontario. 15 cases since new year. (1910, February 9). Toronto Daily Star, p. 1. Fitzgerald, J. G. (1914). A fatal case of rabies in a child. Canadian Journal of Medicine and Surgery, 36(6), 245–247. Foley, A. R. (1964). Rabies – Québec. Epidemiological Bulletin, 8(4), 25. Godfrey criticism on rabies outbreak refuted by Ottawa. (1929, October 23). The Globe, p. 3. Government of Ontario. (1967). Debates and proceedings of the fifth session of the 27th legislature of the province of Ontario, January 25 to June 15, 1967. Speaker: W. Erskine Johnston (P.C. Carlton). Ottawa, ON: Author. Retrieved from https://archive.org/details /v2hansard1967ontauoft/page/2494 Hodgetts, C.A. (1910). Letter to the editor. Canadian Journal of Medicine and Surgery, 27(3), 240–241. Hydrophobia. (1816, March 21). Québec Gazette, pp. 2–3 Hydrophobia at Dawson – Clear case of death from this disease. (1901, May 3, p. 5). The Globe. Johnston, W. (1893). Coroner’s quest: Law in the province of Québec. Read before the Medico-Legal Society, Montreal, May Session, p. 4. Johnstone, J., Saxinger, L., McDermid, R., Bagshaw, S., Resch, L., Lee, B. ... Franka, R. (2008). Human rabies – Alberta, Canada, 2007. Morbidity and Mortality Weekly Report, 57(08), 197–200. Retrieved from https://www.cdc.gov/mmwr/preview/mmwrhtml/mm5708a1.htm

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The Basics of Rabies in Canada King, D. B., Sangalang, V. E., Manuel, R., Marrie, T., Pointer, A. E., & Thomson, A. D. (1978, April 1). A suspected case of human rabies – Nova Scotia. Canada Diseases Weekly Report, 4(13), 49–50. Retrieved from http://publications.gc.ca/collections/collection_2016 /aspc-phac/H12-21-1-4-13.pdf Lessard, R., & Tésio, S. 2008. Les enquêtes des coroners du district de Québec, 1765–1930, une source en histoire médicale et sociale canadienne. Canadian Bulletin Medical History, 25(2), 433–460. https://doi.org/10.3138/cbmh.25.2.433 Loir, A. (1906). La rage au Canada. L’Union Medicale du Canada, 35(12), 683–694. Mad dog’s bite blamed for hydrophobia death. (1927, November 14). The Globe, p. 2. Mad dogs – Hydrophobia. (1814, August 11). Québec Gazette. McCrea, J. (1883). On the treatment of hydrophobia. The Canada Lancet, 15(8), 231–232. McLean, A. E., Black, W. A., Kettyls, G. D., Johnstone, T., Webster, A., & Gregory, D. (1985). A human case of rabies – British Columbia. Canada Diseases Weekly Report, 11(51), 213–214. Retrieved from http://publications.gc.ca/collections/collection_2016/aspc-phac/H12-21-1-11-51.pdf Mclean, D. M., Krause, V. W., Wilson, W. M., & Hawke, W. A, (1960). Rabies following skunk bite. Canadian Medical Association Journal, 82, 315–317. Mitchell, C. A. (1967). Rabies in Québec City, case report of 1839. Medical Services Journal, Canada, May, 809–812. 140 cases of rabies under treatment. (1927, February 28). The Globe, p. 2. Ottawa girl, 4, dies from rabies 3 months after stray cat’s attack. (1967, January 16). The Toronto Daily Star. Over 13,000 dogs killed during rabies epidemic. (1927, July 9). The Globe, p. 1. Parker, R., McKay, D., Hawes, C., Daly, P., Bryce, E., Doyle, P., ... Naus, M. (2003). Human rabies, British Columbia – January 2003. Canada Communicable Disease Report, 29(16), 137–138. Retrieved from http://publications.gc.ca/collections/Collection/H12-21-29-16.pdf Pasteur treatment ordered at Windsor following cat bite. (1928, July 28). The Globe, p. 1 Picard, A.-C. (1984). Human rabies acquired outside of Canada – Québec. Canada Disease Weekly Report, 10(45), 177. Public Health Ontario. (2012). Rabies. Monthly Infectious Diseases Surveillance Report, 1(10), 1–4. Plummer, P. J. G. (1954). Rabies in Canada, with special reference to wildlife reservoirs. Bulletin World Health Organization, 10, 767–774. Provincial Board of Health. (1897). Report of the committee on epidemics, on rabies (pp. 71–72). Sixteenth Annual Report of the Provincial Board of Health of Ontario. Toronto: Warwick Brothers & Rutter. Available at https://archive.org/details /ontariodepthealth1897ontauoft Quarantine U.S. dogs suggests Dr. Godfrey. (1926, January 29). The Toronto Star, p. 3. Rabies, a deadly viral disease. (2013). Pathogens and Global Health, 107(7), 337. https://dx.doi.org/10.1179%2F2047772413Z .000000000171 Rabies contracted by another woman. (1927, November 21). The Globe, p. 21. Rabies diagnosed in Toronto man. (2012, April 16). CBC News. Retrieved from https://www.cbc.ca/news/canada/toronto /rabies-diagnosed-in-toronto-man-1.1175985 Rabies possible cause of death. (1929, July 5). The Montreal Gazette, p. 14. Report of the veterinary director general for the year ending March 31, 1909. (1909). Ottawa, ON: Department of Agriculture. Available from Library and Archives Canada, https://bac-lac.on.worldcat.org/oclc/29657040 Reports of Societies, the Provincial Board of Health. (1895). Dominion Medical Monthly, IV(4), 91–95. Singleton, J. R. (1969). The history of rabies in Canada. The State Veterinary Journal, 24(72), 205–209. Steps taken to prevent rabies outbreak in Montreal. (1926, March 6). The Globe, 1926, p. 2. Turgeon, N., Tucci, M., Teitelbaum, J., Deshaies, D., Pilon, P. A., Carsley, J., ... Wandeler, A. (2000). Public health dispatch – Québec, Canada, 2000. Morbidity and Mortality Weekly Report, 49(49), 1115–1116. Retrieved from https://www.cdc.gov/mmwr/preview /mmwrhtml/mm4949a4.htm Varughese, P. (1983). Rabies in Canada. Canada Diseases Weekly Report, 9(35), 137–140. Victim of hydrophobia succumbs in Montreal. (1926, October 20). The Globe, p. 3. Wallace, R. M., Gilbert, A., Slate, D., Chipman, R., Singh, A., Wedd, C., & Blanton, J. D. (2014) Right place, wrong species, a 20-year review of rabies virus cross species transmission among terrestrial mammals in the United States. PLOS One, 9(10), e107539. https:// doi.org/10.1371/journal.pone.0107539 Webster, W. A., Casey, G. A., Charlton, K. M., & Picard, A.-C., & McLaughlin, B. (1985). Human rabies acquired outside of Canada. Canada Disease Weekly Report, 11(4), 13–14. http://publications.gc.ca/collections/collection_2016/aspc-phac/H12-21-1-11-4.pdf Webster, A., Casey, G.A., Charlton, K. M., Sayson, R. C., McLaughlin, B., & Noble, M. A. (1987). A case of rabies in Western Canada. Canadian Journal of Public Health, 78(6), 412–413. Will go to New York. (1899, August 29). The Globe, p. 9. World Health Organization. (1966). WHO Expert Committee on Rabies, fifth report (Technical Report Series No. 321). Geneva: Author. World Health Organization. (2013). Rabies [Fact sheet #99]. Retrieved from http://www.who.int/mediacentre/factsheets/fs099/en/ Zoonoses – Rabies. (1978). Canadian Veterinary Journal, 19(6), xviii.

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PART 2

The Role of Federal Agencies in Rabies Management

Overview The chapters in Part 2 discuss the roles of the two major federal agencies that have been involved in rabies management: Agriculture Canada (AgCAN), now known as the Canadian Food Inspection Agency (CFIA), in Chapter 4, and Health Canada (HC), now known as the Public Health Agency of Canada (PHAC), in Chapter 5. The goal is to show how the cooperation between them has influenced what is known about rabies and how Canada managed the disease. AgCAN/CFIA has been involved in field activities, surveillance, specimen collection, laboratory diagnosis, data collection, import and export of animals, and vaccines. HC/PHAC has been involved in human health and safety. Woven into the discussion are references to the third federal agency that has played an important role in rabies management in Canada. The Royal Canadian Mounted Police (RCMP) has had a close working association with AgCAN, dealing with collecting specimens and transporting them to the laboratories of CFIA and dog control activities, including vaccination in provinces and territories where the RCMP has operated as a provincial or territorial police force as well (the west, the north, and Maritimes).

4 The Federal Department of Agriculture David J. Gregory Canadian Food Inspection Agency (Retired), Ottawa, Ontario, Canada

Hydrophobia and mad dogs ... This case is attested by two eminent physicians, and they add that “hydrophobia” is without the hope of a relief from medicine. We know of no cure for hydrophobia. This is a frank confession, and I have scarcely a doubt accords with the truth – It is a disease, which, when once having arrived at that pass as to show itself by the usual symptoms in the system, baffles equally the skill of the most learned physician and the nostrums of the boldest empyrick ... It is not so rapid in its progress, but that it may be arrested and entirely counteracted and prevented if proper measures are reasonably resorted to, duly administered, and faithfully persisted in. These means nature has provided in the plant called the Scullcup, which grows almost everywhere in abundance in our country ... that particular one called in Latin Scutellaria latiflora, or side-bearing flower and not that one called Scutellaria galericulata or helmet shaped. The former of these is efficacious in preventing this incurable disease, the latter is not. – “Hydrophobia” (1819, p. 3)

Introduction Early settlers to Canada were hunters and gatherers. With the arrival of American settlers and those from the British Isles in 1815, the human and animal populations increased, people began to urbanize and farms concentrated on growing crops and raising livestock to sustain the increasing population. By 1861 the census covering Upper and Lower Canada, New Brunswick, and Nova Scotia indicated a

human population of just over three million people and an animal population of over 700,00 horses, over 250,000 cattle and oxen, two million sheep, and more than one million swine (Sayers, 1983, p. 262). The beginnings of veterinary medicine were associated with this move towards agriculture. Medical treatment for animals was primitive, and the need for veterinary services increased as animals transported from Europe by ship and then across the continent by rail increased the vulnerability of livestock to diseases. The value placed on Canadian livestock by the veterinary director general (VDG) in his annual report for 1903 amounted to $1,040,410,916.47 (equal to over $22 billion today), which included horses, cattle, sheep, and swine (Report of the Veterinary Director General, 1904, pp. 1–103). The control of contagious and infectious diseases in people and livestock became a priority to ensure their health, for the sake of their survival.

Agriculture Canada before 1900 The first legislation affecting animals was passed by the Government of Upper Canada in 1803, the Act to restrain the custom of permitting horned cattle, horses, sheep and swine to run at large. This Act applied to the larger towns of York (now Toronto), Niagara, and Kingston, without the benefit of the veterinary profession being mentioned. This Act marked the beginnings of livestock control. An Act in 1805 regulated the curing, packing, and inspection of beef and pork to allow for them to move from Upper Canada to Lower Canada, which already had such

The Role of Federal Agencies in Rabies Management

legislation in place (Dukes & McAninch, 1992, p. 58). This was the start of meat inspection for foreign trade. In 1852 the Bureau of Agriculture was set up in TroisRivières, Quebec, a move to organize nationally. By 1865 the Bureau of Agriculture and Statistics had reorganized into the Department of Agriculture and Immigration and moved to Ottawa. The few veterinarians in Canada at this time were graduates of London or Edinburgh University in Britain. By 1807 the fledging department had 27 employees (Health of Animals Branch, 1978). For example, the only veterinary surgeon in the new colony of New Brunswick in 1851 was M. A. Cuming of Saint John, who graduated from Edinburgh University in 1846 (Dukes & McAninch, 1992). The first giant step towards disease control came in 1865 with an Act by the assembly of Upper and Lower Canada to control the importation of animals to prevent the introduction of disease (Dukes & McAninch, 1992, p. 58). Following Confederation in 1867, the Department of Agriculture was officially established in 1868, and an Act of Parliament respecting Contagious Diseases of Animals was passed in 1869, the first agricultural legislation in New Canada and the forerunner of today’s Animal Disease and Protection Act, which in turn led to the start of the Health of Animals operations (Health of Animals Branch, 1978, p. 16). This Act was ineffective because of the lack of trained veterinarians and the absence of quarantine stations. Dr Duncan McEachran, recognizing the need for a veterinary college in Canada, started by teaching short courses on veterinary subjects to agricultural students in 1862. This led to the formation of the Upper Canada Veterinary College, which later became the Ontario Veterinary College, graduating three veterinarians in 1866. A more complete history of the founding of the Ontario Veterinary College and the Ontario Veterinary Association (incorporated in 1879) can be found in Evans and Barker (1976). Dr McEachran founded the Montreal Veterinary College in 1866, and in 1889 this became part of McGill University, as the Faculty of Comparative and Veterinary Science. Following a number of representations to the Canadian government by Dr McEachran, the first quarantine station in Canada was established at Point Levis, Quebec, in 1876 and in 1882, a second quarantine station at Point Edwards, Sarnia (Dukes & Labonte, 1991). The Act was amended in 1879 to add compulsory control measures. With the increase in the numbers and value of the flocks and herds, the Act became unwieldy and on 13 August 1903, the Animal Contagious Diseases Act was approved by Parliament (Dukes & McAninch, 1992). The “proper organisation” and responsibilities of the department were outlined by an Act in 1867 approved by the

first minister of agriculture, the Honourable Jean-Charles Chapais (Dukes & McAninch, 1992, p. 58). These responsibilities included agriculture; immigration/emigration; public health and quarantine; the Marine and Emigrant Hospital in Quebec; arts and manufactures; census and statistics and registration of statistics; patents and inventions; copyright, industrial designs, and trademarks; and “any other duty or power assigned by the Governor-in-Council” (Dukes & McAninch, 1992, p. 58) – an almost impossible task at the time! As an example of its public health responsibilities, in 1900, Dr Higgins, a veterinary pathologist, was sent to Williams Head in British Columbia to establish a laboratory to deal with the large numbers of Japanese and Chinese immigrants who might be infected with the bubonic plague bacillus, Pestis bubonica, public health being a responsibility of the Department of Agriculture. His responsibility was to identify the organism and then prepare an “immunizing substance” (Sayers, 1983, p. 264). Until the passage of the Animal Contagious Diseases Act in 1869, little action was taken by the Dominion Department of Agriculture to control rabies. Lack of personnel and the training of staff prevented all but half-hearted attempts at dog control and muzzling. This was a time of “dog beware” – the dog that looked “mad” was often shot (“Epidemics of Rabies,” 1901, p. 11). The townships of Ingersoll and Woodstock were accused of “exterminating the canine race” (“Hamilton to Be a Dogless Town,” 1909). For humans it was a time of wait and see, cauterize your wounds with fuming nitric acid or silver nitrate, or try the Scullcap treatment (S. lateriflora, a relative of the mint family that is used dried, in tinctures and tea form) (“Hydrophobia,” 1819, p. 3). An Act in 1845 in Lower Canada allowed for confinement of the biting or bitten canine for 40 days (Dukes & McAninch, 1992, p. 58). By 1897 treatment of humans with rabies vaccine was a reality and available at the Pasteur Institute in New York. While the histopathologic signs of rabies were known and a definitive diagnosis required animal inoculation, patients could go to New York for immediate treatment. At this time, the municipality in Ontario paid for the treatment expenses. The development of the Negri body staining diagnostic test for rabies would have to wait until 1905.

Agriculture Canada, 1900–1925 The Animal Contagious Diseases Act, 1869 was revised a number of times: 1903, 1906, 1927, and 1952, and was replaced by the Animal Diseases and Protection Act in 1977

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The Federal Department of Agriculture

commissioner of the NWMP, A. Bowan Perry, in Regina, Assiniboia, commanded 11 veterinary inspectors. It is thought that these officers became the inspectors for the branch, the first in Alberta at Medicine Hat. The Dominion Service moved to Ottawa in 1902 and was reorganized by the first director general, Dr John Gunion Rutherford (VDG from 1902 to 1912), into the Health of Animals Branch, comprising the Contagious Diseases Division and the Pathological Division. Rutherford had recognized the need for veterinary preventive medicine in his report as VDG, saying, “The great economic value of veterinary preventive medicine is receiving each year more full and appreciative recognition ... and our service efficient” (Report of the Veterinary Director General, 1904, pp. 3–26). The branch dealt mainly with cattle and equine diseases until 1905 when rabies became a reportable disease, diagnosis more reliable, and human treatment more available. The development of laboratories and testing methods for rabies in Canada can be found in Chapter 20. Until 1925, there was a continuing movement to upgrade the university courses to produce better qualified veterinarians. In his report summarizing 1905, Rutherford stated, “The Importance of the Dominion having a thoroughly organized and competent staff of Veterinary inspectors cannot be overestimated” (Report of the Veterinary Director General, 1906). The course at the Ontario Veterinary College was producing graduates following a two-year program, often with little basic skills of reading and writing. These veterinarians were not recognized as qualified in the United States. Gradually a three-year course was introduced with entrance requirements. The college was graduating about one hundred veterinarians a year at this time. Many of these moved west, some joined the war effort, and many augmented the Department veterinary personnel in the provinces (Barker, 2006). With the influx of immigrants and their livestock from the United States into Canada, the need to control contagious diseases became more evident. For control to succeed, more veterinarians needed to be employed, quarantine stations established, and good research facilities developed. The above need had been recognized by Dr Rutherford as far back as 1906 in his annual report of that time. To this end, the Animal Diseases Research Institute in Hull was built in 1927. Other research facilities followed later. Salaries paid to inspectors were low and did not attract graduates to the department: “It is a notorious fact that the public service is anything but generous to its professional personnel; it is for this reason that Governmental and civic positions are often regarded merely as a training ground for

(Dukes & McAninch, 1992). Following an amendment to the Act in 1990, it became known as the Health of Animals Act. In 1885 rabies had been included in a list of 13 diseases named under the original Act (Dukes & McAninch, 1992) and by an Order in Council on 10 August 1905 (Report of the Veterinary Director General, 1905, pp. 55–56). Through the Animal Contagious Diseases Act of 1903 (Statutes of Canada, 1903), regulations to control canine rabies were enacted. This meant that all cases of suspected rabies had to be reported and investigated, and control measures had to be implemented. Negri body detection for rabies diagnosis was a reality by this time, and human treatment with rabies vaccine was more readily available. In the 1905 rabies incident, which led to regulations for rabies, veterinary inspectors were instructed to cooperate with city authorities and the local board of health in their control measures. Ottawa, in 1910, imposed fines of $260 under the federal Act for loose dogs and $20 under the Provincial Health Act. Many of the early graduates of the veterinary schools in Quebec and Ontario travelled west and worked for the Royal North West Mounted Police (NWMP), licensed under the Veterinary Surgeons Act of the North-West Territories (NWT), as they were then called (Butts, 2006; Barker, 2006). In 1867 the Dominion of Canada had acquired the NWT, including Alberta, from the Hudson’s Bay Company. Alberta was created by joining the District of Alberta with the Districts of Athabasca and Assiniboia and part of Saskatchewan in 1905. Saskatchewan also became a separate province in the same year. The NWMP had been formed to police the NWT in 1873 (Collections Canada, 2012) and became the arm of the federal government responsible for the enforcement of disease control in domestic animals arriving with settlers from the United States. While the NWMP dealt with the health of their own horses and the imported cattle from the United States, they were involved with dog control during rabies outbreaks in Yukon and the NWT. During the 1901 rabies outbreak in Yukon, the NWMP impounded loose dogs, and citizens were allowed to shoot dogs showing signs of “madness.” Since most outbreaks of rabies at this time involved dogs, they suffered the most. Each outbreak brought out newer, more stringent local regulations: no dogs at large, quarantines or chained for two months or muzzled with metallic guards, indiscriminate population control, and fines. The veterinary director general’s annual report of 1903 (Report of the Veterinary Director General, 1904) lists one inspector and eight veterinary staff sergeants working in the NWT as NWMP members for the branch as far up as Yukon. The first NWMP officers arrived in Fort Calgary in 1875. The

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at this time. Dr Orlan Hall, Health of Animals Branch, Ottawa, stated that “rabies in Canada was controlled entirely through quarantine restrictions. Once diagnosed, the disease was promptly suppressed” (Hall, 1940, p. 148). At that time rabies was thought to be restricted to canines only. Vaccination of pets would follow later. The Health of Animals Branch came into being following a reorganization of the Dominion Service in 1902, and it remained essentially the same for the next 80 years. In 1937 the Branch became the Health of Animals Division under the Production Service (later the Production and Marketing Branch). The veterinary laboratory section went to the Science Service (now Research Branch) as the Animal Pathology Division. By 1953 the laboratories returned to the Health of Animals Division and in 1963, under a reorganization, the division became the Health of Animals Branch once more (Dukes & McAninch, 1992, p. 59). Part of the reason for the return of the Animal Pathology Division to the Health of Animals Division had to do with the foot-and-mouth disease outbreak in Saskatchewan in 1952. At that time the laboratories were associated with the Science Service and not readily available to assist the Health of Animals staff with the outbreak. Dr Walter A. Moynihan was responsible for developing and coordinating these three divisions in 1966.

Figure 4.1: Health of animals inspector’s badge of office. Source: Property of David Gregory.

recent graduates, who depart to richer fields just as soon as an opportunity presents itself ” (Allen, 1922, p. 134). Evans and Barker (1976) quote from an advertisement for veterinary inspectors from 1920: “The initial Salary for the position of Veterinary Inspector is $1,800, and if service is satisfactory a yearly increase is granted until the maximum of $2,400 is attained. Further promotion may then take place to the position of District Veterinary Inspector or of District Supervisor of Meat Inspection” (p. 149). An inspector’s badge of office is shown in Figure 4.1.

Agriculture Canada, 1950–Present While rabies is a reportable disease under the Animal Contagious Diseases Act of 1905, it is also reportable under regulations in all provinces and territories, allowing them to augment rabies control over and above that under federal regulation. For example, during the 1952 rabies outbreak in Alberta, a Central Rabies Control Committee was formed to coordinate the efforts of control by all agencies in the province (see Chapter 7). In 1953 all dogs in Alberta were under quarantine and all were licensed and registered, with destruction of strays, compulsory vaccination, diagnosis, restraint, and muzzling. Depots had been set up to store specimen cans, and the province expended a lot of time and resources in communications. During this period a wildlife depopulation program was put into place. Between 1952 and 1956, 55,889 foxes, 53,364 coyotes, 10,044 lynx, 5461 wolves, and 4130 bears were eliminated. The result was an increase in the moose and deer populations (Ballantyne, 1957, p. 89). Wildlife depopulation programs occurred also in Quebec, Ontario, and Saskatchewan, usually with limited

Agriculture Canada, 1925–1950 Throughout most of its history, the branch consisted of three main divisions: the Contagious Diseases Division, with a regulatory role concerned with eradication and control of major diseases; a Meat Inspection Division, with a meat inspection role concerned with food safety; and an Animal Pathology Division, with a laboratory role concerned with biological product production, diagnostic capability, and research. Quarantines were an integral part of the department’s regulatory disease control strategy. All animals coming into Canada were inspected at its borders and if dictated, quarantined at stations like the one at Point Lévis, ­Quebec. Quarantine was a major component of rabies control

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success unless combined with other actions, such as wildlife vaccination. Those actions also inflamed public opinions and lead to responses such as the following letters to the heads of thee Ontario Veterinary College in 1959:

aimed to supplement the owner for their losses from rabies in domestic livestock, as well as encourage the reporting of rabies in their animals so that preventive action could be taken by the branch veterinarians. The branch would reimburse the owner 40% of the maximum benefit which worked out to cattle, $100; horses, $40; sheep, $16; swine, $16; and goats, $16. This was approved on 8 March 1961 and was retroactive to July 1960. On 1 January 1963 Quebec signed the agreement, followed by Manitoba and New Brunswick. No indemnity would be paid under the Animal Contagious Diseases Act unless death from rabies was certified by a veterinary inspector. One of the arguments for the initiation of indemnity payments by the branch at the time was that it would not cost more than $2000 per year. Later, as the indemnity payment per animal was increased, and the number of animals affected increased, the cost to the branch increased (see Chapter 31 for program operation and Chapter for program costs). The amount paid out in 1989 was $134,009.50 for 462 animals (Agriculture Canada, 1990, p. 13). Today, New Brunswick is not part of the program, and payments are authorized by the Canadian Food Inspection Agency (CFIA) area office for the region.

When do you think you will quit kidding the public about this RABIES BALLYHOO? We know there is no such thing as rabies, and you will never convince us otherwise. What gives? Is this just an excuse to exterminate foxes on account of protection for the hunters of game birds? We never know what you are up to! Send your own heads for examination! (C. D. B., 1959)

Note that C. D. B. refers to the author’s initials only, no surname was given. Five days later the same author wrote: This is a screwy world! This “rabies racket” has cost the taxpayers plenty! It has made a million dollars for the vets and doctors throughout the Dominion and has been responsible for the massacre of our wildlife. (C. D. B., 1959)

Rabies Vaccination

Organizational Changes

Rabies control efforts had changed little from 1905: reporting of incidents, investigation. and dog control measures. However, in 1953, a new dimension was added to these control efforts. The canine rabies vaccine became available from Connaught Laboratories in Toronto (see Chapter 15b), and free vaccination clinics became an integral part of the branch’s control efforts. This was an important step with the rabies outbreaks originating in the north. Dr Ross Singleton, district veterinarian in 1952 for Swan River, Manitoba, was one of the first veterinarians to use this vaccine on dogs in northern Manitoba to control rabies (J. R. Singleton, personal communication, 26 N ­ ovember 2010). It became standard practice for the Royal Canadian Mounted Police (RCMP) to vaccinate dogs in the NWT with vaccine approved and supplied by the branch.

It is said that change is a consistent part of history. The Health of Animals Division has seen many changes and has learned not to repeat past mistakes, to its benefit. While the Health of Animals Division became known as the Health of Animals Branch in 1963, change dictated that the branch head change from veterinary director general to assistant deputy minister. Other title changes included sub-districts and sub-district veterinarians becoming districts and district veterinarians, and districts and district veterinarians becoming regions and regional officers (Reid, 1992). Administratively, the department became known as Agriculture Canada. Change came again in 1979, with the Contagious Diseases, Meat Inspection, and Animal Pathology divisions becoming the Animal Health, Meat Hygiene, and Animal Pathology directorates. Later, the Health of Animals Branch combined with elements of the Production and Marketing Branch to form the Food Production and Inspection Branch. The Animal Health and Meat Hygiene directorates were each divided to create a national headquarters group or division responsible for program planning and regional groups that formed the Veterinary Inspection or Operations Directorate responsible for program implementation. This was followed by the Animal Health and Animal Pathology divisions amalgamating to form the Health of Animals Directorate (Reid, 1992).

Indemnity Payments Before 1960 the Province of Ontario paid an indemnity to owners for loss of their livestock in some parts of the county or municipality. This practice was discontinued by Ontario on 30 June 1960 with the suggestion that the federal government should pay part of the loss (K. F. Wells, VDG, to Dr S. C. Barry, deputy minister of agriculture, personal communication, 9 March 1961). The program

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The Role of Federal Agencies in Rabies Management

More recently, the Animal Pathology Division was renamed the Health of Animals Laboratory Division to place an emphasis on health rather than on disease and more closely identify the division with the Health of Animals Directorate whose needs it services. To reduce the number of senior managers, the headquarters staff of the operational directorate were disbanded, and the regional heads once again report to the branch head. The four Atlantic provinces combined administratively into one region, and Manitoba and Saskatchewan combined as one. From a veterinary point of view, these changes meant that the officer responsible for veterinary programs at the regional and branch head levels might not be a veterinarian. The brucellosis eradication programs (1957 and 1985) significantly increased the numbers and use of lay inspectors in the animal health programs, called primary products inspectors (PPIs) (Reid, 1992). Many district offices (Figure 4.2) had at least one PPI on staff and clerical staff to manage the needs of the

office. While the PPI need originated with the brucellosis eradication program, these personnel also became part of the tuberculosis eradication program and involved in other programs, such as specimen collection of rabies specimens and vaccination clinics for dogs (see Chapter 31).

Improving Disease Reporting Through its mandated disease control programs of quarantines, testing, and eradication for many of its reportable diseases, from the 1900s through to the present time, Canada’s animal health status has become one to be envied and copied around the world. On 7 March 1959, Canada officially became the 63rd member of the veterinary medical world organization for animal health known as the Office International des Epizooties (OIE). The OIE came into existence on 15 June 1924, and in May 2003 became known as the World Organisation for Animal Health but kept its

Figure 4.2: Agriculture Canada’s regional, district and laboratory offices, in 1990. Source: Agriculture Canada (1990).

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The Federal Department of Agriculture

acronym of OIE. In 2011 the OIE had 178 members and served as a reference centre for the World Trade Organization (WTO). The OIE collects and analyses the latest scientific information on animal disease control and makes these data available to all its members. Rabies is included in the list of diseases that Canada reports to the OIE annually or as necessary. Through the earlier years, disease reporting was more often collection by rote but eventually included the location, date, and species. After 1926 reporting became annual (fiscal year) by necessity, and location was reported by province (and the Northwest Territories, until 1950, when rabies was first reported in the Arctic) and county. As more became known about diseases and their different strains, the need to report the location of cases more precisely for disease investigation and control became paramount. In 1977 the Health of Animals Division introduced “the nearest town” location code to increase the spatial resolution of rabies reporting. A codebook of nearest towns to a submitted specimen provided an alphanumeric location indicating the province, county, township, and nearest town within the township (Tinline & Gregory, 1988). While it was an important step in improving rabies reporting, the code system was scrapped because of high error rates in identifying the nearest town (see Chapter 21). The development and introduction of a new laboratory sample control system (LSCS) in 1985, which allowed for computer tracking of specimen submissions to the laboratory, coupled with the redesign of the rabies specimen reporting form, provided the opportunity for the division to introduce an improved location code system. By 1987 this new system, the Universal Transverse Mercator code (UTMC) had been implemented and allowed for computer analysis and mapping of specimens to within one hundred metres anywhere in Canada that was covered by the National Topographical System of 1:50,000 maps (see Chapter 21). More importantly, the code was intended to assist the rabies control efforts in Ontario that were scheduled to be implemented in 1989. Today, this system has been replaced by latitude–longitude references obtained from handheld GPS units or online maps such as Google Earth.

with a president at its head and responsible to the minister of Agriculture and Agri-Food Canada, most services provided before without cost now became potentially cost recoverable. This affected a number of services associated with inspection, such as importation and exportation. This was an effort to offset the decrease in resources allocated by the government to the department and to make the agency more fiscally independent. Rabies and other reportable disease programs were exempt. The CFIA’s involvement in the rabies control program continued to be mandated and regulated by several sections of the Health of Animals Act, the Health of Animals Regulations, the Reportable Disease Regulations, and the Rabies Indemnification Regulations. The objective of the program is to prevent the transmission of rabies from domestic animals to humans. The CFIA meets this objective by carrying out the activities described in the Disease Control Manual, Section 14, Rabies. While the regulations are specific to domestic animals only, the CFIA has contributed for a number of years to the Ontario rabies control program involved with the control of rabies in wildlife (see Chapters 10, 11, 12, and 13). With the use of an oral vaccine baiting program, the number of cases of rabies in wildlife has dropped significantly, resulting in less contact of rabid animals with domestic animals and fewer cases of contact with humans. While contributing financially to the wildlife baiting program, the development of new vaccines, and diagnosis, CFIA’s Biologics Section (see Chapter 16) has  been responsible for the licensing of these wildlife rabies vaccines. The main elements of the CFIA’s rabies control program continue to be (1) the investigation of all rabies suspect cases in domestic animals, with human exposure reported to the public health authorities; (2) the quarantining of all domestic animals suspected of being exposed to a confirmed or suspected rabid domestic or wild animal; (3) the collection of samples for rabies diagnosis from all suspect animals, domestic or wild; (4) the transportation of the specimens to federal laboratories for diagnosis; and (5) the reporting to the appropriate authority. Vaccination of domestic pets is the responsibility of veterinary practitioners and their associations, with the exception of some vaccine shipped to Nunavut for use by the RCMP. Except in Quebec, all dog bite reports are investigated by the provincial and territorial authorities and the appropriate action is taken. As of 1 April 2014, the CFIA withdrew from most field activities concerned with rabies control, handing them over to the provincial and territorial agencies. However, the diagnostic capability and data recording remains with the CFIA Laboratories in Nepean and Lethbridge (see Chapter 20). The number of district offices has decreased under the new program with this reorganization (see Chapter 31).

The Agency (CFIA) A major change occurred in April 1997 when Agriculture Canada became more business orientated and the Canadian Food Inspection Agency (CFIA) was mandated. The CFIA is dedicated to safeguarding food, animals, and plants that enhance the health and well-being of the Canadian people, their environment, and the economy. As an agency, 63

The Role of Federal Agencies in Rabies Management

References Agriculture Canada. (1990). Health of animals overview (6th ed.). Ottawa, ON: Food Production and Inspection Branch. Allen, J. A. (1922). Remuneration for veterinary service. Canadian Veterinary Record, 11, 134–136. Ballantyne, E. E. (1957). Sylvatic rabies and its control in Alberta (Unpublished doctoral dissertation). Available from the Alberta ­Veterinary Medical Association Library. Butts, E. (2006). North-West Mounted Police. The Canadian Encyclopedia. Retrieved from https://www.thecanadianencyclopedia.ca /en/article/north-west-mounted-police Barker, C. A. V. (2006). History of veterinary medicine. The Canadian Encyclopedia. Retrieved from https://www.thecanadianencyclopedia .ca/en/article/history-of-veterinary-medicine C. D. B. (1959, January 10). Letters to “Top brass, Ontario Veterinary College.” Property of David Gregory. Collections Canada. (2012). North West Mounted Police. Library and Archives Canada: Genealogy and family history. Retrieved from http://www.collectionscanada.gc.ca Dukes, T. W., & Labonte, B. (1991). A hundred years of importation: The first animal quarantine station in North America: Levis, Quebec, 1876–1972. Canadian Veterinary Journal, 32, 375–381. Dukes, T., & McAninch, N. (1992). Health of Animals Branch, Agriculture Canada: A look at the past. Canadian Veterinary Journal, 33, 58–64. Epidemics of rabies assumes serious proportions in Dawson. (1901, March 9). The Toronto Daily Star, p. 11. Evans, E. M., & Barker, C. A. V. (1976). Century one: A history of the Ontario Veterinary Association, 1874–1974. Guelph, ON: Authors. Hall, O. (1940). Rabies. Canadian Journal of Veterinary Medicine, IV(5), 146–149. Hamilton to be a dogless town. (1909, May 20). The Toronto Daily Star, p. 1. Health of Animals Branch, Education and Development Division. (1978). The development of the Health of Animals Branch – A resume. Communications, 18, 16–18. Hydrophobia. (1819, June 18). Kingston Chronicle, p. 3. Reid, R. (1992). Changing roles of veterinarians in Agriculture Canada. Canadian Veterinary Journal, 33(4), 233–236. Report of the veterinary director general for the year ending March 31, 1904. (1904). Ottawa, ON: Department of Agriculture. Available from Library and Archives Canada, https://bac-lac.on.worldcat.org/oclc/29657040 Report of the veterinary director general for the year ending March 31, 1905. (1905). Ottawa, ON: Department of Agriculture. Available from Library and Archives Canada, https://bac-lac.on.worldcat.org/oclc/29657040 Report of the veterinary director general for the year ending March 31, 1906. (1906). Ottawa, ON: Department of Agriculture. Available from Library and Archives Canada, https://bac-lac.on.worldcat.org/oclc/29657040 Sayers, C. W. (1983). Early history of the animal pathology division of Agriculture Canada. Canadian Veterinary Journal, 24(8), 262–267. Statutes of Canada. (1903). Ninth Parliament, 3 Edward VII, Vol. I–II, Chapter II. Tinline, R. R., & Gregory, D. (1988). The Universal Transverse Mercator code: A location code for disease reporting. Canadian ­Veterinary Journal, 29, 825–829 Retrieved from https://www.researchgate.net/publication/51387565_The_Universal_Transverse_Mercator _Code_A_location_code_for_disease_reporting.

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5 Health Canada and Rabies Paul Varughese Senior Science Advisor, Public Health Agency of Canada (Retired), Ottawa, Ontario, Canada

Introduction Global Situation Rabies is a public health problem in most parts of the world and occurs in more than 150 countries and territories. Worldwide, more than 55,000 people die of rabies every year, and 40% of people who are bitten by suspect rabid animals are children under 15 years of age. Every year, more than 15 million people worldwide receive a post-exposure preventive regimen to avert the disease – this is estimated to prevent 327,000 rabies deaths (World Health Organization [WHO], 2012).

Human Rabies Disease, Transmission and Incubation Period Rabies in humans is an acute infection causing a progressive viral encephalitis that is nearly always fatal and is regarded universally as one of the most terrifying known diseases, causing inevitable death. The disease onset in humans is generally marked by apprehension, headache, fever, malaise, and sensory changes at the site of the animal bite. Excitability, aerophobia or hydrophobia or both, often with spasm of the swallowing muscles, are frequent symptoms. Delirium with occasional convulsions follows (Heymann, 2004). Human rabies, unlike most other vaccinepreventable diseases, is unique in that is strictly a zoonotic with virtually no human-to-human transmission. Transmission is usually through saliva via the bite of an infected

animal. Although dogs are the main vector of rabies in other parts of the world, in Canada the most recent cases (although rare) have been associated with exposure to bats. Other animals capable of transmitting rabies in Canada include the fox, skunk, and raccoon (Canadian Food Inspection Agency, 2013). Human deaths are usually associated with the victim not seeking immediate medical attention and hence no timely and appropriate post-exposure treatment is given. Reported incubation periods, the interval between exposure (usually a bite) and appearance of rabies encephalitis, are sometimes as short as five or six days, but, in the majority of cases, the incubation period is between 20 and 60 days, and sometimes longer, depending on the site of the bite and the virus dose. During the incubation period, there are no symptoms and no means of diagnosis. Rabies is often unsuspected (Hemachudha et al., 2001) because of vague signs and no reliable rabies exposure history. Clinical laboratory indicators seldom show striking abnormalities, and electroencephalography, computer tomography scans, and magnetic resonance imaging findings are not pathognomonic of rabies (Maschke et al., 2004).

History of Public Health and Department of Agriculture in Canada The federal Department of Agriculture covered federal health responsibilities from 1867 until 1919, when the Department of Health was created. In 1867 an Act was passed under the Honourable J.-C. Chapais (minister of agriculture, 1867 to 1869) providing the Department of

The Role of Federal Agencies in Rabies Management

Agriculture with “proper organization” and defining its responsibilities as agriculture; immigration/emigration; public health and quarantine; the Marine and Emigrant Hospital at Quebec; arts and manufactures; census and statistics and registration of statistics; patents and inventions; and copyright, industrial designs, and trademarks (Dukes & McAninch, 1992). This definition was perhaps the beginning of the modern day concept of “one world, one health,” a realization of a link between animal diseases and public health (World Organisation for Animal Health, 2013). It is estimated that 60% of pathogens that cause disease in humans are of animal origin, not the least of which is rabies (World Organisation for Animal Health, 2013). This definition has led to cooperation between the Departments of Agriculture and Health over the years in the education of graduates and the management of diseases such as rabies. As an example of public health being a Department of Agriculture responsibility, Sayers (1983) notes that, in 1900, Dr Charles Higgins, a veterinary pathologist, went to Williams Head, British Columbia, to establish a laboratory to investigate whether the large number of Japanese and Chinese immigrants might be infected with the bacillus Pestis bubonica. In 1890 the Montreal Veterinary College, then associated with the Faculty of Medicine of McGill University, became the Faculty of Comparative Medicine and Veterinary Science of McGill University (Barker, 1977; see Chapter 20). In 1905 animal rabies was made a reportable disease under the Animal Contagious Diseases Act, 1903 and its Regulations. Veterinary inspectors were instructed to cooperate with city authorities and the local board of health in their control measures. In 1919 the Government of Canada brought together several pieces of legislation pertaining to food, drugs, and control of infectious diseases, and established a national Department of Health. The Department of National Health and Welfare was established in 1944, which became the Department of Health or Health Canada in 1993. In 1996 the Department of Health Act established the legislative and regulatory framework for all matters of health, over which the minister of health presides, which include the protection of the people of Canada against risks to health and the spreading of disease, and the establishment and control of safety standards and safety information requirements for consumer products. Provision was made in the Act for the collection and publication of information bearing on Public Health. The division of Laboratories and Medical Research was created in 1921, and it became the Laboratory of Hygiene in 1925, with two sections: Bacteriology and Pharmacology.

The Pharmacology Section transferred to the Food and Drug Division in 1946. The Laboratory of Hygiene relocated to Tunney’s Pasture, Ottawa, in 1957 to become five sections: Bacteriology, Biologics Control, Clinical Laboratories, Virology, and Zoonoses. The Laboratory of Hygiene became the Canadian Communicable Disease Centre (CCDC) in 1970 but the name was changed to the Laboratory Centre for Disease Control (LCDC) to prevent confusion of CCDC with CDC in the United States. The Health Protection Branch (HPB) was created in 1972 to include the Food Directorate, Drugs Directorate, Environmental Health Directorate, and LCDC. Biologics Control Division became a bureau within LCDC in 1973 and in 1974 became one of seven bureaus within the Drugs Directorate (J. Peart, personal communication, 2013). The Public Health Agency (PHAC) was created in 2004 in response to growing concerns over the ability of Health Canada to respond effectively to public health threats.

Human Rabies in Canada From 1924 to 2019, only 26 deaths from human rabies, or approximately one case every three years, were reported (see Chapters 3b and 27) (Figure 5.1). Ten of the 26 cases (38%) occurred during 1924 to 1929 (Varughese, 2000). In the decade from 2000 to 2010, only three cases were reported, all bat related, from three provinces: Quebec (2000), British Columbia (2003), and Alberta (2007). Twothirds of the 20 reported human rabies cases from 1924 to 1977 were children less than 15 years of age, whereas only one (a nine-year-old) of the seven cases reported since 1977 was in that age group. Over the past few years the incidence of bat strain r­ abies across the country has increased, and of the last five ­human rabies cases in Canada, four followed exposure to bats. Chapter 3b deals with human rabies in Canada from the nineteenth century to the present. Bat rabies in Canada is discussed in Chapter 27 and the provincial and territorial chapters in Part 3 of this book. In Canada, rabies has never been a major cause of human morbidity and mortality, unlike other vaccine-preventable diseases, such as diphtheria, polio, or measles, and had little impact on historical human epidemic events. As risk tolerance for human rabies is virtually zero, one case is too many. However, thousands of Canadians continue to receive rabies vaccine prophylaxis every year, adhering to the recommendations of the Canadian immunization guide.

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Health Canada and Rabies

Figure 5.1: Human rabies deaths in Canada, 1924 to 2019. Source: created from PHAC and CFIA data.

communication, January 15, 1986). Other corrections that were published at an earlier date include the two deaths from rabies and reported to Statistics Canada from Alberta in 1931 (because of erroneous coding) and, in 1961, an Albertan who contracted the disease in the United States in Arizona and died there. The locations of these two cases were removed at the request of Dr John Waters, the provincial epidemiologist in Alberta, and the corrected data were republished in the Canada Diseases Weekly Report (Varughese, 1983).

Surveillance Data Minor discrepancies in historical rabies surveillance data are reviewed and corrected by LCDC staff epidemiologists when officially requested by provincial or territorial public health authorities. Rabies exposure and initial diagnosis may have taken place in one province while the clinical course, treatment, and death may have taken place in another province. In such a case, recorded for national surveillance purposes, it is counted only once. Adjustments are made in consultation with the provinces or territories involved. For example, in July 1985 a rabies case involved a 25-year-old University of British Columbia student from Alberta, who, while working in a summer camp in Alberta, was scratched or bitten on the face by a bat that had flown into his tent. He did not seek any medical help or get any post-exposure treatment in Alberta. He arrived in Vancouver, British Columbia, on 2 September, and developed clinical signs on 25 October, about four weeks after exposure. He received clinical care in the UBC Hospital but died on 25 November 1985 (McLean et al., 1985; Chapter 3b). The permanent address listed in the death registry was Alberta. To avoid duplication, the BC public health authority agreed with Alberta Ministry of Health to count this particular case as an Alberta case, because the exposure took place in Alberta (J. Waters & T. Johnstone, personal

Rabies Management – Health Canada The federal Department of Health (Health Canada) has a broad mandate, and the history of its formation is described above in the section “History of Public Health and Department of Agriculture in Canada.” Health Canada’s mandate is “to help Canadians maintain and improve their health” (2012a). Canadians recognize Health Canada (HC) as the national authority for their protection against risks to health, and, for years, this was achieved through various activities of the former Health Protection Branch (HPB) of HC. Administration of the Food and Drugs Act is a regulatory activity. The broad public health activities are mandated by federal legislation and

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The Role of Federal Agencies in Rabies Management

through its publications, such as the Annual Report of Notifiable Diseases. In the late 1980s, collection of incidence data centrally was transferred to Health Canada, and later to PHAC. Attempts have been made by federal agencies and the Advisory Committee on Epidemiology (ACE) to standardize the case definitions for surveillance purposes. The most recent national case definitions for notifiable diseases are available on the PHAC website, with the date of the last update at the end of the case definition (Public Health Agency of Canada [PHAC], 2012f). Disease-specific case counts, as expected, depend on diagnostic accuracy (clinical or laboratory confirmed) at the time of reporting. In the early part of the twentieth century, public health activities continued to be largely uncoordinated and mostly in response to infectious disease outbreaks (PHAC, 2012c). Within the LCDC, the Bureau of Communicable (Infectious) Diseases, Epidemiology was responsible for national surveillance or monitoring of selected communicable diseases of public health significance, especially vaccine-preventable diseases affecting children and adults. In the past, LCDC provided the coordination and leadership of the two federal public health expert advisory bodies, the National Advisory Committee on Immunization (NACI) and the National Advisory Committee on Epidemiology (ACE). Within PHAC, currently the Centre for Immunization and Respiratory Infectious Diseases is responsible for all immunization-related activities, including support for NACI. LCDC’s mandate was a broad one, derived from the National Health and Welfare Act, which describes the minister’s role, supported by legislation, cabinet directives, and a wide range of federal/provincial-territorial agreements. Eight core function stem from this Act. Activities included the accurate identification of infectious agents in support of patient management. Identification of the rabies virus was carried out by the Canadian Food Inspection Agency (CFIA) laboratories at Lethbridge, Alberta, and Nepean, Ottawa. Other LCDC functions historically included the maintenance of quality control programs for the identification of infectious agents; research and development in diagnostic technology for infectious diseases; national and comprehensive disease surveillance; outbreak investigation; international liaison and collaboration; support for disease control efforts; training; and national leadership, collaboration, coordination, and support of the provincial and territorial ministries in all aspects of public health. Control and reporting of notifiable diseases fall under the jurisdiction of the provinces and territories, and

the federal, provincial, and territorial agreements (known as PTs) (Health Canada, 1995). Roles and responsibilities for Canada’s health care system are shared between the federal and provincial or territorial governments, and the PTs are responsible for the management, organization, and delivery of health services for their residents (Health Canada, 2012b).

Public Health Activities Communicable or infectious diseases (human) such as rabies are of public health significance and therefore the responsibility of HC at the federal level. Its activities in relation to rabies prevention include the following: • national surveillance of the disease • guideline development for pre-exposure and post-exposure prophylaxis and management of patients or cases • vaccine safety monitoring and facilitating PTs with supply of rabies immunobiologicals (vaccines and rabies immune globulins) when needed • collaboration and support for other federal departments or agencies involved in rabies prevention and control (e.g., Canadian Food Inspection Agency and provincial/ territorial ministries of health) • laboratory support services for diagnostic and sero-protection assessment, since the creation of PHAC • provision of technical advice and consultation • international travel health advice for Canadians travelling to rabies risk areas • international collaboration with agencies such as WHO and PAHO, as with other global infectious disease prevention and control programs The following sections deal with HC’s work in rabies management. SURVEILLANCE

Rabies has been listed as a notifiable disease in Canada since 1924. Each province and territory has public health legislation that outlines requirements for reporting the occurrence of selected communicable diseases to public health authorities in their respective jurisdictions. Although the list of notifiable diseases varies across jurisdictions, a selected number of diseases are routinely tabulated nationally through agreement with provincial and territorial epidemiologists or public health authorities (Public Health, 1953, 1959, 1963). Statistics Canada shares this information with federal health officials and agencies

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therefore regulations for notification vary to some extent (Public Health, 1953). New cases of notifiable diseases are reported by physicians to the medical officer of health who in turn reports to the provincial departments of health. The provincial department in turn transmits to the Dominion Bureau of Statistics, now known as Statistics Canada. The provincial and territorial regulations and the system of control and reporting of notifiable diseases in general were under continual review by the provincial or territorial department of health, Department of National Health and Welfare, and the Bureau of Statistics (Public Health, 1959). As a rule, notifications are geographically located according to where the disease was originally diagnosed; deaths on the other hand are registered in vital statistics records according to the person’s place of residence, which may differ from the geographical location at death (Public Health, 1963).

VACCINE SAFETY

Post-marketing surveillance of all human vaccines in Canada is an ongoing activity carried out at the national level by the LCDC, which later became part of PHAC, in collaboration with provincial and territorial ministries of health, health care professionals, and the pharmaceutical industry. National monitoring of adverse events associated with vaccines dates back to 1965, and it was the responsibility of LCDC (PHAC, 2012a). Safety and efficacy assessments of vaccines were conducted by the Bureau of Biologics, as well as a review of protocols and clinical trials, and inspection of production facilities. Some earlier vaccine testing was done at the Animal Disease Research Institute of CFIA as it had the facilities to handle live rabies virus. The Bureau of Biologics was a WHO collaborating laboratory and collaborated with the US National Institutes of Health laboratories and the British National Institute of Biological Control. This collaboration dealt with developing serological tests to measure the amount of glycoprotein in the vaccine, that is, the ability of the vaccine to produce immunity. Reported adverse events surveillance data for vaccines are stored in the Canadian Adverse Events Following Immunization database and used to signal adverse events that may require more in-depth investigation. The main function of the Canadian Adverse Events Following Immunization Surveillance System is to ensure the continued safety of vaccines on the Canadian market by monitoring adverse events following immunization with vaccines (PHAC, 2012b).

NATIONAL ADVISORY COMMITTEE ON IMMUNIZATION

NACI was created in 1964 to advise the federal minister of health (National Health and Welfare, initially through the Dominion Bureau of Health) on immunization practices. Since the creation of PHAC in 2004, NACI has reported to the chief public health officer (CPHO) of Canada. NACI is a national committee of experts in the fields of paediatrics, infectious diseases, immunology, medical microbiology, internal medicine, and public health. The committee makes recommendations for the use of various vaccines currently or newly approved for use in humans in Canada (NACI, 2012). The committee provides ongoing and timely medical, scientific, and public health advice on vaccine-preventable diseases, including rabies. The NACI recommendations are based on current scientific evidence, updated periodically, and published every four years in the Canadian immunization guide. Additional statements and Health Canada updates are also published in the departmental publications such as Canada Communicable Disease Report, formerly Canada Diseases Weekly Report. NACI’s role is similar to that of the Advisory Committee on Immunization Practices in the United States (Advisory Committee on Immunization Practices, 2012). Periodically, PHAC may seek advice from NACI to prioritize rabies vaccination based on risk category of individuals, to conserve vaccine supply. This is generally achieved by postponing the use of the vaccine for non-emergency situations, such as pre-exposure rabies vaccinations, or even an alternative reduced dose by intradermal administration for pre-exposure prophylaxis.

ADVISORY COMMITTEE ON EPIDEMIOLOGY

ACE was a forum of the chief communicable disease control officials (epidemiologists) in each province and territory, who had advised their federal counterparts on matters related to the study and control of diseases since the early 1960s through the former LCDC, the federal centre responsible for all infectious disease control in Canada. The role of ACE in Canada was similar to that of the US Council of State and Territorial Epidemiologists (2012). Since 2000, ACE has been replaced by other federal, provincial, and territorial advisory bodies for public health matters. ACE was also responsible for reviewing and updating the list of nationally notifiable diseases and developing or revising disease-specific case definitions for national surveillance, and had several working groups or subcommittees to fulfil its mandate. PUBLIC HEALTH AGENCY OF CANADA

Prevention and control of communicable (infectious) diseases in Canada, is primarily a provincial and territorial

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The Role of Federal Agencies in Rabies Management

responsibility. Within Health Canada/Health and Welfare Canada, the former LCDC was the agency responsible from 1972 to 2004 for developing disease prevention and control programs. PHAC was established in September 2004 to strengthen Canada’s capacity to protect and improve the health of Canadians and to reduce the pressure on the health care system. In 2006 the Public Health Agency of Canada Act confirmed the agency as a legal entity (PHAC, 2012d). PHAC was created in 2004 in response to growing concerns about the capacity of Canada’s public health system to anticipate and respond effectively to public health threats (PHAC, 2012e). PHAC’s creation was the result of wide consultation with the provinces, territories, stakeholders, and Canadians (in the federal strategy). In addition, it is expected to show federal leadership on issues concerning public health and improved collaboration within and between jurisdictions. PHAC became one of six departments and agencies that make up the Government of Canada’s Health Portfolio, led by Canada’s first CPHO. The CPHO reports to the minister of health. PHAC and the CPHO provide a clear focal point for federal leadership and a­ ccountability in managing public health emergencies. More recently, PHAC took a lead role and was signatory to the Canada rabies plan, discussed in Chapter 30.

had its own challenges, especially in the early part of the twentieth century. For a thorough assessing of the past experience of rabies in humans in Canada, researchers may use a combination of data and information sources. In Canada, collection of vital statistics, including cause-specific deaths from various jurisdictions, is the responsibility of Statistics Canada. Mortality data are based on the information on the death certificate of particular cases at the time of reporting and is also affected by diagnostic accuracy. Because of medical and public health interest, detailed human case reports in Canada are generally published in Canadian medical literature, including Canadian Medical Association Journal and the Canada Communicable Disease Report. Since rabies is almost always fatal, for studying the occurrence (incidence) of human cases in Canada prior to 1950, mortality data collected by Statistics Canada and other published case reports are also generally used as are newspaper reports (see Chapter 3b). A review of published data sources for rabies specific incidence and mortality tabulated by Statistics Canada show that no one system is complete in regard to rabies case counts. Today, almost all human rabies cases in Canada are detected and reported more completely because of better diagnostic capability and increased public health awareness.

RABIES DIAGNOSIS

Following the establishment of a federal Department of Health in 1919, the Food and Drugs Act was introduced in 1920. By the late 1920s, Regulations developed under the Act established specific requirements for licensing drugs. The minister of health had the authority to cancel or suspend a licence for violations of the requirements. A significant reworking of the Food and Drug Regulations did not begin until 1947, but it laid the foundation for the regulations in place today. By 1951, manufacturers were required to file new drug submissions before marketing their drugs. As the regulatory authority, HC is responsible for working to maximize the quality, safety, and efficacy of all biologic drugs. Within HC, the Biologics and Genetic Therapies ­Directorate (BGTD) is responsible for Canada’s vaccines regulatory program in collaboration with the HPFB Inspectorate and the Marketed Health Products Directorate (2012). Before a vaccine can be submitted to HC to be considered for approval, sufficient scientific and clinical evidence must be collected to show that it is safe, efficacious, and of suitable quality. This scientific evidence includes results from h ­ uman clinical trials. For clinical trials performed in ­Canada, a clinical trial application must be filed to BGTD.

DRUG REGULATION IN CANADA

Diagnostic tests for rabies are coordinated through the provincial or territorial public health laboratories or local referring laboratories, as appropriate. Laboratory confirmation of human rabies infection has always been done by the laboratory of CFIA at Nepean, Ottawa (see Chapter 20), and serology at the Public Health Laboratories branch of the Ministry of Health and Long-Term Care, in Toronto, Ontario. Serum neutralization assays are performed at PHAC’s National Microbiology Laboratory (2012) in Winnipeg, Manitoba. Epidemiologic investigation of rabies cases and public health measures are carried out by the local public health authorities in collaboration with local CFIA veterinarians (see Chapter 31). Following the diagnosis or detection of a case, it is reported, per the provincial or territorial public health legislation and protocol, to the local and provincial or territorial public health authorities, which in turn report to the federal departments. Unless the rabies-specific signs of hydrophobia or aerophobia are present, the clinical diagnosis may be difficult. Being a rare disease with varying clinical signs and symptoms and diagnostic difficulties, human rabies case reporting

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are unsuitable, or are unavailable. At times, this includes human rabies vaccines and immune globulins. In vaccine shortage situations, to assist the provinces and territories, PHAC explores the possibility of sourcing vaccine from manufacturers not licensed to sell in Canada.

SPECIAL ACCESS PROGRAM, HEALTH CANADA

The Special Access Program (SAP) provides access to non-licensed (non-marketed) health products for practitioners who are treating patients with serious or life-threatening conditions when conventional therapies have failed,

References Advisory Committee on Immunization Practices. (2012). General committee-related information. Retrieved from https://www.cdc.gov /vaccines/acip/committee/index.html Barker, C. A. V. (1977). John G. Rutherford and the controversial standards of education at the Ontario Veterinary College from 1864 to 1920. Canadian Veterinary Journal, 18(12), 327–340. Retrieved from https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1697714/pdf /canvetj00385-0011.pdf Canadian Food Inspection Agency. (2013). Rabies in Canada. Retrieved from http://www.inspection.gc.ca/animals/terrestrial-animals/ diseases/reportable/rabies/rabies-in-canada/eng/1356156989919/1356157139999 Council of State and Territorial Epidemiologists. (2012). About CSTE. Retrieved from https://www.cste.org/page/About_CSTE Dukes, T., & McAninch, N. (1992). Health of Animals Branch, Agriculture Canada: A look at the past. Canadian Veterinary Journal, 33, 58–64. Retrieved from https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1481176/pdf/canvetj00050-0060.pdf Health Canada. (1995). Health Protection Branch: Business adjustment plan, 1995–96 to 1997–98: The new HPB enterprise at work. Ottawa: Minister of Supply and Services. Health Canada. (2012a). Health Canada’s mandate. Retrieved from https://www.canada.ca/en/health-canada/corporate/mandate.html Health Canada. (2012b). Canada’s health care system. Retrieved from http://www.hc-sc.gc.ca/hcs-sss/medi-assur/index-eng.php Hemachudha, T., Mitrabhakdi, E., & Wacharapluesadee, S. (2001). Clinical aspects of human rabies. In B. Dodet, F. X. Meslin, & E. Heseltine (Eds.), Proceedings of the Fourth International Symposium on Rabies Control in Asia (pp. 10–18). Paris, France: WHO. Heymann, D. L. (2004). Control of communicable disease manual (18th ed.). Washington, DC: American Public Health Association. Maschke, M., Kastrup, O., Forsting, M., & Diener, H. C. (2004). Update on neuroimaging in infectious central nervous system disease. Current Opinion in Neurology, 17(4), 475–480. https://doi.org/10.1097/01.wco.0000137540.29857.bf McLean, A. E., Noble, M. A., Black, W. A., Kettyls, G. D., Johnstone, T., Webster, A., & Gregory, D. (1985). A human case of rabies – British Columbia. Canada Diseases Weekly Report, 11(51), 213–214. Retrieved from http://publications.gc.ca/collections/collection _2016/aspc-phac/H12-21-1-11-51.pdf Marketed Health Products Directorate. (2012). The regulation of vaccines for human use in Canada. Retrieved from http://www.hc-sc .gc.ca/dhp-mps/brgtherap/activit/fs-fi/vaccin-reg-eng.php National Advisory Committee on Immunization. (2012). About NACI. Retrieved from https://www.canada.ca/en/public-health/services /immunization/national-advisory-committee-on-immunization-naci.html National Microbiology Laboratory. (2012). National Microbiology Laboratory. Retrieved from https://www.canada.ca/en/public-health /programs/national-microbiology-laboratory.html Public Health Agency of Canada. (2012a). Reporting adverse events following immunization (AEFI) in Canada: User guide to completion and submission of the AEFI reports. Retrieved from http://www.phac-aspc.gc.ca/im/aefi_guide/index-eng.php Public Health Agency of Canada. (2012b). Reporting adverse events following immunization (AEFI) in Canada. Retrieved from http:// www.phac-aspc.gc.ca/im/aefi-form-eng.php Public Health Agency of Canada. (2012c). The chief public health officer’s report on the state of public health in Canada 2008: Addressing health inequalities. Retrieved from https://www.canada.ca/content/dam/phac-aspc/migration/phac-aspc/cphorsphc-respcacsp/2008 /fr-rc/pdf/CPHO-Report-e.pdf Public Health Agency of Canada. (2012d). List of acts and regulations: Public Health Agency of Canada Act. Retrieved from https:// www.canada.ca/en/public-health/corporate/mandate/about-agency/acts-regulations/list-acts-regulations.html Public Health Agency of Canada. (2012e). About the agency: History. Retrieved from https://www.canada.ca/en/public-health /corporate/mandate/about-agency/history.html Public Health Agency of Canada. (2012f). Case definitions for communicable diseases under national surveillance. Retrieved from http://www.phac-aspc.gc.ca/publicat/ccdr-rmtc/09vol35/35s2/index-eng.php

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The Role of Federal Agencies in Rabies Management Public Health Section, Health and Welfare Division. (1953). Annual report of notifiable diseases. (Catalogue No. CS82-201-PDF). Ottawa: Dominion Bureau of Statistics. Public Health Section, Health and Welfare Division. (1959). Annual report of notifiable diseases. (Catalogue No. CS82-201-PDF). Ottawa: Dominion Bureau of Statistics. Public Health Section, Health and Welfare Division. (1963). Annual report of notifiable diseases. (Catalogue No. CS82-201-PDF). Ottawa: Dominion Bureau of Statistics. Sayers, C. W. (1983). Early history of the Animal Pathology Division of Agriculture Canada. Canadian Veterinary Journal, 24(8), 262–267. Varughese, P. (1983). Rabies in Canada. Canada Diseases Weekly Report, 9, 137–140. Varughese, P. (2000). Human rabies in Canada: 1924–2000. Canada Communicable Disease Report, 26(24), 210–211. World Health Organization. (2012). Rabies [Fact sheet]. Retrieved from http://www.who.int/mediacentre/factsheets/fs099/en/ World Organisation for Animal Health. (2013). One world, One health: OIE-World Organisation for Animal Health. Retrieved from http://www.oie.int/for-the-media/editorials/detail/article/one-health/

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PART 3

A History of Rabies Management in the Provinces and Territories

Overview The chapters in Part 3 describe the experiences of the Canadian provinces and territories with rabies and how they have reacted to that threat. As well, they document how the provinces and territories worked in cooperation with federal and provincial and territorial agencies. Most chapters focus on a single province or territory: Chapter 6 covers British Columbia; Chapter 7, Alberta; Chapter 8, Saskatchewan; Chapter 9, Manitoba; Chapter 10, Ontario; and Chapter 11, Quebec, except for Nunavik, which is covered with the northern territories. Chapter 12, however, deals with the Maritime provinces: Nova Scotia, Prince Edward Island, and New Brunswick. Although Chapter 13 deals with one province, Newfoundland and Labrador, it deals with the two separate land masses that compose that province. Chapter 14, on Canada’s North, includes separate sections for Yukon, the Northwest Territories, Nunavut, and Nunavik, which is the northern portion of Quebec. Rabies management in Canada is a responsibility shared between the federal government and the provinces and territories. The Canadian Food Inspection Agency (CFIA) played a lead role in the diagnosis of rabies and, until 2014, in the collection and transportation of specimens to federal laboratories for testing. The CFIA and its antecedents also played a major role initially in actions to prevent further cases in domestic animals and reduce possible contact with humans – although, as the chapters in this part note, that role has changed over time as provincial and territorial agencies developed their own rabies protocols and control programs. The CFIA has also performed an important role in assisting in cooperation between provinces and territories and in rabies research, in terms of diagnostic testing, vaccine development, and the growing understanding of the genetics of the rabies virus.

Evolution of Canadian Territories and Provinces Canada is a relatively new country, and its territorial and provincial boundaries have changed over time, with the most recent change being the creation of Nunavut on 1 April 1999. Hence, any description of the history of rabies in Canada must include a description

A History of Rabies Management in the Provinces and Territories

of the evolution of the administrative boundaries, which act as the filter through which reporting has taken place. Plate 1 shows the evolution of the administrative boundaries of Canada and their names. The realization of the immenseness of the Canadian North and the precise knowledge of its extent did not come until after numerous early explorations. For example, the Dobbs map of 1744 (upper left – Plate 1), shows a part of California joined to Rupert’s Land and areas named New Britain and Acadia (“Boundaries,” 2001). The remaining maps in Plate 1 provide snapshots of various boundary and name changes in the northern half of the continent since 1713. Early Canadian history was dictated by Britain and France and the fur trade. On 2 May 1670, the Governor and Company of the Adventurers of England trading into the Hudson’s Bay was incorporated by a royal charter from King Charles II. The company was granted a monopoly over the Indigenous trade, especially that dealing with the fur trade. The charter granted trading rights to the Hudson’s Bay Company (HBC) in the region watered by all rivers and streams flowing into Hudson Bay in northern Canada, an area known as Rupert’s Land, after the first director of the HBC, Prince Rupert of Rhine, nephew of Charles I. The company founded its first headquarters at Fort Nelson on the Nelson River in present-day north eastern Manitoba. Its territory encompassed present day Manitoba, most of Saskatchewan, southern Alberta, southern Nunavut, northern parts of Ontario and Quebec, parts of Minnesota and north Dakota, and small parts of Montana and South Dakota. By 1713 France had ceded Acadia and Newfoundland to Great Britain, and Britain recognized rights to Rupert’s Land. France had ceded Louisiana to Spain, to be bought by the United States in 1803, and Ile Royale (Cape Breton), New France, and Ile Saint-John (Prince Edward Island) were ceded to Great Britain by 1763. In the same year, the boundaries of Quebec were set and the Labrador coast lands assigned to Newfoundland. In 1783 Britain recognized the United States; Russia claimed Alaska in 1784, only to be bought by the United States in 1867; and Quebec was divided into two colonies, Upper Canada and Lower Canada, by 1791, to become Canada East and Canada West in 1840. St John’s Island was renamed Prince Edward Island in 1798 (“Boundaries,” 2001). The North-Western Territory was created in 1859 and included all lands not in Rupert’s Land or British Columbia (i.e., what is now Yukon, the provinces of Alberta, Saskatchewan, and parts of Manitoba). By 1867 the provinces of New Brunswick, Nova Scotia, and Canada became a federal state, called the Dominion of Canada, Canada East becoming Quebec and Canada West becoming Ontario. Following this, the Canadian Parliament acquired Rupert’s Land and the North-Western Territories from the Hudson’s Bay Company for $300,000 in 1868, and they became part of Canada in 1870. The North-Western Territory was renamed the North-West Territories and included all present day Yukon, Alberta, Saskatchewan, and parts of present day Northwest Territories, Nunavut, Manitoba, Ontario, Quebec, and Newfoundland and Labrador, but excluded the Arctic Islands, which were transferred to Canada in1880. Manitoba had become Canada’s fifth province in 1870 and British Columbia, its sixth province in 1871 (Historical Atlas, 2001). During 1876, an independent, autonomous territory of the District of Keewatin separated from the North-West Territories and by 1912 became the northern parts of Ontario, Manitoba, and the North-West Territories. By 1882 the southern parts of the North-West Territories became populated and divided into provisional districts, the districts of Alberta, Athabasca, Assiniboia, and Saskatchewan forming present day Alberta and Saskatchewan in 1905. The northern parts of the North-West Territories divided into four districts in 1895: Franklin, made up of the Arctic Islands; Ungava, which remained a regional administrative district of Canada’s NWT from 1895 to 1912 and now forms part of the administrative

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Part Overview

region of Nord-du-Quebec; Yukon, what is today the Yukon Territory created in 1898; and Mackenzie, stretching from Yukon to Keewatin. By 1999 the notion of districts had been abolished with the creation of Nunavut, consisting of the remnants of the former District of Keewatin, most of the Arctic islands of the District of Franklin, and the northwest portion of the District of Mackenzie. Present day Northwest Territories consists of the remainder of Franklin and most of the Mackenzie.

Hudson’s Bay Company As mentioned, HBC controlled a huge area of what is now Canada. By 1870 the trade monopoly of the HBC had been abolished and trade opened to any entrepreneur. This was due in part to the Riel Rebellion and to the finding of a committee looking into the myth propagated by the HBC that the Canadian west was unfit for agricultural settlement and perhaps driven by a falling demand of furs in Europe. During 1850 to 1860 John Palliser and Henry Youle Hind had explored the prairie region of the provinces, and the North-West Mounted Police had completed their 1874 “March West.” The HBC myth was finally laid to rest with the building of the Canadian Pacific Railways line west in 1880 and the development of settlements along the railroad line. While no comprehensive datasets can be used to analyse rabies, fur harvest and animal populations during the tenure of the HBC, it is interesting to speculate whether the fur trade kept the wildlife population, especially foxes, to a level low enough that it did not sustain rabies. It is possible that when demand for fur diminished after the Second World War, the increasing fox population provided the pathway for rabies to spread south, especially in Alberta and along Hudson Bay into Ontario and Quebec.

References Boundaries: Territorial evolution, 1670–2001. (2001). In Historical Atlas of Canada. Retrieved from http://www.historicalatlas.ca

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6 British Columbia David J. Gregory,1 Rowland R. Tinline,2 Eleni Galanis,3 and Ken Cooper4 1

Canadian Food Inspection Agency (Retired), Ottawa, Ontario, Canada Professor Emeritus, Geography Department, Queen’s University, Kingston, Ontario, Canada 3 Physician Epidemiologist, British Columbia Centre for Disease Control, Vancouver, BC, Canada 4 British Columbia Centre for Disease Control (Retired), Vancouver, BC, Canada 2

Place Before 1825 British Columbia was an unchartered, open-to-any-country territory wedged between the Pacific Ocean to its west and the North-Western Territory to its east, with Russia-claimed Alaska to the north and Spanish Louisiana to the south. Its southern border became Oregon following the sale of Louisiana to the French and subsequently to the United States in 1803. The Oregon Boundary Treaty of 1846 redefined BC’s southern border at the 49th parallel, establishing New Caledonia and Vancouver Island, which became a Crown colony in 1849. With the redefinition of the North-Western Territory boundaries in 1859 and 1863 and the joining of Vancouver Island to British Columbia in 1866, British Columbia became the sixth province of the Dominion of Canada in 1871. Its northern border was established in 1898 with the creation of the Yukon Territory (see Overview, Part 3). The capital of BC is Victoria (a name chosen by Queen Victoria in 1859) on the southeast corner of Vancouver Island (region 23 in Figure 6.2). Today, BC is bordered to the west by the Pacific Ocean; the state of Alaska to the northwest; the Yukon and Northwest Territories to its north; the province of Alberta to the east; and the states of Washington, Idaho, and Montana to the south. British Columbia is the third-largest of Canada’s provinces at 944,735 km2. BC has three major landscapes: Vancouver Island, the coast, and the interior. The interior is part of the Western Cordillera of North American with north–south mountain ranges broken into

valleys that form their own physical and cultural regions. The exception is the interior plains in the northeast corner of the province, which is a part of the Alberta Plateau (regions 10 and 22 in Figure 6.2). Because of the successive mountain ranges, the interior of the province has a semi-arid climate with cold winters. The coast is defined by the Coastal Mountains, the Canadian portion of the Cascade Mountains in the United States. Combined with the Kuroshio Current (Japan Current) these mountains give coastal BC a mild, rainy oceanic climate. The southwestern corner of mainland BC is typically referred to as the Lower Mainland, a flat fertile area at the mouth of the Fraser River that cuts inland to the interior (regions 1 and 3 in Figure 6.2). The Census of Canada of 2012 shows almost 2.6 million people living in this area (including the Fraser River Valley), approximately 56.5% of BC’s population of 4.6 million (Statistics Canada, 2013).

The History of Wildlife Rabies in British Columbia Early Rabies (before 1960) Although in BC rabies most commonly occurs in bats, several outbreaks have involved more than one terrestrial mammal in the past. The earliest of these was recorded in 1914 in Victoria, where 38 dogs and 1 cow were confirmed rabid by histological examination (Tabel et  al., 1974). This resulted in 43 premises quarantined: 29 in Nanaimo,

A History of Rabies Management in the Provinces and Territories

13 in Vancouver, and 1 in Victoria (Report of the Veterinary Director General, 1915, p. 12). The veterinary director general’s (VDG’s) reports for 1921, 1922, and 1928 mention premises or herds under quarantine for rabies. These records did not indicate whether there was a positive laboratory diagnosis (Report of the Veterinary Director General, 1921, 1922, 1928). In 1952 an epizootic with foxes in the Arctic began to spread south, eventually affecting most of the provinces of Canada from the northeastern portion of BC to New Brunswick (Tabel et  al., 1974; see Chapter 2). Canadian Food Inspection Agency (CFIA) laboratory records indicate that the outbreak was first noted in BC in April 1953 and involved five red foxes, one wolf, one coyote, one dog, and one cow. There was also a rabid dog in 1954. The rabies strain in these outbreaks was not identified. Although bats were a possible source, this is unlikely since there had been no occurrences of bat strain virus in terrestrial mammals in BC to match the magnitude of these outbreaks; no rabies was diagnosed in bats until 1957. The result was probably due to an incursion of coyotes or foxes from the Alberta plateau; there were many rabies cases there, especially in coyotes as rabies spread quickly southwards in Alberta during the early 1950s. Foxes do not travel as rapidly as coyotes but may be effective vectors of rabies since, because of their smaller size, they may not always kill what they attack (Plummer, 1954). In June 1957, the first positive diagnosis of rabies in a bat in Canada was made for a specimen submitted from Vancouver, BC (Avery & Tailyour, 1960; see Chapters 2 and 6). The bat, identified as a big brown bat (Eptesicus fuscus), had bitten a boy, and the specimen was submitted after a few days for laboratory examination. Since the bat brain was in a state of autolysis, an inoculum was prepared and subsequently injected into six mice. Examination of dead mice brains for Negri bodies was positive in only one mouse brain. Second and third injections into mice allowed for a positive diagnosis. Since then, positive bats have been identified almost every year in BC and have been found in every other province of Canada and in the Northwest Territories. A survey of bats was carried out from July to September following the 1957 outbreak. Specimens were pooled for testing and one of the pools consisting of the little brown bat (Myotis lucifugus) was positive to rabies virus (see Chapter 2 under “The Invasion of Arctic Fox Rabies into Southern Canada”) (Avery & Tailyour, 1960). During 1958 two bats were positive for rabies in the interior of BC, a big brown bat from

the Okanagan valley, and a silver-haired bat (Lasionycteris noctivagans).

Rabies Cases, post 1960 Since 1960 animal rabies cases in BC have slowly increased, levelling off at approximately 12 cases per year (Figure 6.1). Over 95% of those cases (502/527) have been in bats, although the first nine cases in 1953 were related to the outbreak in Alberta – discussed in detail in Chapter 7 – and were primarily in wildlife (five foxes, one wolf, one coyote, one cow, one dog). Submissions data have been available since 1977. There were 248 submissions in 1997, which trended upward to a peak of 505 in 2004. Since then there has been a downward trend and submissions averaged 137 from 2007 to 2017. From 1977 to 2017 bats were 58% of all submissions (5971/10,261), of which 7% were positive for rabies (Table 6.1). In 1969 there was one positive cat, which was probably due to a bat strain. The technology for variant typing of the rabies virus was not available until the 1980s (K. Knowles, personal communication, 20 November 2012). In 1983 an Alberta student died of rabies in BC following a bite from a bat in Alberta. Strain identification was not carried out because a sample of infected material was not available. Then 1984 and 1985 saw cases of rabies in a horse in the Sorrento area and a beaver in Delta, respectively. The horse had a profile of B-2 bat strain isolate (Webster et al., 1986) while the beaver strain was not determined (Copeland et al., 1985). During 1992 and 1993 a cluster of three cats in the Delta area were positive with rabies, one identified with skunk strain. In 2003 a 52-year-old male died of bat strain rabies (see Chapter 3b, Case 40). Since he had not been out of the province in the year before his death, this case was considered to be locally acquired (BC Centre for Disease Control [BCCDC], 2017b). The virus was identified as a bat strain associated with a Myotis species (S. Nadin-Davis, personal communication, 29 November 2012). There was an outbreak of skunk rabies in 2004 in Stanley Park, Vancouver. All the skunks were identified with bat strain rabies infected by the silver-haired bat (S. Nadin-Davis, personal communication, 29 November 2012). A cat from Maple Ridge was positive with bat strain rabies in 2007. The strain was not analysed genetically (S. Nadin-Davis, personal communication, 29 November 2012). With the few exceptions mentioned above, rabies incidence has been in bats. The mountains and valleys of BC

78

British Columbia

Figure 6.1: Positive animal rabies cases reported in BC, 1953–2017. A second order polynomial trend line has been added to the chart. Source: CFIA data.

species in BC. Although Table 6.3 does not list the Eastern red bat, Lasiurus borealis (REB), Cathy Lausen, a bat specialist with Birchdale Ecological Limited, reported three rabies-negative specimens near a wind turbine (C. Lausen, personal communication, 21 March 2013; Nagorsen & Paterson, 2012; see Chapter 27). From 1977 to 2017, CFIA provided data on total bat submissions and positives. As previously noted, 7% of those bat submissions were positive for rabies. Of those positives, rabies was most often diagnosed in the big brown bat, but several species (pallid bat, Antrozous pallidus; fruit bat, Phyllostomidae spp.; and smallfooted bat, Myotis ciliolabrum) had no positives (Table 6.3). Interestingly, little brown bats were submitted more often than big brown bats (1775 compared with 1142), but big brown bats composed almost 49% of all reported positives in bats (Table 6.3). On a regional basis (a regional district equals a Statistics Canada census division) most bat submissions occur in the major population centres (Greater Vancouver and Victoria) and along the Fraser River Valley and the Okanagan district (Table 6.2 and Figure 6.2). This link

Table 6.1  Results for specimens submitted for testing from BC, 1977 to 2017. Type

Total

Neg

Pos

Total Bats Others

10,261 5,971 4,290

9,805 5,528 4,277

430 417 13

% Total 4.2 7.0 0.3

Source: compiled from CFIA data.

and the diversity of its habitats likely play roles in limiting the spread of rabies in terrestrial mammals within the province and from Alberta. BC is home to 137 species of mammals, and another 13 species have been introduced. Even if the 30 marine mammal species of BC are not considered, the province has the most diverse mammal population of any jurisdiction in Canada (Brigham, 2010; Nagorsen, 2010). Community Bat Programs of BC (2014) lists 17 species of bats that have been identified in BC. Fifteen of those show up in submissions from BC, 14 of which have been diagnosed with rabies (Table 6.2, Table 6.3). Therefore, bats at risk comprise almost 11% of mammal

79

Table 6.2  Submissions by bat species by regional district, 1977 to 2017. See Table 6.3 for bat species codes. Regional District Greater Vancouver North Okanagan Fraser Valley Similkameen Central Okanagan Cariboo East Kootenay ThompsonNicola Fraser-Fort George Peace River Central Kootenay ColumbiaShuswap Kootenay Boundary BulkleyNechako SquamishLillooet Sunshine Coast Powell River Charlotte Central Coast Kitimat-Stikine North Rockies Capital Cowichan Valley Nanaimo AlberniClayoquot Comox Valley Strathcona Mount Waddington  Total   % Total  Unknown

Map #

TOTAL

LBB

BBB

CLB

BAT

YUB

LEB

1

1,288

313

310

146

138

129

63

119

1

2

720

270

151

39

57

47

63

31

3 4

507 460

116 152

104 66

27 35

115 39

55 49

36 40

22 23

5

280

57

65

19

25

44

25

6 7

242 221

139 108

22 29

4 12

28 26

21 3

8

98

31

14

9

11

9

74

32

6

3

14

SHB NLB

KEB

LLB

HRB

WSB

TBB

FRB

WEB

PLB

FCB

FAB

FUB

LNB

SPB

36

10

19

0

0

1

1

1

1

0

0

0

0

39

5

4

5

7

0

2

0

0

0

0

0

0

0

3 31

21 4

4 3

1 6

0 9

0 0

0 1

0 0

0 2

1 0

0 0

1 0

0 0

1 0

8

27

0

3

2

5

0

0

0

0

0

0

0

0

0

13 15

3 11

9 7

1 3

1 2

0 2

1 2

0 1

0 0

0 0

0 0

0 0

0 0

0 0

0 0

0 0

11

9

6

3

0

2

0

1

0

1

0

0

0

0

0

0

0

3

4

1

5

1

5

0

0

0

0

0

0

0

0

0

0

0

10

78

54

2

2

11

0

4

2

0

0

3

0

0

0

0

0

0

0

0

0

0

0

11

83

32

7

7

12

8

3

3

6

0

1

2

2

0

0

0

0

0

0

0

0

0

12

51

18

9

1

4

8

4

0

4

0

3

0

0

0

0

0

0

0

0

0

0

0

13

40

17

5

2

4

7

2

0

0

0

2

1

0

0

0

0

0

0

0

0

0

0

14

24

14

0

0

3

3

0

1

1

1

1

0

0

0

0

0

0

0

0

0

0

0

15

33

8

1

8

4

4

2

4

0

1

1

0

0

0

0

0

0

0

0

0

0

0

16

24

5

1

3

0

2

8

1

1

2

1

0

0

0

0

0

0

0

0

0

0

0

17 18 19 20 22 23

24 22 7 4 0 581

2 10 3 2 0 119

3 0 0 0 0 173

5 6 1 0 0 95

6 2 0 0 0 54

4 2 1 0 0 66

4 2 0 0 0 32

0 0 0 0 0 14

0 0 0 1 0 0

0 0 1 0 0 15

0 0 1 1 0 5

0 0 0 0 0 4

0 0 0 0 0 0

0 0 0 0 0 2

0 0 0 0 0 1

0 0 0 0 0 0

0 0 0 0 0 0

0 0 0 0 0 0

0 0 0 0 0 1

0 0 0 0 0 0

0 0 0 0 0 0

0 0 0 0 0 0

24

407

92

81

95

36

40

40

6

0

12

1

1

0

2

0

1

0

0

0

0

0

0

25

371

77

60

85

33

56

42

2

0

7

4

1

0

1

0

3

0

0

0

0

0

0

26

91

30

6

14

10

14

12

2

0

2

1

0

0

0

0

0

0

0

0

0

0

0

27 28

83 84

24 20

11 11

14 14

5 8

8 14

13 13

0 1

0 0

4 1

4 2

0 0

0 0

0 0

0 0

0 0

0 0

0 0

0 0

0 0

0 0

0 0

29

27

4

0

10

4

3

2

0

0

3

1

0

0

0

0

0

0

0

0

0

0

0

5971

1775 29.7 26

1142 19.1 5

657 651 11.0 10.9 1 2

603 10.1 1

453 7.6 2

263 4.4 3

138 2.3 0

123 2.1 3

66 1.1 0

44 0.7 0

27 0.5 0

9 0.2 3

6 0.1 0

5 0.1 0

3 0.1 0

2 0.0 0

1 0.0 0

1 0.0 0

1 0.0 1

1 0.0 0

47

Note: Map # refers to regional districts in Figure 6.2. Source: compiled from CFIA data.

British Columbia

Table 6.3  Submissions by species of bats (1977 to 2017) showing percentage of total submissions and percentage of total positives. Code

Name

Scientific Name

Total

N

P

% Tot

%P

LBB BBB CLB BAT YUB LEB SHB NLB KEB LLB HRB WSB TBB FRB PLB SPB FCB* FAB* FUB* LNB*  

Little brown bat Big brown bat Californian bat Unspecified Yuma myotis Long-eared myotis Silver-haired bat Northern bat Keen’s bat Long-legged bat Hoary bat Western small-footed bat Townsend’s big-eared bat Fringed bat Pallid bat Spotted bat Fruit bat (Caribbean) Fruit bat (Africa/Asia) Fruit bat Leaf-nosed bat  

Myotis lucifugus Eptesicus fuscus Myotis californicus   Myotis yumanensis Myotis evotis Lasionycteris noctivagans Myotis septentrionalis Myotis keenii Myotis volans Lasiurus cinereus Myotis ciliolabrum Corynorhinus townsendii Myotis thysanodes Antrozous pallidus Euderma maculatum          Totals

1775 1142 657 651 603 458 263 138 123 66 44 27 9 6 3 1 2 1 1 1 5971

1734 936 625 629 579 416 223 137 116 58 31 25 8 3 3 0 2 1 1 1 5528

37 204 26 15 21 39 40 1 6 8 13 2 1 3 0 1 0 0 0 0 417

29.7 19.1 11.0 10.9 10.1 7.7 4.4 2.3 2.1 1.1 0.7 0.5 0.2 0.1 0.1 0.0 0.0 0.0 0.0 0.0 100.0

2.1 17.9 4.0 2.3 3.5 8.5 15.2 0.7 4.9 12.1 29.5 7.4 11.1 50.0 0.0 100.0 0.0 0.0 0.0 0.0

Note: The CFIA database codes included five instances of WEB, which were all negative. Those codes were corrected and changed to LEB. Species marked * are exotics, probably submitted from zoos. Source: compiled from CFIA data.

Active Surveillance for Rabies in British Columbia

seems obvious given that most rabies reporting in BC is passive surveillance geared towards protection of humans. Hence, submissions are usually made as a consequence of direct or probable contact with humans or domestic animals. Furthermore, human habitation offers bats a wide range of possible roosting and hibernation areas (see Table 6.4). Finally, reporting is geared to CFIA district offices which are, in turn, linked to population centres such as Abbotsford, Cranbrook, Dawson Creek, Oliver, Osoyoos, Surrey, Vancouver/Richmond, Vernon, Victoria, and Williams Lake (CFIA, 2012). Most bat submissions (96%) were made between May and October when bats are active (Table 6.4). Almost 97% of all positive bats were in the same period. The bat species in BC eat a diet of arthropods. This means that the potential for rabies exposures is greatest in the period from late spring to the start of frost in the fall, when bats emerge from hibernation to feed on insects. Submissions from November to March do occur and are associated with species that have been observed to awake from hibernation periodically during the colder months (Nagorsen & Brigham, 1993).

In some situations, cases of rabies in bats and terrestrial animals in BC were followed by active surveillance to determine the extent of the outbreak. Publicity, resulting from the June 1957 incident in which a young boy from Vancouver was bitten by a big brown bat, led to some 200 bats being collected between July and September 1957. For efficiency the specimens were pooled and one pool, containing little brown bats, showed the rabies virus. In July the next year, a boy from Okanagan was bitten by a big brown bat. This was followed by 42 submissions, all negative. In August 1958, a man from Osoyoos, BC, was bitten by a silver-haired bat that proved positive for rabies. Neither of these humans became infected. During 1957–1958 some 289 bats were tested for rabies (Avery & Tailyour, 1960). The following species of bats were represented in that sample: long-eared, little brown, Yuma, Californian, big brown, silver-haired, hoary, and Townsend’s big-eared. In 1985 a positive rabies case in a beaver from Delta, BC, led to a survey of aquatic wildlife in the area. A total of 45 beaver and 98 muskrats were collected and all tested negative.

81

A History of Rabies Management in the Provinces and Territories

Figure 6.2: Submissions of bats by regional districts in BC, 1977 to 2017. Source: compiled from CFIA data.

Similarly, the 2004 positive skunk case in Stanley Park in downtown Vancouver prompted a survey of terrestrial animals in the area. A total of 27 skunks and 11 raccoons were submitted for diagnosis. Three additional skunks were found positive for rabies virus. All four positive skunks had a bat strain variant that subsequent phylogenetic analysis showed was the silver haired bat variant. All the raccoons tested negative.

province focuses on pre- and post-exposure prophylaxis of humans, vaccination of companion animals, testing of suspect animals, isolation of exposed animals, and ongoing education and communication with the public and health care professionals. BC has not implemented wildlife control programs as many other provinces have done because of the lack of terrestrial rabies. Until 2014, the CFIA and the regional health authorities (HAs) were involved in some or all of these management activities. The Royal Canadian Mounted Police (RCMP) and other provincial agencies played minor roles. As of 1 April 2014, the CFIA was no longer involved in rabies animal management; it no longer collects animal samples for testing nor does it investigate and quarantine domestic animals suspected of having rabies. These

Rabies Management in British Columbia General Considerations Given that there are relatively few animal rabies cases in BC and most cases are in bats, rabies management in the

82

British Columbia

Table 6.4  Submissions by species of bats, 1977 to 2017, by month. Species

H

Total

Jan

Feb

Mar

Apr

May

Jun

LBB BBB CLB BAT

H H H H

YUB LEB SHB NLB KEB LLB HRB WSB TBB FRB PLB SPB FCB LNB FUB

Jul

Aug

Sep

Oct

Nov

1,775 1,142 657 651

2 3 3 2

2 2 12 3

9 7 14 3

13 25 16 9

58 92 46 10

202 159 96 42

495 296 130 274

593 367 155 180

336 156 136 90

55 26 41 24

6 4 5 11

4 5 1 3

H H H H H H   H H H H

603 458 263 138 123 66 44 27 9 6 3

    6       1        

1 1 13   1            

5 2 10 1     1        

12 5 13   1            

14 12 25 5 7     4      

66 32 24 16 16 3   2 2 2  

176 88 23 29 20 22 2 11 3   1

203 138 41 59 46 22 16 1 3 3 1

104 151 56 24 27 15 20 8     1

21 26 31 3 5 4 3 1 1 1  

1 3 10 1              

   

H * * *

1 2 1 1

  1   1

       

  1    

       

       

       

       

       

    1  

1      

       

FAB

*

1

 

 

1

 

 

 

 

 

 

 

 

 Total

 

5971

19

35

54

94

273

662

1570

1828

1125

243

41

  % Total

 

 

0.3

0.6

0.9

1.6

4.6

11.1

26.3

30.6

18.8

4.1

0.7

Dec

11       1                   25 0.4

Notes: Species marked H are known to hibernate in BC (C. Lausen, personal communication, 21 March 2013). Species marked * are exotics (Table 6.3) but don’t affect the overall trends in this table. Source: compiled from CFIA data.

activities have been transferred to the provinces and territories. In BC, the HAs have taken on the responsibility of coordinating the collection and submission of samples of animals that have exposed humans. Private veterinarians are collecting and submitting samples of animals that exposed domestic animals. Private veterinarians are also coordinating the observation of exposed domestic animals.

quarantines. Other actions carried out by the CFIA are communicating and notifying the appropriate wildlife and human health personnel, updating the manual of procedures, communicating and disseminating data and rabies brochures, providing and shipping rabies cans for rabies suspect specimens to the CFIA laboratory in Lethbridge, Alberta, and completing laboratory diagnosis of rabies and reporting results to the appropriate persons.

Canadian Food Inspection Agency (prior to 2014)

Royal Canadian Mounted Police (prior to 1995)

As a reportable disease under the Health of Animals Act and Regulations (Department of Justice, 2011), all suspected cases of rabies in animals or contact with potentially rabid animals must be reported by veterinarians to the nearest CFIA inspector. BC has 10 district offices, as far south as Osoyoos, as far east as Cranbrook, north to Dawson Creek, and west to Victoria and Vancouver, with the head office in Vancouver reporting to the western area office in Calgary, Alberta. The inspector takes the appropriate action following an investigation. Until recently, the CFIA was involved in animal bite incidents and follow-up observations and

As it did in many of Canada’s provinces, the RCMP has played an important role in the management of rabies in earlier years. With isolated communities to service and a lack of knowledge and understanding of the disease at that time, rabies management was one of dog control efforts through leashing, muzzling, and euthanizing stray animals, as well as disseminating information. As animal vaccine became available in 1950, the RCMP vaccinated dogs in some communities under the mandate of the Health of Animals Act and Regulations. The RCMP helped with the

83

A History of Rabies Management in the Provinces and Territories

collection and transport of suspected rabies specimens to the nearest laboratory for diagnosis. Since 1995, however, with diminished resources and the lack of a mandate, the RCMP has essentially withdrawn from the rabies management program.

(RPEP) at the recommendation of the MHO. (R. Birtles, personal communication, 2011)

The specimen was never tested for rabies as those involved refused to provide the specimen to the EHO. Prior to 2014, the CFIA district veterinarian was the federal contact for investigating suspect domestic animal rabies and authorizing the transport and analysis of the specimen. Since 2014, the province has taken over these responsibilities. The specimen is still shipped for diagnosis to the CFIA Animal Disease Research Institute (ADRI) in Lethbridge, Alberta. Laboratory results are usually received within 24 hours, transmitted to the CFIA office, and forwarded to the HA office for further action. The Animal Health Centre (AHC) laboratory in Abbotsford, operated by the BC Ministry of Agriculture, on occasion receives animals suspected of dying from rabies. The AHC conducts an immunohistochemical test for rabies. If positive, the sample is submitted to ADRI for confirmation.

BC Health Authorities OVERVIEW

Rabies management at the provincial level in BC is under the mandate of the Ministry of Health as authorized by the Public Health Act and the Regulations pursuant to the Act. The Act gives authority to the medical health officer (MHO) to take action to prevent the spread of infectious diseases, and the Regulations prescribe the reporting of rabies and other communicable diseases and further preventive measures (BC Laws, 2008). The MHOs and other professionals in the Health Authorities (HAs) have to carry out this responsibility jointly with the CFIA, which is authorized by the Health of Animals Act and the Reportable Diseases Regulations (CFIA, 2014; Department of Justice, 2011, 2012). Public health services in BC are provided by HAs: Northern Health, Interior Health, Fraser Health, Vancouver Coastal Health, Island Health, and First Nations Health. The Provincial Health Services Authority  – a non-geographic authority – is responsible for specialized health care and has a provincial scope. One of its agencies, the BC Centre for Disease Control (BCCDC) provides consultative service and biologics to the MHOs, public health nurses (PHNs), environmental health officers (EHOs), and administrative staff in the HAs for the risk assessment and risk management of rabies, and the recording of incidents. The following incident illustrates the difficulties of history taking:

PROTOCOL

The BCCDC (2011b, Chapter 1) has developed a rabies guideline for use by the HAs to assess and manage rabies contacts. This has been developed by BCCDC in consultation with HA representatives. This document provides information on risk assessment and management, and operational guidance (e.g., data entry). It is updated frequently to reflect evidence, best practice and changing operations. The HAs may use the rabies guideline to develop a local policy or guideline that reflects regional practices.

Risk Assessment

On receiving an animal exposure call, the HA staff (EHO, PHN, or MHO) interviews the person to determine the animal species and its behaviour, the geographic location of the exposure, the nature of the exposure, and the vaccination history, if available. The HA decides on the need for rabies post-exposure prophylaxis (RPEP). If direct contact occurred and there was a break in the skin or exposure of mucous membranes, the HA contacts CFIA to discuss arrangements for submission of the animal for rabies testing. The CFIA inspector collects and ships the specimen for testing. When this is not possible, a HA staff member, the RCMP or a conservation officer collects and ships the specimen. Depending on the result, RPEP may be started, continued, or discontinued. If a dog, cat, or ferret exposed a human, a 10-day observation period may be used to rule out rabies. One example provides an insight into the dilemma of specimen collection and transport in remote areas.

The EHO determined that a bat had hit the windshield of a driver’s truck. The animal was stunned by the impact and the driver tried to administer mouth-to-mouth resuscitation to the bat! When it didn’t seem to recover, the driver put the bat in a leather glove. Later, trying to retrieve the bat it was found to have crawled out, so it was taken home to be shown to the children, and then kept in the kitchen cupboard. Later, found in the pantry, it was assumed that the children had handled and moved it. The driver, also a taxidermist, at first refused to give the bat up to the CFIA for testing, claiming it was no longer available! The driver and his family all received rabies post-exposure prophylaxis

84

British Columbia

even WHO-approved vaccines will deteriorate without a sufficient refrigeration system, which may not be readily available in developing countries. The BC rabies guideline also directs health care providers in providing RPEP to previously immunized individuals. For individuals in highrisk occupations, or travellers heading off to endemic areas for lengthy periods, the guideline also provides direction on pre-exposure prophylaxis. If a domestic animal is potentially exposed to rabies, the CFIA may put the animal under observation (45 days) or quarantine (six months) to decrease the risk of transmission of rabies to others.

Kemano, BC, is a small community that exists primarily to service a hydro dam to provide power to the aluminum smelter (and much of the area) in Kitimat, in northwestern BC. People leaving the community would sometimes leave behind pet cats, which would become feral. One such cat ventured onto the playground of the school and scratched about 14 children. The cat was euthanized on a Thursday with the head to be sent to the Animal Diseases Research Institute (ADRI) in Lethbridge. The RCMP arranged for the cat to be sent by helicopter via Kitimat to Terrace. From there the MHO arranged that the specimen would be sent to Lethbridge through Vancouver to Edmonton, and then through the Edmonton municipal airport to the Lethbridge municipal airport, and then to ADRI with arrival on Friday afternoon. Saturday came, and there was no word of the specimen! The MHO and the shipper began frantically calling to try and locate a cat’s head. The MHO was trying to avoid immunizing 14 children with biologicals that were not readily obtainable. The specimen was finally located in Edmonton – someone had held it, thinking it was better to route it through Vancouver and Calgary. The cat’s head made it to ADRI by Sunday, and fortunately, tested negative. (W. P. Moorehead, personal communication, 2011).

Risk Communication

BCCDC and the HAs have made seasonal press releases, generally in April or May, regarding bats and rabies in BC. BCCDC and the HAs post information on their websites to advise the public on rabies prevention. Healthlink BC (2012) provides information through the Health Files. Rabies is potentially a travel-acquired illness for Canadians who travel to enzootic parts of the world (Nicolie, 2002). Pre-travel advice and pre-exposure prophylaxis may be necessary to decrease this risk (Krause et al., 1999; Zimmer, 2012). Many people from BC travel to countries where rabies is common, and diagnosis and treatment may be absent or not immediately available. Indeed, as the next section illustrates, in 2012 over 57% of those persons in BC receiving RPEP were exposed outside Canada.

Risk Management

Based on the risk assessment, the MHO makes a decision regarding the need for RPEP. If this is required, the PHN typically makes the arrangements for RPEP. BC follows the National Advisory Committee on Immunizations (NACI) recommendation and has reduced the number of rabies vaccine doses during RPEP to four vaccinations from five for immuno-competent individuals (Public Health Agency of Canada [PHAC], 2009). The United States developed the evidence for this approach and approved a similar protocol in 2010. The rabies guideline also provides guidance to MHOs to help them assess the RPEP that travellers may have received while abroad. In some circumstances, the guideline also recommends taking a blood sample for rabies antibody titre to be determined at the National Microbiology Laboratory in Winnipeg. If the titre comes back at >0.5 IU/ mL, sufficient protection against the rabies virus has been accorded. Another concern, apart from counterfeit vaccine, is the problem of biologicals that have not received World Health Organization (WHO) pre-qualification. The guideline spells out which vaccines have received approval from WHO to provide assistance to the MHO in deciding the validity of RPEP received abroad, including a concern that

Human Exposure to Animals

In its annual summary of reportable communicable diseases on the BCCDC website, the province shows the following rabies data: the number of human exposures to animals that require RPEP and the gender, age, seasonality, location, type of exposure, and animal species involved. An exposure is a report of an individual exposed to an animal or a human that presents a risk of rabies infection; it does not mean that an animal specimen was necessarily tested and, therefore, these data provide an additional insight into how a province handles risk management regarding rabies. Data for analysis for 2003 to 2012 were obtained in June 2013 with a written application by the authors to BCCDA from the now defunct integrated Public Health Information System (iPHIS). Data after 2012 was extracted directly from annual summaries of reportable communicable diseases on the BCCDA website (BCCDC, 2016, 2017a). Limitations of the data include the following: some exposures occurring outside BC in which the exposed person(s) received the complete RPEP series may not be included, prior to 2009 there was no standardization of data entry, and after 2009

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only exposures for which the MHO recommended RPEP were reported. Overall, the number of reported rabies exposures has decreased over time. Over the 2003–2016 period, almost 31% of all exposures occurred outside the province. Beginning in 2008, exposures occurring within BC dropped sharply (Figure 6.3) while exposures outside BC have increased and, from 2010 onwards, exposures outside BC usually have exceeded those inside the province (Figure 6.3). The decrease inside BC correlates with two policy changes announced in August 2008 and in 2009 that are discussed next. The reason for the increase in outside exposures is unclear although it could be related to increased travel in countries where rabies is enzootic. In July 2008 there was a recommendation that only exposures that led to RPEP should be reported. While this did not occur in every instance, the reported inside BC exposures dropped, as shown in Figure 6.3. Further, the proportion of exposed individuals receiving RPEP increased for both inside and outside BC exposures to over 80% and 90%, respectively (Table 6.5). The higher values for outside exposures reflect the higher risk of travelling in enzootic areas and, typically, less detailed information on the circumstances of the exposure. As well, there were striking differences in the type of exposure inside and outside BC for 2003–2012 (Table 6.6). Bites were by far the highest reported type of exposure outside the province. This contrast is also observed in the animals involved in the exposures inside and outside BC (Table 6.7). Dogs dominate exposures occurring outside BC while bat exposures dominate inside BC. There were four exposures among health

personnel who were involved with the human rabies case in BC in 2003. None of those exposures resulted in RPEP. The 10 exposures linked to a human outside BC occurred in 2012. Those people were part of a medical team travelling to another country where they were exposed to human rabies. All 10 exposures resulted in RPEPs. Exposures inside and outside BC also vary by age (Figure 6.4). In older adults (>40 years), the proportion exposed inside and outside BC is about the same. In younger age groups, there is a greater proportion of children exposed within BC and a greater proportion of young adults exposed outside BC. This may reflect different travel patterns by age category. The high number of bat exposures in BC was in part related to the policy before 2008. The 2007 BCCDC Annual Summary of Reportable Diseases (2008, p. 100) stated the old policy that RPEP must be offered “when a bat is present in a room and the person cannot provide a history that excludes any possible bite, scratch or mucous membrane exposure (e.g., child in a room with a bat present).” In August 2008, however, this policy changed: “RPEP is no longer recommended in BC if a bat is found in a bedroom and there is no evidence of direct contact with the bat” (BCCDC, 2011a, p. 102). The result of the policy change was dramatic. Between 2003 and 2008, the mean annual number of exposures by bats was over 224, and it dropped to fewer than 45 from 2009 to 2012, a fivefold decrease. This was also the major reason for the overall drop in exposures reported in BC (Table 6.5). The rationale for the policy change is that the risk of rabies when there is no evidence of physical contact is

Figure 6.3: Rabies exposures inside and outside BC over time, 2003 to 2016. Source: created from BCCDC data.

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Table 6.5  Rabies post-exposure prophylaxis (RPEP) recommended for exposures inside and outside the province, BC, 2003 to 2012. Inside Year 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012  Total

RPEP 204 241 173 124 257 120 76 46 41 66 1348

Total 306 300 218 283 338 161 92 54 46 66 1864

Table 6.6  Exposures by type for inside and outside BC, 2003 to 2012. Exposure Blank Bat in same room Bite Handling Nearby Saliva (bite) Saliva (non-bite) Scratch Unknown  Total

Outside % 66.7 80.3 79.4 43.8 76 74.5 82.6 85.2 89.1 100 72.3

RPEP 17 40 44 27 41 70 65 64 78 89 535

Total 34 56 44 44 48 76 68 69 84 92 615

% 50 71.4 100 61.4 85.4 92.1 95.6 92.8 92.9 96.7 87

Inside 63 3.4% 475 25.5% 408 21.9% 283 15.2% 333 17.9% 10 0.5% 38 2.0% 118 6.3% 136 7.3% 1,864

7 9 480 8 8 8 20 67 8 615

Outside 1.1% 1.5% 78.0% 1.3% 1.3% 1.3% 1.3% 10.9% 1.3%

Source: compiled from BCCDC data.

Source: compiled from BCCDC data.

Table 6.7  Exposures inside and outside BC by species, 2003 to 2012. Species

exceedingly low. Only two human cases of bat-variant rabies in the United States and Canada between 1950 and 2007 had unrecognized bat exposure while sleeping in a bedroom (De Serres et al., 2008). De Serres et al. (2009) found 2.7 million people would have to be vaccinated (using RPEP) to prevent a single case of rabies from the bat-in-bedroom scenario, at a cost of $2.1 billion. The likelihood of human rabies from a bat-in-bedroom scenario in BC is 1 case every 675 years. BCCDC then recommended that “occult bat exposures” without evidence of physical contact – when a bat is found in a room with individuals who had been asleep or who were not competent to identify or communicate an actual physical contact with the bat – did not warrant RPEP, unless physical contact could not be ruled out. The policy and practice changed, effective August 2008, and this recommendation was included in the BC rabies guideline in February 2009. The guideline does not seek to provide zero risk but a reasonable, sustainable risk. The NACI followed suit with its statement in support of this policy in November 2009 (PHAC, 2009). Automatically qualifying people for RPEP based on finding a bat in the bedroom had been an expensive policy. Using a cost of $1000 per person for biologicals and averaging the number of people exposed to animals from 2003 to 2007 (not all ­received RPEP) before the new guideline suggested that RPEP cost about $300,000 per year (De Serres et al., 2009). For 2009 and 2011, the first three years under the new guideline, the average cost for RPEP in BC was calculated at ­approximately $124,000 per year, a savings of $176,000 per year. An earlier study by Stephen, Daly, and Martin in BC provides a comparison of costs for the public health response

Bat Cat Dog Ferret Fox Human Raccoon Skunk Squirrel/chipmunk Other Not recorded Unknown  Total

Inside 1,524 84 129 2 1 4 28 2 10 55 3 22 1,864

81.80% 4.50% 6.90% 0.10% 0.10% 0.20% 1.50% 0.10% 0.50% 3.00% 0.50% 1.20%  

Outside 42 54 367 0 1 10 8 0 0 127 3 3 615

6.80% 8.80% 59.70% 0 0.20% 1.60% 1.30% 0 0 20.70% 0.50% 0.50%  

Source: compiled from BCCDC data.

to rabies in BC for 1989 to 1994 (Stephen et  al., 1996). The average cost of RPEP was estimated at $450/person; the physician costs of administering the therapy at $150/ person, based on an initial assessment and five visits for immunization; and the cost of investigating and testing the animals at $165/animal. In the study period, 282 humans were exposed and 1459 animals tested for a total cost of $410,000. The cost did not include ancillary medical costs associated with wound management, public health and veterinary costs associated with tracing contacts and quarantines, the cost of storing and transporting the rabies vaccine and immune globulin, and the costs of pre-exposure rabies immunization for people and animals. VACCINATION OF DOMESTIC PETS

British Columbia, like many of Canada’s provinces, has a well-established system of veterinary clinics, offering a wide range of services, including rabies vaccination. These

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Figure 6.4: Exposures inside and outside BC by age category, 2003–2012. Source: created from BCCDC data.

are often associated with the larger cities and towns. All the veterinarians practising in BC are mandated by the College of Veterinarians of British Columbia (2012) to promote and enforce standards of veterinary practice. Working with the CFIA inspectors and those of the HAs, veterinarians promote regular vaccination for domestic pets, including that for rabies.

responsibility to the provinces. Currently, under the BC Rabies Control Program, any veterinarian who suspects rabies in an animal either alive or dead, informs the BCCDC public health veterinarian to obtain assistance with risk assessment and management (BCCDC, 2017b). In the case of human involvement with a suspect rabid animal, the local public HAs under the direction of the medical health officer are involved to determine the risk and need for ­post-exposure treatment. Assistance for the risk assessment and management of domestic animals is ­obtained from the public health veterinarian of the BCCDC, and ­assistance regarding wild animals is obtained from the wildlife veterinarian from Forests, Lands and Natural Resources Operations. The veterinarian or the EHO is responsible for submitting specimens from the suspect rabid animal with human or domestic animal contact to the CFIA Lethbridge laboratory for diagnosis. As part of increased surveillance for bats in BC, in the event that no human or animal contact has occurred, the specimen may be sent to the Animal Health Centre at Abbotsford for diagnosis. A positive immunohistochemical test is reported to CFIA, and the sample is sent to CFIA for confirmation. Table 6.8 shows rabies cases between 2014 and 2017 under this surveillance protocol. Of the 46 bats diagnosed as positive in this period, 19 (41%) had no human or animal contact. As shown previously in Table 6.3, the big brown bat and the little brown bat are the most often diagnosed species.

OUTSIDER CLINICS

Many of the BC communities north of the 54-degree parallel do not receive regular veterinary care, areas such as Burns Lake, Smithers, Terrace, and Kitimat. Here, charity groups such as the Canadian Animal Assistance Team (CAAT), offer neutering and spay clinics, as well as deworming and rabies vaccinations once a year. In 2011 CAAT visited First Nations in Burns Lake area for ten days and carried out 250 surgeries and 328 vaccinations including deworming. Chris Robinson, executive director CAAT, argues there is a real need for this service given that many people with pets had to be turned away (personal communication, 7–9 March 2012). CAAT returned to the Burns Lake area in 2012.

Rabies 2014–2017 Rabies is a reportable disease, under the Health of Animals Act of CFIA and also to the chief veterinary officer (CVO) in BC under the Reportable and Notifiable Disease Regulation, pursuant to the BC Animal Health Act (2014). The CVO shares the rabies reports in animals with the provincial health officer under an information sharing agreement. As noted, as of 1 April 2014, the CFIA is no longer involved with managing rabies cases in Canada, leaving this

Discussion With few exceptions, bats have been the major vector of rabies in BC – this makes the province unique in Canada. The big brown bat accounts for almost 50% of rabies

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positives, even though it has fewer submissions than the little brown bat. Fortunately, the big brown bat has not been associated with a single human rabies case in almost 20 years. Greater concern should be shown regarding the silver-haired bat, with 15% of positives and far fewer submissions (Table 6.3), primarily from the more populous Greater Vancouver area. The solitary and inconspicuous silver-haired bat has been associated with 15 of the 21 human deaths in the United States and has been found to react more aggressively when rabid (Pape et  al., 1999). Furthermore, despite the lower number of submissions of the silver-haired bat, more of those submissions have occurred in the winter months than any other species. Increased odds of a submitted bat being rabid were associated with species that exhibit inconspicuous roosting habits, such as the silver-haired bat, as opposed to the more gregarious bats with conspicuous roosting habits, such as the big brown bat or the little brown bat (Patyk et al., 2012). This is a potentially significant public health issue in North America and requires a continuing awareness of bat rabies by provincial and federal authorities. Patyk and colleagues (2012) suggest that bat biologists be used when necessary to identify bat species and that wildlife and veterinary students be given a course on bat identification. As climate variations continue to occur and affect hibernating species and, therefore, extend the annual window for exposures, continuing surveillance and proper identification of species involved is very important. As Table 6.8 has shown, extending surveillance efforts to include bats with no human or animal contact increases the number of cases diagnosed and, hopefully, increases the awareness of the extent of rabies in the province. Rabies surveillance, however, is relatively costly. Between 1977 and 2017, 7.5% (417/5528) of bat submissions were diagnosed as positive for rabies in BC (see Chapter 34 for specimen costs). This compares closely to the national surveillance data for bat rabies in the United States between 2001 and 2009 (Patyk et  al., 2012). Over all species, 25 submissions were required to find one positive case. Currently, BC reports only an average of 12 animal rabies cases per year, primarily in bats. The only reported human deaths in BC were in 2003 and 2019 (see Chapters 3b and 27). BC has shown it is possible to reduce costs somewhat without increasing risk by changing the requirements for RPEP if bats are found in a bedroom. Provided there is no evidence of physical contact, RPEP is not recommended. The results of this policy change in August 2008 have been dramatic: since then, reported exposures and recommended RPEPs have dropped sharply,

Table 6.8  Positive bats by year and species, 2014 to 2017. Species Bat Big brown bat California bat Hoary bat Little brown bat Long-eared bat Silver-haired bat Yuma bat  Total

Code BAT BBB CLB HRB LBB LEB

2014   3 (1)     3 (3)  

2015 1 3 (2)     3 (1) 1

SHB

2 (1)

1

YUB  

1 9

  9

2016 4 6 (5)     3   2 2 (1) 17

2017   3 (2) 6 (1) 1   1 (1)     11

Total 5 15 (10) 6 (1) 1 9 (4) 2 (1) 5 (1) 3 (1) 46 (19)

Note: The portion of cases with no human or animal contact are shown in parentheses. Source: compiled from BCCDC data.

resulting in an estimated savings of $176,000 per year. Health personnel also report that the clarity of the new policy has helped eliminate uncertainty and has reduced the administrative workload while maintaining an appropriate ­response to risk (E. Galanis, personal communication, 4 July 2013). Exposures and treatments in BC have an additional feature that appears to be unique in Canada. At present, RPEPs resulting from exposures of BC residents travelling outside the province or country exceed RPEPs recommended for exposures inside the province. Exposures inside the province typically involve bats, and exposures outside the province are usually associated with dog bites. Provincial authorities can do little about travellers, aside from educating them to recognize and avoid potential risky situations and to have pre-exposure prophylaxis. BC seems well positioned to identify and adapt to future changes: it is isolated from the rabies experience in the rest of Canada; it has an excellent reporting system; and it has a well-worked-out system for prevention and control. It does not have a terrestrial wildlife control program in place but, given that bats are the major problem, this is not necessary at the present time. BC’s current challenges are (1) the increasing human rabies exposures for BC residents travelling outside the country, (2) the lack of rabies control for bats, and (3) if the climate continues to warm, bat hibernation times will diminish leading to an increased risk of rabies exposure. To date the transition of animal rabies risk assessment and specimen control activities from the CFIA to the province in 2014 does not appear to have affected response to rabies situations. The long-term effect remains to be seen on both BC and Canada wide rabies reporting.

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Acknowledgments The co-authors would like to acknowledge the assistance of Dr Erin Fraser, public health veterinarian, BC Centre for Disease Control in clarifying the recent changes to the program for rabies management in BC and providing data on the bat surveillance carried out on bats with no human or animal contact for 2013 to 2017.

References Avery, J. R., & Tailyour, J. M. (1960). Isolation of the rabies virus from insectivorous bats in British Columbia. Canadian Journal Comparative Medical Veterinary Science, 24, 143–146. BC Centre for Disease Control. (2008). 2007 epidemiology report: 2007 British Columbia annual summary of reportable diseases. R­etrieved from http://www.bccdc.ca/resource-gallery/_layouts/15/DocIdRedir.aspx?ID=BCCDC-288-3352 BC Centre for Disease Control. (2011a). 2010 epidemiology report: 2010 British Columbia annual summary of reportable diseases. ­Retrieved from http://www.bccdc.ca/resource-gallery/_layouts/15/DocIdRedir.aspx?ID=BCCDC-291-28 BC Centre for Disease Control. (2011b). Chapter 1: Management of specific diseases – Rabies. In Communicable disease control manual. Retrieved from http://www.bccdc.ca/health-professionals/clinical-resources/communicable-disease-control-manual /communicable-disease-control BC Centre for Disease Control. (2016). 2015 epidemiology report: 2015 British Columbia annual summary of reportable diseases. ­Retrieved from http://www.bccdc.ca/resource-gallery/Documents/Statistics%20and%20Research/Statistics%20and%20Reports /Epid/Annual%20Reports/2015CDAnnualReportFinal.pdf BC Centre for Disease Control. (2017a). 2016 epidemiology report: 2016 British Columbia annual summary of reportable diseases. ­Retrieved from http://www.bccdc.ca/resource-gallery/Documents/Statistics%20and%20Research/Statistics%20and%20Reports /Epid/Annual%20Reports/2016CDAnnualReportFinal.pdf BC Centre for Disease Control. (2017b). BC rabies guidance for veterinarians. Retrieved from http://www.bccdc.ca/Documents/BC %20Rabies%20Guidance%20for%20Veterinarians_Nov%202017.pdf BC Laws. (2008). Public Health Act [SBC 2008], C.28. Retrieved from http://www.bclaws.ca/EPLibraries/bclaws_new/document/ID /freeside/00_08028_01 Brigham, M. (2010). Bats of British Columbia. Retrieved from E-Fauna BC website: http://ibis.geog.ubc.ca/biodiversity/efauna /BatsofBritishColumbia.html Canadian Food Inspection Agency. (2012). Area and regional offices-western area. Retrieved from http://www.inspection.gc.ca/ about-the-cfia/offices/eng/1313255382836/1313256130232 Canadian Food Inspection Agency. (2014). Positive rabies in Canada, 2013. Retrieved from http://www.inspection.gc.ca /animals/terrestrial-animals/diseases/reportable/rabies/rabies-in-canada/positive-rabies-2011-2013-/eng/1406218460196 /1406218461478 Community Bat Programs of BC. (2014). BC’s bat species. Retrieved from https://www.bcbats.ca/index.php/bat-basics/bc-bat-species Copeland, L., Gregory, D., & Webster, A. (1985). Rabid beaver incident – British Columbia. Canada Diseases Weekly Report, 11, 214–215. College of Veterinarians of British Columbia. (2012). CVBC mandate. Retrieved from http://www.cvbc.ca/CVBC1/About/CVBC1 /About.aspx Department of Justice. (2011). Health of Animals Act, S.C. 1990, c. 21. Retrieved from http://laws-lois.justice.gc.ca/eng/acts/H-3.3/ Department of Justice. (2012). Reportable diseases regulations, SOR/91-2. Retrieved from http://laws-lois.justice.gc.ca/eng/regulations /SOR-91-2/index.html De Serres, G., Dallaire, F., Côte, M., & Skowronski, D. M. (2008). Bat rabies in the United States and Canada from 1950 through 2007: Human cases with and without bat contact. Clinical Infectious Diseases, 46(9), 1329–1337. https://doi.org/10.1086/586745 De Serres, G., Skowronski, D. M., Mimault, P., Ouakki, M. Maranda-Aubut, R., & Duval, B. (2009). Bats in the bedroom, bats in the ­belfry: Reanalysis of the rationale for rabies post exposure prophylaxis. Clinical Infectious Diseases, 48(11), 1493–1499. https://doi .org/10.1086/598998 Healthlink BC. (2012). Healthlink BC files: Rabies. https://www.healthlinkbc.ca/services-and-resources/healthlinkbc-files#health-files-r Krause, E., Grundmann, H., & Hatz, C. (1999). Pre-travel advice neglects rabies risk for travellers to tropical countries. Journal of Travel Medicine, 6(3), 163–167. https://doi.org/10.1111/j.1708-8305.1999.tb00854.x Nagorsen, D. (2010). An introduction to the mammals of British Columbia. Retrieved from E-Fauna BC website: http://ibis.geog.ubc .ca/biodiversity/efauna/mammals.html

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British Columbia Nagorsen, D. W., & Brigham, R. M. (1993). Bats of British Columbia. In Royal British Columbia Museum handbook (Vol. 1: The ­Mammals of British Columbia). Vancouver, BC: UBC Press. Nagorsen, D.W., & Paterson, B. (2012). An update on the status of red bats, Lasiurus blossivilli and Lasiurus borealis, in British Columbia. Northwestern Naturalist, 93(3), 235–237. https://doi.org/10.1898/12-01.1 Nicolie, L. (2002) Rabies: Still with us. The Canadian Journal of Infectious Diseases, 13(2), 83–84. https://doi.org/10.1155/2002/149410 Pape, W. J., Fitzsimmons, T. D., & Hoffman, R. E. (1999). Risk of rabies transmission from encounters with bats, Colorado, 1977–1996. Emerging Infectious Diseases, 5(3), 433–437. https://doi.org/10.3201/eid0503.990315 Patyk, K., Turmelle, A., Blanton, J. D., & Rupprecht, C. E. (2012). Trends in national surveillance data for bat rabies in the United States: 2001–2009. Vector-Borne and Zoonotic Diseases, 12(8), 666–673. https://doi.org/10.1089/vbz.2011.0839 Plummer, P. J. G. (1954). Rabies in Canada, with special reference to wildlife reservoirs. Bulletin World Health. Organisation, 10, 767–774. Public Health Agency of Canada. (2009). National Advisory Committee on Immunization: Recommendations regarding the management of bat exposures to prevent human rabies. Retrieved from http://origin.phac-aspc.gc.ca/publicat/ccdr-rmtc/09vol35/acs-dcc-7 /index-eng.php Report of the veterinary director general for the year ending March 31, 1915. (1015). Ottawa, ON: Department of Agriculture. Available from Library and Archives Canada, https://bac-lac.on.worldcat.org/oclc/29657040 Report of the veterinary director general for the year ending March 31, 1921. (1921). Ottawa, ON: Department of Agriculture. Available from Library and Archives Canada, https://bac-lac.on.worldcat.org/oclc/29657040 Report of the veterinary director general for the year ending March 31, 1922. (1922). Ottawa, ON: Department of Agriculture. Available from Library and Archives Canada, https://bac-lac.on.worldcat.org/oclc/29657040 Report of the veterinary director general for the year ending March 31, 1928. (1928). Ottawa, ON: Department of Agriculture. Available from Library and Archives Canada, https://bac-lac.on.worldcat.org/oclc/29657040 Statistics Canada. (2013). Population by year by province and territory. Retrieved from http://www.statcan.gc.ca/tables-tableaux /sum-som/101/cst01/demo02a-eng.htm Stephen, C., Daly, P., & Martin, M. (1996). The public health response to suspected rabies exposure in British Columbia (1989–1994). Canadian Veterinary Journal, 37, 163–164. Tabel, H., Corner, A. H., Webster, W. A., & Casey, C. A. (1974). History and epizootiology of rabies in Canada. Canadian Veterinary Journal, 15(10), 271–281. Webster, W. A., Casey, G. A., & Charlton, K. M. (1986). Major antigenic groups of rabies virus in Canada determined by anti-­ nucleocapsid monoclonal antibodies. Comparative Immunology Microbiology Infectious Diseases, 9(1), 59–69. https://doi .org/10.1016/0147-9571(86)90076-7 Zimmer, R. (2012). The pre-travel visit should start with a “risk conversation”. Journal of Travel Medicine, 19(5), 277–280. https://doi .org/10.1111/j.1708-8305.2012.00631.x

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7 Alberta Margo J. Pybus Alberta Fish and Wildlife Division and University of Alberta, Edmonton, Alberta, Canada

Place Alberta has its origins in Rupert’s land, the North-Western Territory, and the fur traders who arrived in the early 1700s. The land was occupied before this date by Indigenous peoples going back thousands of years (see Overview, Part 3). From 1874 to 1898, the North-west Territories (as it then was called) was subdivided several times to create Manitoba in 1870 and the Districts of Keewatin (1876), Ungava, Athabasca, Mackenzie, Alberta, Saskatchewan and Assiniboia by 1895. Yukon was created as a separate territory by 1898, and by 1905 Alberta and Saskatchewan were created, respectively, as the eighth and ninth provinces of Canada with their boundaries as they are today (see Overview, Part 3). Alberta was named after Princess Louise Caroline Alberta, the fourth daughter of Queen Victoria and Albert, the prince consort. Lake Louise and Mount Alberta also are named in honour of Princess Louise (Natural Resources Canada, 2016). Alberta lies between the 49th and 60th North parallels, separated from British Columbia on the west by the Rocky Mountains, Montana on the south, Saskatchewan to the east, and the Northwest Territories to the north (Government of Alberta, 2013). With Edmonton as its capital, Alberta has an area of 661,190 km2 and had a population of 3.9 million people in 2012 (Statistics Canada, 2013). Alberta has four physiographic regions: alpine, boreal forest, parkland, and prairie (Figure 7.1). It is home to a broad biodiversity of wildlife and habitats across a range of natural ecosystems. In the context of rabies, there are many large carnivores such as the grizzly and black bear

(Ursus arctos, U. Americanus), as well as smaller carnivores of the canine and feline families, including coyotes (Canis latrans), wolves (Canis lupus), red fox (Vulpes vulpes), lynx (Lynx canadensis), bobcat (Lynx rufus), and cougar (Puma concolor). Northern Alberta has the world’s largest free-roaming bison herd (Bison bison) in Wood Buffalo National Park, which is Canada’s largest national park and a UNESCO (United Nations Educational, Scientific and Cultural Organization) World Heritage site. Alberta is the only province in Canada and one of the few places worldwide free of the Norwegian rat. This is the result of an ongoing rat-control program initiated by the Alberta government in the early 1950s (Bourne, 1998), which became the model for Alberta’s skunk rabies control program.

The History of Rabies in Alberta Early Rabies, before 1960 The history of rabies in Alberta appears to begin in 1906. Early reports of rabies in Alberta are in the annual reports of the veterinary director general (VDG; Report of the Veterinary Director General, 1909, p. 10; see Chapter 2) for the Canada Department of Agriculture. The Report of the Veterinary Director General in 1910 describes an outbreak that occurred in the fall of 1909 in Red Deer, Alberta, because of a dog imported from Hamilton, Ontario. Five premises were placed under quarantine, and the incident led to the regulation to restrict importation of animals (Report of the Veterinary Director General, 1911, p. 10). By

Alberta

Figure 7.1: Map of Alberta showing the four major physiographic regions and skunk control zone along the Alberta-Saskatchewan border. Source: compiled from Natural Resources Canada base maps.

1910 the VDG reported four premises under quarantine in Red Deer (Report of the Veterinary Director General, 1910). The outbreak continued, and for the Report of the Veterinary Director General, 1913 (p. 13), 42 premises were under quarantine for rabies in the districts of Edmonton (1 premise), Victoria (32 premises), and Medicine Hat (8 premises). No further cases were reported until 1917 (Report of the Veterinary Director General, 1917, p. 7) and 1918 (Report of the Veterinary Director General, 1918, p. 11), when one premise in Calgary and one in Edmonton were quarantined. Reports of animal rabies have been maintained by the federal Department of Agriculture since 1926 and show an outbreak in 1927 in Alberta involving six dogs and one cow (Report of the Veterinary Director General, 1927, p. 14).

During the early 1950s, an epizootic of arctic variant rabies in red foxes and coyotes spread south from the Arctic into the prairie provinces (Plummer, 1954; Tabel et  al., 1974). The first case in Alberta was in a fox during June 1952 (Ballantyne, 1958, p. 88). The disease quickly spread 1100 kilometres in eight months throughout Alberta with the involvement of coyotes (Ballantyne & O’Donoghue, 1954). From 1952 to 1958, there were 186 rabid animals reported in Alberta (Table 7.1 and Figure 7.1). While Saskatchewan and Manitoba did not react to the outbreak, more than 180,000 animals were trapped, shot, or poisoned in Alberta from 1952 to 1954 (Ballantyne & O’Donoghue, 1954). That total, considered a minimum estimate, included about 100,000 animals from northern Alberta: 50,000 foxes,

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Positive cases of rabies in bats were first seen in 1971, peaking between 1973 and 1980 then declining to a few cases per year, with a minor increase in 2016–2017 (Table 7.1 and Figure 7.2). Today, rabies in wildlife in Alberta is found only in bats. Ten species of bats occur in Alberta (Government of Alberta, 2018; Table 7.2). Despite the little brown bat (Myotis lucifugus) being the species most often tested, rabies is most often seen in the big brown bat (Eptesicus fuscus). The first report of rabies-positive skunks in Alberta was in 1971. This outbreak was an extension of the east-to-west spread of skunk rabies across Manitoba and Saskatchewan then into eastern Alberta (Tabel et al., 1974; see Figure 8.1). With the exception of 1977 (no positive cases), small foci of rabid skunks continued through to 1994 with peaks in 1980 (54 cases) and 1987 (36 cases) (Pybus, 1988a; Rosatte et al., 1986). By 1994, no further skunk cases were found (Figure 7.2 and Table 7.1). Note that the values in Figure 7.2

35,000 coyotes, 4200 wolves, 7500 lynx, 1850 bears, 500 skunks (Mephitis mephitis), 64 cougars, 4 badgers (Taxidea taxus), and 1 wolverine (Gulo gulo). An additional 60,000 to 80,000 coyotes were killed in the agricultural areas of southern Alberta (Ballantyne & O’Donoghue 1954). After 1955, the only case of rabies in a fox in Alberta was in 1998 in Evansburg, west of Edmonton. Further details of rabies in this time period are given in the section “Response to Rabies in the 1950s.” The spread of this outbreak is illustrated in Chapter 2, Figure 2.2.

Rabies post 1960 Rabies was not reported again until 1970, with the exception of one dog and one cow in 1965 and 1966, respectively. The reappearance of rabies in 1970 involved 17 cases in dogs, livestock, coyotes, and wolves, and in 1971 rabid skunks were found for the first time (Table 7.1, Figure 7.1).

Table 7.1  Positive rabies cases, Alberta, 1927 to 2017. Years with no rabies between 1927 and 1952 were omitted. Year

Total

Bat

Skunk

1927 1952 1953 1954 1955 1956 1957 1958 1959 1960 1961 1962 1963 1964 1965 1966 1967 1968 1969 1970 1971 1972 1973 1974 1975 1976 1977 1978 1979 1980 1981 1982 1983 1984 1985

7 19 89 51 41 16 0 1 0 0 0 0 0 0 1 1 0 0 0 17 22 16 39 26 25 39 18 5 15 66 34 51 40 13 12

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 8 30 20 21 28 10 5 12 11 9 7 5 5 4

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 2 4 6 6 3 11 7 0 3 54 24 43 32 7 8

Dom

Live

Wild

Fox

6 5 35 12 7 3 0 1 0 0 0 0 0 0 1 0 0 0 0 6 4 1 1 0 0 0 0 0 0 1 1 0 3 1 0

1 3 13 23 13 6 0 0 0 0 0 0 0 0 0 1 0 0 0 5 7 1 1 0 0 0 1 0 0 0 0 1 0 0 0

0 2 19 14 19 7 0 0 0 0 0 0 0 0 0 0 0 0 0 5 6 2 1 0 1 0 0 0 0 0 0 0 0 0 0

0 8 14 2 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

Other 0 1 8 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 (Continued)

94

Alberta

Year 1986 1987 1988 1989 1990 1991 1992 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2012 2013 2014 2015 2016 2017 Total % Total

Total 7 47 28 18 42 13 11 13 2 3 2 8 6 3 3 4 6 4 3 1 5 1 1 2 3 2 4 4 4 10 7 931

Bat 6 7 8 6 12 6 5 8 2 2 2 8 4 3 3 3 6 4 3 1 4 0 1 2 2 2 3 4 4 10 7 316 33.9

Skunk 1 36 19 12 25 7 3 5 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 318 34.2

Dom 0 2 0 0 4 0 2 0 0 1 0 0 1 0 0 1 0 0 0 0 1 0 0 0 1 0 1 0 0 0 0 102 11.0

Live 0 2 1 0 1 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 81 8.7

Wild 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 76 8.2

Fox 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 26 2.8

Other 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 12 1.3

Dom = cat/dog; Live = livestock. Source: compiled from CFIA data.

Rabies Management Alberta

and Table 7.1 were a combination of the Canadian Food Inspection Agency’s (CFIA) passive surveillance and Alberta’s own active surveillance. The management of the outbreak in skunks is discussed in this chapter under “Skunk Rabies, 1970 to 1993.”

General Considerations Alberta has no history of enzootic terrestrial rabies variants. Thus incursions of rabies are viewed as an unwanted invader against which the province has waged war successfully for many years. Coordinated rabies control programs that began in the early 1950s were refocused in the 1970s and continue today. Current and cumulative evidence (Table 7.2) suggests that the province remains free of arctic fox (Alopex lagopus) and prairie skunk rabies, the two terrestrial variants for which there is a significant risk of incursion into Alberta. The key to the ongoing success of rabies control in Alberta has been a collaborative process among governments, agencies, stakeholders, and interested parties. The next section, therefore, provides an overview of the relationships that played an important role in maintaining Alberta’s rabies control programs, how the interactions

Active Surveillance Active surveillance began in the early 1970s and concentrated on skunks, the primary vector at the time. Since the skunk outbreak was thought to have come across the eastern border with Saskatchewan, active surveillance efforts in Alberta targeted the border from the United States north to Cold Lake (Pybus, 1988a; Rosatte et al., 1986, and control zone in Figure 7.1). This surveillance was to assess the magnitude of any skunk outbreak and provide warning of further incursions. The results are shown in Table 7.2. The specimens were collected by provincial wildlife and municipal field specialists using gassing, shooting, or trapping and examined, for the most part, in the CFIA laboratory at Lethbridge.

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A History of Rabies Management in the Provinces and Territories

Figure 7.2: Annual rabies-positives in Alberta 1952–2017. “Wild” includes coyote, wolf, and fox but is primarily coyote. Source: compiled from CFIA data.

changed over time, and how they flourished and provided benefits to all involved. Additional details of directed wildlife rabies control in Alberta are found in Chapter 28, on skunk rabies ecology and epizootiology.

Lands and Forests (there were no designated wildlife staff in 1950); 77 pest control specialists with the Field Crops Branch of Alberta Agriculture; staff veterinarians with the federal Department of Agriculture; and local members of the Royal Canadian Mounted Police (RCMP). George Mitchell, the first provincial game biologist, was hired in 1952 to manage the program (Fish and Wildlife Historical Society, 2005). There was a province-wide mobilization of government and non-government people and resources to literally wage an integrated war against the invading rabies virus. All three levels of government – federal, provincial, and municipal – were fully engaged, along with trappers, ranchers, Indigenous peoples, and the general public. Ballantyne and O’Donoghue (1954) put the rabies control effort in perspective: “The province is three times the size of the British Isles, or five times the size of New York State. Its northern-south dimension is 750 air miles, slightly

Response to Rabies in the 1950s As the invasion of arctic fox rabies variant swept southwards out of the Northwest Territories in 1952 (Ballantyne, 1957, 1958; Ballantyne & O’Donoghue, 1954), this variant appeared in coyotes, cats, dogs, and livestock (see Table 7.2 and Figure 2.2). The province responded with a massive province-wide multi-pronged approach coordinated by Alberta Department of Agriculture and led primarily by Drs Ballantyne and O’Donoghue, staff veterinarians with the Veterinary Services Branch. This program was delivered in conjunction with forestry staff of Alberta Department of 96

Alberta

Table 7.2  Bat species, Alberta, by laboratory code, species name, total number of submissions, negatives (N), positives (P), and unknown (U), 1992 to 2017. Code LBB BBB SHB BAT NLB HRB LEB LLB REB WSB YUB

Name Little brown bat Big brown bat Silver-haired bat Unspecified Northern bat Hoary bat Long-eared myotis Long-legged bat Eastern red bat Western small-footed bat Yuma myotis Total

Scientific Name Myotis lucifugus Eptesicus fuscus Lasionycteris noctivagans Myotis septentrionalis Lasiurus cinereus Myotis evotis Myotis volans Lasiurus borealis Myotis ciliolabrum Myotis yumanensis

Total 769 483 396 159 42 31 5 9 4 25 1 1.924

N 755 429 367 152 41 22 5 9 4 23 0 1,807

P 4 48 24 3 1 9 0 0 0 2 1 92

U 20 12 10 8 0 0 0 0 0 0 0 50

%P 0.5 9.9 6.1 1.9 2.4 29.0 0.0 0.0 0.0 8.0 100.0 4.8

Source: compiled from CFIA data.

Another key component in the success of the 1950s lay in organizing the primary activities among various agencies and interest groups as described in the following paragraphs. The provincial Agricultural Department had the lead role and provided much of the footwork in getting things done; helped with federal vaccination clinics; provided leak-proof metal cans, heavy rubber gloves, disinfectant, head collection techniques, and history forms to those submitting heads for testing; received heads from field sites and forwarded them to the federal testing lab in Lethbridge; established container depots all across Alberta at ranger stations, veterinary offices, agriculture offices, and RCMP detachments; and designed and delivered coyote control in farming areas. The provincial public health authorities delivered the human health component of the education programs; advised agriculture, wildlife, or RCMP staff about how to deliver the message in remote areas; and provided the Pasteur treatment to approximately 200 persons exposed to potentially infected animals. The director of forestry and his staff of 70 forest superintendents and forest rangers developed and delivered predator control in forested regions in conjunction with trap-line operators and contract trappers. Primary components included approximately eight thousand kilometres of double trap-lines used to encircle settled areas; 15 contract trappers focused exclusively on removing local populations of wolves, coyotes, and cougars; poisoning by cyanide pellets, strychnine cubes, strychnine eggs, or sodium fluoroacetate 1080; and a lesser degree of snaring, trapping, and shooting. Legislative protection for red foxes (enacted because of limited populations in previous decades) was removed in all parts of Alberta to enable rabies control efforts.

greater than the distance from New York City to Chicago. Half of its area is forest, mainly in the northern half and west along the Rockies; the remainder is farm land, varying from wooded and semi-wooded country to bald prairies in the southeast. The population includes over 1,000,000 people, approximately 1,800,000 cattle, 1,400,000 hogs, 250,000 horses, 340,000 sheep, and 10,000,000 poultry.” FOUNDATIONS OF SUCCESS AND TASK SHARING

One of the key elements of the 1950s control program was recognition and integration of the roles and authorities at multiple levels of government. The Alberta Central Rabies Control Committee (CRCC) was formed to advise on and coordinate all aspects of the activities (Ballantyne & O’Donoghue, 1954). The committee had no legal power but was deemed essential. Sitting at the table were representatives from federal departments of agriculture, Indian affairs, and the RCMP; and provincial departments of agriculture, health, and lands and forests. Other members included the Alberta Veterinary Medical Association and the medical officer of health for the City of Edmonton. The absence of human cases of rabies during the 1950s outbreak (Ballantyne, 1958) was interpreted as a mark of the success of the overall program and the coordinating efforts of the CRCC. A key element of the 1950s program was the provision of an extensive province-wide rabies education used to inform a naïve population regarding this new disease in Alberta. The CRCC produced and distributed rabies educational materials to each schoolroom in Alberta (Ballantyne  & O’Donoghue, 1954) and prepared media materials for radio and press. CRCC concluded that every adult in ­ Alberta heard about rabies before the educational program was completed (Ballantyne & O’Donoghue, 1954). 97

A History of Rabies Management in the Provinces and Territories

Carnivores were targeted in all programs, and specific efforts were taken to avoid killing big game ungulates. The following, from several of Ballantyne’s works (1957, 1958), shows the extent of the efforts:

for rabies testing. Local authorities led the way in dog control efforts and the City of Edmonton (human population 200,000) destroyed over 1200 dogs in the winter of 1953– 1954. Similarly, field reports of clinical cases and whatever heads were collected for testing were often organized through provincial forest rangers, registered trappers, and RCMP (Ballantyne & O’Donoghue, 1954). In many ways the combined all-out assault against rabies in the 1950s set the stage for response to subsequent incursions of terrestrial rabies variants. The cooperation, communication, and consultation among the various partners and rabies control committee members served everyone well and provided a network on which to address new risks as they occurred.

Supplies issued, 1951–1956, for the war on rabies in Alberta’s agricultural areas 628,000 strychnine cubes, 106000 cyanide capsules, >  45,680 bullets; 39,960 coyote “getters”, 27,250 lure scent jars (2 oz. each), >17,296 snares, 1899 “1080” baits, 440 traps of differing sizes. (1957, p. 171) Bait carcasses: 29 horses, 1 cow, 200 lb fish, 303 lb lard, 2,645 lb beef fat and tallow, 1,421 lb meat, 2,124 eggs, 2 cases of sardines, and $22.81 of canned dog food. These supplies were in addition to recycling carcasses from trap-line and poison efforts as bait for further removals. (1957, p. 158) Minimum kill in forested areas, October 1952 to March 1956 55,889 foxes, 53,364 coyotes, 10,000 lynx, 5,461 wolves, 4,130 bears, 664 skunks, 69 cougars, 18 fisher, 4 badgers, 1 wolverine, 657 dogs killed through Municipal By-Laws and Animal Diseases and Contagious Act (1957, p. 160) Minimum kill in farmed areas, fall 1952 246,800 coyotes. (1957, p. 171)

Skunk Rabies, 1970 to 1993 After a 14-year quiescent period, terrestrial rabies flared up again in 1971 (Table 7.1, Figure 7.1). This time, however, it was the prairie skunk rabies variant, and the threat came from Saskatchewan in the east rather than the north (Pybus, 1988a). Skunks live in relatively close proximity to human populations, and the potential for rabies in skunks posed a direct risk to people and livestock. The CRCC was re-established and expanded, and the chair shifted from provincial agriculture to provincial health, reflecting the overarching human health concerns. The committee was managed by Dr John Waters, director of communicable diseases, Alberta Social Services. Other primary members were Alberta Agriculture (Dr Ralph Christian, director of animal health, and Joe Gurba, head of pest control), Alberta Fish and Wildlife (Dave Neave, director of wildlife), Agriculture Canada (Dr Bill Yates, head of Rabies Unit, Animal Diseases Research Institute Lethbridge), and Dr L. G. Gould, Calgary regional veterinarian, Health of Animals), representatives from affected counties, and a representative of the Alberta Veterinary Medical Association. Ancillary research projects were delivered in conjunction with the Fish and Wildlife Division (John Gunson) and the Western College of Veterinary Medicine in Saskatoon (Dr John Iverson). The 1970s program shifted to a targeted focus on striped skunks and the associated biology, risks, and control of free-ranging skunks. Rather than province-wide indiscriminate wildlife removals, a narrow corridor of generalized skunk removal (30-kilometre-wide population-reduction program of poisoning, trapping, and shooting from the Montana border to Cold Lake, Alberta) was implemented along the Alberta–Saskatchewan border (Figure 7.1). In

The federal Department of Agriculture Canada, Health of Animals quarantined all dogs in Alberta, organized dog vaccination clinics (free in northern regions but not free south of the 55th parallel), and investigated possible rabid animal reports (along with forest rangers and RCMP). The RCMP enforced the dog quarantines, assisted with dog vaccination clinics, and responded to public reports of sick animals. Municipal authorities of all cities, towns, villages, municipalities, and counties were mandated to provide bylaws requiring dogs to be tied up and provided destruction of stray dogs (as requested by the province). They provided many local dog vaccination clinics. Response from local authorities was “practically 100%” (Ballantyne & O’Donoghue, 1954). Indigenous band councils passed by-laws limiting the number of dogs per owner to two, except sled dogs, and ordering the destruction of strays. Given the scale of the operations, activities were often shared by various agencies. Provincial forest rangers and municipal pest control officers assisted the RCMP in enforcing the dog restrictions in the improvement districts and delivery of remote dog vaccination clinics. They also delivered the wildlife control programs and collected heads

98

Alberta

addition, an intensive three mile radial depopulation was implemented where ever a rabid skunk was detected (Alsager, 1973; Gunson et al., 1978). Skunks were removed by trapping, shooting, night-lighting, and placing poisoned eggs but these activities occurred only in habitats and areas frequented by skunks. The program was delivered in conjunction with the area under active rat control (Bourne, 1998). In general, provincial authorities delivered the surveillance and control programs and the federal agriculture agency provided diagnostic testing at its laboratory in Lethbridge. The provincial rabies biologist and a rabies technician (employees of the Fish and Wildlife Division but paid by Alberta Agriculture) were responsible for the design and delivery of the field activities, in conjunction with municipal field personnel in the rabies risk areas. Over time, the provincial rabies biologists included Dave Showalter, Rick Rosatte, and Margo Pybus. Targeted areas of removal shifted with minor outbreaks of skunk rabies in specific counties through the 1970s, 1980s, and early 1990s (Pybus, 1988a, 1988b). The problems occurred along the eastern or southern borders and probably reflected an incursion of skunk rabies from neighbouring Saskatchewan or Montana. Further details on skunk rabies control are given in Chapter 28. The skunk rabies programs hinged on early, persistent, and consistent response to the identified risk, in conjunction with good science, broad communication, and integrated collaboration among CRCC members. Population reduction (live-trapping with wire traps) and euthanasia, kill-trapping (using Conibear traps), shooting, and poisoning were implemented in three counties of southern Alberta as a rabies control between 1980 and 1983 (about 2400 skunks were euthanized). A five-kilometre-radial depopulation zone was established around the location of rabid skunks. The cost of the reduction program during 1980 to 1983 was about $5 to $15/km2 and rabies was again controlled in Alberta (Rosatte, 1986) with only one rabid skunk in 1986 (Pybus,1988a). Rabies in skunks reappeared the next year, 1987 (with 36 cases), dropped, and then rose again in 1990 (25 cases), but has not been detected since 1994. The rabies management program appears to have been effective: rabies in skunks in Alberta has not been diagnosed despite ongoing surveillance in risk areas along the eastern and southern provincial borders.

government regarding testing ongoing rabies surveillance samples. In 2010, a memorandum of understanding was signed between the province and CFIA whereby the province would pay for laboratory services provided by CFIA to diagnose survey samples and limit the number of samples submitted. The committee is chaired by Dr Margo Pybus, provincial wildlife disease specialist, Alberta Fish and Wildlife, reflecting a past personal history with the committee that started as a rookie provincial rabies biologist at the CRCC table in 1982 under the early guidance of Drs John Waters (Alberta Health) and Ralph Christian (Alberta Agriculture). The role of the committee changed again following modifications to the federal rabies programs implemented by CFIA in 2014. The current triumvirate of provincial health, agriculture, and wildlife representatives form the nucleus of the CRCC in conjunction with Alberta’s public health veterinary position. Additional members of the CRCC include a representative of federal agriculture (Canadian Food Inspection Agency) and a municipal representative from the County of Cardston speaking on behalf of the four at-risk counties along the borders with Saskatchewan and Montana (Cardston, Warner, Forty Mile, and Cypress).

Discussion The rabies history in Alberta is characterized by the northto-south invasion of rabies primarily in coyotes between 1952 and 1956; the east to west invasion of rabies in skunks beginning in 1971, which persisted until 1993; and the ongoing presence of rabies in bats that began in conjunction with the invasion of rabies in skunks. Rabies in domestic animals (cats and dogs) and livestock spiked during the coyote invasion and, since then, has been very low and sporadic. Rabies in wild carnivores appeared to die out completely by 1975 with the sole exception of a rabid fox in 1998. The source of the virus in these isolated outbreaks remains unknown without genetic analysis. In retrospect, the arctic fox variant drove the invasion in the 50s and the skunk variant drove the invasion in the 1970s. Since 1999 the province has been free of terrestrial enzootic rabies. To some extent, this can be attributed to Alberta’s aggressive control campaigns against the terrestrial invasions characterized by integrated communication and shared responsibilities among all levels of government and in consort with stakeholders and the public. Rabies in bats, however, has persisted since 1971, peaking in the mid-1970s, then gradually declining to the

Rabies Today The coordinated approach to prevent rabies incursions continues today. The Alberta CRCC was renewed yet again in 2009 to address changes implemented by the federal

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A History of Rabies Management in the Provinces and Territories

present levels of 10 or fewer positives per year and fewer than 150 submissions per year. This pattern is similar to several other provinces and other jurisdictions in North America where after an invasion in terrestrial species, bat rabies sometimes appears. Current control programs generally concentrate on bats that display clinical signs of rabies or bats that have direct contact with people. In Alberta, the provincial wildlife agency played the lead role in understanding the biology of bats (a series of publications by Dave Schowalter (1980) and the risks associated with bats (Pybus, 1986; Rosatte, 1985, 1987), while the provincial health agency dealt with managing the human health risks and communications.

In the 1970s, the Fish and Wildlife Division undertook active surveillance programs in known bat summer colonies. Data indicated most bats were not infected with rabies, and even when an individual bat could be traced back to its home roost, additional rabid bats rarely were found when whole bat colonies were depopulated (Schowalter, 1980). Ancillary to the public surveillance program, the provincial wildlife agency also undertook bat research projects and extensive public information programs. Further details on bat rabies in Canada are given in Chapters 2 and 27. The public generally appreciates bats for their inherent value in delivering ecosystem services rather than viewing them as something to fear.

References Alsager, D. E. (1973). The control of rabies vectors in Alberta. Edmonton: Alberta Department of Agriculture. Ballantyne, E. E. (1957). Sylvatic rabies and its control in Alberta (Unpublished thesis, University of Toronto). Permission granted to use in its unpublished form by the Alberta Veterinary Medical Association. Ballantyne, E. E. (1958). Rabies control in Alberta wildlife. Veterinary Medicine, 23: 87–91. Ballantyne, E. E., & O’Donoghue, J. G. (1954). Rabies control in Alberta. Journal of the American Veterinary Medical Association, 125, 316–326. Bourne, J. B. (1998). Norway rat exclusion in Alberta. In R. O. Baker & A. C. Crabb (Eds.), Proceedings of the Eighteenth Vertebrate Pest Conference. Davis, CA: University of California, Davis. Retrieved from DigitalCommons@University of Nebraska-Lincoln website: http://digitalcommons.unl.edu/vpc18/32 Fish and Wildlife Historical Society. (2005). Fish, fur, and feathers: Fish and wildlife conservation in Alberta, 1905–2005. Edmonton, AB: Fish and Wildlife Historical Society and Federation of Alberta Naturalists. Government of Alberta. (2013). Climate and geography. Retrieved from https://www.alberta.ca/about-alberta.aspx Government of Alberta. (2018). Bats management. Retrieved from https://www.alberta.ca/bat-management.aspx Gunson, J. R., Dorward, W. J., & Schowalter, D. B. (1978). An evaluation of rabies control in skunks in Alberta. Canadian Veterinary Journal, 19, 214–220. Natural Resources Canada. (2016). Origin of the names of Canada and its provinces and territories. Retrieved from https://www.nrcan .gc.ca/earth-sciences/geography/place-names/origins-geographical-names/9224 Plummer, P. J. G. (1954). Rabies in Canada, with special reference to wildlife reservoirs. Bulletin of the World Health Organization, 10, 767–774. Pybus, M. J. (1986). Rabies in insectivorous bats of western Canada, 1979 to 1983. Journal of Wildlife Diseases, 22(3), 307–313. https:// doi.org/10.7589/0090-3558-22.3.307 Pybus, M. J. (1988a). Rabies and rabies control in striped skunks, Mephitis mephitis, in three prairie regions of western North America . Journal of Wildlife Diseases, 24(3), 434–449. https://doi.org/10.7589/0090-3558-24.3.434 Pybus, M. J. (1988b). Rabies control by skunk depopulation in southern Alberta, 1983–1986. Prairie Naturalist, 20, 7–14. Report of the veterinary director general for the year ending March 31, 1909. (1909). Ottawa, ON: Department of Agriculture. Available from Library and Archives Canada, https://bac-lac.on.worldcat.org/oclc/29657040 Report of the veterinary director general for the year ending March 31, 1910. (1910). Ottawa, ON: Department of Agriculture. Available from Library and Archives Canada, https://bac-lac.on.worldcat.org/oclc/29657040 Report of the veterinary director general for the year ending March 31, 1911. (1911). Ottawa, ON: Department of Agriculture. Available from Library and Archives Canada, https://bac-lac.on.worldcat.org/oclc/29657040 Report of the veterinary director general for the year ending March 31, 1913. (1913). Ottawa, ON: Department of Agriculture. Available from Library and Archives Canada, https://bac-lac.on.worldcat.org/oclc/29657040 Report of the veterinary director general for the year ending March 31, 1917. (1917). Ottawa, ON: Department of Agriculture. Available from Library and Archives Canada, https://bac-lac.on.worldcat.org/oclc/29657040

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Alberta Report of the veterinary director general for the year ending March 31, 1918. (1918). Ottawa, ON: Department of Agriculture. Available from Library and Archives Canada, https://bac-lac.on.worldcat.org/oclc/29657040 Report of the veterinary director general for the year ending March 31, 1927. (1927). Ottawa, ON: Department of Agriculture. Available from Library and Archives Canada, https://bac-lac.on.worldcat.org/oclc/29657040 Rosatte, R. C. (1985). Bat rabies in Alberta. Canadian Veterinary Journal, 26, 81–85. Rosatte, R. C. (1987). Bat rabies in Canada: History, epidemiology and prevention. Canadian Veterinary Journal, 28, 754–756. Rosatte, R., Pybus, M., & Gunson, J. R. (1986). Population reduction as a factor in the control of rabies in Alberta. Journal of Wildlife Diseases, 22(4), 459–467. https://doi.org/10.7589/0090-3558-22.4.459 Schowalter, D. B. (1980). Characteristics of bat rabies in Alberta. Canadian Journal of Comparative Medicine, 44, 70–76. Statistics Canada. (2013). Population estimates on July 1st, by age and sex. Retrieved from https://www150.statcan.gc.ca/t1/tbl1/en /tv.action?pid=1710000501 Tabel, H., Corner, A. H., Webster, W. A., & Casey, C. A. (1974). History and epizootiology of rabies in Canada. The Canadian Veterinary Journal, 15(10), 271.

101

8 Saskatchewan Byrnne Rothwell Woodwedge Consulting (Deceased), Shellbrook, Saskatchewan, Canada

Place Saskatchewan became a province in 1905 by the Saskatchewan Act (Government of Canada, 2015), which amalgamated parts of the Districts of Assiniboia, Athabasca and Saskatchewan (see Overview, Part 3). The province had been explored as early as 1690 and settled by Europeans in 1774 but was initially inhabited by Indigenous peoples including the Athabaskan, Algonquian, Atsina, Cree, Saulteaux, and Sioux. The first permanent European settlement was a Hudson’s Bay post at Cumberland House, founded in 1774 by Samuel Hearne (Parks Canada, n.d.). Initial settlement of the west occurred between 1875 and 1890, with a second wave from 1903 to 1914, mainly from Britain and the United States. A third wave occurred from 1919 to 1930 after the First World War, comprising mainly British, US, and East European settlers. This was followed by the Great Depression and the Second World War. Today, Saskatchewan, one of the prairie provinces, is bordered on the west by Alberta and to the north by the Northwest Territories (NWT), and has Manitoba as its eastern border and the US states of Montana and North Dakota on its southern boundary (Figure 8.1). It has a land mass of 592,534 km2 and had an estimated population of 1,079,958 in 2012. Its capital is Regina. Saskatchewan contains two major natural regions: the Canadian Shield in the north, which is mostly covered by boreal forest with the exception of the Lake Athabasca Sand Dunes, and the Interior Plains in the south. The Interior Plains is the northern limit of the Great Plains region of North America, characterized by grassland areas composed

of short-grass, mixed grass, and fescue grass. A narrow band of aspen parkland separates the grasslands from the northern boreal forest, all providing a variety of suitable habitats for the skunk to exist (see Figure 8.1).

Rabies in Saskatchewan Rabies was not reported in Saskatchewan until 1905. Between 1906 and 1944, sporadic outbreaks of rabies occurred in Saskatchewan, Ontario, and Quebec (Hayes & Dryden, 1970). During that time, cross-border incursions from the United States occurred, the first in 1905 from North Dakota into North Portal and a second outbreak in July 1905 at Oxbow, farther north (Report of the Veterinary Director General, 1906). All dogs involved were destroyed. Dogs were also involved in the 1907 outbreak at Moosomin, on the Manitoba border, involving American settlers (Report of the Veterinary Director General, 1911; see Chapter 2). In his report of 1909, Dr Rutherford, the veterinary director general (VDG), reported 94 premises under quarantine in at Qu’Appelle (Report of the Veterinary Director General, 1909). His report of 1915 (Report of the Veterinary Director General, 1915) listed two premises under quarantine, one each in Qu’Appelle and Regina. These later cases of rabies were probably diagnosed using staining for Negri bodies. No reports of rabies in Saskatchewan were published between 1915 and 1940, when a single case of a dog with rabies occurred. Rabies reappeared in 1952 in two dogs as an extension of an epizootic in arctic fox (Alopex lagopus) spread from the NWT through northern Alberta

Saskatchewan

Figure 8.1: Saskatchewan showing the three natural regions, the place names used in the text, and the spread of rabies into the province. The arrows and dates show the time, species, direction, and entry points of rabies. Source: Derived from maps provided by Natural Resources Canada and the National Atlas of Canada. Produced by R. Tinline, Queen’s University.

to Lac la Loche in Saskatchewan (Plummer, 1954). The following year one dog and a red fox (Vulpes vulpes) were found to be rabid. Again in 1954, rabies was diagnosed in three red foxes, three dogs, one coyote (Canis latrans), two cows, and one pig. Rabies then disappeared until 1963. In 1963 wildlife rabies spread from Manitoba to Saskatchewan in striped skunks (Mephitis mephitis). The increase in skunk cases continued (Table 8.1) as the disease spread from southeastern Saskatchewan westward, reaching

the Alberta–Saskatchewan border by 1970 (Gunson et  al., 1978; Charlton et al., 1988). Then, as now, rabies in skunks dominated the incidence data, averaging over 80% of all positives. Annual incidence in skunks remained high but cycled with peaks initially four years apart, then gradually lengthening to seven years (Pybus, 1988). Incidence peaked in 1987 (610 cases) and subsequently declined to about 15 cases per year in the past decade (Table 8.1 and Figure 8.2). Incidence in cats, dogs, and livestock has been low but is correlated

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A History of Rabies Management in the Provinces and Territories

Table 8.1  Rabies-positives in Saskatchewan, 1940 to 2017. Year

Total

1940 1952 1953 1954 1955 1956 1957 1958 1959 1960 1961 1962 1963 1964 1965 1966 1967 1968 1969 1970 1971 1972 1973 1974 1975 1976 1977 1978 1979 1980 1981 1982 1983 1984 1985 1986 1987 1988 1989 1990 1991 1992 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012

1 2 5 10 0 0 0 1 0 0 0 0 4 24 31 45 51 85 48 61 53 66 268 127 117 162 212 119 100 120 229 128 136 185 231 435 610 193 66 55 49 76 109 24 28 21 16 76 140 171 46 27 24 25 24 33 17 33 24 21 34 24

Skunk

Live

Bat

Dom

Fox

Other

Rac

Wild

0 0 0 0 0 0 0 0 0 0 0 0 1 12 15 25 42 66 25 28 30 54 217 102 96 142 184 100 73 108 205 112 128 162 205 392 553 171 46 34 42 66 92 18 14 15 11 61 121 142 26 20 18 19 18 21 12 25 15 17 24 13

0 0 0 3 0 0 0 0 0 0 0 0 2 9 11 13 7 9 11 10 11 9 27 16 5 12 14 10 15 7 10 9 6 10 12 26 25 11 2 5 1 3 10 0 3 2 1 3 10 10 5 5 1 3 2 6 1 3 0 0 1 2

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 1 1 0 0 7 6 9 3 6 3 4 2 2 3 7 5 8 7 11 10 5 6 6 6 9 4 2 8 4 11 13 1 4 3 1 4 0 2 4 1 5 5

1 2 4 3 0 0 0 1 0 0 0 0 1 3 5 7 2 8 11 18 9 2 8 8 9 2 5 4 5 2 9 5 0 9 5 12 20 3 7 6 1 1 1 0 2 0 2 3 4 8 2 1 1 0 2 2 2 3 5 3 4 4

0 0 1 3 0 0 0 0 0 0 0 0 0 0 0 0 0 1 1 0 1 0 13 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 2 1 0 0 0 0 0 0 1 0 0 1 0 0 1 0 0 2 1 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 1 0 1 0 0 0 0 0

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 1 0 0 0 0 0 1 0 2 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 1 0 0 0 0 0

0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 3 1 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 (Continued)

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Year 2013 2014 2015 2016 2017  Total   % Total

Total 13 21 27 53 22 5,158

Skunk 5 10 12 22 13 4200 81.4

Live 0 1 0 4 1 395 7.7

Bat 6 10 13 24 7 260 5.0

Dom 2 0 2 3 1 255 4.9

Fox 0 0 0 0 0 21 0.4

Other 0 0 0 0 0 13 0.3

Rac 0 0 0 0 0 7 0.1

Wild 0 0 0 0 0 7 0.1

Note: Live = livestock; Dom = cat/dog; Rac = raccoon; Wild = coyote; Other = a variety of rodents, etc. There were no cases from 1941 through 1951. Source: compiled from CFIA data.

temporally with incidence in skunks. Coincident with peaks and troughs in the cycles in skunks, the disease expanded or contracted across the southern half of the province within the grasslands and aspen parklands regions shown in Figure 8.1. Pybus (1988) examined spread between 1963 and 1986, noting that rabies moved rapidly across the grasslands but invaded the aspen parklands slowly and did not persist. Rabies was diagnosed in bats in 1970. Since then incidence in bats has averaged just over five cases per year, although rabies waxed and waned with major peaks every 12 to 15 years (1977, 1989, 2001, and 2016). Although still low, the peak in 2016 was approximately double previous peaks. This persistent pattern of incidence in bats and recent increase is consistent with experience in other areas in Canada, suggesting that the disease dynamics in bats may have changed in recent years. But only future data will shed light on whether the change is temporary or depicts a new pattern of rabies in insectivorous bats on the prairies. Table 8.2 shows submissions of bats from Saskatchewan for testing between 1985 and 2017. Although Saskatchewan Wildlife Federation (2019) lists eight species of bats in Saskatchewan, only seven are shown in the submissions table. No specimens from long-legged bats (Myotis volans) were tested. For Saskatchewan, the overall percentage of positive tests in submissions was 9.2%. Approximately 69% of all submissions were big brown bats, and 159 of those were positive, about 80% of all diagnosed cases of rabies in bats. The silver-haired bat and hoary bat accounted for about 18% of rabies-positives. The little brown bat, while numerous in the province and second highest in submissions, accounted for only 1% of the positive cases. This is also the pattern in other provinces. The big brown bat is most often associated with human dwellings and thus more often a submission positive (Pybus, 1986). The number of bat submissions in Saskatchewan is almost eight times higher than in neighbouring Manitoba (Table 8.3). Manitoba (see Chapter 9) has a similar terrestrial rabies ecology driven by skunks and roughly similar

submissions for all other species. While the big brown bat dominated submissions and positive diagnoses in bats in Saskatchewan over the 1985–2012 period, big brown bat submissions in Manitoba were very low (11 samples between 1985 and 2012), and there were no positive diagnoses. Whether these numbers represent a reporting bias or differences in habitat for this species is not known. On the other hand, prevalence of rabies in silver-haired bats is high in tested bats in both provinces, dominating both submissions and positives in Manitoba and being the runner-up in Saskatchewan.

Rabies Management in Saskatchewan Several factors have affected rabies management in Saskatchewan: (1) ecological factors, (2) rural attitudes to wildlife, (3) changes in agricultural practice, (4) changes in veterinary education, (5) better biologics, and (6) increased cooperation between various agencies.

Ecological Factors Adult skunks are relatively sedentary, travelling short distances within their home range. The population turnover is rapid, with fewer than 5% of adult males and 8% of females shown to be older than three years (Schowalter & Gunson, 1982). The skunks of the parkland and northern prairie region exhibit long periods of inactivity in communal winter dens, containing on average six individuals. Denning occurs from October to December, breeding occurring within the dens during February and March, and parturition and growth happen in the den between April and June. Dispersal of the juveniles occurs in July, August, and September, which gives them adequate time to run into rabid skunks before they look for communal dens themselves. The mean incubation period of 40 days recorded in captive skunks could explain the increased rabies cases in

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Figure 8.2: Positive rabies cases in Saskatchewan, 1952 to 2017. Source: compiled from CFIA data.

Table 8.2  Bat submissions and results (N = negative, P = positive) in Saskatchewan, 1985 to 2017. Code BBB LBB SHB HRB NLB REB LEB LLB BAT

Species

Total

N

P

% Total

Big brown bat (Eptesicus fuscus) Little brown bat (Myotis lucifugus) Silver-haired bat (Lasionycteris noctivagans) Hoary bat (Lasiurus cinereus) Northern long-eared (Myotis septentrionalis) Red bat (Lasiurus borealis) Long-eared bat (Myotis evotis) Long-legged bat (Myotis volans) Unidentified  Total

1,496 299

1,331 295

159 3

10.6 1.0

295

260

31

10.5

37

31

4

10.8

10

10

0

0.0

7 5 0 218 2,149

7 4 0 203 1,938

0 1 0 13 198

0.0 20.0 0.0 6.0 9.2

Source: compiled by author from CFIA data.

the late fall (Gunson et al., 1978). Using data from 1963 to 1986, Pybus (1988) showed a pattern of troughs and peaks over four years. First comes an invasion period of three to four years, followed by an epizootic phase of two to three years, and then a silent phase of one to three years. This is followed by an enzootic phase of two to three years. Pybus also argued that, in the absence of any meaningful rabies control programs in Saskatchewan, the interaction between virus and skunks may be the major factor in the cyclic regulation of skunk populations in the province. Pybus further noted an absence of cyclic variations in rabies in neighbouring Montana and Alberta where control programs were more aggressive.

Rural Attitudes to Wildlife Population reduction as a means to control rabies in Alberta appears successful but has to be a sustained effort (Rosatte, 1985). Unknowingly, the fur trade in Rupert’s Land provided population control during the height of the fur trade of the eighteenth, nineteenth, and twentieth centuries. When the demand for fur decreased, wildlife populations increased. As a consequence rabies in wildlife also increased in the 1940s and eventually spread from the Arctic into Alberta in 1950. During the 1952 to 1956 epizootic in Alberta, the Central Rabies Control Committee (CRCC) was formed, a multi-agency committee that advised and

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shot, poisoned, trapped or fumigated a number of predators (aiding rabies control) including 310 skunks, 149 foxes, 14 coyotes, 18 dogs, 10 cats, 7 porcupines, and 1 lynx (Agriculture Canada, 1964). With the resurgence of skunk rabies in 1985 in Saskatchewan, a need for increased public awareness and an organized skunk management program was recognized (Harvey, 1987), but a population reduction program was never implemented. Management efforts concentrated on prevention through the use of (1) pet vaccination, (2) vaccination of high-risk humans, (3) the reporting of suspect cases to Agriculture Canada, and (4) rabid skunk control coordinated by the municipalities on a voluntary basis and conducted by local farmers. In total, the efforts at population reduction were minimal, lacked coordination, and relied heavily on the voluntary efforts of the public (Pybus, 1988).

Table 8.3  Comparison of submissions by species between Saskatchewan and Manitoba, 1985 to 2017. Species

Total

MB

SK

Skunk Dom Live Raccoon Bat

7,977 15,336 3,045 1,165 2,674

3,143 7160 1,569 645 307

4,834 8,176 1,476 520 2,367

Source: compiled from CFIA data.

coordinated the management efforts. The key provincial management measure recommended was wildlife depopulation (Ballantyne, 1957). Following the destruction of 180,000 foxes in this period by trapping, poisoning, gassing, and shooting, Alberta remained virtually rabies-free until 1969 (Rosatte, 1985). An outbreak of skunk rabies began in Saskatchewan in about 1963 and gradually spread north and west towards the Alberta border. Despite attempts at local eradication by poisoning and gassing in Saskatchewan (Gunson, 1978; Pybus, 1988) rabies crossed into Alberta by 1971, prompting the reactivation of the CRCC and the establishment of a buffer zone (known as the border population reduction zone, Rosatte, 1985; see Chapter 7) 29 kilometres wide and 612 kilometres long, from Cold Lake to the Alberta-US border targeting all skunks (Alberta Fish and Wildlife, 2010). This would have provided some control of rabid skunks returning to Saskatchewan. In the 1960s, Saskatchewan’s management efforts for rabies were centred on public, veterinary, and medical awareness of skunks and rabies (Pybus, 1988). Specific control programs were considered too labour intensive and expensive. Farmers in the southeast of Saskatchewan were encouraged to use smoke bombs to kill skunks in their dens, but this effort was not coordinated and was little used. With the extension of the outbreak into Alberta and the formation of the buffer zone in the 1970s, a limited number of poison eggs and smoke bombs were used by conservation officers in areas known to have skunk activity. Again, there was little coordination and little result. Management efforts relied on local efforts, again with little effect (Pybus, 1988). For residents of the Saskatchewan parkland (more aptly described as the forest fringe) during several decades, cases of rabies in farm animals were rarely reported. Carnivores (timber wolves, bush wolves, coyotes, bears, and foxes) were considered a threat to profitable livestock production and were, therefore, shot on sight and actively trapped in winter for fur and supplemental income. For example, from February to May 1964, provincial wildlife personnel

Agricultural Practice There have been major changes in the manner in which agriculture is practiced in western Canada. The destruction of habitat as in past times, for many species, but particularly for that of the main vectors of rabies – the skunk and the bat – continued apace. Over the last 60 years there has been a progressive rebuilding of the farm infrastructure. Virtually all buildings are now footed with concrete foundations and metal-clad. Leaky wooden bins on skids are a thing of the past, having been replaced by large hopper-bottom steel structures. Yards are now mown regularly, or growth of weeds and grass controlled with weed killer. Gone are the cull lumber piles, square bale stacks, dilapidated barns, and chicken coops. Gone, too, are the hedge rows, the “savings bush” that the skunk and bat called home (Hwang et  al., 2007). Although the skunk may still find safe haven and suitable habitat on the grassland prairie, the modern grain farm provides little to entice a wild animal to set up house. Encounters with skunks are rare and most likely to occur at a campground rather than on the homestead. Today, many northern lake resort villages and provincial and national parks provide enhanced habitat for skunks, with no one to bother them during the week and a renewed food supply on the weekend.

Veterinary Education Postwar, there was a spirit of optimism and an increasing level of prosperity in the rural countryside in western Canada. Programs were developed to attract and provide

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A History of Rabies Management in the Provinces and Territories

for the new veterinary graduates, including scholarship programs, purebred sire area livestock improvement programs, and in Saskatchewan, the establishment of the veterinary service district (VSD) program in 1945 (Saskatchewan Rural Veterinary Services, 1945). In 1951–1952, foot-andmouth disease was diagnosed in Saskatchewan, and the full realization of the need for a strong veterinary force became apparent. Dr Kenneth Wells, as veterinary director general, recognized this need, and greatly increased the staffing, implemented continuing education programs, and opened Health of Animals district offices across the west. A rabies diagnostic laboratory system was established at Lethbridge in 1952, enhancing the level of preparedness to deal with a major disease incursion. In the mid-1960s the Western College of Veterinary Medicine was established in Saskatoon, to accept students from the four western provinces and to provide many more practitioners. A rural veterinary clinic program followed, with many veterinary service districts matching funds from the Saskatchewan Department of Agriculture to build clinics in an attempt to ensure continued veterinary service.

by local councils, the Public Health Authority, the RCMP, and the veterinary profession in Saskatchewan. When the Public Health Authority intervenes, wildlife populations are monitored under provincial law, except in national parks where jurisdiction is federal. Protocols are in place covering laboratory reporting, procedures to be followed at the district offices, and actions in concert with Public Health (see Chapter 31). CFIA now licences all rabies vaccines approved for use in Canada through the Veterinary Biologics Section (see Chapter 16). CFIA also regulates animal imports and requires that pets over three months of age imported into Canada have proof of rabies vaccination (CFIA, 2019). Until 2014, CFIA was mandated to investigate any domestic animal exposure to potentially rabid wildlife and to work closely with provincial, Indigenous, and federal public health authorities for rabies incidents involving human contact. Consultation occurred between the CFIA district veterinarian from nine district offices, the head office in Regina, the area office in Calgary, and Public Health regarding local rabies epidemiology and potential exposure details, before submission of samples for rabies testing. CFIA continues to report rabies results directly to Public Health Authorities when humans are involved. In early programs, CFIA oversaw post-exposure management of pets and livestock exposed, or potentially exposed, to rabies, where controls were determined by the CFIA district veterinarian based on current CFIA policy. The importance of timely rabies vaccination, especially the first booster after one year, was emphasized by the CFIA and practitioners alike. With a large urban bat population and rural skunk populations, the potential still exists for rabies contact. Private practitioners play an important role on the front line, protecting the public from rabies by promoting awareness of rabies, administering rabies vaccines to domestic pets, and advising clients on rabies prevention. All biting incidents must be reported to the local Public Health Authority. Public Health will investigate the biting incident and determine the human health risk. A list of Public Health contacts and a map of Saskatchewan Health Regions are listed on the Saskatchewan Veterinary Medical Association website (www.svma.sk.ca). Municipalities play a role in rabies management by enforcing licensing of pets, investigating aggressive behaviour in dogs and cats, providing subsidized spay and neuter clinics, and picking up stray pets as needed. Saskatchewan does have a Zoonotics Committee, which has representatives from the Saskatchewan Ministry of Agriculture, Ministry of Health, Ministry of Environment and Resource Management, and the CFIA. Rabies is only one of a number of diseases

Better Biologics The development of more effective biologics, with safer and more effective vaccines, gave the profession a wider range of options for disease prevention and management. Continuing education was assured with regular programming and as a condition of licensure under the by-laws of the regulatory body of the profession. Education of the public by the profession through easy and direct access, client consultation, articles in local papers, and radio and television coverage provided the conduit for dissemination of important information upon which client decisions might be based. There was recognition of the likely interface with wildlife and the degree of risk was evaluated. Value was placed on working dogs because of their initial cost and training, and the affluence of the pet-owning public meant greater numbers of domestic pets were seen regularly by a veterinarian and kept up to date with vaccination and routine care.

Agency Cooperation With the wane of traditional hunting and fishing, the motor toboggan replaced the sled dog as a means of travel in the north. But we still see the need for dog control, responsible ownership, and management, including rabies vaccination in northern communities. This is encouraged and facilitated

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Saskatchewan

of interest, but through this committee, input into the Saskatchewan health revision of the rabies response policy is achieved (B. Althouse, personal communication, 31 March 2010). Since 1 April 2014, CFIA ended its involvement with managing rabies control in Saskatchewan. A rabies response program has been developed under the Animal Health and Welfare Agency and involves the Ministry of Environment, the Ministry of Health, and the program’s rabies risk assessment veterinarian (RRAV). A wild animal suspected of having rabies is reported to the local conservation officer of the Ministry of Environment. Human exposure to potential rabies cases is reported to the local public health officer or the Saskatchewan public health line (by dialling 811) of the Ministry of Health. Under the rabies response program, provincial private veterinarians collect samples from suspect animals and submit these for testing under the direction of the RRAV. All samples with possible contact between suspect rabid animals and human b ­ eings are sent to CFIA Lethbridge for diagnosis. All p ­ ositive samples for rabies using the immunohistochemical test require confirmation at a ­ CFIA laboratory. Test results and any response and follow-up activity are coordinated by the RRAV. Since 2014, rabies diagnosis, using the immunohistochemical test (IHC) was introduced at the prairie diagnostic services (PDS) laboratory in Saskatoon. Veterinary clinics can submit specimens for rabies diagnosis to PDS. While the IHC test for rabies is not accredited by the CFIA, samples with positive results are then submitted to CFIA Ottawa for confirmation. This passive surveillance of suspect rabid bats with no human or domestic animal contact has resulted in the reporting of five positive bats in 2015, ten in 2016 and four in 2017. These were added to the CFIA totals of the years 2015 (12 positives), 2016 (24 positives) and 2017 (7 positive). While positive rabies cases are usually in skunks and bats, there is some spillover into domestic animals. In 2014 one horse was diagnosed with rabies; in 2015 two dogs; in 2016, two

cats and one dog, one goat, one sheep, one cow, and one horse; in 2017 one dog and one bovine were diagnosed with rabies.

Discussion Until the Saskatchewan government takes a more active role in rabies management, rabies in skunks and bats will continue to be a concern. Rabies can spill over into the livestock and domestic pet population and thus be a threat to human populations. With a continued global warming we may expect to see more warmer-clime bats appearing in greater numbers (Willis & Brigham, 2003). Therefore, surveillance for bat rabies should continue, combined with education and rabies vaccination of pets and those people at risk. As long as there is an open provincial and US border and good denning locations for the skunks, rabies will continue to be a problem in Saskatchewan. Incursions of skunks can occur from Alberta (although there are no known cases of rabies in skunks in Alberta since 1994) and from Montana at any time, while a continuing cycle of rabies within the Saskatchewan population will occur. Although arctic fox rabies remains enzootic in northern Canada, no red foxes have been diagnosed with rabies since 1985 and no coyotes since 1978. As in all jurisdictions, continuing education for the public and professionals is essential to rabies management as people need to be reminded. CFIA provides up-to-date rabies statistics for the province (CFIA, 2018). The Saskatchewan Veterinary Medical Association links to government of Saskatchewan Environment and Health web pages that provide additional information regarding rabies and rabies programs in the province (Saskatchewan Veterinary Medical Association, 2018). The University of Saskatchewan also provides good information on rabies subjects such as bats in the province (University of Saskatchewan, 2011).

Acknowledgments Unfortunately, the author of this chapter died before this book went to press. Rowland Tinline and David Gregory, the volume co-editors, updated the data and figures to 2017 and described recent changes in the management of rabies. We are grateful for the careful review of those updates by Dr Margo Pybus (author of Chapter 7) and the assistance of Dr Wendy Wilkins, disease surveillance veterinarian, Government of Saskatchewan, in clarifying current practices in the management of rabies in Saskatchewan.

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References Agriculture Canada. (1964, July 7). Newsletter of the Health of Animals Division. Alberta Fish and Wildlife. (2010). Rabies and rabies management. Wildlife Info Bulletin # 5. Retrieved from https://open.alberta.ca /dataset/1277549b-1d4b-468e-8026-f788225c2d05/resource/54ac03ac-5daa-4579-98f5-defa69c45fdb/download/2009 -RabiesRabiesManagement-2009.pdf Ballantyne, E. E. (1957). Sylvatic rabies and its control in Alberta (Unpublished thesis, University of Toronto). Permission granted to use in its unpublished form by the Alberta Veterinary Medical Association. Canadian Food Inspection Agency. (2018). Rabies cases in Canada. Retrieved from http://www.inspection.gc.ca/animals /terrestrial-animals/diseases/reportable/rabies/eng/1356138388304/1356152541083 Canadian Food Inspection Agency. (2019). Importing or travelling with pets. Retrieved from http://inspection.gc.ca/animals /terrestrial-animals/imports/policies/live-animals/pets/eng/1326600389775/1326600500578 Charlton, K. M., Webster, W. A., Casey, G. A., & Rupprecht, C. E. (1988). Skunk rabies. Review of Infectious Diseases, 10(4), s626–s628. https://doi.org/10.1007/978-1-4613-1755-5_5 Gunson, J. R., Dorward, W. J., & Schowalter, D. B. (1978) An evaluation of rabies control in skunks in Alberta. Canadian Veterinary Journal, 19, 214–220. Government of Canada. (2015). The Saskatchewan Act – Enactment No.13: The Saskatchewan Act, 1905, 4-5 Edw. VII, c. 42 (Can). Retrieved from Department of Justice website: https://www.justice.gc.ca/eng/rp-pr/csj-sjc/constitution/lawreg-loireg/p1t131.html Harvey, D. (1987). Rabies and skunk control. Pest Control Newsletter, 3, 4–6. Hayes, L. B., & Dryden, I. M. (1970). Epizootiology of rabies in Saskatchewan. Canadian Veterinary Journal, 11(7), 131–136. Hwang, Y. T., Larivière, S., & Messier, F. (2007). Local and landscape den selection of striped skunks on the Canadian prairies. Canadian Journal of Zoology, 85(1), 33–39. https://doi.org/10.1139/z06-192 Lundquist, B., & Sims, M. (2010). Rabies and biting incidents. SVMA Newsletter, 45(2), 8–9. Parks Canada. (n.d.). Cumberland House National Historic Site of Canada. Retrieved from Canada’s Historic Places website: https:// www.historicplaces.ca/en/rep-reg/place-lieu.aspx?id=1139 Plummer, P. J. G. (1954). Rabies in Canada, with special reference to wildlife reservoirs. Bulletin World Health Organization, 10, 767–774. Pybus, M. J. (1986). Rabies in insectivorous bats of western Canada, 1979 to 1983. Journal Wildlife Diseases, 22(3), 307–313. https://doi .org/10.7589/0090-3558-22.3.307 Pybus, M. J. (1988). Rabies and rabies control in striped skunks (Mephitis mephitis) in three prairie regions of western North America. Journal of Wildlife Diseases, 24(3), 434–449. https://doi.org/10.7589/0090-3558-24.3.434 Report of the veterinary director general for the year ending March 31, 1906. (1906). Ottawa, ON: Department of Agriculture. Available from Library and Archives Canada, https://bac-lac.on.worldcat.org/oclc/29657040 Report of the veterinary director general for the year ending March 31, 1909. (1909). Ottawa, ON: Department of Agriculture. Available from Library and Archives Canada, https://bac-lac.on.worldcat.org/oclc/29657040 Report of the veterinary director general for the year ending March 31, 1911. (1911). Ottawa, ON: Department of Agriculture. Available from Library and Archives Canada, https://bac-lac.on.worldcat.org/oclc/29657040 Report of the veterinary director general for the year ending March 31, 1915. (1915). Ottawa, ON: Department of Agriculture. Available from Library and Archives Canada, https://bac-lac.on.worldcat.org/oclc/29657040 Rosatte, R. C. (1985). The use of population reduction as a technique to combat rabies in Alberta, Canada. Great Plains Wildlife Damage Control Workshop Proceedings, 316, 69–77. Retrieved from DigitalCommons@University of Nebraska, Lincoln website: https:// digitalcommons.unl.edu/gpwdcwp/316 Saskatchewan Ministry of Health. (2010). Rabies and human health. Saskatchewan Veterinary Medical Association Newsletter, 45(3), 8–9. Saskatchewan Rural Veterinary Services. (1945). Bill No. 24 of 1945: An Act respecting Veterinary Services in Rural Areas in ­Saskatchewan. Canadian Journal of Comparative Medicine and Veterinary Science, 9(4), 108–110. Retrieved from https://www.ncbi.nlm.nih .gov/pmc/articles/PMC1661024/ Saskatchewan Veterinary Medical Association. (2018). Retrieved from https://www.svma.sk.ca/ Saskatchewan Wildlife Federation. (2019). Saskatchewan bats. Retrieved from https://swf.sk.ca/wp-content/uploads/2014/09 /Saskatchewan-Bats.pdf Schowalter, D. B., & Gunson, J. R. (1982). Parameters of population and seasonal activity of striped skunks, Mephitis mephitis, in ­Alberta and Saskatchewan. Canadian Field-Naturalist, 96, 409–420. University of Saskatchewan. (2011). Information on bats. Retrieved from http://www.usask.ca/dhse/file Willis, C. K. R., & Brigham, M. R. (2003). New records of eastern red bat, Lasiurus borealis, from Cypress Hills Provincial Park, Saskatchewan: A response to climate change. The Canadian Field Naturalist, 117(4), 651–654. https://doi.org/10.22621/cfn.v117i4.819

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9 Manitoba Tim Pasma Ontario Ministry of Agriculture, Food and Rural Affairs, Guelph, Ontario, Canada

Place Manitoba is a prairie province with an area of 650,000 square kilometres and over 110,000 lakes, bordered by Ontario to the east, Saskatchewan to the west, Nunavut and the Northwest Territories to the north, and the US states of North Dakota and Minnesota to the south. It adjoins Hudson Bay to the northeast and it is the only prairie province with a coastline (Figure 9.1). The original province of Manitoba was a square, 1/18 of its current size, and was known as the postage stamp province. Its borders expanded in 1881, but Ontario claimed a large portion of the land, the disputed portion being awarded to Ontario in 1889. Manitoba grew by absorbing land from the Northwest Territories and attained its present day size in 1912 (see Overview, Part 3). Manitoba has four vegetation regions, from north to south: tundra, boreal forest, parkland, and grassland, with wildlife inhabiting all these regions (McGillivray, 2006). Wildlife species were important in the settlement of Manitoba, as the Indigenous peoples hunted animals and the Metis trapped animals for the fur trade (McGillivray, 2006), and by 1870 when Manitoba was founded, the fur trade was the primary industry (Welsted, 1996). Modern-day Manitoba was first inhabited by Indigenous peoples, with Ojibwa, Cree, Dene, Sioux, Mandan, and Assiniboine peoples founding settlements with hunting, mining, and agriculture in the area before contact with the first Europeans (Weir, 2012).

As the fur trade declined, intense competition between the Hudson’s Bay Company and the North West Company, as well as the establishment of agriculture, led to the near-extinction of many wildlife species (McGillivray, 2006; Warkentin, 2000). During the Depression, many people turned to hunting to make a living, and this also depleted wildlife populations (Robertson, 2004). In 1930 the Government of Manitoba assumed control of natural resources from the federal government and established hunting regulations, wildlife refuges, rehabilitation projects, and management programs that were successful in increasing wildlife numbers (Robertson, 2004). Today, wildlife capable of transmitting rabies is abundant across Manitoba, including bats and terrestrial carnivores such as the ­arctic fox, coyote, lynx, raccoon, red fox, skunk, and wolf (Environment and Climate Change Canada and Canadian Wildlife Federation, 2005).

Rabies in Manitoba Early departmental reports indicate the extensive (and expensive) work of district veterinarians who travelled throughout the province and diagnosed and recorded cases of disease (Government of Manitoba, 1889). In 1893 the Diseases of Animals Act renamed the position of district veterinarian as inspector, and Manitoba’s first provincial veterinarian, Dr S. J. Thompson, gave the first annual report outlining the health status of animals in Manitoba (Government of Manitoba, 1893). Although

A History of Rabies Management in the Provinces and Territories

Figure 9.1: Manitoba. Places shown are named in the text. Source: created using publicly available maps from Natural Resources Canada.

there were reports of shootings of mad dogs in Winnipeg as early as 1879 (see “Early Management Efforts”), the first reported outbreak of rabies in Manitoba was in dogs in the area of Elkhorn and Shoal Lake in 1906 (see Chapter 2). Dr McGillivray, Dominion veterinarian, went to the area to investigate the outbreak, quarantined the affected dogs, and took samples. Dr Gordon Bell, provincial bacteriologist in Winnipeg, diagnosed the disease after inoculating rabbits with the samples and identifying the virus. Interestingly, while inoculating the rabbits, Dr Bell accidently pricked himself and promptly decided to take the Pasteur treatment in Chicago as a precaution (“Fears Hydrophobia,” 1906).

A concurrent outbreak in Moosomin, Saskatchewan, was also reported and Dr Bell diagnosed rabies from a horse’s head that was sent to him from the area (“Rabies at Moosomin,” 1907a). Dr McGillivray also went to Moosomin, Saskatchewan, to investigate the outbreak and subsequently ordered that dogs in 12 surrounding townships be either muzzled or tied up, with heavy fines for those who did not comply (“Rabies at Moosomin,” 1907b). In his 1907 report to the medical officer of health for Winnipeg, Dr Bell stated that five animals had been inoculated for rabies and that the strict quarantine of animals during the Shoal Lake epidemic had prevented human cases of rabies (“Winnipeg Is a Healthy City,” 1908). Isolated cases of rabies in dogs

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Manitoba

were reported from Minnedosa, Manitoba, in 1910 (Tabel et  al., 1974). In 1951 rabies was diagnosed on specimens obtained from widely separated localities in the north: Fort Churchill in northern Manitoba; Fort Smith in the then Northwest Territories, Lake Harbour on Baffin Island; and Sugluk and Povungnituk in northern Quebec (Plummer, 1954). The Nepean Laboratory (Ottawa) reported a case from Manitoba in 1952 (Table 9.1). Because of the diagnoses of rabies in Alberta, Saskatchewan and northern Manitoba, Dr Alfred Savage, Manitoba’s first animal pathologist, reported that 1953 was a year of watching and waiting, during which diagnosis could be required at any time (Government of Manitoba, 1953). Savage was concerned that wildlife would introduce the disease from the United States into the dog population in south-eastern Manitoba and then into Winnipeg. In 1954 the departmental report acknowledged that rabies was indeed present in this agricultural section of Manitoba and considered it sobering for city and public health officials that rabies was present within 65 kilometres of Winnipeg. Even though Manitoba had wildlife and

livestock in close proximity, Savage did not see rabies as a major issue for livestock as only 13% of animals diagnosed in the United States were farm animals (Government of Manitoba, 1954). He was concerned with the lack of a coordinating authority or a designated provincial veterinarian to help organize the delivery of veterinary services in Manitoba (Government of Manitoba, 1954). By 1955 he conceded, however, that the threat of rabies in the city of Winnipeg had not been realized (Government of Manitoba, 1955). Only sporadic cases of rabies occurred between 1954 and 1956 in southern Manitoba (see Table 9.1). An epizootic of rabies in striped skunks that began in 1959 in Carmen, Manitoba (“Rabies Outbreak in Carman Area,” 1959) was thought to have originated from North Dakota or Minnesota as rabies in skunks had been enzootic in those states for years (Tabel et al., 1974). This outbreak continued to build across southern Manitoba in 1959 and then spread westward across Saskatchewan and into Alberta by 1971 (Charlton et al., 1988). Rabies also appeared in northern Manitoba. In Churchill, the Royal Canadian Mounted

Table 9.1  Rabies incidence by species in Manitoba, 1952 to 2017. Year

Total

Skunk

Live

Dom

Fox

Bat

Other

Wild

Raccoon

1952 1953 1954 1955 1956 1957 1958 1959 1960 1961 1962 1963 1964 1965 1966 1967 1968 1969 1970 1971 1972 1973 1974 1975 1976 1977

1 3 5 3 8 1 2 29 18 83 119 199 38 50 56 25 82 57 24 63 76 98 60 84 92 114

0 0 0 0 0 0 1 28 15 66 98 173 13 34 41 21 66 37 19 50 51 85 45 66 62 93

0 0 0 0 0 0 0 0 2 4 14 16 19 11 12 2 14 18 5 11 16 11 11 12 22 15

0 2 0 1 8 1 0 1 0 10 5 8 6 4 0 0 1 2 0 2 7 2 3 3 5 4

1 1 3 2 0 0 0 0 0 2 2 2 0 0 0 1 1 0 0 0 1 0 0 2 1 2

0 0 0 0 0 0 0 0 0 0 0 0 0 1 1 1 0 0 0 0 0 0 1 0 1 0

0 0 1 0 0 0 1 0 1 0 0 0 0 0 1 0 0 0 0 0 0 0 0 1 0 0

0 0 1 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 1 0 0 0 1 0

0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 (Continued)

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A History of Rabies Management in the Provinces and Territories

Year 1978 1979 1980 1981 1982 1983 1984 1985 1986 1987 1988 1989 1990 1991 1992 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012 2013 2014 2015 2016 2017 Total % Total

Total

Skunk

Live

Dom

Fox

Bat

Other

Wild

60 48 53 170 124 51 54 48 74 54 37 41 62 92 137 84 77 37 24 57 172 227 237 53 47 49 78 73 65 39 50 32 40 21 25 28 15 18 16 14 4,073

46 35 42 151 111 43 47 43 57 36 24 33 52 77 117 68 62 28 18 46 138 187 199 37 35 35 68 59 39 30 43 24 33 17 18 21 11 12 9 9 3,224 79.2

12 11 8 10 7 7 1 3 7 14 12 4 7 12 12 14 9 2 3 3 18 22 23 11 4 6 4 5 16 6 4 2 2 1 2 2 3 3 4 2 513 12.6

2 1 3 7 6 1 4 2 4 4 1 2 0 3 4 2 2 2 1 4 11 8 12 3 3 3 5 4 6 2 2 2 3 1 3 3 1 2 2 3 209 5.1

0 0 0 2 0 0 0 0 5 0 0 1 2 0 0 0 0 3 1 3 2 2 0 1 3 2 1 3 0 0 0 2 0 0 2 1 0 0 0 0 57 1.4

0 0 0 0 0 0 1 0 0 0 0 1 0 0 3 0 3 2 1 0 1 2 1 0 2 2 0 0 3 1 1 1 2 2 0 0 0 1 1 0 36 0.9

0 0 0 0 0 0 0 0 0 0 0 0 1 0 1 0 1 0 0 1 2 3 0 1 0 1 0 0 1 0 0 0 0 0 0 0 0 0 0 0 17 0.4

0 1 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 1 0 0 0 1 0 0 0 0 0 0 0 0 9 0.2

Raccoon 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 1 0 0 0 0 1 0 0 0 0 0 0 0 1 0 0 0 0 8 0.2

Source: compiled from CFIA data.

Police ordered over 20 dogs to be shot following an attack by a rabid wolf (“Rabid Cat Bit Man Test Shows,” 1962). Federal veterinarians confirmed a third rabies outbreak in the north in the Sawbill district northwest of Lynn Lake (“Rabies Strikes Again,” 1962). By the end of 1962, Health of Animals veterinarians reported that the incidence of

diagnosed cases had increased by 20% (“Rabies Rises Sharply,” 1963). Incidence then peaked in 1963 (Table 9.1, Figure 9.2). Coincident with the rise in wildlife was an increase in rabies in domestic animals (cats and dogs) and the potential of increasing contact with humans. For instance, in 1962, a rabid cat bit a resident of North Kildonan

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Figure 9.2: Rabies incidence in Manitoba, 1952 to 2017. Source: created from CFIA data.

that she was not told, by either the federal veterinarian or the provincial health department, to avoid humans having contact with the puppies (“Rabies Warning Never Issued,” 1982; Fitzgerald & McKinley, 1982). Twenty Steinbach residents received rabies prophylaxis after handling a litter of puppies in contact with a rabid skunk (Rance, 1984). Eleven people in Roblin were treated after handling a kitten infected with rabies (Turner, 1992). A single raccoon was positive to rabies in 2000 from skunk strain rabies (MAF, 2000). Sixty-five members of the public and 25 veterinary staff required rabies treatment after two pups contracted rabies following placement with a Winnipeg animal rescue facility (Lett & Horbal, 2005; Millar, 2005). Bat rabies was first diagnosed in Manitoba in 1965 to 1967, with one case in each year. Then it occurred only sporadically until 1992, when there were three cases, and another three cases in 1994. Overall, bats are a small but continuing human health concern compared to rabies in skunks (Table 9.1). CFIA submissions data (Table 9.2) reports eight species of bats submitted for testing in 1985–2017. More little brown bat and big brown bat specimens were submitted than any other species but had few positives. The silver-haired bat and the hoary bat together accounted for almost 90% of positives. There were far fewer bat submissions and positives in Manitoba compared to its adjacent prairie province, Saskatchewan (see Chapter 8). The reason is not known.

just north of Winnipeg and caused a scare that vacated the streets and flooded local veterinarians with requests for vaccinations (“Rabies Empties Streets,” 1962). Another rabid cat entered City Hall and bit three city employees (“Rabies Confirmed,” 1964). Cases in livestock also rose during this period and, with rabies established in the skunk population of Manitoba, there was a low level but steady reporting of rabies in livestock (Table 9.1). After the peak in 1963, the number of diagnosed cases peaked in four- to seven-year cycles driven by incidence in the skunk population. Incidence in livestock and ­domestic animals (cats and dogs) was low but their temporal patterns were significantly statistically correlated (Pearson’s (r), p < .01) with incidence in the skunk population (Table 9.1, Figure 9.2). An unfortunate consequence of exposure to domestic animals was the treatment required for large numbers of people. A Winnipeg pet shop sold a litter of rabid skunks that bit 14 people (“Rabid Skunk Bites Five,” 1969; Riley, 1969). The Manitoba government later enacted a ban on the ownership of skunks with an exception for zoos and research facilities (“‘Pets’ Banned,” 1977). A total of 42 Niverville residents required treatment after handling a litter of puppies that had been in contact with a rabid skunk. This case was characterized by miscommunication as the federal veterinarian allegedly failed to notify public health authorities of the rabies diagnosis. The owner of the puppies, who phoned the provincial health department, claimed

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A History of Rabies Management in the Provinces and Territories

Table 9.2  Bat submissions and test results from Manitoba, 1985 to 2017. Code

Species

Total

Negative

Positive

% Total

LBB BBB SHB HRB NLB LLB PLB REB BAT  

Little brown bat, Myotis lucifugus Big brown bat, Epitesicus fuscus Silver-haired bat, Lasionycterius noctivagans Hoary bat, Lasiurus cineresus Northern long-eared bat, Myotis septentrionalis Long-eared bat, Myotis evotis Pallid bat, Antrozous pallidus Red bat, Lasiurus borealis Unidentified Totals

116 112 104 38 5 2 1 3 14 395

114 112 86 30 5 2 1 2 14 366

2 0 18 8 0 0 0 1 0 29

1.7 0.0 17.3 21.1 0.0 0.0 0.0 33.3 0.0 7.3

Source: compiled from CFIA data.

an outbreak in Yankton, North Dakota, the local board of health recommended that dogs be either muzzled or shot (“Yankton a Plague of Hydrophobia,” 1886). Killing parties were organized following an outbreak of rabies in dogs and cattle in Calhoun County, Florida (“Rabies in Florida,” 1887).

Rabies Management in Manitoba Manitoba responded in several ways to outbreaks of rabies. Early initiatives against the disease included improved diagnostic services, the monitoring and reporting of disease outbreaks, and education. Later, the response involved government incentives and indemnity programs, municipal by-laws requiring vaccination of domestic animals, quarantine regulations, and a prohibition on the ownership of skunks. The province has also worked closely with the federal Canadian Food Inspection Agency (CFIA) and many other agencies, Today, Manitoba’s Zoonotic Diseases Steering Committee coordinates the response by multiple agencies to rabies (Manitoba Agriculture, Food and Rural Initiatives [MAFRI], 2012).

Diagnostic Capability Through the years, Manitoba built a strong capability for diagnosing and monitoring disease through field and laboratory services. The Government of Manitoba supported the response against rabies, and Winnipeg was an important centre for the diagnosis and treatment of rabies. In 1935 the province opened a veterinary diagnostic laboratory in the University Building on Kennedy Street in Winnipeg and moved the facility to the University of Manitoba campus in 1938 (Ellis, 1971). This was timely, as a severe outbreak of western equine encephalomyelitis occurred in 1937, and the laboratory was extensively involved in diagnosing and researching the disease and distributing a vaccine to the municipalities (Government of Manitoba, 1938, 1939). The veterinary laboratory issued its first report in 1939 and since then has been responsible for summarizing disease events for the annual departmental report (Government of Manitoba, 1939). Although the Dominion Health of Animals Branch had primary responsibility for identifying cases of rabies, the new Manitoba veterinary diagnostic laboratory was involved in diagnosing some cases of rabies. In 1947 an outbreak of what was called Northern dog disease occurred in dogs and white foxes, with symptoms similar to rabies. The veterinary laboratory examined the brains of affected animals but did not diagnose rabies; the laboratory was able

Early Management Efforts Early newspaper articles reflect the public’s interest in rabies, or hydrophobia as it was known at the time. Journalists followed stories such as the development of rabies vaccine by Louis Pasteur (“An Invaluable Discovery,” 1884) and a twohour fight with a rabid wolf (“Fighting a Mad Wolf,” 1891). Political commentary alleged that all western Conservatives – as well as a few Liberals – were suffering from rabies (“A Mental and Moral Disease,” 1903). An advertisement promoted California as a land free from tornadoes, cyclones, sunstroke, and rabies (“Science of Home-Making,” 1899). Newspapers also reported on outbreaks in various areas and reflected the management measures in use before diagnostic tests and vaccination were available. Reports of shootings of “mad” dogs in Winnipeg were common (“City and Provincial,” 1879; “City and Country,” 1890). During

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to isolate a neurotropic virus, a finding that was confirmed by the New York State Veterinary College (Government of Manitoba, 1947). Two years later, the laboratory tested three dog brains that were negative for rabies (Government of Manitoba, 1949) and tested two suspect cases in cows during 1953–1954 (Government of Manitoba, 1954). As the disease spread across Manitoba, the veterinary laboratory assisted the Health of Animals Branch by preparing and shipping animal heads to the Animal Diseases Research Laboratory in Hull, Quebec (Government of Manitoba, 1954). Between 1947 and 1985 all Manitoba diagnoses were conducted at Nepean, Ottawa. Subsequently all diagnoses were conducted at Lethbridge, Alberta. Today, CFIA’s five district offices work with their provincial and territorial counterparts, the head office in Winnipeg, and its area office in Calgary to provide regular rabies management to the province.

1974). The intent of the program was to encourage farmers to report cases of the disease to better control it. The provincial and federal governments shared the cost of the program, with the province paying 60% of the expenses. A farmer would receive $300 for an affected cow and a lesser amount for smaller livestock. The program was retroactive to 1 January 1972, and the Veterinary Services Branch took over administration of the program beginning in 1989 (Government of Manitoba, 1990). Table 9.3 summarizes the Rabies Indemnity Program’s total expenditures between 1990 and 2007.

Vaccination Domestic animal vaccines became available by 1952. District veterinarian Dr Ross Singleton was one of the first veterinarians to vaccinate dogs in northern Manitoba to prevent the spread of rabies (R. Singleton, personal communication, 2003). The Dominion Health of Animals Branch vaccinated dogs within a 19-kilometre radius of the United States border in 1952–1953, in an attempt to prevent the entry of rabies from neighbouring Minnesota and North Dakota where rabies had been present for years (Government of Manitoba, 1953). The Northern Affairs Department implemented rabies vaccination requirements for pets and livestock entering Riding Mountain National Park following an outbreak in Alberta in 1957. This requirement was lifted in 1961 despite the protests of the Game and Fish Association and the Manitoba Gun Dog Association who believed the requirement was prudent given the high level of rabies in Manitoba at the time (“No Rabies Check,” 1962). In the early 1960s, a decade after rabies appeared in Manitoba, various municipalities implemented provincial requirements to vaccinate pets for rabies. The town of Boissevain, 270 kilometres southwest of Winnipeg, and the surrounding rural municipality of Morton, were the first municipalities in Manitoba reported to require rabies vaccinations in dogs (“Rabies Shots Made Compulsory,” 1962). The nearby town of Killarney followed suit and several other rural municipalities in the area considered similar by-laws. By the end of 1962, several municipalities, including the towns of Boissevain, Brandon, Elkhorn, Killarney, and Minnedosa, and the rural municipalities of Morton and Portage la Prairie had mandatory rabies immunization provisions in their by-laws (“Rabies Vaccine May Be Required,” 1962). At the same time, Winnipeg city council began considering compulsory rabies vaccinations for pets. The

Education The provincial Department of Agriculture also informed Manitobans about rabies. When the number of animal cases doubled and the number of people given post-exposure treatment quadrupled in 1963, the Department (combined with the Department of Conservation), collaborated with the Health of Animals Branch and the provincial Game Branch to produce and distribute a bulletin about the disease (Government of Manitoba, 1963). Brochures were published with information on rabies management. Eventually, monthly rabies case numbers were published on the website of the Manitoba Veterinary Medical Association. Since 2014, when the province took over responsibility for submitting specimens for testing, Manitoba Public Health has published an annual summary of rabies surveillance data (https://www.gov.mb.ca/health/publichealth/diseases/ rabiessurveillance.html).

Indemnity As rabies became established in Manitoba, the management response evolved into government incentive programs and regulation. In 1960, the Manitoba government announced a bounty for skunks and raccoons, not only to combat the high incidence of rabies in animals but also to address the large number of raccoons that were killing chickens (“Skunk Bounty Planned,” 1960). In 1974 Manitoba Agriculture Minister Samuel Uskiw announced a compensation program for farmers whose livestock were diagnosed with rabies (“Farmers to Get Assistance,”

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A History of Rabies Management in the Provinces and Territories

requirement was defeated (“Can’t Get New $5 Licence,” 1973; “Rabies Shot Not Needed Annually,” 1973; “Rabies Rule Change Requested,” 1973). The Manitoba Academy of Veterinary Medicine (which became the Winnipeg Academy of Veterinary Medicine) then wrote a letter to the city’s Civic Finance Committee asking it to repeal the section requiring proof of rabies vaccination for licensing. The Academy strongly recommended rabies vaccination but felt that vaccination was not necessary in all cases, especially for animals that were not likely to be in contact with wildlife (“Rabies: 78 Cases Here,” 1973). In addition, the city was experiencing administrative problems as veterinarians were not recording expiry dates on the vaccination certificates (“Rabies Rule Change,” 1973). The Civic Finance Committee voted in favour of repealing proof of rabies vaccination for licensing and referred the matter to the Civic Environment Committee for a decision. The Civic Environment Committee, however, reversed the recommendation after the provincial medical health director and the director of the Health of Animals Branch spoke in favour of compulsory vaccination (“No Change Urged,” 1973). The Winnipeg Academy of Veterinary Medicine reiterated its position that rabies vaccination was recommended but it should not be connected to licensing requirements. However, the Civic Environment Committee unanimously recommended no change to the licensing by-law and referred the decision to the Executive Policy Committee, which supported the recommendation (“Rabies Rule Supported,” 1973). Winnipeg city council followed the recommendation and kept the vaccination requirement (“Rabies Shots Backed,” 1973). Within a year, however, the city’s Civic Finance Committee reviewed an administrative report by the city’s treasurer that advised removing the mandatory vaccination requirement, as licensing revenue declined when the requirement was implemented (“Dog Fee Rise Urged,” 1974; “Committee Cool,” 1974). The committee drafted amendments to the by-law which were subsequently reversed by the Executive Policy Committee (“Late Fee Fine Urged,” 1974; “City Committee Wants,” 1974). Once again in 1975, the city’s Civic Finance Committee reviewed the by-laws, but this time decided to retain the rabies vaccination provision (“Higher Dog Rate Unleashed,” 1975). The city’s medical officer of health and the Manitoba Academy of Veterinary Medicine lobbied for rabies education programs instead of compulsory vaccination, but the committee felt that the vaccination requirement provided protection and peace of mind.

Table 9.3  Rabies Indemnity Program expenditures, 1990 to 2007.

n/a = not listed in the annual report Year

Expenditure

1990–1991 1991–1992 1992–1993 1993–1994 1994–1995 1995–1996 1996–1997 1997–1998 1998–1999 1999–2000 2000–2001 2001–2002 2002–2003 2003–2004 2004–2005 2005–2006 2006–2007

$5,000 $14,040 $7,958 $10,540 n/a $1,853 $3,300 $6,450 $16,967 $21,570 $18,343 $4,900 $3,400 $2,260 $2,600 $8,205 $10,800

Source: Manitoba Department of Agriculture annual reports for years listed.

ensuing debate lasted for several decades and illustrates how varying medical opinions, financial considerations, and advocacy groups can confound what seems like a simple issue of public health. At that time Winnipeg’s Civic Health and Welfare Committee decided against compulsory rabies vaccination as a requirement for the purchase of a dog licence on the advice of Dr R. G. Cadham, the city’s medical officer of health. Dr Cadham argued that mandatory rabies vaccination was good in theory but would be difficult to enforce, especially with over 800 stray dogs in Winnipeg and cats that did not require licences. Instead, he recommended that city council educate citizens about the disease and prevention through vaccination (“Obligatory Pet Shots Opposed,” 1962). In 1972 Winnipeg amalgamated with 12 bordering municipalities including Tuxedo, Charleswood, and St Boniface. It drafted a new licensing by-law for several municipalities requiring vaccination of pets but the requirement for vaccination was not in the draft by-law (“Dec. 4, Debate,” 1972). In early 1973 Winnipeg city council passed this licensing by-law and added the requirement for rabies vaccination, despite varying medical opinions on whether it was necessary and the opinion of the Manitoba Academy of Veterinary Medicine that it was not necessary. It had been 20 years since rabies last occurred in a dog in Winnipeg. A motion to remove the

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A subcommittee of the Civic Finance Committee reviewed the licensing by-laws later that year and recommended removing the annual vaccination requirement because of an increased quarantine period following a bite and the three-year coverage of some rabies vaccines, but the city’s Executive Policy Committee again rejected the proposal and recommended that the Civic Environment Committee review the matter (“Ending Rabies Shot Opposed,” 1975). Winnipeg city council agreed and asked the Civic Environment Committee to consider the issue and consult with community groups (“Dog Fees, Fines,” 1975). In an editorial, a local clergy stated that proposed increases in licensing fees and the mandatory rabies requirement was an example of mankind’s inhumanity, as children would be denied pets and owners would be required to pay more or euthanize their animals (Egler, 1976). The Civic Environment Committee proposed that dogs be vaccinated every two years (“2nd Year Easy One,” 1976). The Manitoba Veterinary Medical Association stated that a veterinarian should decide whether an animal should be vaccinated and that the city should also require rabies vaccinations for cats (“Vets Want Say,” 1976). The rabies vaccination debate then subsided until 1987, when a consultant and former director of the Winnipeg Humane Society reviewed the city’s animal control by-laws and recommended that the city license cats with a mandatory vaccination requirement (Spiers, 1987). In 1990 an ad-hoc animal control committee considered mandatory licensing and rabies vaccination for cats in response to an increase in stray cats; however, this recommendation was opposed by the Manitoba Cat Club (McFarland, 1990). The city of Winnipeg considered removing the rabies vaccination requirement in 1997, but this was opposed by the Manitoba Veterinary Medical Association, which also proposed that veterinarians sell licences in their clinics (“City Has to Become Serious,” 1997; Owen, 1997). The Civic Executive Committee considered licensing for cats and removing the rabies vaccination requirement, and estimated that there were 100,000 dogs in the city, with 50,000 of these vaccinated and only 8,000 licensed (Rollason, 1997). It was also reported that the city was considering lobbying the Manitoba government to make rabies vaccination mandatory (“Reining in Cats,” 1997). By the end of 1997, the city’s licensing notice stated that proof of vaccination was no longer required for licensing (“The City of Winnipeg,” 1997). Today, Winnipeg’s pound by-law requires that all dogs and cats in the city must be vaccinated for rabies and that proof of vaccination must be shown when asked. Exemptions are granted if veterinarians write a letter stating that the animal cannot be vaccinated for medical ­reasons (City of Winnipeg, 2019).

Quarantine In the past, domestic dogs and cats biting or scratching humans were often quarantined by the district veterinarian after assessment for risk of contact with rabies. Today, quarantines are established by the local Health Department following a biting incident. The quarantines are used to assess the rabies status of dogs following incidents where humans were bitten.

Wildlife Ownership In 1970, following an incident the previous year of exposure in people who bought skunks from a Winnipeg pet shop (Riley, 1969), the province made a change under the Public Health Act to require that persons who wish to keep skunks as pets must obtain permission from the local medical officer of health (“Dampers on Pet Skunks,” 1970). No medical officers, however, were willing to grant permission, and in 1977 an Order in Council made a new regulation that banned skunk ownership altogether except in a zoo (“‘Pets’ Banned,” 1977).

Current Practice In 2006 the Manitoba government appointed the province’s first chief veterinary officer, Dr Wayne Lees. This office established the Zoonotic Diseases Steering Committee, a multi-agency, multi-jurisdictional group to facilitate the surveillance, risk assessment, and response for zoonotic diseases (Government of Manitoba, 2006). The Department of Conservation noted an overpopulation of raccoons in Winnipeg and that a reduction strategy would be required in the future (Government of Manitoba, 2008, 2009). The committee facilitated a project to map locations of raccoon latrines with the incidence of Baylisascaris procyonis (Sexsmith, 2009), an initiative designed to assist control efforts of the animal should rabies infect the raccoon population. There are several legislative requirements to report rabies in Manitoba. In July 2007 the Reportable Diseases Regulation of the Animal Health Act came into effect, requiring all federally reportable diseases, including rabies, to be reported to the chief veterinary officer. In February 2009 the Reporting of Diseases and Conditions Regulation under the Public Health Act was passed, requiring that reports of rabies, including a negative test result, be sent to a medical officer or public health nurse.

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A History of Rabies Management in the Provinces and Territories

As of 1 April 2014, the CFIA stopped managing rabies control activities in Manitoba. The provincial Rabies Management Program is coordinated by Manitoba Rabies Central, a collaborative program involving the Manitoba Department of Health, Healthy Living and Seniors, and Sustainable Development. Since rabies is a reportable disease under the Health of Animals Act, the Public Health Act, and the Animal Diseases Act, all suspected cases of rabies in animals and humans must be reported. All rabies suspect exposures (animal or human) are evaluated through a collaborative One Health approach. For general information about rabies or to report human exposure to an animal suspected of having rabies Health Links/Info Santé is the appropriate contact. To report domestic animal exposure to an animal suspected of having rabies (no human exposure), the chief veterinary officer should be notified. To report any animals acting strangely or dead animals, the local Sustainable Development office is the appropriate contact. Diagnosis of rabies is left to the federal government via the CFIA (see Chapter 31). Previously, suspect rabies case samples were sent to the CFIA laboratory at Lethbridge, but because of delays in-transit of the specimens, they are now routed to CFIA in Ottawa. Manitoba does not undertake active surveillance of rabies through its Rabies Management Program. Wildlife is tested for rabies only if a risk assessment indicates that the animal could have rabies and had contacted a domestic animal or human (S. Richards, personal communication, 2015). It is possible that the redistribution of responsibilities in the management of rabies in Manitoba after 2013 has affected disease reporting. Annual reported cases of rabies in 2014–2017 are approximately 50% less than in 2013 and much lower, on average, than in the previous decade (Table 9.1). Annual submissions have also declined by 50% since 2013. These data may reflect an apparent long-term decline in rabies in skunks, the primary wildlife rabies vector in the province (Figure 9.1). Chapter 21, on passive surveillance, further discusses the potential impact of CFIA’s 2014 decision on disease reporting and rabies management in Canada.

Discussion Rabies in Manitoba shares many of the characteristics of rabies in its western neighbour, Saskatchewan. The virus circulates within the skunk (Mephitis mephitis) population, and there is the constant threat of new introductions from the US border states. Cases in domestic and livestock populations are driven by rabies in the skunk population. Fortunately, large spillover into the fox population or raccoon population has not occurred nor has a major threat arisen from arctic fox rabies in the northern territories (Table 9.2). Aside from the traditional measures of quarantine and vaccination for domestic animals and public education about the danger of rabies, there has been no effort to eliminate rabies in the skunk population in Manitoba. As noted in Chapter 8, the difference in bat submissions between Manitoba and Saskatchewan is huge: from 1985 to 2017 Saskatchewan submitted eight times as many bat specimens as Manitoba, despite both provinces having similar species distributions of bats, agricultural base, and climate. One can only speculate on why this difference occurs. Although submissions in all other species categories are higher in Saskatchewan than in Manitoba, the ratio of the difference (1.23) is relatively small compared to bat submissions. There are approximately 2.3 times as many farms in Saskatchewan than Manitoba (Statistics Canada, 2006), but Manitoba has slightly more people (about 1.18 times total and 1.27 times rural in 2006) than Saskatchewan. Hence, differences in the potential number of contacts seem unlikely to account for the magnitude of the difference in bat submissions. A possibility is that provincial officials differ on defining the circumstances that warrant submission when bats are involved. Other provinces (British Columbia, Ontario, and Quebec; see Chapters 6, 10, and 11, respectively) noted dramatic changes in bat submissions when their protocols for defining risk changed. Without detailed comparison of the circumstances resulting in submissions in each province, however, it is unlikely that the disparity in bats submissions between provinces will be completely understood.

Acknowledgment The author would like to thank Dr Shauna Richards, operations veterinarian – One Health – rabies, of the Manitoba Department of Agriculture for her contribution in clarifying the operation of Manitoba’s current rabies program.

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References Can’t get new $5 licence till dog has rabies shot. (1973, January 11). Winnipeg Free Press, p. 63. Retrieved from https:// newspaperarchive.com/winnipeg-free-press-jan-11-1973-p-61/ Charlton, K. M., Webster, W. A., Casey, G. A., & Rupprecht, C. E. (1988). Skunk rabies. Review of Infectious Diseases, 10(Suppl. 4), S626–S628. https://doi.org/10.1007/978-1-4613-1755-5_5 City and country. (1890, June 11). Manitoba Daily Free Press, p. 6. Retrieved from https://newspaperarchive.com /winnipeg-free-press-jun-11-1890-p-6/ City committee wants $10 dog fee. (1974, April 13). Winnipeg Free Press, p. 77. Retrieved from https://newspaperarchive.com /winnipeg-free-press-apr-13-1974-p-77/ City has to become serious about educating pet owners. (1997, July 15). Winnipeg Free Press, p. 12. Retrieved from https:// newspaperarchive.com/winnipeg-free-press-jul-15-1997-p-12/ City of Winnipeg. (2019). City of Winnipeg animal services agency – pound by-law no. 2443/79 extracts. Retrieved from https://­ winnipeg.ca/cms/animal/pdfs/RPO.pdf The City of Winnipeg, Community Services Department, Animal Services Division, licence notice. (1997, December 20). Winnipeg Free Press, p. 12. Retrieved from https://newspaperarchive.com/winnipeg-free-press-dec-20-1997-p-12/ City and provincial. (1879, June 12). Manitoba Daily Free Press, p. 1. Retrieved from https://newspaperarchive.com/winnipeg -free-press-jun-12-1879-p-1/ Committee cool to dog fee rise idea. (1974, March 6). Winnipeg Free Press, p. 3. Retrieved from https://newspaperarchive.com /winnipeg-free-press-mar-06-1974-p-3/ Dampers on pet skunks. (1970, February 5). Winnipeg Free Press, p. 8. Retrieved from https://newspaperarchive.com /winnipeg-free-press-feb-05-1970-p-8/ Dec. 4, Debate on upping price of dog licences. (1972, November 7). Winnipeg Free Press, p. 3. Retrieved from https:// newspaperarchive.com/winnipeg-free-press-nov-07-1972-p-3/ Dog fee rise urged. (1974, February 27). Winnipeg Free Press, p. 3. Retrieved from https://newspaperarchive.com /winnipeg-free-press-feb-27-1974-p-3/ Dog fees, fines will cost more. (1975, November 20). Winnipeg Free Press, p. 3. Retrieved from https://newspaperarchive.com /winnipeg-free-press-nov-20-1975-p-3/ Egler, H. (1976, January 3). The saviour suffered most painful death – Inhumanity not new. Winnipeg Free Press, p. 90. Retrieved from https://newspaperarchive.com/winnipeg-free-press-jan-03-1976-p-90/ Ellis, J. H. (1971). The Ministry of Agriculture in Manitoba. Winnipeg, MB: Queen’s Printer. Ending rabies shot opposed. (1975, November 15). Winnipeg Free Press, p. 3. Retrieved from https://newspaperarchive.com /winnipeg-free-press-nov-15-1975-p-3/ Environment and Climate Change Canada and Canadian Wildlife Federation. (2005). Mammal fact sheets. Retrieved from Hinterland Who’s Who website: http://www.hww.ca/en/wildlife/mammals/ Farmers to get assistance. (1974, February 5). Winnipeg Free Press, p. 16. Retrieved from https://newspaperarchive.com/ winnipeg-free-press-feb-05-1974-p-16/ Fears hydrophobia: Dr Ball taking Pasteur treatment – Inoculated himself by accident. (1906, April 16). Manitoba Free Press, p. 9. ­Retrieved from https://newspaperarchive.com/winnipeg-free-press-apr-16-1906-p-9/ Fighting a mad wolf: Terrific struggle with a dangerous guest hidden in a house. (1891, September 26). Manitoba Daily Free Press, p. 2. Retrieved from https://newspaperarchive.com/winnipeg-free-press-sep-26-1891-p-2/ Fitzgerald, M. A., & McKinley, P. (1982, June 9). Federal Department cited in rabies case. Winnipeg Free Press, p. 9. Retrieved from https://newspaperarchive.com/winnipeg-free-press-jun-09-1982-p-9/ Government of Manitoba. (1889). Report of the Department of Agriculture and Immigration for the year ending December 31, 1889. ­Winnipeg, MB: Author. Government of Manitoba. (1893). Report of the Department of Agriculture and Immigration for the year ending December 31, 1893. ­Winnipeg, MB: Author. Government of Manitoba. (1938). Annual Report, Department of Agriculture and Immigration 1937–1938, fiscal year ending April 30, 1938. Winnipeg, MB: Author. Government of Manitoba. (1939). Annual Report, Department of Agriculture and Immigration 1938–1939, fiscal year ending April 30, 1939. Winnipeg, MB: Author. Government of Manitoba. (1947). Department of Agriculture and Immigration, Annual Report, 1946–1947, fiscal year ending March 31, 1947. Winnipeg, MB: Author.

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A History of Rabies Management in the Provinces and Territories Government of Manitoba. (1949). Department of Agriculture and Immigration, Annual Report, 1948–1949, fiscal year ending March 31, 1949. Winnipeg, MB: Author. Government of Manitoba. (1953). Department of Agriculture and Immigration, Annual Report, 1952–1953, fiscal year ending March 31, 1947. Winnipeg, MB: Author. Government of Manitoba. (1954). Department of Agriculture and Immigration, Annual Report, 1953–1954, fiscal year ending March 31, 1954. Winnipeg, MB: Author. Government of Manitoba. (1955). Department of Agriculture and Immigration, Annual Report, 1954–1955, fiscal year ending March 31, 1955. Winnipeg, MB: Author. Government of Manitoba. (1963). Annual Report of the Department of Agriculture and Conservation for the year ended March 31, 1963. Winnipeg, MB: Author. Government of Manitoba. (1990). Annual report 1989–1990, Agriculture. Winnipeg, MB: Author. Government of Manitoba. (2006). Annual report 2005–2006, Agriculture. Winnipeg, MB: Author. Government of Manitoba. (2008). Manitoba Conservation annual report. Winnipeg, MB: Author. Government of Manitoba. (2009). Manitoba Conservation annual report. Winnipeg, MB: Author. Higher dog rate unleashed. (1975, March 12). Winnipeg Free Press, p. 3. Retrieved from https://newspaperarchive.com /winnipeg-free-press-mar-12-1975-p-3/ An invaluable discovery. (1884, May 21). Manitoba Daily Free Press, p. 1. Retrieved from https://newspaperarchive.com /winnipeg-free-press-may-21-1884-p-1/ Late fee fine urged. (1974, April 10). Winnipeg Free Press, p. 3. Retrieved from https://newspaperarchive.com/winnipeg -free-press-apr-10-1974-p-3/ Lett, D., & Horbal, J. (2005, January 11). Rabies turns up in pups Vaccinations Ordered. Winnipeg Free Press, p. B1. Retrieved from https://newspaperarchive.com/winnipeg-free-press-jan-11-2005-p-13/ Manitoba Agriculture and Food. (2000). Rabies report 2000. Winnipeg, MB: Author. Manitoba Agriculture, Food and Rural Initiatives. (2012). Annual report, 2011–2012. Retrieved from https://www.gov.mb.ca/finance /publications/pubs/annualrep/2011_12/agriculture.pdf McFarland, J. (1990, April 24). Janet McFarland, Councillors ponder ways to keep cats from roaming city. Winnipeg Free Press, p. 3. ­Retrieved from https://newspaperarchive.com/winnipeg-free-press-apr-24-1990-p-3/ McGillivray, B. (2006). Canada – A nation of regions. Don Mills, ON: Oxford University Press. A mental and moral disease. (1903, January 16). Manitoba Free Press, p. 4. Retrieved from https://newspaperarchive.com/ winnipeg-free-press-jan-16-1903-p-4/ Millar, K. (2005, January/February). Another litter of pups positive for rabies. MVMA News and Views eNewsletter, 6. No change urged in rabies bylaw. (1973, March 6). Winnipeg Free Press, p. 3. Retrieved from https://newspaperarchive.com /winnipeg-free-press-mar-02-1973-p-9/ No rabies check on pets into park. (1962, May 28). Winnipeg Free Press, p. 3. Retrieved from https://newspaperarchive.com /winnipeg-free-press-may-28-1962-p-3/ Obligatory pet shots opposed. (1962, August 29). Winnipeg Free Press, p. 2. Retrieved from https://newspaperarchive.com /winnipeg-free-press-aug-29-1962-p-2/ Owen, B. (1997, February 25). Rabid skunk focuses issue Vets urge city to keep rabies shot part of license. Winnipeg Free Press, p. 48. Retrieved from https://newspaperarchive.com/winnipeg-free-press-feb-25-1997-p-48/ “Pets” banned, skunks on receiving end of stink over health risk. (1977, March 11). Winnipeg Free Press, p. 1. Retrieved from https:// newspaperarchive.com/winnipeg-free-press-mar-11-1977-p-1/ Plummer, P. J. G. (1954). Rabies in Canada, with special reference to wildlife reservoirs. Bulletin of the World Health Organization, 10, 767–774. Rabid cat bit man test shows. (1962, February 1). Winnipeg Free Press, pp. 1, 10. Retrieved from https://newspaperarchive.com /winnipeg-free-press-feb-01-1962-p-10/ Rabid skunk bites five, 14 infected. (1969, August 22). Winnipeg Free Press, p. 1. Retrieved from https://newspaperarchive.com /winnipeg-free-press-aug-22-1969-p-1/ Rabies at Moosomin. (1907a, July 17). Manitoba Free Press, p. 2. Retrieved from https://newspaperarchive.com /winnipeg-free-press-jul-17-1907-p-2/ Rabies at Moosomin. (1907b, August 9). Manitoba Free Press, p. 29. Retrieved from https://newspaperarchive.com /winnipeg-free-press-aug-09-1907-p-29/ Rabies confirmed cat bites city employee. (1964, September 29). Winnipeg Free Press, p. 1. Retrieved from https://newspaperarchive .com/winnipeg-free-press-feb-14-1963-p-8/

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Manitoba Rabies empties streets. (1962, February 2). Winnipeg Free Press, pp. 1, 5. Retrieved from https://newspaperarchive.com /winnipeg-free-press-feb-02-1962-p-1/ Rabies in Florida. (1887, June 16). Manitoba Daily Free Press, p. 1. Retrieved from https://newspaperarchive.com/winnipeg -free-press-jun-16-1887-p-1/ Rabies outbreak in Carman area. (1959, May 9). Winnipeg Free Press, p. 4. Retrieved from https://newspaperarchive.com /winnipeg-free-press-may-09-1959-p-4/ Rabies rises sharply in ’62 spreads to domestic animals. (1963, February 14). Winnipeg Free Press, p. 8. Retrieved from https:// newspaperarchive.com/winnipeg-free-press-feb-14-1963-p-8/ Rabies rule change requested. (1973, February 13). Winnipeg Free Press, p. 3. Retrieved from https://newspaperarchive.com /winnipeg-free-press-feb-13-1973-p-3/ Rabies rule supported. (1973, March 9). Winnipeg Free Press, p. 9. Retrieved from https://newspaperarchive.com /winnipeg-free-press-mar-09-1973-p-9/ Rabies: 78 cases here. (1973, March 2). Winnipeg Free Press, p. 9. Retrieved from https://newspaperarchive.com /winnipeg-free-press-mar-02-1973-p-9/ Rabies shot not needed annually. (1973, January 12). Winnipeg Free Press, p. 2. Retrieved from https://newspaperarchive.com /winnipeg-free-press-jan-12-1973-p-2/ Rabies shots backed. (1973, March 22). Winnipeg Free Press, p. 75. Retrieved from https://newspaperarchive.com /winnipeg-free-press-mar-22-1973-p-75/ Rabies shots made compulsory. (1962, January 27). Winnipeg Free Press, p. 3. Retrieved from https://newspaperarchive.com /winnipeg-free-press-jan-27-1962-p-3/ Rabies strikes again northern Manitoba huskies attacked; tests under way. (1962, March 7). Winnipeg Free Press, p. 3. Retrieved from https://newspaperarchive.com/winnipeg-free-press-mar-07-1962-p-3/ Rabies vaccine may be required for all city dogs. (1962, August 25). Winnipeg Free Press, p. 1. Retrieved from https://newspaperarchive .com/winnipeg-free-press-aug-25-1962-p-3/ Rabies warning never issued: Health Department “inaction” linked to spread of rabies in Niverville. (1982, June 8). Winnipeg Free Press, p. 8. Retrieved from https://newspaperarchive.com/winnipeg-free-press-jun-08-1982-p-8/ Rance, L. (1984, July 7). Rabies vaccine administered after skunk infects puppies. Winnipeg Free Press, p. 15. Retrieved from https:// newspaperarchive.com/winnipeg-free-press-jul-07-1984-p-15/ Reining in cats. (1997, September 19). Winnipeg Free Press, p. 16. Retrieved from https://newspaperarchive.com /winnipeg-free-press-sep-19-1997-p-16/ Riley, S. (1969, August 23). Pet shop sold skunk. Winnipeg Free Press, pp. 1, 6. Retrieved from https://newspaperarchive.com /winnipeg-free-press-aug-23-1969-p-1/ Robertson, J. (2004). Resource management: A history of the successes and failures of wildlife and fishery resource management in ­Manitoba. Dauphin, MB: Author. Rollason, K. (1997, September 17). Free roaming cats may catch fines. Winnipeg Free Press, p. 4. Retrieved from https:// newspaperarchive.com/winnipeg-free-press-sep-17-1997-p-4/ Science of home-making: Why so successfully studied and practiced in California. (1899, February 13). Manitoba Morning Free Press, p. 2. Retrieved from https://newspaperarchive.com/winnipeg-free-press-feb-13-1899-p-2/ 2nd year easy one for pets. (1976, February 3). Winnipeg Free Press, p. 3. Retrieved from https://newspaperarchive.com/ winnipeg-free-press-jan-03-1976-p-90/ Sexsmith, J., Whiting, T., Green, C., Orvis, S., Berezanski, D., & Thompson, A. B. (2009). Prevalence and distribution of Baylisascaris procyonis in urban raccoons (Procyon lotor) in Winnipeg, Manitoba. Canadian Veterinary Journal, 50(8), 846–850. Skunk bounty planned. (1960, March 5). Winnipeg Free Press, p. 5. Retrieved from https://newspaperarchive.com/ winnipeg-free-press-mar-05-1960-p-5/ Spiers, D. (1987, April 21). City pound review targets cat owners. Winnipeg Free Press, p. 6. Retrieved from https://newspaperarchive .com/winnipeg-free-press-apr-21-1987-p-6/ Statistics Canada. (2006). Agriculture overview, Canada and the provinces, Table 1.1. Retrieved from https://www150.statcan.gc.ca/n1 /pub/95-629-x/1/4123801-eng.htm#46 Tabel, H., Corner, A. H., Webster, W. A., & Casey, C. A. (1974). History and epizootiology of rabies in Canada. Canadian Veterinary Journal, 15(10), 271–281. Turner, R. (1992, August 31). Rabies scare strikes Roblin. Winnipeg Free Press, p. 15. Retrieved from https://newspaperarchive.com /winnipeg-free-press-aug-31-1992-p-15/

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A History of Rabies Management in the Provinces and Territories Vets want say on rabies shots – For cats, too. (1976, March 12). Winnipeg Free Press, p. 8. Retrieved from https://newspaperarchive.com /winnipeg-free-press-mar-12-1976-p-8/ Warkentin, John. (2000). A regional geography of Canada: Life, land and space. Scarborough, ON: Prentice-Hall Canada. Weir, T. R. (2012). Manitoba. Retrieved from the Canadian Encyclopedia website: https://www.thecanadianencyclopedia.ca/en/article /Manitoba Welsted, J. (1996). The geography of Manitoba: Its land and its people. Winnipeg, MB: University of Manitoba Press. Winnipeg is a healthy city: Dr Bell’s report. (1908, January 3). Manitoba Free Press, p. 21. Retrieved from https://newspaperarchive.com /winnipeg-free-press-jan-03-1908-p-21/ Yankton a plague of hydrophobia. (1886, June 14). Manitoba Daily Free Press, p. 1. Retrieved from https://newspaperarchive.com /winnipeg-free-press-jun-14-1886-p-1/

124

10 Ontario Rowland R. Tinline1 and Rick Rosatte2 1

Professor Emeritus, Department of Geography, Queen’s University, Kingston, Ontario, Canada Wildlife Research and Development Section, Ontario Ministry of Natural Resources (Retired), Peterborough, Ontario, Canada

2

Place Ontario is Canada’s second-largest province with a land area of 908,608 km2 (Figure 10.1) and a population of 13,448,494 in 2016 (Statistics Canada, 2017). The area was originally settled by Algonquin and Iroquoian speaking peoples, and the name Ontario was derived from the Iroquois word meaning “beautiful lake,” “beautiful water,” or “big body of water.” Although always linked to the Great Lakes, the boundaries and the name have changed over time in response to settlement, language, conflict, and political accommodation (Overview, Part 3). For the years relevant to this chapter, the area was part of Quebec until 1791, when it was split into an English Upper Canada (the upstream part of the St Lawrence River that includes what is currently southern Ontario, plus a strip of land adjacent to the northern shore of Lake Superior) and French Lower Canada (the downstream part of the St Lawrence River). After unrest and rebellion against British rule was coupled with the fear of American expansion, a federal union of all British North American colonies was proposed. In 1867 the British North America Act was enacted, creating the Dominion of Canada with four provinces: Nova Scotia, New Brunswick, Quebec, and Ontario, with the last two being the former areas of Upper and Lower Canada. Over the next 45 years Ontario claimed land to the north and west, including, at one time, southeastern Manitoba (see Overview, Part 3). The claims were finally settled in 1912 when the current boundaries were adopted as shown in Figure 10.1.

From a rabies perspective, the topography shown in Figure 10.1 can be split into five regions: the Hudson and James Bay Lowlands, the Canadian Shield, eastern Ontario (E), central Ontario (C), and southwestern Ontario (SW). Each region has played a role in the distribution, spread and persistence of rabies in Ontario. Land in the north along the coasts of Hudson Bay and James Bay is low and swampy. This was the area where the first cases of rabies in foxes (arctic and red) occurred and is the continuing link with the enzootic arctic fox rabies area in Nunavut (see Chapter 26b on the arctic fox and Chapter 14c on Nunavut). The Canadian Shield has a low and rolling rocky Precambrian topography covered by boreal forest interspersed with thousands of lakes and rivers. It covers most of northern Ontario, south of the Hudson Bay and James Bay lowlands and extends into southcentral and eastern Ontario, where the boreal forest transitions to a mixed forest of hardwoods and softwoods. The Shield, for the most part, has acted as a barrier to limit the southward and northward spread of rabies from the lowlands. The southern extension of the Shield, the Frontenac Axis, narrows as it crosses the St Lawrence River, creating the Thousand Islands and linking the Canadian Shield to the Adirondacks in northern New York. It has provided a barrier to the spread of fox rabies between southeastern and central Ontario. Eastern Ontario is dominated by the lowlands of the St Lawrence River and Ottawa River – a relatively flat area of good agriculture with remnants of the original mixed forest. This agricultural area extends eastward along the St Lawrence River valley into Quebec and has been the

A History of Rabies Management in the Provinces and Territories

Figure 10.1: Topographic relief of Ontario.

Source: created from base maps from Natural Resources Canada.

conduit for the spread of fox rabies between Ontario and Quebec and subsequently into the Maritimes. Central Ontario lies along the northern shore of Lake Ontario, taking in the southern fringes of the Canadian Shield and extending to the major concentrations of population surrounding Toronto and Hamilton and to the Niagara Escarpment.

These boundaries contain areas of excellent farm land that sustain a relatively large small-mammal population and provide with many opportunities to interact with domestic animals and livestock. The Niagara Escarpment runs from the western tip of Lake Ontario north to Georgian Bay and then along the southern shore of Georgian Bay and up the

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southward invasion of what was later identified as the Arctic fox strain of rabies (see Chapter 29).

Table 10.1  Rabies incidence in Ontario, 1926 to 1946. Domestic

Livestock

Year

Total

Dog

Cat

Cow

1926 1927 1928 1929 1930 1931 1933 1934 1937 1939 1942 1943 1944 1945 1946

30 39 69 75 67 1 17 1 1 14 5 23 50 35 15

25 33 44 54 35 1 9 1 1 10 5 22 46 29 14

0 2 7 4 1 0 0 0 0 1 0 1 1 1 0

4 3 15 9 20 0 3 0 0 3 0 0 2 5 0

Totals % Total

442

Horse Sheep 0 0 0 0 1 0 1 0 0 0 0 0 1 0 0

1 1 3 6 7 0 3 0 0 0 0 0 0 0 0

Pig

Invasion of Arctic Fox Rabies

0 0 0 2 3 0 1 0 0 0 0 0 0 0 1

329

18

64

3

21

7

74.4

4.1

14.5

0.7

4.8

1.6

During the early 1950s, rabies spread southwards from NWT, initiating the most intensive rabies epizootic in Canadian history. The outbreak included Alberta, northern British Columbia, Saskatchewan, Manitoba, Ontario, and Quebec. In the west it was driven by wolves and coyotes (see Chapter 2) and in Ontario, by the red fox (Johnston & Beauregard, 1969). Diagnosed cases in red foxes first showed up in northern Ontario in 1954 as part of a spread around the west coast and east coasts of Hudson Bay and James Bay, respectively. Southward spread was rapid (Figures 10.3 to 10.7) covering most of southern Ontario by 1958. Figure 10.8 shows that the spread into southern Ontario in two streams. The first stream passed around Georgian Bay, through the district of Parry Sound, and then bifurcated at Lake Simcoe, with one arm fanning out into southwestern Ontario and spreading into the peninsular areas by 1960, and the other arm moving into central Ontario until its progress was impeded by the Canadian Shield and its extension, the Frontenac Axis, east of Kingston. The second stream came across the Ottawa River from the Quebec side and spread west until it, too, slowed at the Frontenac Axis. These streams set the pattern for the spatial distribution of rabies in southern Ontario for the next 35 years.

Source: compiled from CFIA data.

Bruce Peninsula. It is an uplifted plateau that slopes south and west and provides a distinct eastern boundary for the rich fertile area of southwestern Ontario that, like central Ontario, sustains large small-mammal populations and provides opportunities for interaction with other species. Southwestern and central Ontario reported over 75% of rabies cases in Ontario from 1927 to 2017. Winters in the north are cold and long, and summers are typically short and warm, although sudden swings in temperature are common. Winters in the south are shorter and less severe. Summer temperatures in the south are much warmer, but they are moderated by the Great Lakes. Snow cover is typically two to three months but lake effect snow squalls can extend this period in several areas. The combination of physiography and climate has influenced the distribution and persistence of rabies in the province.

Enzootic Rabies The southwards expansion peaked in 1958 at almost 2500 cases, waned, then quickly rebounded by 1968 to level out at 1730 cases (Table 10.2, Figure 10.9). Rabies has remained enzootic in southern Ontario to the present, although incidence declined dramatically beginning in 1989 after the introduction of Ontario’s Oravax wildlife vacation campaign, discussed later in this chapter. The distribution of hotspots in incidence in 1958 (Figure 10.7) set the pattern for incidence in Ontario until the early 1990s when the impact of the Oravax campaigns became evident. The dominant pattern showed a case concentration in southeastern Ontario to the east of the Frontenac Axis and a case concentration in southwestern Ontario centred in counties south of Georgian Bay (Figures 10.9 and 10.10). Although the pattern waxed and waned over time, the variations were cyclical and predictable with cycles of three to six years. Using time series analysis, Tinline and MacInnes (2004) demonstrated that within this overall pattern there were 13

Rabies in Ontario Rabies has been reported in Ontario since the early nineteenth century. Rabies cases in Ontario until 1953 were associated with sporadic and scattered outbreaks in canines and subsequent spillover into cats and livestock in southern Ontario. These patterns are shown in Table 10.1 and Figure 10.2. Between 1947 and 1952 no rabies cases were reported in Ontario. During this lull rabies in foxes was diagnosed by Plummer (1954) in Baker Lake, Northwest Territories (NWT). Subsequently, there was a massive

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A History of Rabies Management in the Provinces and Territories

Figure 10.2: Diagnosed cases of ­rabies in Ontario, 1926 to 1953. Source: created from CFIA data.

stable clusters of townships, which they called rabies units (Figure 10.11). Those units had different behaviours in terms of species distribution, persistence, and periodicity. Since peaks in the time series in adjacent units were not synchronous (as one unit waned, an adjacent unit peaked) they argued that the overall pattern revealed a metapopulation structure that contributed to the persistence of rabies in southern Ontario. Earlier analysis of this structure based on county-level data helped Ontario plan its oral vaccination control campaigns (MacInnes et al., 1988). The work of Nadin-Davis and colleagues (see Chapter 29) on N and T gene variation in the arctic fox rabies virus in Ontario provided further support for the existence of sub-populations of foxes in the region. They identified four arctic fox variants in southern Ontario and argued that the distribution of those variants was related to the topographical features that appeared to have influenced the initial patterns of spread through the sub-populations of foxes in southern Ontario. The mapping of the distribution of those variants correlated well with the rabies units delineated in Figure 10.11. They also identified a fifth variant in northern Ontario that was even more closely related to the

viruses that circulate in northern Canada. They cautioned that future southern incursions of arctic fox variant rabies are likely. By the 1960s rabies was well established in red foxes and striped skunks in the agricultural lands of southern Ontario (an area of approximately 100,000 km2). Less than 3% of all cases in Ontario had occurred in northern Ontario. Table 10.2 shows that foxes and skunks have accounted for over 65% of all cases in Ontario. Spillover into livestock, dogs, and cats accounted for another 30% of cases. Bats (2.5%) have been the only other major contributor to incidence in Ontario until the recent invasions of the raccoon strain of rabies discussed in “The Invasions of Raccoon Rabies” in this chapter. Between 1958 and 1989 Ontario had about 85% of the rabies cases in all of Canada. Incidence in foxes drove incidence in skunks, livestock, and domestic animals. Incidence in skunks had been highly correlated with incidence in foxes since the late 1950s. Typically incidence in skunks lagged incidence in foxes by one to three months – the incubation period of the disease. On an annual basis the number of cases in skunks was typically 40% to 60% of that in foxes.

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Figure 10.3: Diagnosed cases of rabies in Ontario in 1954. Source: created from CFIA data.

For a brief period in the early 1980s, skunk incidence began to match fox incidence (Figure 10.12, Table 10.2). Since this change occurred across southern Ontario, it seemed likely that some widespread change in the environment had affected animal behaviour. We suspect that below average snow cover for several years in the early 1980s, particularly 1980 and 1983, was the driving factor. Skunks are not true hibernators, denning up in cold weather but occasionally venturing out to forage. Hence, lower snow cover allows increased foraging which leads to better survival, more chances for reproduction, higher populations, and, therefore, more potential contacts for the spread of rabies. By 1984 snow cover across southern Ontario reverted to more historical patterns and fox incidence again surpassed skunk incidence. By the early 1990s the ongoing Oravax control program began to have a major effect by reducing rabies cases in foxes. By 1995 only five cases of rabies in foxes were reported. Although cases in skunks also dropped, the effect was not as great. From 1995 to 2017 there were 136 rabies cases in foxes and 485 cases in skunks in Ontario. The continuing concern with skunks led to major design changes in the Oravax bait and its application that are described

in the chapters on vaccine development (Chapter 17) and aerial baiting (Chapter 19). No new cases were reported from 2013 to 2015 (Figure 10.13, Table 10.2). In 2016–2017, however, there were 121 cases in skunks. This increase was a spillover from the epizootic in raccoons around Hamilton, Ontario (see “The Invasions of Raccoon Rabies” in this chapter). Cases in domestic animals (cat/dog) also dropped sharply as fox rabies was controlled (Table 10.2). While cases in livestock were also reduced, they did not drop as fast and lingered until incidence in skunks dropped. Presumably pets were more likely to be involved with foxes while livestock had more opportunity to be involved with both skunks and foxes. Over 97% of rabies cases occurred in southern Ontario, with the highest concentration of cases per 100 km2 in the southwest (Table 10.3). This regional distribution of cases likely reflects habitat and land use differences rather than the number of potential observers in an area. The central region, for example, has the highest population but includes metropolitan Toronto and a large portion of the Canadian Shield to the north, both of which offer fewer

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A History of Rabies Management in the Provinces and Territories

Figure 10.4: Diagnosed cases of rabies in Ontario in 1955. Source: created from CFIA data.

in bats are not known. The following paragraphs discuss the impact of publicity and changes in policy recommendations on specimen submissions and, by implication, the number of diagnosed cases. Figure 10.15 shows submissions involving bats spiked in 2001 then declined in 2009. The reason for this increase is not known, but it may be reaction to an incident in Montreal, Quebec, in 2000. A boy was bitten by a bat and died a month later as a result of the bite. The bat was later identified as a silver-haired bat (Lasionycteris noctivagans) (Elmgren et  al., 2002; see Chapter 3b). The sixth edition of the Canadian Immunization Guide (National Advisory Committee on Immunization, 2002) begins a discussion on rabies with reference to the Quebec case and a caution that of the last five human deaths in Canada, four of those were caused by exposure to bats. While the fifth edition of the guide published in 1998 contained the same recommendations about submitting specimens, it was not prefaced by the caution about bats and human deaths. A similar reaction was noted in Quebec (see Chapter 11). The decline in submissions followed changes implemented in 2008 to Ontario’s administrative policy outlining the circumstances

opportunities for wildlife species with rabies. The relative distribution of cases in various species also shows the effect of habitat. Cases in skunks and livestock are more concentrated in the southern regions (Table 10.4). Cases in foxes are relatively more important in the north as factors of climate and habitat limit the populations of skunks, bats, and raccoons. It is interesting, however, that the proportions of cases in domestic animals (cat/dog) vary little between regions, suggesting that the pet vaccination efforts have had a similar effect across the province.

Incidence in Bats Rabies in bats was diagnosed for the first time in Ontario in 1961. Since then the number of cases per year has, despite fluctuations, increased, slowly peaking in 2003 and then declining (Figure 10.14). Over the past decade, incidence has averaged about 25 diagnosed cases per year. Most reported cases in bats occurred in southern Ontario while only four reported cases in northern Ontario. The pattern of annual incidence in bats is not correlated with incidence in any other species, and the factors affecting reported incidence

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Ontario

Figure 10.5: Diagnosed cases of rabies in Ontario in 1956. Source: created from CFIA data.

exhibits. Bats classified as Keen’s bat (Myotis keenii), a species typically found in British Columbia, should probably have been recorded as the northern long-eared bat (Myotis septentrionalis). Overall, the big brown bat (Eptesicus fuscus) and little brown bat (Myotis lucifugus) account for 79% of all submissions. Five percent of submissions proved positive with rabies. Despite the low numbers of submissions, the hoary bat (Lasiurus cinereus) and the silver-haired bat had the highest rates for positive tests (24% and 12.5%, respectively).

for handling bat rabies post-exposure prophylaxis (PEP). The new policy stated that “PEP is no longer indicated for the scenarios where people are sleeping unattended in a room where a bat was found, or a bat is discovered in close proximity to an individual who is cognitively impaired or near a young child. In the following recommendations PEP is only indicated where there is direct contact with a bat” (Public Health Ontario, 2009, p. 4). That change was based on research by De Serres and colleagues who found the risk from bats when no physical contact occurs is very low. The research was published in 2009 (De Serres et al., 2009). Quebec and British Columbia made similar decisions, and submissions from those provinces also declined (see Chapters 11 and 6). Note that submissions of companion animals (cats/dogs) continued to decline steadily despite the publicity surrounding the boy’s death (Figure 10.15). Eight species of bats have been reported in Ontario (Schneider & Pautler, 2018) Those species are marked with an asterisk in Table 10.5, which shows specimens submitted between 1985 and 2017. Although 15 species are shown, it is likely that four of those species (long-legged bat, pallid bat, fruit bat, and vampire bat) are exotics, probably from

Submissions in Other Species Submissions data became readily available with the arrival of the Canadian Food Inspection Agency’s (CFIA’s) digital laboratory information system in 1985. Submissions for all species for 1985 to 2017 are shown in Table 10.6. Given the system’s priority of protecting human life, it is no surprise that 32% of all submissions were dogs and cats, although only 3% of those submissions proved positive. Overall, of the 157,878 specimens submitted for diagnosis, 12.8% were positive for rabies.

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Figure 10.6: Diagnosed cases of ­rabies in Ontario in 1957. Source: created from CFIA data.

the St Lawrence River in southeastern Ontario in Leeds and Grenville County, and on Wolfe Island, an island in the St Lawrence River between Canada and the United States (Figure 10.16) (Rosatte et al., 2007a). Incidence increased rapidly but control efforts (see “Evolution of Wildlife Rabies Management in Ontario”) were very effective, and the last raccoon case occurred in 2005. Most of the cases (124 of 132) were confined to Leeds and Grenville County, and the small outbreak on Wolfe Island (six cases) was eliminated in 2000. Of the 132 cases of raccoon strain rabies, only two spilled over into other species, with two cases occurring in skunks. Ontario remained free of rabies in raccoons for almost eight years between 2007 and 2015. Then on 2 December 2015, animal control officers in Stoney Creek, a suburb of Hamilton, trapped a raccoon that was stumbling around. Tore Buchanan (personal communication, 19 October 2017), the coordinator of the Wildlife Research and Monitoring Section of the Ontario Ministry of Natural Resources and Forestry (OMNRF), described the events that followed. The raccoon was caged in their van and suspected of distemper since distemper had been widespread in the area

With the introduction of the Oravax control program, submissions have dropped steadily over the years. The only exception was 1997 as the impending invasion of the raccoon strain of virus from New York provided the impetus to submit more samples in an attempt to discover the first cases of that strain. Since then submissions for all species have continued to decline to approximately 2000 per year, approximately 21% of the total in 1985. In contrast, however, incidence in 2012 had declined to 1.5% of the total in 1985, a dramatic illustration of the effect of Ontario’s control programs but also a strong reminder that cost of surveillance (submissions and testing) continues well beyond the end of control programs. This effect has been noted by Nunan et al. (2002).

The Invasions of Raccoon Rabies By the late 1990s, the arctic fox strain of rabies in raccoons had run its course (Table 10.2), although a few cases continued to be diagnosed across the province. In 1999, however, the first cases of the long-awaited invasion of the raccoon strain from New York appeared along the north shore of

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Figure 10.7: Diagnosed cases of rabies in Ontario in 1958. Source: created from CFIA data.

end other cases were found 17 kilometres to the west and southwest. Given the wide distribution of these cases and the unexpected circumstances that led to the first diagnosis, it seemed likely rabies had been in the area for some time. Three factors probably influenced the delayed detection of rabies in the Hamilton area. First, by 2015, Ontario had not reported any rabies cases in raccoons for 10 years, so there was little expectation of other cases, especially since the trap-vaccinate- release (TVR) barrier (see “Trap-Vaccinate-Release (TVR)”) on the Canadian side of the Niagara River had been successful since 1995 against rabies incursions from northwestern New York. Second, canine distemper was widespread in the area and raccoons with this disease exhibit the unusual behaviours (disorientation, aimless wandering) often associated with rabies. Finally, analysis of whole-genome sequences derived from isolates of the raccoon rabies virus collected in Canada and adjacent US states demonstrated that (1) the strain of raccoon virus in the Hamilton area was distinct from isolates circulating in neighbouring northwestern New York, and (2) it was closely related to a strain from southeastern New York (Trewby et al., 2017). Thus, the outbreak in the

for the past year. Then they received a call to pick up two pit bulls that were roaming at large near a school. The dogs, Lexus and Mr Satan, were put in the van. Mr Satan ripped open the cage with the raccoon and fought with and killed it. Since the dogs were unvaccinated and, given the fight, the raccoon was submitted for rabies testing to CFIA. Two days later on the afternoon of Friday, 4 December, the test result came back positive for the raccoon strain of the virus. The dogs were subsequently vaccinated and quarantined. Because of the positive test, 16 raccoon and skunk specimens that had been previously collected by Animal Services for disposal were tested the following week using the direct rapid immunohistochemical test (dRIT); three were positive. By the end of 2015, 10 cases had been diagnosed. Incidence rose throughout 2016, reaching a maximum of 15 cases per month, with a total of 255 cases by the end of the year. Incidence decreased by 53% in 2017, with 119 cases by the end of the year. At the time of writing, incidence remained at lower levels (Figure 10.17). Within a week of the first diagnosed case, a case was found 26 kilometres south of the first case, and by month’s

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A History of Rabies Management in the Provinces and Territories

Figure 10.8: The spread of rabies into southern Ontario. The contours show the interpolated location of rabies in the last quarter of the year using the mid-point of townships as the data points. The clustered contours along the Frontenac Axis show the barrier effect of the Canadian Shield. The arrows show the general direction of spread. Source: created from CFIA data.

Hamilton area was most likely initiated by a raccoon transported over 500 kilometres from southeastern New York. If a raccoon from northwestern New York had simply crossed over the Niagara River, we would expect more cases in the area near the border and a spread from east to west in the Niagara region rather than west to east as was observed (Figure 10.18). The outbreak continued to spread both southwest and southeast in 2016 within a radius of 45 kilometres of the first diagnosed case. This rate of spread is similar to rates observed as the raccoon rabies virus spread through the northeast states in the United States (Moore, 1999). Spread slowed in 2017, extending only another 11 km beyond

the radius established by the end of 2016. The slowdown was most likely the result of the very extensive and aggressive control measures undertaken by OMNRF that are described in the section “Controlling the 2015–2017 Outbreak in the Hamilton Area.” A possible factor aiding the initial spread and subsequent slowdown may have been the weather. The Hamilton area in December 2015 was abnormally warm, with daily highs that reached up to 16°C. Furthermore, the Ontario Ministry of Transport’s winter severity index (Figure 10.19) indicates that the winter of 2015–2016 was mild, a favourable situation for the survival and movement of raccoons. The winter of 2016–2017 was severe and could have impacted the survival and

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Table 10.2 Rabies incidence in Ontario, 1953 to 2017. Year 1953 1954 1955 1956 1957 1958 1959 1960 1961 1962 1963 1964 1965 1966 1967 1968 1969 1970 1971 1972 1973 1974 1975 1976 1977 1978 1979 1980 1981 1982 1983 1984 1985 1986 1987 1988 1989 1990 1991 1992 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012 2013

Total 2 2 103 142 325 2,493 638 227 862 790 870 1,148 1,021 1,002 1,048 1,730 1,719 1,187 1,777 1,480 1,318 1,229 1,722 1,273 1,162 1,357 1,407 1,416 1,557 2,107 1,860 1,382 1,984 3,273 2,007 1,832 1,905 1,634 1,238 1,305 1,254 611 328 158 97 81 100 187 212 202 126 106 96 82 106 79 49 39 26 29 28

Fox

Skunk

Livestock

Dog/Cat

Bat

0 2 68 100 270 1,236 226 103 448 329 329 471 389 453 464 868 782 446 858 558 469 497 872 674 565 757 678 476 611 1,030 735 689 990 1,648 929 937 909 836 584 721 701 254 126 34 16 5 12 32 26 41 6 3 3 2 0 2 3 0 0 0 0

0 0 0 0 3 110 122 36 77 127 194 204 188 145 199 219 283 277 288 310 268 213 200 149 152 195 315 552 516 531 647 322 446 721 518 448 516 316 325 227 194 142 100 72 39 33 46 58 58 46 22 24 17 23 30 25 8 10 1 1 0

0 0 18 12 28 947 210 56 206 204 247 279 273 265 256 400 383 309 388 411 387 340 447 283 285 258 236 213 271 308 260 193 333 488 312 244 252 276 173 194 194 111 65 22 11 8 14 13 18 8 7 16 11 12 11 9 9 0 1 0 0

2 0 16 26 20 188 70 29 120 113 97 180 155 121 109 210 219 137 190 166 161 143 154 149 135 115 132 118 129 178 150 102 144 281 169 148 153 142 79 104 114 68 19 5 4 3 1 8 6 10

0 0 0 0 0 0 0 0 1 4 2 5 8 7 6 8 15 8 16 11 19 18 16 9 16 14 23 30 19 22 47 51 35 45 36 22 32 25 44 21 24 16 16 24 27 31 18 34 57 73 74 56 61 42 62 38 29 29 24 25 27

2 2 2 2 5 0 0 0 2 1

Raccoon 0 0 0 2 2 7 7 0 3 5 0 3 5 6 9 13 10 4 22 17 5 6 11 3 3 4 5 12 2 16 8 12 19 32 20 14 14 17 9 16 7 6 1 0 0 1 9 40 43 22 16 5 2 1 0 0 0 0 0 0 0

Wildlife 0 0 0 1 2 2 3 2 6 8 1 4 2 5 3 8 21 2 11 6 4 11 16 5 3 14 13 10 7 19 8 7 12 45 17 10 25 15 22 19 17 14 1 0 0 0 0 1 3 2 1 0 0 0 0 0 0 0 0 0 0

Other 0 0 1 1 0 3 0 1 1 0 0 2 1 0 2 4 6 4 4 1 5 1 6 1 3 0 5 5 2 3 5 6 5 13 6 9 4 7 2 3 3 0 0 1 0 0 0 1 1 0 0 0 0 0 1 0 0 0 0 1 0 (Continued)

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A History of Rabies Management in the Provinces and Territories

Year 2014 2015 2016 2017 Total % Total

Total

Fox

Skunk

Livestock

Dog/Cat

Bat

Raccoon

Wildlife

Other

18 24 288 149

0 0 1 1

0 0 84 37

0 1 1 4

0 0 1 1

18 13 29 20

0 10 171 86

0 0 0 0

0 0 1 0

56,009

25,275

11,429

11,191

5,310

1,502

763

408

131

45.1

20.4

20.0

9.5

2.7

1.4

0.7

0.2

Source: compiled from CFIA data.

Figure 10.9: Diagnosed cases of rabies in Ontario in 1968. Source: created from CFIA data.

movement of raccoons and, therefore, the progress of the epizootic in 2017. Another aspect of the epizootic was the high spillover into the skunk population in 2016–2017. In contrast, of the 132 cases of rabies the 1999–2005 raccoon strain invasion into eastern Ontario, only two were in skunks. Eastern ­Ontario was primarily rural, while the spatial distribution of cases in skunks (Figure 10.20) shows that skunk cases were concentrated in clusters in the suburbs surrounding the old city of Hamilton. A predominant feature of the landscape that appears to affect the distribution of rabies cases in skunks is the Niagara escarpment, as shown in Figure 10.20. The

escarpment rises 90–100 metres shaping drainage patterns in the area and providing cover and resources for wildlife along its slopes and the valleys it creates. Cases in skunks were clustered in the valleys east and west of the older part of Hamilton and in the suburban areas on top of the escarpment. The spillover into skunks is a concern since results from previous baiting campaigns show that skunks are harder to vaccinate than other species. Vaccinating skunks has been shown to require closer distribution of baits and higher densities of baits, which increase the cost of control. As well, the incubation period in skunks can be months rather than weeks (Charlton, 1997) a factor that could allow the

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Ontario

Figure 10.10: Diagnosed cases of rabies in Ontario in 1978. Source: created from CFIA data.

and the inoculation of live animals. Rabies was made a reportable disease in 1905 under the Animal Contagious Diseases Act, 1903 of the Department of Agriculture (see Chapter 4). By 1926 reporting of rabies cases was mandated, and rabies was reported from different areas of Canada (see Chapter 2). In 1947, the first cases of wildlife rabies were diagnosed (Plummer, 1954) in the Northwest Territories. Vaccination of domestic animals against rabies was started in 1952 with the advent of a vaccine for dogs and its use in the northern outbreak. Rabies management at this time focused on vaccinating domestic pets, post-exposure treatment in humans, and public education in the hope that the disease would run its course. Up to 1950 the actions of the Department of Agriculture towards rabies management had focused on domestic animals: reporting of rabies cases, diagnosis through submission of specimens at the federal laboratories, quarantines, vaccination of pets, and public awareness through reports and brochures (see Chapters 31 and 33). Treatment of humans in Ontario with contact to rabid animals is discussed in Chapter 32.

skunk population to become a reservoir for the raccoon strain of rabies. A striking feature of the distribution of cases in skunks and raccoons was the limited spread into the southwest tip of Halton region (the city of Burlington). Because of the escarpment, the major expressways in this area squeeze into the narrow corridor adjacent to the shoreline of Lake Ontario – a factor used to advantage by the control efforts in that area (“Controlling the 2015–2017 Outbreak in the Hamilton Area”).

Rabies Management in Ontario Early Management Efforts Rabies management before 1900 was aimed at dog control efforts, elimination of strays, muzzling and fines, education, and treatment of humans in New York. After 1900 diagnosis of rabies became a reality through the demonstration of Negri bodies by staining (see Chapter 20)

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A History of Rabies Management in the Provinces and Territories

Figure 10.11: Oravax baiting in Ontario, 1989 to 2012. The numbers show the rabies units. The thick lines superimposed on rabies units show the baiting areas by time period – for example, units 1 and 2 (eastern baiting area) were baited between 1989 and 1995. Units 3 and 4 (the central baiting area) were baited between 1994 and 2003. In both cases the western boundaries of the baiting areas were baited first and then the rest of the area was baited. The rabies units (7, 8, 9, 10, and 11) in the southwestern baiting area were treated between 1996 and 2012. Rabies lingered in those areas as the physiographic boundaries between units were not as distinct as those between the central and eastern baiting areas. The baiting area within the southwest was reduced as incidence declined. Units 5, 12, and 13 were never baited as incidence in those areas had always been sporadic and linked to incidence in the main areas. Hence, as rabies was controlled in the main areas, there was no need to bait the outlying areas. Some townships between the borders of adjacent units could not be assigned to a specific unit. Those townships were termed transition units and are shown as shaded areas in this figure. These areas were treated as they represented the areas through which rabies could spread between adjacent units. Note that an entirely separate control operation took place for raccoons in 1999–2002. The approximate area of the combined control program for raccoons is shown as a dark rectangle in unit 2. Source: created from CFIA data.

From 1954 to 1961 Dr Audrey Fyvie, a veterinarian with the Department of Lands and Forests (subsequently the name changed to the Ontario Ministry of Natural Resources, OMNR, and as of 2014 the Ontario Ministry of Natural Resources and Forestry, OMNRF) recorded and reported the progress in wildlife rabies in the province. Like Plummer in 1954 (see Chapter 18), Fyvie began thinking about controlling rabies in wildlife and, in 1962, hired a young biologist, David Johnston, to track this outbreak and

Evolution of Wildlife Rabies Management in Ontario THE EARLY YEARS: 1954–1979

As rabies pushed south and spread across southern Ontario, a growing number of agencies and individuals took up the challenge of controlling wildlife rabies. From 1954 to 1979 Ontario established the groundwork for research and inter-agency co-operation that led to the province’s very successful wildlife control programs that began in 1989.

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Ontario

Figure 10.12: Rabies incidence in Ontario for the main species involved (99% of all cases), 1953 to 2017. Source: created from CFIA data.

Figure 10.13: Wildlife rabies incidence in Ontario, 1998 to 2017. Source: created from CFIA data.

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A History of Rabies Management in the Provinces and Territories

a cabinet submission in 1979, with the cabinet approving $1.3 million for five years (Davies, 2003). At this time, the role of the IMCR ended and the Rabies Advisory Committee (RAC) was born with a mandate to ­advise OMNR on a means of immunizing wildlife, particularly foxes in Ontario against the arctic fox strain of rabies. Its purpose was twofold: to provide a liaison between provincial and federal agencies concerned with and involved in rabies control and to bring together experts from all fields of rabies knowledge to develop a complete control program, and the committee continues that work to this day. The first chairman of RAC, appointed in 1979, was Dr Andrew, J. Rhodes, director of the Public Health Laboratories, Ontario Ministry of Health. Members included Dr Duncan Sinclair (veterinary medicine, physiology, dean of Arts and Science, Queen’s University), Dr Klaus Nielsen (immunology, Agriculture Canada-ADRI, now CFIA-OLF), Dr Leslie Spence (virology, University of Toronto), Dr Steven Smith (ecology, University of Waterloo), Dr Ken McDiarmid (veterinarian, Ministry of Agriculture and Food), Dr David Gregory (chief of zoonoses, Agriculture Canada), and Dr Donald Barnum (Ontario Veterinary College, University of Guelph). Over the next 30-plus years, working in conjunction with the Rabies Research and Development Unit (RRDU) in OMNR, RAC oversaw contracts to researchers in various Canadian universities, research companies, and other agencies, as shown below, and whose contributions are documented in this chapter, elsewhere in this book, or cited in the literature:

Table 10.3  The regional distribution of rabies cases in Ontario, 1926 to 2017. Region

Cases

Area in km2

Southwest Central Southeast North

23,969 17,219 13,599 1,526

37,920 39,272 37,933 793,482

Cases/ 100 km2

Population

Cases/ 1000

63.2 43.8 35.9 0.2

2,917,993 7,247,711 1,773,301 733,016

8.2 2.4 7.7 2.1

Note: “North” combines the data for the Hudson Bay and James Bay lowlands with the northern Canadian Shield. The remaining regions in this table are described in the introduction to this chapter. The population column was derived from 2011 census data. Source: compiled from Statistics Canada and CFIA data. Table 10.4 Regional distribution of incidence by species (%) in Ontario, 1926 to 2017. Species

Southwest

Central

Southeast

North

Fox Skunk Livestock Cat/Dog Bat Raccoon Wildlife Other

40.9 21.7 22.6 10.5 2.4 1.4 0.3 0.2

42.6 22.5 19.4 10.0 3.1 0.9 1.1 0.3

52.0 16.4 16.8 9.1 2.8 1.9 0.8 0.1

65.1 6.9 14.8 8.5 1.2 0.3 2.4 0.7

Source: compiled from CFIA data.

explore control measures (D. Johnston, personal communication, October 2011). Vaccination appeared to be the best option, an opinion supported by the World Health Organization Expert Committee in 1966. In 1967 a four-yearold girl died of rabies near Ottawa, Ontario, after being bitten by a rabid cat. The resulting publicity stimulated the Ontario legislature to allocate funds towards the control of rabies (Davies, 2003). An Inter-Departmental Committee (IDC) was formed in 1968, comprising the Departments of Health, Agriculture, and Lands and Forests. The IDC was later renamed the Inter-Ministerial Committee on Rabies (IMCR) when departments were reorganized as ministries. Its mandate was to develop an oral vaccine to immunize wildlife. In the same year the Ontario Department of Health provided a five-year grant to Connaught Laboratories to develop an oral vaccine for wildlife, and the Ontario Department of Lands and Forests raised $175,000 to develop baits and conduct studies on fox and skunk biology and movements (Davies, 2003). Although the Ontario Ministry of Health did not renew the grant to Connaught Laboratories, funding for rabies research was sought through

• vaccine and bait development: Connaught Laboratories (Lawson); Inoform Limited; Langford Laboratories; American Cyanamid and its subsidiary, Ayerst Canada; Animal Disease Research Institute (ADRI, Wandeler); University of Toronto (Campbell); McMaster University (Previc, Graham); Microbix Limited; Artemis Technologies (Beresford, Beath) • animal biology: University of Western Ontario (Fenton) • virus typing: ADRI (Nadin-Davis, Wandeler), University of Toronto (Campbell, Barton) • spatial analysis and simulation: Queen’s University GIS Lab (Tinline, Pond, Rees, Ball, Honig) • aerial delivery systems: Infoform Limited (Mancini), Redford Robotics (Smith), OES Inc. and Queen’s GIS Lab (Ball, Tinline, Fielding) • aviation services: Ontario Provincial Air Services (Ayers) Early in this process, key administrators in OMNR, together with members of RAC, understood the need to involve

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Figure 10.14: Diagnosed cases of rabies in bats in Ontario, 1961 to 2017. Source: created from CFIA data.

Figure 10.15: Annual submissions for dogs/cats and bats in Ontario, 1985 to 2017. Source: created from CFIA data.

government, academia, and industry. As Dr Sinclair said early in his tenure on RAC, “If this effort succeeds it will be an excellent example of co-operation at a level seldom seen in Canada” (personal communication, October 1980).

Bait drops were then conducted in Huron County during 1975 to 1977, with baits thrown by hand from a low-flying Cessna 172 aircraft (see Chapter 19). Early in 1980 RAC realized that an inactivated virus would not work as an oral vaccine for wildlife. Experiments by Connaught Laboratories found that sponge baits containing a vaccine derived from low-titre attenuated Evelyn-Rokitnicki-Abelseth (ERA) rabies virus and covered with tallow produced rabies-virus-neutralizing antibodies in foxes. An aerial trial with 13,900 of these baits revealed two weaknesses: the titre had to be higher and the bait more impact resistant. This led to the production of a higher titre ERA vaccine and the

1980–1989: VACCINE, BAIT, AND DELIVERY

The period 1980 to 1989 was one of intense activity aimed at developing a vaccine, developing a bait, and devising a bait delivery system. These activities are fully covered in Chapters 17 and 19. In sum, following several small-scale trials with baits distributed by hand, OMNR determined that distribution on a large scale would have to be done by aircraft.

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A History of Rabies Management in the Provinces and Territories

Table 10.5 Bat submissions in Ontario, 1985 to 2017. Species BBB LBB NLB KEB SHB HRB REB LNB EPB LLB PLB FAB VPB ESB EVB BAT

* * * * * * *

*

Common Name

Scientific Name

Total

Negative

Positive

Big brown bat Little brown bat Northern long-eared bat Keen’s bat Silver-haired bat Hoary bat Red bat Leaf-nosed bat Eastern pipistrelle Long-legged bat Pallid bat Fruit bat (Africa/Asia) Vampire bat Eastern small-footed bat Evening bat Unspecified

Eptesicus fuscus Myotis lucifugus Myotis septentrionalis Myotis keenii Lasionycteris noctivagans Lasiurus cinereus Lasiurus borealis) Phyllostomidae Perimyotis subflavus Myotis volans Antrozous pallidus

23,261 2,694 163 118 144 102 80 15 6 3 2 2 1 0 0 193

21,776 2,633 161 116 126 78 66 15 5 3 2 2 1 0 0 160

1,224 43 2 2 18 24 8 0 1 0 0 0 0 0 0 15

86.8 10.1 0.6 0.4 0.5 0.4 0.3 0.1 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.7

26,784

25,144

1,337

100.0

Live

Skunk

Wild

Myotis leibii Nycticeius humeralis

Totals

% Total

Source: compiled from CFIA data. Table 10.6 Submission of specimens by species to CFIA, 1985 to 2017. Year

Total

Dom

Rac

Bat

1985 1986 1987 1988 1989 1990 1991 1992 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012 2013 2014 2015 2016 2017

9,529 11,790 8,782 8,154 8,499 7,744 6,947 6,593 7,105 5,355 4,642 4,044 7,494 4,934 4,109 4,195 4,918 4,534 4,060 3,469 3,823 3,969 3,611 3,810 2,630 1,958 1,910 1,995 1,885 902 1,124 1,745 1,619

2,589 3,425 2,576 2,568 2,655 2,444 2,217 2,151 2,379 2,023 1,702 1,643 1,502 1,406 1,264 1,323 1,294 1,267 1,238 1,321 1,151 1,089 1,111 1,331 1,138 944 913 876 927 361 537 634 671

1,186 1,021 746 727 867 855 901 676 810 767 882 695 3,485 553 1,088 994 1,133 839 689 398 664 721 282 332 263 159 165 214 170 51 145 419 288

709 653 590 473 475 414 487 350 455 318 295 238 329 506 488 533 1180 1,327 1,262 1,048 1,254 1,326 1,644 1,506 786 508 515 620 535 390 331 447 462

1,285 1,965 1,154 1,169 1,184 1,140 868 1,066 1,055 563 433 398 1,246 1,624 377 343 291 249 139 98 226 219 84 84 51 35 30 26 20 6 6 8 3

1,498 1,645 1,446 1246 1266 1,107 929 837 947 590 474 386 371 373 339 354 342 270 237 200 169 183 181 192 127 115 80 95 105 33 46 61 55

1,174 1,596 1,237 1,053 1,092 1,035 810 852 831 582 453 327 262 210 196 231 275 299 245 189 163 175 167 219 172 131 164 133 90 49 49 70 83

1,048 1,398 983 863 894 691 664 585 571 452 351 325 265 223 302 358 370 245 215 185 182 228 131 132 86 58 35 25 31 11 6 105 55

40 87 50 55 66 58 71 76 57 60 52 32 34 39 55 59 33 38 35 30 14 28 11 14 7 8 8 6 7 1 4 1 2

157,878

50,670 32.1

23,185 14.7

22,454 14.2

17,445 11.0

16,299 10.3

14,614 9.3

12,073 7.6

1,138 0.7

Total % Total

Fox

Dom = dog/cat, Rac = raccoon, Liv = livestock; Wild = wildlife. Source: compiled from CFIA data.

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Other

Ontario

Figure 10.16: Raccoon rabies cases in Ontario, 1999 to 2005.

The raccoon strain virus was responsible for the six cases on Wolfe Island (part of Frontenac County) and the 126 cases in Leeds and Grenville County. Because the mapping is by county the entire land area of Frontenac County (west of Leeds and Grenville) is shown, but cases were only on Wolfe Island. Cases in other counties were strains other than raccoon strain. The arrows show the invasion route from the United States. Source: created from CFIA data.

development of the blister-pack bait. Derek Mancini and Paul Johansen of Inoform Ltd, in cooperation with Connaught Laboratories, developed the machinery and procedures to mass produce the blister-pack bait referred to as the Ontario blister pack by 1989. The bait drops using the Cessna aircraft worked but illustrated that for large-scale control operations, the aircraft had too small a payload. Precise delivery and navigation were also a problem. The switch to using Twin Otters with a much larger payload, the development of a bait machine used inside the aircraft to control bait delivery, and the development of improved navigation systems are documented in Chapter 19.

This period also saw two other developments. First, in areas where air drops were not feasible, control methods were supplemented by hand placing ERA baits on the ground, such as throughout metropolitan Toronto to control fox rabies. Some 112,700 baits were placed and a further 188,100 baits in 1994 to 1998 were placed throughout the Greater Toronto Area (Davies, 2003). Second, tetracycline HCL was chosen as a biomarker for monitoring bait acceptance in 1973. The use of this biomarker in Ontario is described in Chapter 24b. Before the massive control programs began in 1989, careful testing was done to ensure that any tetracycline entering the food

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A History of Rabies Management in the Provinces and Territories

Figure 10.17: Diagnosed rabies cases in raccoons and skunks, 2015 to 2017. Source: created from CFIA data.

Figure 10.18: Raccoon rabies cases in the Hamilton area, 2015 to 2017. Source: created from CFIA data.

chain, should livestock accidentally ingest baits, was below acceptable standards (Black et al., 1985).

a sufficient dose to reliably produce sufficient rabies-neutralizing antibodies in large numbers of these animals. A trap-vaccinate-release (TVR) method was employed on these two species, which involved the live-capture of skunks and raccoons and vaccination with an injectable inactivated vaccine called Imrab (Rosatte et al., 1992). Typically, TVR programs were employed from July to October

TRAP-VACCINATE-RELEASE (TVR)

Unfortunately the ERA bait was not as effective in raccoons and skunks as in foxes. The problem was a combination of bait design and bait pickup, which did not result in 144

Ontario

Figure 10.19: Winter severity index for the Hamilton Niagara Region. The index is on a scale from 0 to100 and represents of combination of different weather factors (e.g., snowfall, temperature, freezing rain, rain, and amount of blowing snow). Source: Ministry of Transportation Ontario.

Figure 10.20: Rabies cases in skunks in the Hamilton area, 2016 to 2017. Source: created from CFIA data.

when capture success was good, and young animals were old enough to respond to vaccination. TVR continued to be used to control rabies in wildlife in rural and urban areas, especially targeting raccoons and skunks (Rosatte et al., 1992; Rosatte et al., 2009; Sobey et al., 2010). For example, raccoons and skunks were vaccinated using TVR from 1987 to 1995 in a portion of metropolitan Toronto

(Scarborough) (Rosatte et al., 1992). During those years, 5458 raccoons and 1663 skunks were captured (using 180,534 trap-nights), vaccinated, and released in Scarborough. OMNR initiated another TVR program in 1994 in Niagara Falls, Ontario. The objective of this proactive program was to vaccinate a sufficient number of raccoons in a 680 km2 145

A History of Rabies Management in the Provinces and Territories

area of the Niagara frontier to prevent raccoon rabies from spreading should a case appear. At that time, raccoon rabies was close to Niagara in nearby New York State – just across the river from the TVR area. From 1994 to 2007, 64,778 raccoons and 3532 skunks were captured and vaccinated using 742,289 trap-nights (Rosatte et al., 2009). That represented, on average, 54% to 78% of the raccoon population. To date, the Niagara Falls, Ontario, area has been free of raccoon rabies despite cases in adjacent New York State. Another proactive TVR program was initiated along the St Lawrence River in 1995 as it was anticipated that raccoon rabies would likely enter Ontario via rabid raccoons crossing the river from New York State. From 1995 to 2007, 31,843 raccoons and 4435 skunks were captured and vaccinated with Imrab along the St Lawrence River. About 43% to 83% (mean) of the raccoon population was vaccinated (Rosatte et al., 2007b). At the time of writing the TVR program along the St Lawrence River has been replaced by Ontario’s oral rabies vaccination aerial baiting program (ORV) described in the following sections.

to insert the rabies G-protein into human adenovirus type 5, which when administered to mice, produced high rabies antibody titre. Several alterations to this adenovirus construct produced a construct termed HAdRG1.3, which became the master seed of choice. In 1994 Microbix Ltd signed a licensing agreement with McMaster University, which gave the firm primary rights to produce the adenovirus recombinants developed at the university. RAC granted Microbix $100,000 to develop master seeds of HAdRG1.3. By 1998, however, Microbix expressed lack of interest in future development of HAdRG1.3, and it was transferred to Artemis Technologies Ltd for production in 1999 (see Chapter 17c). Their work resulted in ONRAB in 2008, and this is the vaccine of choice in current rabies management in Canada. While the development of the human adenovirus construct proceeded, OMNR received permission to use the American bait with vaccinia-rabies glycoprotein recombinant vaccine (V-RG) in Ontario, and during 1999 and 2003, 2.8 million baits were distributed. During 1985–1986 experiments to develop a bait that could be mass produced led to the tallow-covered blister-pack bait, the Ontario bait (OB). This had a chicken flavour as an attractant mixed with a tallow-microbond wax matrix. During 1989 in southwestern Ontario, 389,886 of these baits were dropped. Then, 1993 to 1996 saw extensive testing of multiple bait types, vaccine containers, and attractants leading to the Ontario slim bait for use in raccoons. A vanilla-icing sugar attractant was added that was effective for foxes and raccoons. It had a single label and a green colour to camouflage it from birds and humans. By 1999 this bait was in full use in Ontario (Davies, 2003). After many years of bait development research (­Bachmann et  al., 1990; Rosatte & Lawson, 2001; Rosatte et al., 2007c), a bait matrix and vaccine container was developed that was palatable to foxes, skunks, and raccoons. In addition, the recombinant vaccine called ONRAB had been developed and proven to be effective, stable, and safe in laboratory experiments (Knowles et  al., 2009a, 2009b; ­Lutz-Wallace et al., 1995; Prevec et al., 1990; Yarosh et al., 1996) in these species. During 2006 ONRAB baits were used in an experiment in southwestern Ontario. These baits proved to be very effective in free-ranging raccoons, with vaccine efficacy values ranging from 79% to 90% for bait densities of 75 to 400/km2 (Rosatte et  al., 2009). Results were promising in skunks but experiments were required to refine bait density and flight-line spacing to optimize vaccine efficacy in that species (Rosatte et  al., 2011). Efficacy and challenge

1990–PRESENT: VACCINE, BAIT, AND DELIVERY

In 1990 Connaught Laboratories discontinued its involvement in bait and vaccine production for OMNR. Its contract was transferred to Guelph-based Langford Laboratories. Langford sold out to American Cyanamid Ltd in 1991, which, in turn was taken over by American Home Products Inc (AHP) in 1994. A Canadian affiliate of AHP, Ayerst Canada, continued rabies vaccine and bait production. By 1997 Ayerst withdrew from its contract with OMNRF. Artemis Technologies Inc was awarded the new contract by OMNRF; built new facilities in Guelph, Ontario; and has continued vaccine production and bait manufacture since then (Davies, 2003; see Chapter 17c). While baits with ERA vaccine was used in numerous aerial and hand-baiting exercises during 1988 to 1993, experiments continued to find a vaccine and bait for use against rabies collectively in skunks, foxes, and raccoons, as well as improvements to their aerial delivery. Isolation of the gene for rabies G-protein had been accomplished and patented by Wistar Institute, Philadelphia, in 1978. A licence was obtained by Natural Sciences and Engineering Research Council to use the gene in Canada, and Connaught Laboratories received the gene. First attempts by Dr James at Connaught to insert this gene into Escherichia coli were unsuccessful, as were attempts by Dr Campbell at the University of Toronto to insert the gene into canine adenovirus. Dr Campbell took the problem to Drs Prevec and Graham at McMaster University (see Chapter 17a). They managed

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experiments on raccoons, skunks, and red foxes that were offered ONRAB baits in captivity were also carried out during the late 2000s.

In addition to population reduction and TVR, 3.6  million V-RG rabies vaccine baits were distributed over a 4000 to 9000 km2 area in eastern Ontario as part of the control program for raccoon rabies from 1999 to 2006 (Rosatte et  al., 2008). These combined operations succeeded in eliminating the raccoon variant of rabies from Ontario, with the last case being reported in September 2005 (Rosatte et al., 2009). The successful control program resulted in estimated savings to Ontario of $8  million to $12 million annually (Rosatte, 2011). Ontario has remained vigilant as the disease remains enzootic in northern New York State. In addition to the threat of dispersing infected animals from New York, human assisted movements of raccoons from the United States and Quebec into Ontario have been well documented (Cullingham et al., 2008; Rosatte et al., 2007d; Rosatte et al., 2010). Ontario continues to have a contingency plan for rapid response to any future outbreak. Like the original plan that was implemented so effectively to eliminate the 1999 invasion (Rosatte et al., 1997), the current plan includes keeping a supply of ONRAB baits in cold storage, having the necessary funding for a control program, and maintaining a roster of trappers, biologists, and so on, to implement control (D. Donovan, personal communication, October 2012).

POINT INFECTION CONTROL (PIC)

Point infection control (PIC) is a method developed by OMNRF to control or eliminate a point source infection of disease (i.e., a rabies case or cases). PIC typically employs a combination of different tactics, including population reduction and parenteral vaccination of vectors or oral rabies vaccination with baits. While the objective of population reduction is to remove incubating or clinical animals from the point source area, parenteral and baiting oral rabies vaccination (ORV) zones are actually buffer zones of vaccinated animals in case incubating or clinical animals are missed during the population reduction phase and disperse out of the zone. When just population reduction and TVR were used during a PIC, it was practical to limit the area of control to under 2000 km2. This reflects the complicated logistics, cost, and time involved in trapping animals over large areas. For example, during 2003, it took nine trappers about four months (early July to early November) to TVR an area of 680 km2 in Niagara Falls, Ontario. Each trapper had a truck, 100 live traps, and equipment, and trapped for five days/four nights each week. The cost of the program (not including the price of traps) was about $300/km2 – the cost was related to the amount of trapping effort employed and desired level of vaccination (e.g., 60% vs 70% of the population vaccinated) (Rosatte et al., 2009). Raccoon rabies was first reported in a raccoon in Canada in eastern Ontario during July 1999 (Wandeler & Salsberg, 1999). Although a proactive TVR program had been in place in a 720 km2 area along the St Lawrence River during 1998, the case was unfortunately located about 40 kilometres east of the TVR area, just north of Prescott, Ontario (Rosatte et al., 2001). A point infection control program, using population reduction, TVR, and ORV with V-RG baits was initiated within 24 hours of the first case being diagnosed, as directed by the contingency plan that had been in place since the mid-1990s (Rosatte et al., 1997; Rosatte et al., 2001). In total, 8311 raccoons and 1449 skunks were euthanized, and 20,129 raccoons and 2735 skunks vaccinated using TVR, during 17 PIC operations in eastern ­Ontario between 1999 and 2005 (Rosatte et al., 2009). During some of the PIC operations, only TVR was used to contain single cases of raccoon rabies. TVR and population reduction costs varied between $300/km2 and $500/km2, depending on the level of trapping effort (Rosatte et al., 2009).

FIELD BIOLOGY

OMNRF had a wide ranging field biology program in addition to its vaccine and bait development programs. Initially the focus of this program was to better understand the biology of the vectors involved so that this information could inform future control programs. That work produced data on animal reproduction, mortality, animal interactions, habitat use, and seasonal movements, all of which became necessary input for the modelling efforts described in the next section. Ontario became a pioneer in the development of radio tracking equipment (Voigt & Lotimer, 1981) and data analysis (Voigt & Tinline, 1980) in attempting to understand red fox movement, behaviour, and the use of habitat. Indeed, the development of radio collars led to a spinoff private company (Lotek), whose wildlife and fish monitoring systems are used in over 100 countries. Recent versions of this equipment have been used to study raccoon movements (Totton et al., 2004). Field studies also attempted to understand animal contact behaviour (Totten et al., 2002), but this was limited by the logistics and great cost of such an exercise. Field work also concentrated on bait design, placement, dispersion, and uptake studies. Work on bait design and attractants is discussed in Chapter 17, and work on bait

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dispersion and placement is described in Chapter 19. What distinguished Ontario’s effort from all other jurisdictions in North America was the coordinated effort to identify and understand the many factors contributing to a successful control program – an approach that achieved demonstrable success.

immunity was achieved when the immunity levels in the population were 70% or greater. The challenge, however, was that early field experiments with air dropped vaccine baits (see Chapter 19) showed that achieved immunity levels in test populations did not exceed 50%. The question then became: under what circumstances would 50% immunity levels control rabies? Experiments with the OFM showed that, given the observed behavioural characteristics of fox populations in Ontario, rabies would not persist in populations with densities less than two animals per square kilometre. Given this density threshold, model experiments also showed that control could be achieved if baiting was done after rabies had peaked in any area. In effect, the combination of population reduction as a result of the disease, coupled with a 50% reduction in susceptibility in the remaining population from vaccination, de facto achieved herd immunity. The caveat, in those circumstances, was that the vaccination program would have to be continued for five years before rabies could be eliminated from the population. Other experiments on the spread of rabies in populations with no vaccination demonstrated that given the animal densities and movement patterns observed in Ontario, rabies rapidly died out in isolated areas that were less than 3000 to 5000 km2. As the next section indicates, these findings were important considerations in implementing Ontario’s first full-scale trial of aerial baiting in eastern Ontario and one factor that explained why the fox strain of rabies died out in Quebec (see Chapter 11).

SIMULATION MODELLING

Ontario has also used simulation modelling as a planning tool in organizing its Oravax campaign to eliminate the enzootic fox rabies in southern Ontario. Initial simulation efforts began in 1977 when Glenn Grant, a post-graduate student at Queen’s University working under the supervision of Rowland Tinline (Queen’s) developed, at the request of David Johnston (OMNRF), a simulation model of a fox population with rabies (Grant, 1977). Subsequent work by researchers at Queen’s University and OMNR produced the Ontario fox model (OFM) that allowed users to experiment with both vaccination and population reduction control methods (Tinline et  al., 1985). Four key features of that model distinguished it from previously reported modelling work looking at rabies control, such as Anderson (1981) and Coyne (1989). First, the model was spatial, recognizing that animal movements and animal densities varied across space and that those variations would have a significant impact on the spread of rabies in an animal population. Second, the model was individual in the sense that each animal in the population was treated separately in terms of its life events: birth, death, movement, and interaction with other animals (although reproductive behaviour was not explicitly modelled). Third, the model was stochastic so that individual behaviour over time was determined from probability distributions representing births, gender, mortality, movement, etc. Although the outcomes of simulation experiments with stochastic models are necessarily variable, the variance in output allows researchers to better understand the sensitivity of outcomes resulting from a given set of animal behaviour or control decisions on mortality and vaccination. Finally, the details of animal behaviour that resulted in the probability distributions were based on the results of the extensive field biology efforts outlined in the chapters in Part 6 of this book. Using behavioural data from the area under investigation rather than estimating model parameters from data culled from studies in many different areas was an important consideration in validating the model and increasing confidence that the results could be used to evaluate control programs. Initial results from the modelling work on spatially homogeneous test populations demonstrated that herd

IMPLEMENTING THE ORAVAX CONTROL PROGRAM

In 1988, the rabies control program in Ontario was at a crossroads. Years of study had developed methods with great promise, but there was no commitment to full scale testing and implementation. Steve Smith, the new chair of RAC, promised Lyn Macleod, the minister of Natural Resources, that in return for stable funding, the province would move immediately to implement control. Smith further promised the minister that “if RAC had not made significant progress within one year towards a field program to suppress rabies in Ontario I would return to her office and recommend that RAC and the rabies program be terminated immediately” (S. Smith, personal communication, 4 April 2011). The province’s subsequent commitment to funding and Smith’s resolve mobilized RAC and OMNR. The date for a full-scale field trial was set for the fall of 1989. Contracts were set for the production of the bait delivery machinery (see Chapter 17); bait production was

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begun (see Chapter 19); OMNR and Aviation Services (see Chapter 19) arranged to use Twin Otters as the delivery aircraft and secured the approvals to modify the aircraft for the bait machine (see Chapter 19); and OMNRF began to organize the logistics for the field trial. The remaining concern was where to begin. Eastern Ontario (as defined by a north south line along the western side of Lennox and Addington County extending north to the Ottawa River) was chosen for several reasons. First, work by Tinline (1988) had shown that eastern Ontario was a self-contained rabies unit, with the Canadian Shield acting as a barrier to the west and north and the Ottawa River and St Lawrence River as barriers to the east and south. Furthermore, this unit had a very regular three- to four-year cycle (Figure 10.21) and rabies incidence was dominated by foxes (Table 10.2), the species that had been most responsive to uptake of the baits and subsequent seroconversion for immunity. Second, incidence along the periphery of this unit had already peaked by 1988, so the animal population was lower, and although the core was peaking at that time, it would be declining in 1989–1990. This meant baiting would take place over a less dense population. Therefore, as the simulation experiments had shown, this would mean the vaccination efforts would be more effective. Finally, despite a massive effort to produce baits, only about 390,000 baits would be available to cover an experimental area of almost 30,000 km2. Hence, at a projected drop density of 20 baits per square kilometre, this meant only two-thirds of the chosen area could be baited. Given that the eastern Ontario rabies unit had well-defined physical boundaries, baiting in 1989 was targeted at the outer boundaries of the eastern Ontario unit, leaving rabies to die out within these boundaries. Baiting over the entire unit was continued for another five years. As predicted, the impact was immediate and rabies in foxes disappeared by 1995 (Figure 10.21). The strategy of complementing physical barriers with vaccination barriers was continued over the next several years as the control program moved west to concentrate on rabies units in central Ontario and then southwestern Ontario. As noted in Chapter 19, flight-line spacing, baiting density, and type of bait were changed, especially in southwestern Ontario, as the program evolved to target skunks and raccoons during the 1999–2002 raccoon rabies invasion in eastern Ontario.

have contained the outbreak and that it should end within a couple of years. This outbreak and the associated control efforts have been significant for many reasons: • In 2015 it appeared that Ontario was on the way to controlling terrestrial rabies. The introduction of the virus via long-distance transport, while not unexpected, became a major test of OMNRF’s contingency plans. • This outbreak occurred in one of the most urbanized areas of Canada, unlike previous outbreaks of raccoon rabies in eastern Ontario, Quebec, and New Brunswick. • In 2014 CFIA withdrew from the collection of samples for rabies testing, leaving each province and territory to manage its own collection and risk assessment procedures. The raccoon rabies outbreak has tested how well the agencies mandated by the province to handle rabies have cooperated to deal with this change. • OMNRF has continued to develop surveillance and control methods. It has adopted the intensive use of dRIT testing for rabies during this outbreak with excellent results. As well, OMNRF made several improvements in its aerial baiting technology and adopted the use of baiting stations to distribute vaccine baits. • Control of this outbreak is heavily focused on the use of ONRAB vaccine baits, as opposed to the previously successful tactics used in eastern Ontario of depopulation in conjunction with TVR. • Control appears to have been achieved despite serology results that indicate that much lower vaccination rates were achieved compared to previous baiting campaigns. • Distemper may be a complicating factor. The Hamilton area was in the midst of a major outbreak of distemper when the raccoon strain of virus was introduced. A large portion of all rabies cases showed the animals also had been exposed to distemper. How the interplay of the two viruses affected the course of the epizootic and control efforts is still under investigation. In 2015, the sudden appearance of raccoon rabies in the Hamilton area initiated a major test of Ontario’s contingency plans for controlling an outbreak of rabies. Reaction was immediate. On Monday following the Friday, 4 December confirmation of the raccoon strain in Stoney Creek, OMNRF met with Hamilton’s Public Health staff and Animal Control Services to coordinate contingency planning, begin public awareness campaigns, and ensure collection of specimens for testing. That same day, drawing from stored reserves of ONRAB baits, OMRNF personnel began hand baiting an 8 km2 grid around the

CONTROLLING THE 2015–2017 OUTBREAK IN THE HAMILTON AREA

At the time of writing, the outbreak of the raccoon strain of the rabies virus was ongoing but declining numbers and slowing spread suggest that, to date, control procedures

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Figure 10.21: Rabies cases in foxes in eastern Ontario, 1956–2004. Source: created from CFIA data.

dead animals, trappers, vaccinated against rabies, were hired to collect those specimens. Media coverage was extensive and public awareness was high. By March 2016, the surveillance network was collecting and using dRIT to test up to 240 samples per week, and the extent of the outbreak was well defined. This load overwhelmed the OMNRF dRIT lab, and collecting agencies were allocated limits so that the overall sample load dropped to 100 per week. Based on this surveillance OMNRF implemented a spring baiting in April 2016 to further contain spread. From 1 April to 3 May 2016, almost half a  million baits were aerially dropped: 344,119 by Twin Otter, 85,852 via helicopter, and 63,356 by hand. The following summer and fall control campaign between 11 July and November put out almost another 900,000 baits: 484,850 by Twin Otter, 137,400 by helicopter, and 255,336 by hand (Figure 10.22). This area included baiting in Perth County around a case of fox strain rabies that was not related to the ongoing epizootic of raccoon strain rabies. Hand baiting covered the urban areas of the outbreak (dark shaded area in Figure 10.22). The urban baiting worked at limiting rabies spread ­towards Toronto, and rabies has not spread past the southwest tip of the Halton region (Figures 10.18 and 10.20). The enhanced surveillance zone was also extended ­northwest through Perth County to Lake Huron to monitor the concurrent re-emergence of arctic fox strain rabies in that area. Control efforts in 2017 covered much the same area as in 2016 (Figure 10.23). Another 1.1  million baits were

initial case. By 9 December they began Oravax baiting at 150 baits/km2 using helicopters to cover four-kilometre-radius zones around the locations where three additional cases had been reported. Although warm weather in December may have assisted raccoon movement and spread, it also allowed aerial baiting that, in typical years, would have stopped in October. Adjacent health units were notified, and on 11 December Haldimand County submitted a specimen found dead in a field which subsequently proved positive by dRIT. It was 25 kilometres south of the 4 December case. The weather remained warm and by 16 December aerial baiting in rural areas via Twin Otter aircraft, helicopter baiting in rural/urban areas, and hand baiting in urban areas created a control zone 25 kilometres around the initial case and the Haldimand County case. As the weather worsened, this became the limit of baiting for 2015. Enhanced surveillance was initiated another 25 kilometres beyond the control zone, with crews from OMNRF and Animal Control Services submitting road kills and animals found dead in other locations, and euthanizing and submitting animals found acting strangely in this area. The surveillance network was expanded and enhanced during early 2016 with additional cases detected (Figure 10.22). OMNRF developed a network of other animal control agencies, including road maintenance crews and humane societies, to collect, tag, and freeze specimens for OMNRF collection. In a few cases, where municipal employees were reluctant or unable to collect

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Figure 10.22: Baiting area April to May 2016 showing Twin Otter flight-lines and hand-baiting operations (solid shading). Source: created from OMNRF data.

distributed between July and September 2017. This included urban hand baiting in July through September, aerial baiting through August and September, and aerial baiting for foxes in the Perth County area in September. Another major aspect of the ongoing epizootic has been the effective interagency cooperation for submitting rabies suspect animals for testing. Ontario developed a contingency plan for submitting animals for testing (an effort led by Dr Catherine Filejski from the Ontario Ministry of Health and Long-Term Care), after CFIA announced it was transferring its sample-collecting role to the provinces and territories, although it remains responsible for testing samples using the fluorescent antibody test (FAT) and maintaining records. In the Hamilton area, Hamilton Public Health Services deals with preventing rabies in humans, assessing situations for sample submission where contact between humans and animals suspected of rabies may have occurred, issuing PEP, and educating the public on rabies awareness. The Ontario Ministry of Agriculture, Food, and Rural Affairs coordinates with veterinarians to decide on sample submission and post-exposure management of companion animals and livestock exposed to suspected rabid wildlife. OMNRF, in turn, handles enhanced surveillance and testing in wildlife where no contact is believed to have occurred with humans, companion animals, or livestock, and runs wildlife rabies control programs. As well,

OMNRF plays a major role as liaison between these agencies. Animal Control agencies and provincial and municipal road crews were also involved in specimen collection. All agencies cooperated in an extensive public outreach campaign via social media, media interviews, trade shows, interest groups, and information posters from the involved agencies. For example, Hamilton Public Health Services launched the “Rabies Is Real” public awareness campaign in September 2016, urging people to avoid wild animals, report animals that are acting strangely, and vaccinate their pets, and if they are bitten or scratched by an animal, to contact local health services (Lobo et al., 2018). In sum, it appears that a side benefit of this epizootic, so soon after CFIA’s withdrawal from its central collection role, has been to reinforce and strengthen the links between agencies in Ontario and demonstrate how to respond in the event of further outbreaks. An additional feature of this outbreak has been OMNRF’s extensive use of dRIT as a field screening test for rabies. Originally developed by Centers for Disease Control and Prevention in Atlanta (Lembo et al., 2006) for countries with limited facilities and resources, the test, correctly carried out, is comparable in sensitivity and specificity to the FAT test, the gold standard of rabies testing currently used by CFIA (Middel et al., 2017). The test takes less than an hour and total cost (reagents, overhead, and labour) is less than $20 per test

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Figure 10.23: Surveillance and control operations in 2016. The zone marked R is baiting targeted at the raccoon strain; the zone marked F is baiting targeted at the fox strain; and the ES zone is the extension of enhanced surveillance in zones F and R. Bait densities for the raccoon were 150 baits/km2 and bait density in the fox area was 300 baits/ km2 – a value aimed at the skunk population thought to be the long-time reservoir of the fox rabies strain of the virus. Source: created from OMNRF data.

(T. Buchanan, personal communication, 19 October 2017). In contrast, FAT testing costs about $80, although if the cost of packaging and shipping to the CFIA lab is added, the cost per test becomes about $238 (see Chapter 34). As well, because of shipping time, obtaining results can take two days or more. Ontario has been testing dRIT since 2009, and that work is described in Chapter 24b. Hence, the province was ready to use dRIT from the outset of the 2015 outbreak. Over the next two years, 384 raccoons and skunks tested positive in the outbreak area. Only 12 of those specimens had been submitted via traditional passive surveillance, that is, when there is human, pet, or livestock contact with a suspected rabid animal and the specimen is sent directly to CFIA for testing. Over 25 months, from December 2015 to December 2017, some 8700 mammalian specimens from the enhanced surveillance area (Figure 10.23) were submitted and tested

with dRIT. Of these, 97% were raccoons or skunks, although many other small mammal species were tested. This experience has demonstrated the reliability of dRIT testing to compliment FAT. All dRIT positives are submitted to CFIA for confirmatory testing with FAT. After two small changes in procedure in early 2016, agreement with FAT has been 100% (Middel et al., 2017; see Table 21.10 in Chapter 21). In sum, the accuracy of dRIT and its speed, low cost, and ease of use has meant that OMNRF has developed an overview of the progression and the extent of the epizootic at a level of detail impossible in the past. Preliminary results of vaccination rates from the ONRAB baiting in 2016 appeared to be much lower than was expected (T. Buchanan, personal communication, 19 ­October 2017). Previous studies of raccoon vaccination results using ONRAB in rural habitats of Ontario had produced vaccination

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rates of 40% to 71% with a mean of 58%. Vaccination rates in Quebec in rural raccoons were 51% with ONRAB (see Chapter 11) and proved effective at eliminating raccoon strain rabies from that province by 2017. Although, at the time of writing, the epizootic appears to be under control, the low seroconversion results make it unclear what the future holds. Several areas of research are attempting to improve vaccination results through the investigation of topics, including urban rabies vector species densities in the Hamilton area, which may require a greater density of vaccine baits; opossum competition for vaccine baits; alternative or more attractive food sources in urban areas; the potential for immunosuppression of vector species caused by the high prevalence of distemper virus; the potential for rabies vector species to have been pre-exposed to human adenovirus from their urban proximity to humans, which could potentially reduce the effectiveness of the human adenovirus construct of the ONRAB vaccine; the smaller home range size of urban rabies vector species, which requires greater bait dispersal; and whether attempts to measure vaccination rates of rabies vector species are incorrect. It is possible that two or more of these issues are confounding vaccination attempts. The most interesting hypotheses is that seroconversion or the impact of the raccoon rabies virus on animals is affected by the ongoing epizootic of canine distemper virus (CDV) in the area (Jardine et al., 2018). Over 98% of animals submitted for testing in Hamilton had CDV. To date some 69% of raccoons and 20% of skunks infected with rabies were also infected with CDV. If co-infection is a factor, the mechanism is not known. Hopefully, ongoing research and continued monitoring for the presence of both viruses

in samples submitted for testing may provide clues on the effect of co-infection. In sum, the vaccination campaigns appear to be containing the outbreak, but lower than expected results from serology studies leave many questions unresolved about the processes involved and whether control will be successful in the long run.

Discussion The rabies wildlife invasion in Ontario was met with foresight and resolve from a number of scientists and administrators in OMNR and associated agencies. Their work led to new approaches for rabies management that include (1) recognizing that rabies is not just one strain but several species-specific strains that are geographically differentiated; (2) understanding that rabies management requires a “one health” approach – an integration of control measures for wildlife with traditional preventive measures, such as vaccination in humans, pets, and livestock; (3) developing new technologies for vaccines, baits, and delivery mechanisms for controlling wildlife rabies; (4) conducting new research on the biology of the vector species; (5) using modelling techniques to evaluate control strategies; (6) adopting and extensively using dRIT testing for large-scale wildlife surveillance; (7) realizing that successful management of the disease requires cooperation between government agencies (federal, provincial, territorial, and municipal), research institutions (university and commercial), and private industry; and (8) continuing to be vigilant and to avoid complacency.

Acknowledgments For almost 60 years researchers and staff from OMNRF, CFIA, Connaught Laboratories, and various Canadian universities and private industry have made invaluable contributions to rabies research and control in Ontario, which we have tried to document in this chapter. At the time of writing, these contributions were being used to the fullest to combat the raccoon rabies outbreak. We want to thank Tore Buchanan, the current coordinator of the Wildlife Research and Monitoring section of Ontario Ministry of Natural Resources and Forestry, for his help and guidance in documenting these ongoing efforts.

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A History of Rabies Management in the Provinces and Territories Black, W. D., Copeland, K. F. T., Leslie, K., & Luescher, A. (1985). Antibiotic residues in animals exposed to sponges used for oral rabies vaccination: An executive summary of a report prepared for the Ontario Ministry of Natural Resources at the Ontario Veterinary College, Guelph, Ontario. [Memo]. Available upon request from OMNFR at [email protected] Charlton, K. M., Nadin-Davis, S., Casey, G. A., & Wandeler, A. (1997). The long incubation period in rabies: Delayed progression of infection in muscle at the site of exposure. Acta Neuropathologica, 94(1), 73–77. https://doi.org/10.1007/s004010050674 Coyne, M. J., Smith, G., & McAllister, F. E. (1989). Mathematical model for the population biology of rabies in raccoons in the mid-­ Atlantic states. American Journal of Veterinary Research, 50(2), 2148–2154. Cullingham, C., Pond, B., Kyle, J., Rees, E. E., Rosatte, R. C., & White, B. N. (2008). Combining direct and indirect genetic methods to estimate dispersal to estimate dispersal for informing wildlife disease management decisions. Molecular Ecology, 17(22), 4874–886. https://doi.org/10.1111/j.1365-294X.2008.03956.x Davies, C. (Ed.). (2003). Operational review of the Ontario wildlife rabies control program. Ottawa, ON: Ontario Ministry of Natural ­Resources. Available upon request from OMNFR at [email protected] De Serres, G., Skowronski, D. M., Mimault, P., Ouakki, M., Maranda-Aubut, R., & B. Duval. (2009). Bats in the bedroom, bats in the belfry: Reanalysis of the rationale for rabies post exposure prophylaxis. Clinical Infectious Diseases, 48, 1493–1499. https://doi .org/10.1086/598998 Elmgren, L. D., Nadin-Davis, S. A., Muldoon, F. T., & Wandeler, A. L. (2002). Diagnosis and analysis of a recent case of human rabies in Canada. The Canadian Journal of Infectious Diseases, 139(2), 129–133. http://doi.org/10.1155/2002/235073 Grant, G. (1977). A simulation model of a fox population with rabies (Unpublished master’s thesis). Department of Geography, Queen’s University, Kingston, Ontario, Canada. Gurba, J. B. (1974). Rabies vector control in Alberta. In W. V. Johnson (Ed.), Proceedings of the Sixth Vertebrate Pest Conference. Davis, CA: University of California, Davis. Retrieved from DigitalCommons@University of Nebraska-Lincoln website: http:// digitalcommons.unl.edu/vpc6/19 Jardine, C., Buchanan, T., Ojkic, D., Campbell, G., & Bowman, J. (2018). Frequency of virus coinfection in raccoons (procyon lotor) and striped skunks (mephitis mephitis) during a concurrent rabies and canine distemper outbreak. Journal of Wildlife Diseases, 54(3), 622–625. https://doi.org/10.7589/2017-04-072 Johnston, D. H., & Beauregard, M. (1969). Rabies epidemiology in Ontario. Bulletin of the Wildlife Disease Association, 5(3), 357–370. https://doi.org/10.7589/0090-3558-5.3.357 Knowles, M. K., Nadin-Davis, S., Sheen, M., Rosatte, R., Mueller, R., & Beresford, A. (2009a). Safety studies on an adenovirus vaccine for rabies (AdRg1.3-ONRAB®) in target and non-target species. Vaccine, 27(47), 6619–6626. https://doi.org/10.1016 /j.vaccine.2009.08.005 Knowles, M. K., Roberts, D., Craig, S., Sheen, M., Nadin-Davis, S. A., & Wandeler, A. I. (2009b). In vitro and in vivo genetic stability studies of a human adenovirus type 5 recombinant rabies glycoprotein vaccine (ONRAB®). Vaccine, 27(20), 2662–2668. https:// doi.org/10.1016/j.vaccine.2009.02.074 Lembo, T., Niezgoda, M., Velasco-Villa, A., Cleaveland, S., Ernest, E., & Rupprecht, C. E. (2006). Evaluation of a direct, rapid immunohistochemical test for rabies diagnosis. Emerging Infectious Diseases, 12(2), 310–313. https://doi.org/10.3201/eid1202.050812 Lobo, D., DeBenedet, C., Fehlner-Gardiner, C., Nadin-Davis, S., Anderson, M., Buchanan, T., ... Hopkins, J. (2018) Raccoon rabies outbreak in Hamilton, Ontario: A progress report. Canadian Communicative Diseases Report, 44(5), 116–121. https://doi.org/10.14745 /ccDrv44i05a05 Lutz-Wallace, C. A., Wandeler, A., Prevec, L., Sidhu, M., Sapp, T., & Armstrong, J. (1995). Characterization of human adenovirus 5: rabies glycoprotein recombinant vaccine re-isolated from orally vaccinated skunks. Biologicals, 23(4), 271–277. https://doi .org/10.1006/biol.1995.0045 MacInnes, C. D., Tinline, R., Voigt, D., Broekhoven, L., & Rosatte, R. R. (1988). Planning for rabies control in Ontario. Review of Infectious Diseases, 10(Suppl. 4), 665–669. https://doi.org/10.1093/clinids/10.Supplement_4.S665 Middel, K., Fehlner-Gardiner, C., Pulham, N., & T. Buchanan. (2017). Incorporating direct rapid immunohistochemical testing into large-scale wildlife rabies surveillance. Tropical Medicine and Infectious Disease, 2(3), 21. https://doi.org/10.3390/ tropicalmed2030021 Moore D. A. (1999). Spatial diffusion of raccoon rabies in Pennsylvania, USA. Preventive Veterinary Medicine, 40(1), 19–32. https:// doi.org/10.1016/S0167-5877(99)00005-7 National Advisory Committee on Immunization. (2002). Canadian immunization guide (6th ed.). Ottawa: ON: Minister of Health. Retrieved from Government of Canada Publications website: http://publications.gc.ca/collections/Collection/H49-8-2002E.pdf Nunan C. P., Tinline, R. R., Honig, J. M., Ball D. G., Hauschildt, P., & LeBer, C. A. (2002). Postexposure treatment and animal rabies, Ontario, 1958–2000. Emerging Infectious Diseases, 8(2), 214–217. https://doi.org/10.3201/eid0802.010177 Plummer, P. J. G. (1954). Rabies in Canada, with special reference to wildlife reservoirs. Bulletin of World Health Organization, 10, 767–774.

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Ontario Prevec, L., Campbell, J., Christie, B. S., Belbeck, L., & Graham, F. L. (1990). A recombinant human adenovirus vaccine against rabies. Journal of Infectious Diseases, 161(1), 27–30. https://doi.org/10.1093/infdis/161.1.27 Public Health Ontario. (2009). Ontario rabies prevention and control protocol. Retrieved from Ontario Legislative Library website: http://www.ontla.on.ca/library/repository/mon/23008/294695.pdf Pybus, M. (1988). Rabies and rabies control in striped skunks (Mephitis mephitis) in three prairie regions of western North America. Journal of Wildlife Diseases, 24(3), 434–49. https://doi.org/10.7589/0090-3558-24.3.434 Rosatte, R. C., Power, M., MacInnes, C., & Campbell, J. (1992). Trap-vaccinate-release and oral vaccination for rabies control in urban skunks, raccoons and foxes. Journal of Wildlife Diseases, 28(4), 562–571. https://doi.org/10.7589/0090-3558-28.4.562 Rosatte, R. C., MacInnes, C., Williams, R., & Williams, O. (1997). A proactive prevention strategy for raccoon rabies in Ontario, ­Canada. Wildlife Society Bulletin, 25, 110–116. Rosatte, R., & Lawson, K. (2001). Acceptance of baits for delivery of oral rabies vaccine to raccoons. Journal of Wildlife Diseases, 37(4), 730–739. https://doi.org/10.7589/0090-3558-37.4.730 Rosatte, R., Donovan, D., Allan, M., Howes, L. A., Silver, A., Bennett, K., ... Radford, B. (2001). Emergency response to raccoon rabies introduction in Ontario. Journal of Wildlife Diseases, 37(2), 265–279. https://doi.org/10.7589/0090-3558-37.2.265 Rosatte, R., MacDonald, E., Sobey, K., Donovan, D., Bruce, L., Allan, M., ... Muldoon, F. (2007a). The elimination of raccoon rabies from Wolfe Island, Ontario: Animal density and movements. Journal of Wildlife Diseases, 43(2), 242–250. https://doi. org/10.7589/0090-3558-43.2.242 Rosatte, R., Donovan, D., Allan, M., Bruce, L., Buchanan, T., Sobey, K., ... Muldoon, F. (2007b). Rabies in vaccinated raccoons from ­Ontario, Canada. Journal of Wildlife Diseases, 43(2), 300–301. https://doi.org/10.7589/0090-3558-43.2.300 Rosatte, R., Tinline, R., & Johnston, D. (2007c). Rabies control in wild carnivores. In A. Jackson & W. Wunner (Eds.), Rabies (2nd ed., pp. 595–634). San Diego, CA: Academic Press. Rosatte, R., Donovan, D., Allan, M., & Davies, J. C. (2007d). Human assisted movements of raccoons (Procyon lotor) and opossums (Didelphis Virginia) between the United States and Canada. Canadian Field Naturalist, 121(2), 212–213. https://doi.org/10.22621/cfn.v121i2.450 Rosatte, R., Allan, M., Bachmann, P., Sobey, K., Donovan, D., Davies, J. C., ... Schumacher, C. (2008). Prevalence of tetracycline and rabies virus antibody in raccoons, skunks, and foxes following aerial distribution of V-RG baits to control raccoon rabies in Ontario, Canada. Journal of Wildlife Diseases, 44(4), 946–964. https://doi.org/10.7589/0090-3558-44.4.946 Rosatte, R., Donovan, D., & Davies, J. C. (2009). The control of raccoon rabies in Ontario, Canada, proactive and reactive tactics. ­Journal of Wildlife Diseases, 45(3), 772–784. https://doi.org/10.7589/0090-3558-45.3.772 Rosatte, R., Ryckman, M., Ing, K., Proceviat, S., Allan, M., Bruce, L., Donovan, D., & Davies, J. C. (2010). Density, movements, and survival of raccoons in Ontario, Canada: Implications for disease spread and management. Journal of Mammalogy, 91, 122–135. https:// doi.org/10.1644/08-MAMM-A-201R2.1 Rosatte, R., Donovan, D., & Davies, J. C. (2011). High density baiting with ONRAB¯ rabies vaccine baits to control Arctic variant rabies in striped skunks in Ontario, Canada. Journal of Wildlife Diseases, 47(2), 459–465. https://doi.org/10.7589/0090-3558-47.2.459 Schneider, D., & Pautler, P. (2018). A guide to bats in Ontario. Ontario Nature Magazine. Retrieved from https://onnaturemagazine .com/bat-guide.html Sobey, K., Rosatte, C., Bachmann, P., Buchanan, T., Bruce, L., Donovan, D., ... Wandeler, A. (2010). Filed evaluation of an inactivated vaccine to control raccoon rabies in Ontario, Canada. Journal of Wildlife Diseases, 46(3), 818–831. https://doi.org /10.7589/0090-3558-46.3.818 Statistics Canada. (2017). Ontario [province] and Canada [country] (table). Census profile. 2016 census. Retrieved from https:// www12.statcan.gc.ca/census-recensement/2016/dp-pd/prof/details/Page.cfm?Lang=E&Geo1=PR&Code1=35&Geo2=&Code2 =&Data=Count&SearchText=Ontario&SearchType=Begins&SearchPR=01&B1=All&GeoLevel=PR&GeoCode=35 Territorial Evolution, 1670–2001. (2012). Retrieved from Historical Atlas of Canada Online Learning Project website: http:// www.historicalatlas.ca/website/hacolp/national_perspectives/boundaries/UNIT_17/U17_Timeline/U17_timeline_1713.htm Tinline, R. R. (1988). Persistence of rabies in wildlife. In J. Campbell & K. Charlton (Eds.), Rabies (pp. 301–322). Dordrecht, The ­Netherlands: Kluwer Academic Publishers. Tinline, R. R., & MacInnes, C. D. (2004). Ecogeographic patterns of rabies in southern Ontario based on time series analysis. Journal of Wildlife Diseases, 40(2), 212–221. https://doi.org/10.7589/0090-3558-40.2.212 Tinline, R. R., Voigt, D. R., & Broekhoven. L. (1985). A spatial simulation model for rabies control. In P. Bacon (Ed.), Population ­dynamics of rabies in wildlife (pp. 311–349). London, England: Academic Press. Totton, S. C., Rosatte, R. C., Tinline, R. R., & Bigler, L. L. (2004). Seasonal home ranges of raccoons, Procyon lotor, using a common feeding site in rural eastern Ontario: Rabies management implications. Canadian Field-Naturalist, 118(1), 65–71. https://doi .org/10.22621/cfn.v118i1.884 Totton, S. C., Tinline, R. R., Rosatte, R. C., & Bigler, L. L. (2002). Contact rates of raccoons at a communal feeding site in rural eastern Ontario. Journal of Wildlife Diseases, 38(2), 313–319. https://doi.org/10.7589/0090-3558-38.2.313

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A History of Rabies Management in the Provinces and Territories Trewby, H., Nadin-Davis, S., Real, L., & Biek, R. (2017) Processes underlying rabies virus incursions across US–Canada border as ­revealed by whole-genome phylogeography. Emerging Infectious Diseases, 23(9), 1454–1461. https://doi.org/10.3201/eid2309.170325 Voigt, D., & Tinline, R. (1980). Strategies for analyzing radio tracking data. In J. C. Amlaner & D. W. Macdonald (Eds.) A handbook on biotelemetry and radio tracking: Proceedings of the International Conference on Telemetry and Radio Tracking in Biology and Medicine (pp. 387–404). Oxford, England: Elsevier. Voigt, D., & Lotimer, J. S. (1981). Radio tracking terrestrial furbearers: System design, procedures and data collection. In J. A. Chapman & D. Pursely (Eds.), Worldwide furbearer conference (General Technical Report PSW-GTR-157; pp. 1151–1188), Washington, DC: U.S. Forest Service, Department of the Interior. Wandeler, A., & Salsberg, E. (1999). Raccoon rabies in eastern Ontario. Canadian Veterinary Journal, 15, 731. Yarosh, O., Wandeler, A., Graham, F. L., Campbell, J. B., & Prevec, L. (1996). Human adenovirus type 5 vectors expressing rabies glycoprotein. Vaccine, 14(13), 1257–1264. https://doi.org/10.1016/S0264-410X(96)00012-6

156

11 QUEBEC Denise Bélanger,1 Pierre Canac-Marquis,2 Ariane Massé,2 and Rowland R. Tinline3 1

Université de Montréal (Retired), Montreal, Quebec, Canada Ministère des Forêts, de la Faune et des Parcs du Québec, Quebec, Canada 3 Professor Emeritus, Geography, Queen’s University, Kingston, Ontario, Canada 2

Place Quebec is Canada’s largest province, occupying 1.4 million km2 or 15.0% of Canada’s land mass, with a population of 8,164,361 (Statistics Canada, 2017). It is bounded on the north by Ungava Bay and Hudson Straits; to the west by Hudson Bay, James Bay, the Ottawa River, and Ontario; on the south, by the states of New York, Vermont, New Hampshire, and Maine; and to the east by the Labrador Coast, the Gulf of St Lawrence, and New Brunswick (Figure 11.1 and Overview, Part 3). The northern connection and the long shared borders with Ontario, New Brunswick, and the United States have played important parts in the history of rabies in Quebec, and they remain important concerns for rabies management in the province as long as rabies persists in the north or the United States. Quebec has six eco-regions (Figure 11.1) that overlay three main physiographic areas: the Canadian Shield, the St Lawrence River Valley, and the Appalachian Region. The St Lawrence Valley is the most fertile, developed, and most populous region, and this southern plain coincides with the eastern temperate forest eco-region. The valley was the major corridor for the movement of fox rabies to New Brunswick. The Canadian Shield is a vast rocky, swampy, and lake area, extending from the St Lawrence River Valley north to the Ungava Region and taking in the tundra, taiga, the Hudson Plain, and most of the northern forests. Rabies in the tundra, taiga and Hudson Plain has been dominated by incidence of rabies in arctic foxes (Vulpes lagopus) and red foxes (Vulpes vulpes) while the northern forests have served as an interface zone between arctic and

red foxes. Arctic tundra covers the northern tip of Quebec (Figure 11.1) and is the home of the polar bear (Ursus maritimus), arctic fox, and arctic hare (Lepus Arcticus). It is a non-forested zone covered with lichens and mosses. The taiga zone is found between the tundra and northern forests region and consists of some vegetation (spruce, fir, and dwarf shrubs) and provides suitable habitat for species such as the caribou (Rangifer tarandus). South of the taiga to the St Lawrence Valley lies the boreal forest zone that is dominated by cold-tolerant pine, spruce, larch, poplar, fir, and birch forests. In the south these forests transition to stands with an increasing number of deciduous species, such as maple, ash, beech, and oak. The southern areas, especially the St Lawrence Valley, support a wide array of mammals susceptible to rabies, including red foxes, skunks, and raccoons, and have been the focus of rabies control efforts in Quebec. Bats have also been involved in rabies in Quebec and a silver haired-bat was suspected to be responsible for the last human death in the province in 2000 (see the section “Submissions, 1985–2017”; see Chapter 3b, Case 39).

Rabies in Quebec Animal and Human Rabies before 1950 Rabies-like disease had been recorded in Quebec on several occasions: in 1814 a dog, assumed to be rabid, bit a young boy; in 1816 a large dog bit a boy; in 1816 a cat attacked a lady. Each resulted in the death of the individual involved (Blaisdell, 1992; see Chapter 3b). In 1819 the Duke

A History of Rabies Management in the Provinces and Territories

Figure 11.1: Eco-regions of Quebec. Source: created from Natural Resources Canada maps.

of Richmond was reportedly bitten by his pet fox in Sorel when he tried to separate it from playing with his dog. Alternative reports suggest that the bite could have come from a dog in Quebec City, but the whole story is in doubt (see Chapter 3a). Commenting on a human rabies case in 1839, Dr Mitchell suggests that canine rabies existed in the early years of the nineteenth century in Quebec City, so the offending dog was probably rabid (Mitchell, 1967). Beginning in 1867 the annual Report of the Minister of Agriculture for the Dominion of Canada included information of various infectious diseases diagnosed in domestic animals, but rabies in Quebec was not reported until 1915 and then only as premises quarantined (Report of the Veterinary Director General, 1915). The 1921 report

mentions three animals quarantined for rabies in Quebec (Report of the Veterinary Director General, 1921). In January 1926 an outbreak of rabies affecting domestic animals occurred in the Low District of Quebec and eventually spread to the Montreal area and to Ottawa, Ontario (Report of the Veterinary Director General, 1926, 1927; Tabel et al., 1974). The report suggests the outbreak was due to hunting dogs imported the year before from the United States and thus the outbreak was probably due to canine rabies. Table 11.1 shows the confirmed number of rabies cases for 1926–1934 diagnosed at the federal laboratory in Hull, Quebec. Cases in dogs dominated incidence in this period. For this period each Report of the Veterinary Director General (1926, 1927, 1928, 1929, 1930, 1931, 1932, 1933, 1934, 1935) was

158

Quebec

Table 11.1  Confirmed rabies cases in Quebec, 1926 to 1934. Annual reporting began in 1926, and there were no further cases until 1953 (see Table 11.3). Year

Total

Dog

1926 1927 1928 1929 1930 1931 1932 1933 1934

68 59 28 21 13 7 0 0 3

52 42 19 12 11 5 0 0 3

 Total

199

144

Cow

Sheep

Cat

Pig

Horse

8 8 6 5 2 2 0 0 0

4 9 1 4 0 0 0 0 0

1 0 2 0 0 0 0 0 0

2 0 0 0 0 0 0 0 0

1 0 0 0 0 0 0 0 0

31

18

3

2

1

Table 11.2  Number of outbreaks in Quebec, affected and quarantined animals, 1926 to 1935 based on fiscal year (April 1 of previous year to March 31 of reported year). The reports did not list species.

Source: compiled from CFIA data.

Year

Outbreaks

Affected

Quarantined

1926 1927 1928 1929 1930 1931 1932 1933 1934 1935

1 16 15 n/a 11 6 4 n/a 1 2

28 61 44 19 23 7 6 n/a 1 3

193 2210 2669 n/a 839 171 195 31 107 141

Note: n/a means no data were available. Source: compiled from Report of the Veterinary Director General, 1926–1935, Canada Department of Agriculture.

based on a fiscal year (31 March of one year to 1 April of the next year) and showed the number of outbreaks, the number of animals affected (rather than positives) in those outbreaks, and the number of animals quarantined (Table 11.2). Quarantines were the main control method.

(Figure 11.3). This increase and subsequent decrease was related to a change in the criteria for submissions of bats described in the next section.

Animal Rabies after 1950

Submissions, 1985 to 2017

Canadian Food Inspection Agency (CFIA) data indicate that rabies was absent or not reported in Quebec from 1936 to 1952. In 1953 it reappeared with three rabid foxes and five dogs (Table 11.3). From then to 2017, almost 50% of all cases were in rabid foxes with associated cases in livestock (24.2%), dogs and cats (13.4%), skunks (5.5%), and raccoons (2.3%). Incidence in foxes drove incidence in other species (Figure 11.2) until 1999 by which time control efforts in Ontario in the 1990s had eliminated fox rabies in eastern Ontario (see Chapter 10) and joint Ontario-Quebec baiting campaigns along the Ottawa River Valley eliminated a major source of infection for fox rabies in Quebec. Until that time, as Table 11.4 illustrates, incidence in other wildlife species was significantly correlated (p < .01) with incidence in foxes. Since 2000 overall incidence has been low but marked by an invasion of the raccoon viral strain of rabies from Vermont in 2006–2009. Only raccoons, skunks, and one fox have been found with the raccoon rabies virus strain. There was no correlation between incidence in raccoons and other species. Incidence in domestic animals (cat/dog) was very low and there were no cases in livestock after 2004. The raccoon rabies invasion was quickly controlled by programs initiated by Quebec that are described in the section “Raccoon Rabies.” Cases in bats were sporadic, but submissions increased dramatically in the 2000s as did reported cases

From 1985 onwards, when CFIA adopted a new laboratory data management system, digital data on submissions have been available. Table 11.5 shows the number of submissions by species to CFIA when human or domestic animal contact was reported from 1985 to 2017. Submissions are dominated by domestic animals: dogs and cats were almost 59% of the total during this entire period but only 12.9% of positives. The discrepancy between the large numbers of submissions for pets relative to their contribution to diagnosed cases probably reflects both the close relationship people have with pets and the widespread fear that aggressive behaviour in pets could be the result of rabies. The fear factor in citizens also probably shows up in the sharp increase of bat submissions (Table 11.5) after the death of a boy in Montreal from a bat bite in 2000 (see Chapter 3b, Case 39). The media produced many stories about this incident. Furthermore, on an official level, there was encouragement to submit bat specimens for testing. The sixth edition of Health Canada’s Immunization Guide (National Advisory Committee on Immunization, 2002) begins its discussion on rabies by referring to this case and cautions that of the last five human deaths in Canada four of those resulted from exposure to bats. Although the fifth edition of the guide published in 1998 contained the same recommendations about submitting specimens, it was not

159

A History of Rabies Management in the Provinces and Territories

Table 11.3  Rabies-positives in Quebec, 1953 to 2017. Year

Total

1953 1954 1955 1956 1957 1958 1959 1960 1961 1962 1963 1964 1965 1966 1967 1968 1969 1970 1971 1972 1973 1974 1975 1976 1977 1978 1979 1980 1981 1982 1983 1984 1985 1986 1987 1988 1989 1990 1991 1992 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010

8 2 1 36 326 50 26 40 111 46 56 184 210 77 231 243 243 115 143 292 215 198 146 33 37 94 84 37 10 13 26 49 32 57 35 133 136 493 642 685 387 116 22 62 38 14 10 22 17 25 22 12 21 15 81 40 16 7

Fox 3 1 1 19 160 14 10 23 52 22 20 80 38 18 125 126 98 45 83 145 89 79 60 11 17 45 54 10 2 2 18 17 14 37 30 99 84 313 344 427 240 68 10 33 17 12 5 11 8 4 5 3 4 0 2 1 1 0

Livestock 0 0 0 17 132 27 14 11 36 12 28 70 145 46 71 56 89 51 40 97 98 77 54 12 4 25 16 11 3 3 3 1 6 5 0 8 12 88 104 66 31 7 4 12 7 1 0 0 0 0 1 1 0 0 0 0 0 0

Domestic

Bat

5 1 0 0 28 6 1 3 15 7 6 25 25 12 27 40 45 17 14 35 22 38 26 8 12 22 9 7 1 1 3 10 6 3 2 15 18 34 93 96 64 32 2 13 11 0 2 3 1 0 3 0 4 2 0 0 3 0

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 2 0 1 0 2 0 2 0 0 1 0 2 0 2 1 1 0 2 1 1 5 7 1 2 5 1 2 0 1 7 8 19 13 7 12 8 15 5 9 7

Skunk 0 0 0 0 3 2 1 3 6 5 1 0 1 1 6 13 5 1 1 5 2 4 2 2 2 2 4 4 4 4 2 18 4 10 1 7 17 40 64 59 34 3 1 2 1 1 1 0 0 0 0 0 0 1 6 6 2 0

Raccoon 0 0 0 0 0 0 0 0 1 0 1 0 0 0 0 1 1 0 1 2 0 0 1 0 0 0 0 0 0 0 0 0 0 1 0 0 2 9 16 19 7 0 0 0 0 0 0 0 0 1 0 0 0 4 58 27 0 0

Coy/Wlf 0 0 0 0 2 0 0 0 1 0 0 0 1 0 1 4 3 1 2 7 3 0 1 0 0 0 1 4 0 1 0 1 1 0 1 1 1 8 15 10 7 2 0 0 0 0 1 0 0 1 0 1 1 0 0 1 1 0

Other 0 0 0 0 1 1 0 0 0 0 0 1 0 0 1 2 2 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 1 1 0 1 1 3 2 0 1 0 0 0 1 0 0 0 0 0 0 0 0 0 0 (Continued)

160

Quebec

Year

Total

Bat

Skunk

2011 2012 2013 2014 2015 2016 2017

17 18 15 8 18 6 14

7 10 0 1 2 1 3

0 0 0 0 0 0 0

1 5 0 1 2 0 3

9 2 14 6 13 5 8

0 0 1 0 0 0 0

0 0 0 0 1 0 0

0 1 0 0 0 0 0

0 0 0 0 0 0 0

6618

3283 49.6

1602 24.2

890 13.4

210 3.2

365 5.5

153 2.3

86 1.3

21 0.3

 Totals   % Total

Fox

Livestock

Domestic

Raccoon

Coy/Wlf

Other

Coy/Wlf = Coyote + wolf. Source: compiled from CFIA data.

Figure 11.2: Annual number of rabies cases in Quebec, 1953 to 2017. Source: created from CFIA data.

Table 11.4  Time series correlations (Pearson product-moment coefficient), 1953 to 1999, comparing incidence in several species with incidence in foxes. Species

prefaced by the caution about bats and human deaths. By 2008 research by Dr De Serres and colleagues (De Serres et al., 2009) found the risk of transmission of rabies from bats is very low where there is no recognized physical contact. Subsequently, Quebec, Ontario, and British Columbia began to limit submissions in situations where there was no human contact. The decrease in bat submissions in Quebec after 2008 is clear from Table 11.5. Interestingly, this change did not appear to affect the number of diagnosed cases of rabies in bats (Figure 11.3).

1953–99

Livestock Cat/Dog Bat Skunk Raccoon Coyote + Wolf

0.57 0.91 0.55 0.89 0.90 0.89

Source: compiled from CFIA data.

161

A History of Rabies Management in the Provinces and Territories

Figure 11.3: Number of rabies cases in raccoons and bats in Quebec, 1961 to 2017. The peak in raccoon incidence in 2006–2009 was related to the raccoon strain of rabies. Source: created from CFIA data.

Table 11.5  Submissions when human or domestic animal contact was reported in all species for Quebec, 1985 to 2017. Year

Total

Domestic

Bat

Raccoon

Fox

Other

Livestock

Skunk

Coy/Wlf

1985

913

585

28

60

41

115

52

27

5

1986

1,113

614

16

153

73

125

57

64

11

1987

853

583

10

40

57

93

48

19

3

1988

1,080

604

14

46

181

101

83

34

17

1989

1,037

582

18

50

154

121

67

35

10

1990

2,291

988

63

195

464

197

267

89

28

1991

2,904

1,372

38

234

562

208

312

114

64

1992

3,721

1,828

105

370

615

299

294

150

60

1993

3,036

1,691

35

243

373

274

285

95

40

1994

2,208

1,365

45

179

163

200

193

45

18

1995

1,708

1,158

25

211

77

97

97

33

10

1996

1,792

1,274

17

146

129

93

100

25

8

1997

1,764

1,317

24

92

83

105

104

28

11

1998

1,378

1,065

23

57

61

96

62

10

4

1999

1,444

1,074

33

94

70

76

73

19

5

2000

1,899

1,135

158

249

131

108

66

45

7

2001

2,002

1,208

283

215

84

125

51

24

12

2002

1,966

1,142

402

178

67

92

44

32

9 (Continued)

162

Quebec

Year

Total

Domestic

Bat

Raccoon

Fox

Other

Livestock

Skunk

Coy/Wlf

2003

2,261

1,262

719

93

47

75

44

16

5

2004

2,064

1,172

659

57

33

79

48

11

5

2005

1,999

1,154

574

98

24

79

49

10

11

2006

2,277

1,154

511

425

36

71

24

53

3

2007

2,306

1,146

661

294

24

87

48

37

9

2008

1,759

1,095

362

118

13

75

60

28

8

2009

1,581

1,033

257

94

24

77

60

25

11

2010

1,406

1,037

202

40

18

51

45

11

2

2011

1,318

943

192

57

26

46

34

15

5

2012

741

491

94

63

20

34

21

13

5

2013

410

217

84

39

12

20

32

6

0

2014

142

67

25

10

6

11

21

0

2

2015

196

80

49

22

5

15

14

7

4

2016

139

41

47

14

3

15

16

3

0

2017

151

38

62

17

7

12

11

4

0

51,859  

30,515 58.8

5,835 11.3

4,253 8.2

3,683 7.1

3,272 6.3

2,782 5.4

1,127 2.2

392 0.8

 Totals   % Total

Coy/Wlf = coyote + wolf. Source: compiled from CFIA data.

1957 (Figure 11.4). This movement paralleled the southward movement in neighbouring Ontario (see Chapter 10). By then, rabies had spilled over into the livestock and companion animal populations (Table 11.3). Rabies then reached the Gaspe Peninsula in 1965. Fox incidence waned throughout the valley then slowly built up during the early 1970s in the St Lawrence River Valley but was concentrated to the south in the eastern townships and along the Ottawa River Valley bordering Ontario (Figure 11.5). By 1982 there were only two fox cases in Quebec in the Vaudreuil-Soulanges area, a Quebec municipality at the eastern tip of Ontario (Figure 11.5). Rabies cases remained low until an outbreak on the Ontario side of the Ottawa River Valley spilled over into Quebec and then moved north east along the St Lawrence River Valley (Figure 11.6) as it did in the 1960s. This epizootic died out in southern Quebec in 2000. We speculate that the success of the control efforts in eastern Ontario eliminated a major source of infection and that the eastern temperate forest area of the St Lawrence River Valley (Figure 11.1) is not a large enough area to allow rabies to persist. Lagacé (1998) provides a detailed examination of rabies in Quebec from 1958 to 1997. Of the 6618 reported cases in all animals from 1953 onwards, only 133 were located in the north (Nunavik; see Chapter 14d). This is likely not a

No significant changes in reporting cases over time occurred in other species. The temporal patterns of submissions for all other species (Table 11.5) were significantly correlated (p < .05) to each other and followed the patterns of incidence. As mentioned, they did vary in reporting efficiency. For example, less than 0.5% of other submissions proved positive while almost 49% of all fox submissions were diagnosed positive. Typically, a higher percentage of wildlife submissions proved positive than did submissions of domestic animals. As of 1 April 2014, the federal government ended collection and submission of animal specimens for rabies testing by CFIA. They are now the responsibility of the provincial and territorial government agencies. Criteria used to submit samples were adjusted with these changes, which may explain the decrease in the total number of submissions to CFIA between 2014 and 2017 (Table 11.5).

Fox Rabies in Southern Quebec Fox rabies entered Quebec through Nunavik from the Arctic, Nunavut, and the Northwest Territories after 1947. Rabies moved rapidly south along the coasts of Hudson Bay and James Bay and then through Rouyn-Noranda, apparently following the valley of the Ottawa River, reaching Gatineau by

163

A History of Rabies Management in the Provinces and Territories

Figure 11.4: Invasion of arctic fox rabies in Quebec, 1954 to 1965. Source: created from CFIA data.

true reflection of incidence in the north given the small number of observers but it illustrates why, for practical purposes, control efforts have focused on southern Quebec. While no data exist for viral isolates during the 1953– 1999 years, rabies in foxes was likely the arctic fox strain. The same strain probably affected the other terrestrial species and, therefore, the virus in outbreaks in skunks and raccoons was likely the arctic fox variant. Viral isolates collected on foxes and analysed since 2000 (see Chapter 29) are all arctic fox strain. In 1964 a girl was bitten by a rabid skunk in Huntington and died a month after infection (see Chapter 3b, Case 33). The variant was not typed but was most likely a fox variant virus. A 2002 raccoon sample was shown to be big brown bat rabies variant (S. Nadin-Davis, personal communication, 25 June 2019). As previously mentioned, it appears that the arctic fox strain has almost disappeared from southern Quebec presumably because of the efforts in Ontario to control fox rabies and the joint Ontario-Quebec control program in the Ottawa Valley in the1990s. Since 2000, only 62 cases of fox rabies have occurred in the province. Thirty-five of those have been north of the 55th parallel (in Nunavik) in red and arctic foxes, 19 and 16, respectively. The remaining 27 were red foxes, with

25 found in mid-northern latitudes, of which four were found near the border with Labrador coincident with an outbreak in that area. Only two cases were reported south of the St Lawrence River (Saint-Odilon and Saint-Jean-surRichelieu). Recent work by Nadin-Davis (see Chapter 29) strongly suggests that the strain of the arctic fox virus (N5) circulating in Quebec since 2000 is similar to the current strain circulating in the Arctic that evolved after the initial invasion of rabies in the 1950s. With the decline in fox rabies in the south has come a decline in domestic animal cases, and no reports of rabies in livestock since 2004 (Table 11.3).

Bat Rabies Eight species of bats are found in Quebec (Table 11.6), and the first case of bat rabies was diagnosed in Quebec in 1968. Between 1968 and 1984, CFIA did not require recording of species, and information on species was limited. Since 1985, the big brown bat has been the bat species most submitted (Table 11.7). The last recorded human death in Quebec in 2000 was attributed to a bat in the same room as the victim, but the bat was captured and released outside and, therefore, was not tested. However, the virus variant

164

Quebec

Figure 11.5: Fox rabies incidence in Quebec in 1972. The dot in the Vaudreuil-Soulanges area represents the location of the two cases of fox rabies in Quebec in 1982. Source: created from CFIA data.

isolated from the human patient’s saliva was similar to the variant that circulates in the silver-haired bat (Elmgren et al., 2002; see Chapter 3b, Case 39).

and New York State, the Quebec government in 1995 set up a steering management committee coordinated by the Ministry of Health. Under this authority, the Scientific Committee (SC) was formed with the mandate of proposing strategies to prevent the entry of raccoon rabies into Quebec. The SC was composed of individuals from different disciplines and from different ministries of the Quebec government, including the Ministère de l’Environnement et de la Faune (MEF), Ministère de l’Agriculture, des Pêcheries et de l’Alimentation du Québec (MAPAQ), Ministère de la

Raccoon Rabies In the 1990s Quebec experienced an epizootic of fox rabies while raccoon rabies was advancing north along the eastern US seaboard. With that threat, especially from Vermont

165

A History of Rabies Management in the Provinces and Territories

Figure 11.6: Fox rabies in Quebec, 1991. Rabies spilled over from the Ontario side of the Ottawa River Valley and then spread along the St Lawrence River Valley. There was another intrusion from the northeast, near Labrador. Source: created from CFIA data.

Santé et des Services sociaux (MSSS), Agriculture and Food Canada, and the Université de Montréal (faculté de médecine vétérinaire). A report was completed by the SC (Comité Scientifique, 1996) that reviewed the epizootic in the eastern United States and established the costs of an epizootic in Quebec based on the numbers of rabies cases generated by the epizootic in Massachusetts, New Jersey, New York, Maryland, and Pennsylvania. This report noted that an epizootic in raccoons could result in several hundred cases each year, and this would have a major impact on the costs and activities of various government agencies and the public. In 1996 the four last cases nearest to Quebec were in Clinton

County in New York State, about 60 kilometres from the border. Several scenarios were developed to predict the entry of rabies into Quebec, assuming that rabies control and surveillance programs were maintained in the United States. One of those was considered the most realistic: rabies would be present in Quebec in 1997 and would reach Montreal in 1999. The speed of spread was estimated at 40 kilometres per year (Comité Scientifique, 1996). The SC further recommended that the government of Quebec participate in the US effort to eliminate raccoon rabies. The government of Quebec received financial support from CFIA to assist the oral rabies vaccination (ORV)

166

Quebec

Table 11.7 Rabies cases in Quebec by species of bats, 1985 to 2017. One bat was identified as a Keen’s bat (Myotis keenii) reported in British Columbia. It is not known whether this was a classification error.

Table 11.6  Species of bats reported in Quebec.

Reported Species Bats in Quebec Big brown bat Eastern red bat Eastern small-footed bat Hoary bat Little brown bat Northern long-eared bat Silver-haired bat Tricoloured bat (previously eastern pipistrelle)

Scientific Name

Submissions CFIA Diagnosed Code Rabies-Positive

Eptesicus fuscus Lasiurus borealis

BBB REB

yes yes

Myotis leibii

ESB

no

Lasiurus cinereus Myotis lucifugus Myotis septentrionalis Lasionycteris noctivagans

HRB LBB

Perimyotis subflavus

Year

Total BBB LBB HRB EPB REB SHB KEB LEB BAT

1985

1

1

0

0

0

0

0

0

0

0

1986

1

0

1

0

0

0

0

0

0

0

yes yes

1988

2

2

0

0

0

0

0

0

0

0

LEB

yes

1989

1

1

0

0

0

0

0

0

0

0

SHB

yes

1990

1

1

0

0

0

0

0

0

0

0

1991

5

4

0

0

0

0

0

1

0

0

1992

7

7

0

0

0

0

0

0

0

0

1993

1

1

0

0

0

0

0

0

0

0

1994

2

2

0

0

0

0

0

0

0

0

1995

5

5

0

0

0

0

0

0

0

0

1996

1

1

0

0

0

0

0

0

0

0

1997

2

2

0

0

0

0

0

0

0

0

1999

1

1

0

0

0

0

0

0

0

0

2000

7

6

0

0

1

0

0

0

0

0

2001

8

6

0

1

1

0

0

0

0

0

2002

19

17

1

0

0

0

1

0

0

0

2003

13

8

1

0

0

2

0

0

1

1

2004

7

7

0

0

0

0

0

0

0

0

2005

12

9

1

2

0

0

0

0

0

0

2006

8

8

0

0

0

0

0

0

0

0

2007

15

14

1

0

0

0

0

0

0

0

2008

5

5

0

0

0

0

0

0

0

0

2009

9

9

0

0

0

0

0

0

0

0

2010

7

6

0

1

0

0

0

0

0

0

2011

9

8

1

0

0

0

0

0

0

0

2012

2

2

0

0

0

0

0

0

0

0

2013

14

14

0

0

0

0

0

0

0

0

2014

6

4

0

0

0

0

0

0

0

2

2015

13

12

0

0

0

0

0

0

0

1

2016

5

4

0

1

0

0

0

0

0

0

2017

8

6

0

0

0

0

1

0

0

1

197 173

6

5

2

2

2

1

1

5

3.0

2.5

1.0

1.0

1.0

0.5

EPB

yes

campaign in northern Vermont east of Lake Champlain between 1997 and 2005, and subsequently transferred $1,210,000 ($150,000 in 1997, $260,000 in 2000, $600,000 between 2002 and 2005, and $100,000 in each of 1998 and 1999) to the diagnostic laboratory of the College of Veterinary Medicine of the University of Cornell (Messier & Lambert, 2006). The program was under the direction of Drs Donald Lein and Laura Bigler who were responsible for the raccoon vaccination program in Vermont. In 1999 rabies cases were detected in Vermont within 25 kilometres of the Quebec border (Messier & Lambert, 2006). This triggered the first aerial vaccination campaign in the southern part of Quebec, along the border with Vermont. The goal was to build a vaccination barrier (20 kilometres from south to north, and 60 kilometres from east to west) along the border to prevent the northwards spread of the virus through valleys of the Appalachian Mountains. In June 2000 four cases were reported in Vermont within 26  kilometres of the Quebec border. From 2000 onwards, a vaccination barrier created by using air-dropped baits was maintained in Quebec along the Vermont border, but it was extended both south to north and west to east. During those years, vaccinia rabies glycoprotein recombinant vaccine (RABORAL V-RG) baits (fish polymer) were used at a bait density of 75 baits/km2. These campaigns were carried out with the collaboration of the Ontario Ministry of Natural Resources (OMNR) and the team from Cornell University. In 1999 the SC initiated an emergency plan with the goal of rabies elimination in Quebec (Comité Scientifique, 1999). This plan included a point infection control (PIC) strategy based on the Ontario model described in Chapter 10. The plan consisted of a population reduction zone of trapped

 Total   % Total

 

87.8

0.5 2.5

BBB = big brown bat, LBB = little brown bat, HRB = hoary bat, EPB = Eastern pipistrelle/tricoloured bat, REB = eastern red bat, SHB = silver-haired bat, KEB = Keen’s bat, LEB = northern longeared bat, BAT = unidentified bat species. Source: compiled from CFIA data.

167

A History of Rabies Management in the Provinces and Territories

raccoons and skunks in a five-kilometre radius from the index case, surrounded by a trap-vaccinate-release (TVR) zone in another five-kilometre radius. A further vaccination barrier using air-dropped baits could also be added surrounding the TVR zone, typically at a radius of 30 kilometres. A simulation exercise in the field following the written plan was performed in 2003; the government of Quebec felt ready to react promptly if a rabid animal (raccoon strain) was detected in Quebec. Furthermore, in 2000, Quebec began active surveillance along its border with New York and Vermont, investigating road kills and animals with suspected clinical signs of rabies. These efforts were coordinated by the MSSS in collaboration with the Société de la faune et des parcs (FAPAQ), MAPAQ, CFIA, and regional public health agencies (see Chapter 24a). With the first case of raccoon rabies in 2006, the SC also initiated a program of enhanced surveillance that included gathering and collating information from a wide variety of sources, including specimens from raccoon rabies control operations (e.g., depopulation, TVR), road

mortalities, commercial fur harvests, and citizen notifications, and samples submitted from wildlife zoos, animal rehabilitation centres, and control of nuisance animals. This program is detailed in Chapter 24a.

Management and Control of Raccoon Rabies in Quebec Raccoon rabies entered Quebec in 2006 and was controlled by 2009. The extent of the epizootic and the overall surveillance area are shown in Figure 11.7. The remainder of this section details the campaign that eliminated raccoon rabies in Quebec. FIRST CASE AND THE EMERGENCY PLAN IS ACTIONED, 2006

A crucial part of detecting the first case of rabies in Quebec was the enhanced surveillance along the US border as noted in the previous section. On 31 May 2006, a CFIA personnel road patrol picked up a road kill raccoon in

Figure 11.7: Raccoon rabies cases in Quebec, 2006 to 2009. Source: created from Scientific Committee data.

168

Quebec

Figure 11.8: Emergency response actions in 2006, highlighting the four rabies cases (black dots), the reduction zones (dark continuous contours), the trap-vaccinate-release (TVR) zones (dotted contours), and the aerial oral rabies vaccination (ORV) area (filled grey). Since only 4.2 kilometres separated the two first rabies cases, the reduction and TVR zones overlapped greatly, creating several subzones. The actions conducted in each sub-zone during phase 1 in June and phase 2 in August are shown in bold. For example, “RED 1/TVR 2” indicates that reduction was conducted in phase 1 and TVR in phase 2, whereas “TVR 2” indicates that only TVR was conducted during the phase 2 in August. Source: adapted from Canac-Marquis et al., 2007.

Dunham (Montérégie region), located about 10 kilometres north of the northern Vermont border, and sent it for testing at CFIA laboratory in Nepean, Ontario. This specimen tested positive (2 June) and was the first positive raccoon strain case in Quebec. It was also the first terrestrial rabid animal in the Montérégie region since 1997, and the closest case detected in Vermont was located 15 kilometres from the border in 1999. After the discovery of a first case in Quebec, Vermont enhanced its own surveillance in the northeast part of Lake Champlain, and from late October 2006 seven rabies cases were detected (five raccoons, two skunks), a few at less than 10 kilometres from the border of Quebec. Between November 2006 and the end of February 2007, there were 16 positive cases in Vermont, less than 25 kilometres from the border. One of those was located less than five kilometres from Quebec. The elimination emergency plan (i.e., a PIC operation) was put into action 7 June 2006. Two other cases were discovered between June and mid-September 2006, and two PICs and one additional TVR operation in the city

limits of Cowansville were performed (Figure 11.8). On average, each operation lasted 15 days, 10 of which were dedicated to trapping; between 11 and 104 people were involved in the operations; and 7225 animals were trapped. The SC also distributed vaccine baits (RABORAL V-RG coated-sachet baits) by aircraft around the PIC zones (about 30 kilometres around the first two PICs) in August 2006 (Figure 11.8). A total of 120,000 vaccine baits were dropped over an area of 2271 km2 at a target density of 70 baits/km2, resulting in an overall density of 53 baits/km2. The target density is the desired density for good habitat but the aircraft navigator uses a standard protocol to stop baiting in areas with low animal density, such as water bodies or mountainous areas, so that overall bait density is lower than the target density for a vaccination zone. In November a citizen reported another dead raccoon, which was diagnosed as rabid. No other action was taken at that time of the year. To coordinate the different partners and agency groups involved in raccoon rabies management, a decisional and

169

A History of Rabies Management in the Provinces and Territories

an operational structure was put into place in 2006. This structure was composed of an Interministerial Committee (IC) and operational subcommittees (control and communication) grouping scientific experts, and an organizational representative. The SC created in the 1990s continued its activities and now provides recommendations on raccoon rabies management to the IC. A surveillance committee was added in 2007. A meeting was planned and led by Quebec Health (MSSS) officials on 8 December 2006, with representatives from OMNR, New Brunswick Health, the US Department of Agriculture (USDA), Animal and Plant Health Inspection Service, and US Wildlife Services to develop additional contingency actions for enhanced surveillance for 2007, TVR in the spring in Vermont, ORV in late summer, and close coordination between Vermont and Quebec.

control efforts would be mainly based on ORV. A PIC, however, would be considered around a detected case thought to be an outlier (located far spatially from the epizootic). At the end of 2007, the SC concluded that the ultimate goal of elimination was still considered realistic but it could take up to five years to eliminate raccoon rabies from Quebec territory (based on the experience of Ontario and New Brunswick with raccoon rabies). In April 2007, a report was addressed to the Conseil des ministres du Gouvernement du Québec to ensure a budget for the next three years. INTRODUCTION OF HAND BAITING, 2008

In 2008, 32 more rabid cases in raccoons and skunks were diagnosed. Close to one million baits were aerially distributed during August 2008 over 9430 km2 (702,000 ONRAB at target densities of 75 and 150 baits/km2 and overall density of 82 and 108 baits/km2; and 220,000 RABORAL V-RG coated-sachet baits at target densities of 100 and 150 baits/ km2 and overall densities of 87 and 112 baits/km2). Targeted hand baiting was done in certain rural areas in the spring and summer 2008 (1060 km2) focusing on raccoon and skunk habitats. Hand baiting was performed by experienced professional local raccoon trappers familiar with prime habitat for raccoons and skunks. ONRAB baits were also dropped using a helicopter in forest patches around cities on the south shore of Montreal (60,000 baits over 272 km2). From 2008 onwards, the IC was under the leadership of MRNF, and the presidency of the SC under a professor of the Faculty of Veterinary Medicine at Université de Montréal. The SC included biologists, epidemiologists, veterinarians, physicians, and animal wildlife technicians. The committee had clear mandates: (1) advise the IC on the control program, including surveillance, vaccination, and communication; (2) follow the epizootic in the northern US states and in neighbouring the provinces (Ontario and New Brunswick); and (3) conduct applied research to improve the vaccination and surveillance programs and communication methods. Furthermore, the SC developed an emergency plan for the urban Montreal area, should a case be discovered there. In 2008 the MSSS requested a cost-benefit study for the SC (see “A Cost-Benefit Study”), and an integrated web database was developed to support the surveillance program and its stakeholders (see Chapter 24a).

PICS AND THE INTRODUCTION OF ONRAB BAITS, 2007

On 13 May 2007 another rabid raccoon was discovered through passive surveillance in St-Armand, located a few kilometres from the Vermont border. This finding led to a massive response between 10 June and 3 September, which included PIC, bait drops (RABORAL VR-G and ONRAB) and the involvement of many people (30 to 90) from different organizations: Ministère des Ressources naturelles et de la Faune (MRNF), MAPAQ, MSSS, CFIA, the Fédération des Trappeurs Gestionnaires du Québec, OMNR, New Brunswick Health, and the United States Department of Agriculture. The PICs covered about 1800 km2 and were performed in four consecutive phases; 5074 raccoons and skunks were vaccinated intramuscularly, and 7642 animals were euthanized (Guérin et  al., 2008). ORV operations consisted of 330,000 RABORAL V-RG coated-sachet baits distributed aerially over 3900 km2 (target densities of 75, 125, and 130 baits/km2) and 120,000 ONRAB baits over 1000 km2 (target density of 150 baits/km2 and overall density of 120 baits/km2) (Guérin et al., 2008). Between 15 May and 9 July, 34 rabies cases were diagnosed, for a total of 66 before the end of December 2007. No cases were detected west of the Richelieu River, except for a red fox (testing at CFIA showed raccoon strain) at Laprairie (15.4 kilometres from Montreal) in November 2007. No emergency action was taken then given the time of year. No species, other than raccoon and skunk, besides that fox, were diagnosed with raccoon rabies in 2007. The SC realized that rabies elimination based primarily on PIC operations was becoming unrealistic, logistically and economically, given that the infected zone was more than 1500 km2. Consequently, the SC decided that any future

REFINING AERIAL AND HAND BAITING, 2009

In May 2009 two rabid skunks were discovered via passive surveillance, north of Champlain Lake in Venise in Quebec. At the same time, SC started hand-baiting operations in

170

Quebec

areas where there were positive cases in 2008 and on the shore of Lake Memphremagog (Figure 11.9). Professional trappers distributed ONRAB baits in preferred raccoon and skunk habitats (target density of 150 baits/km2 and overall bait density of 30 baits/km2). Aerial baiting was conducted between August 17 and 22, with 946,400 ONRAB baits dropped over 11,485 km2 of Montérégie and Estrie regions (target and estimated overall density of 150 baits/km2 and 83 baits/km2, respectively). At the end of August, urban areas and agricultural areas near urban settlements on the south shore of Montreal were also hand baited (overall density of 30 to 65 baits/km2) because they were considered ideal habitat for raccoons and skunks. The year 2009 was a turning point in the ORV campaigns as SC started to use hand baiting on a larger scale (more than 3100 km2), modifying the aerial distribution of baits to focus on raccoon and skunk habitat (see “Movements and Habitat Use of Raccoons and Skunks in Fragmented Agricultural Landscapes”) and using only ONRAB baits. During that same period, the surveillance system was redesigned according to the risk of detecting a rabid case in the sampling zones (Figure 24a.2 in Chapter 24a), since the number of cases seemed to decrease greatly, and the SC wanted greater confidence in its capacity to detect a case. The whole surveillance area was then subdivided into 50 km2 hexagonal cells, with each cell categorized according the level of risk (see Chapter 24a). No other rabid animals were found that year.

August in areas judged as potential ports of entry for ­rabies in Quebec, such as the valleys connecting Canada and the United States on a south–north axis (Figure 11.9). The valleys were considered travel corridors and good raccoon habitat as they connected with high-risk areas located along the border with Vermont and New York. In 2006, the SC goal was to stop vaccination after two years of being free of rabies. However, in 2011, considering the infection pressure from the United States was still an important factor within a zone of 80 kilometres south of the Quebec border, the SC concluded that it was impossible to stop vaccination interventions or the enhanced surveillance program in Quebec, if Quebec wanted to stay free of the disease. The SC had to convince the government of Quebec to continue its efforts until the risk of rabies reintroduction into Quebec is significanly reduced along bordering US states. In 2015 an outbreak of raccoon rabies was diagnosed in Franklin County, New York State, with 15 cases within 15 kilometres of Quebec. On 29 May 2015 a rabid raccoon was confirmed in the Quebec portion of the Akwesasne First Nation reserve near Franklin County, where no vaccination campaign had ever been conducted. In response to the outbreak, surveillance was intensified and ORV baiting adjusted to increase raccoon immunity along the border. No other cases were discovered in Quebec and the SC ensured that surveillance and control operations were annually adapted to the current epidemiological situation in Quebec and neighbouring states. In 2017 the SC started to recommend a reduction in the extent of the ORV zone (Figure 11.9). These changes were considered possible because raccoon rabies variant cases decreased in 2016 in northern New York, Vermont, and New Hampshire, likely as a result of ONRAB baits used in these states (Gilbert et al., 2018).

OPTIMIZATION FROM 2010 ONWARDS

Since 2010 the SC has worked on optimizing surveillance, vaccination, and communication strategies to keep Quebec free from raccoon rabies. This has included patrolling roads in high-risk zones; communicating with the public and emphasizing their important role helping to detect suspect rabid animals and reporting them; and refining vaccination strategies, as noted in the previous sections, in an attempt to increase the seroprevalence of the barrier along the US border to 65% (barrier of 10 kilometres south to north), and around 50% north of this high-risk area (40  kilometres south to north) (see “Fall Serological Studies Post-Baiting”). The annual recurrent vaccination operations have been mostly aerial in the forest dominant areas and hand baiting in the agricultural part of the landscape (Figure 11.9). In fact, the SC decided that areas of good habitat for raccoons and skunks in which the plane off-time was more than 65% would be more ­efficiently covered by hand baiting by professional trappers. Moreover, hand baiting would also be conducted in spring and in

FALL SEROLOGICAL STUDIES POST-BAITING

Every year after 2007, about six to eight weeks after the last day of the ORV campaign in August, a post-baiting serological study (competitive enzyme-linked immunosorbent assay [c-ELISA] positive threshold of 25% inhibition and 26% inhibition for raccoon and skunks sera, respectively; CFIA, 2009, Fehlner-Gardiner et al., 2012) was conducted to evaluate the protection associated with the vaccinated barrier and any subsequent risk to follow. Based on the results, the SC adjusted the baiting strategy as required. Sampling plots were delineated according to yearly defined objectives and criteria set by the SC. Up to 164 raccoons were trapped by sampling plot, for a total of 277 to 697 individuals captured and tested for a given year. The

171

A History of Rabies Management in the Provinces and Territories

a

b

c

d

Figure 11.9: Oral rabies vaccination (ORV) zones in (a) 2009, (b) 2010, (c) 2011, and (d) 2017 in southern Quebec. The aerial baited areas are highlighted and the hand baited areas are hashed. ONRAB baits were distributed in preferred raccoon and skunk habitat for hand baiting, and in forest patches and adjacent edges for aerial vaccination. From 2009 to 2017, hand baiting zones were extended in dominant agricultural areas, and overall bait densities were adjusted to raccoon abundance (see the section “Raccoon and Skunk Abundance and Baiting Densities”). The ORV zone was reduced in 2017 as rabies cases in the northeastern United States decreased. Overall bait densities shown represent the total number of baits used divided by the area of the baited zones. Source: authors

results (the percentage of raccoons positive to the c-ELISA) varied over time and according to the zone sampled but ranged between 35% and 56% for raccoons and between 11% and 17% for skunks (Mainguy et al., 2012). Multiple factors influenced field immunogenicity in raccoons; the probability of being seropositive increased with age, bait density, and number of previous ORV campaigns, whereas it decreased with raccoon abundance and proportion of residential areas near each capture (Mainguy et al., 2012). Nevertheless, the aim was 60%–65% immunity for raccoons in high risk zones just north of the New York and Vermont borders. The SC stopped monitoring serology in skunks after 2010 because it was unable to explain the low seroprevalence (Mainguy et al., 2012) and wanted to simplify the post-ORV study, as skunks were in relatively low abundance compared to raccoons in southern Quebec (see

“Raccoon and Skunk Abundance and Baiting Densities”). In addition to information on herd immunity, post-ORV studies provided novel insights into the population dynamics of raccoons and skunks. Age-structure analysis indicated that juveniles composed between 42% and 51% of trapped raccoons, and 61% and 68% of trapped skunks, respectively (Mainguy et al., 2012). These results, combined with the work of Jolicoeur et al. (2011) on raccoon reproduction, supported the need to implement vaccination at least once per year. TOWARDS A MORE EFFICIENT AND SUSTAINABLE PROGRAM

To adapt vaccination strategies from Ontario and the United States to the Quebec landscape, many research projects were initiated from 2008 to 2017.

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in the interior of large agricultural fields. Instead, the SC decided to concentrate on aerial baiting only in forested patches and a 30-metre-wide strip on their edges. This was also supported by field experiments showing contact rates of wildlife with ONRAB baits were higher in forested patches than in crop fields (Boyer et al., 2011). No baiting would be conducted in areas with elevations higher than 400 metres. This change in the bait distribution lowered the vaccine budget costs significantly with an estimated 604,500 fewer baits needed. However, results on large-scale movements of raccoons and skunks confirmed that no discrete barrier could limit rabies spread into the Montérégie and Estrie regions of Quebec nor from the United States. This confirmed the need to conduct large-scale ORV campaigns on both sides of the Richelieu River and along the 250 kilometres of the Unites States–Quebec border.

A Cost-Benefit Study

One of the first studies undertaken was a cost-benefit study of the control program in Quebec (Shwiff et  al., 2013). The Ontario rabies model (ORM), a stochastic simulation model (see Chapter 10) was used to determine the potential spread of raccoon rabies from the 2006 index case, and animal testing, human exposure investigations, and incidence rates of human post-exposure prophylaxis (PEP) were recorded. The potential savings from reduced numbers of animals tested, human exposure investigations, and human PEP treatments were calculated, which ranged from C$47 million to C$53 million. Economic efficiency was determined for approximately half of the modelled scenarios, with the greatest benefit-cost ratios resulting from reduced future control program costs.

Movements and Habitat Use of Raccoons and Skunks in Fragmented Agricultural Landscapes

Raccoon and Skunk Abundance and Baiting Densities

Several approaches were used to understand movements and habitat use by raccoons and striped skunks. First, the SC monitored 54 raccoons and 12 skunks with global positioning system (GPS) collars to assess habitat selection within their seasonal home range. Overall, this study showed that during the maturation stage of corn fields (1 August to 15 October), raccoons modified their use of the corn fields depending on variations in density of raccoons and corn-forest edge, whereas striped skunks mainly used agricultural corridors (a 10-metre buffer around corn and other crop fields). According to preliminary results, raccoons frequently used forests during this period as 65% of GPS locations were recorded in this habitat during the day versus 35% at night (Tardy et  al., 2014.) In addition to animal monitoring, the SC carried out several studies that used genetic relatedness to determine how landscape features influenced raccoons’ and skunks’ dispersal (Côté et al., 2012; Rioux Paquette et al., 2014; Talbot et al., 2012). The results from genetic analyses corroborated the telemetry study showing that edges are important movement corridors (Rioux Paquette et  al., 2014; Talbot et al., 2014). Moreover, the results showed that rivers and highways appeared to be a weak barrier to gene flow of raccoons and skunks, suggesting little impact on their movements; therefore, they were unlikely to prevent rabies spread (Côté et al., 2012; Rioux Paquette et al., 2014; Talbot et al., 2012). These findings were supported by animal recaptures during post-ORV studies. These studies provided important insights to developing appropriate baiting strategies for agriculturally fragmented landscapes. They confirmed that baiting was not required

Using data collected during the control operations and post-ORV studies, the population density ranged between 6 and 18 raccoons/km2 and 1 to 2 skunks/km2 in areas along the vaccinated barrier (Jolicoeur et  al., 2009). The highest raccoon counts were in areas where forest patches and corn fields were highly interspersed (Houle et  al., 2011). Based on these results, it became evident that baiting densities could not be homogenous throughout the more than 10,000 km2 vaccination zone and needed to be adjusted to raccoon densities in the target areas. Specifically, aerial baiting densities were defined according to area specific raccoon densities: low (fewer than 5 raccoons/km2), medium (5 to 10 raccoons/km2), and high density (more than 10 raccoons/km2), which correspond respectively to overall bait densities of 75, 100, and 125 baits/km2 and to target densities of 105, 145, and 250 baits/km2 (Figure 11.9) (Mainguy & Canac-Marquis, 2011). Hand-baited overall densities were established between 50 and 70/km2 because baits in these cases were positioned with much more precision on the ground (Figure 11.9). By linking bait density to raccoon abundance, the SC developed a cost-effective control program with reduced costs (number of vaccine used) while limiting the probability of further spread.

Assays Using ONRAB Baits

Since the first use of ONRAB baits in Quebec during 2007, the SC has been involved in several assays to evaluate bait effectiveness for the control of rabies in raccoons. From 2007 to 2010 and later in 2015 and 2016, ONRAB baits

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used during the ORV campaigns were tested by CFIA to assess vaccine potency. Results confirmed that vaccine titres were stable from days 0 to 35 after distribution in the field. In 2008 field comparison between ONRAB baits in Quebec and RABORAL VR-G in the state of Vermont showed that the percentage of seropositive raccoons was greater using ONRAB (51%) than VR-G (38%) (Mainguy et  al., 2013). In 2009 a field experiment using camera traps showed that raccoons accounted for most of the contacts with the baits compared to the other 13 wildlife species also observed (Boyer et al., 2011). Preliminary results from cafeteria trials using camera traps deployed in 2017 showed that raccoon preferred to consume ONRAB (54% of the time) over other offered sources of food such as wild grape (23%) and corn (20%). These findings, in addition to other work conducted in Ontario, confirmed that the ONRAB vaccine bait is an appropriate tool to control raccoon rabies.

simulated raccoons had the highest contact rate in forests, anthropogenic areas, and agricultural corridors, suggesting high heterogeneity in the pathways of rabies spread. These modelling studies show that ongoing efforts to prevent the entry of raccoon rabies from the United States must take into account the complex interplay between host density, landscape composition, and functional connectivity within the vaccine barrier. Control operations must be intensive enough to ensure die-out rather than create conditions that would allow the disease to persist. ELEMENTS OF SUCCESS

Quebec has been free of raccoon rabies since 2009, with the exception of one case in 2015. Elimination in a relatively short period (four years) was likely due to the following factors. First, the SC developed strong teamwork. Second, the composition of the expert members on the SC was stable, and their dedication contributed greatly to that success. This structure has also helped to defend the program. Third, the SC had great collaboration with researchers from many institutions including OMNRF, CFIA, USDA, and Dr Bigler from Cornell in the initial phases of its work. Fourth, the leadership taken by the University of Montreal in directing the SC added credibility to the recommendations as the university was seen as a neutral partner. Fifth, the program had centralized funding. Sixth, the SC incorporated resources, advice, and technological developments, such as ONRAB, from other jurisdictions. Seventh, a permanent organizational structure (described in the introduction to this section of the chapter) gave the Quebec government ownership of the program, which allowed integrated and rapid planning and coordinated research on a battlefield small enough to permit intensive and concentrated efforts. Quebec has been able to fine-tune its unique control and surveillance techniques and plans based on its specificities in terms of landscape, raccoon population distribution, and social context. Finally, dedicated personnel and very knowledgeable field technicians and trappers were involved in surveillance and control activities. The SC remained together through all those years. During each year, the members met and discussed all aspects of the program, and at the end of each year, they discussed the results of the past season (surveillance data, control operations, and serological data). Surveillance and vaccination strategies for the next year were then developed at those meetings to submit to the IC for discussion and approval. The plan was always developed considering the epidemiological situation in the United States and in neighbouring provinces, the type of vaccination intervention, past serological results, the quality of the surveillance

Modelling Studies

Several studies using ORM have been performed for different purposes. At first, the ORM was used to model an epizootic of rabies in raccoons without vaccination, and then with a control program, to estimate the human population at risk in the study zone for the cost-benefit analysis (Shwiff et al., 2013). Simulations were also used to estimate the risk of potential corridors providing raccoon rabies entry from Vermont into Quebec. The location of the rabies cases in Vermont and the results of those simulations influenced where, when and how baits were to be distributed in Quebec. Another study examined the effectiveness of vaccination barriers against the spread of rabies in environments with varying habitat quality and landscape structure (Rees et al., 2011, 2013). As expected, in homogenous, high-quality landscapes, increasing barrier width together with higher levels of achieved immunity (more than 60%) reduced rabies incidence and decreased the probability of breaching the barrier. On the other hand, these experiments demonstrated that the heterogeneous spatial distribution of hosts has a strong confounding effect on the efficacy of vaccination. For example, in landscapes with overall poor habitat but with large patches of good habitat, vaccination at low and intermediate levels was counterproductive because the outcome shifted from burnout of rabies to persistence, similar to observations by Smith and Harris (1991) in their modelling of fox rabies in urban areas in Britain. Characterizing movement behaviours of radio-collared raccoons and integrating those behaviours in an individual-based model was also useful for understanding rabies spread in complex landscape (Tardy et al., 2018). This study also demonstrated that

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system, the immunological barrier in place in Quebec, the risk to public health, and potential budget constraints.

that will minimize the costs without compromising its efficiency. Future work will be to adjust surveillance and control operations in response to decreasing cases in New York, Vermont, and New Hampshire (Gilbert et al., 2018), and the eventual southwards displacement of the vaccine barrier in the United States. A new challenge is to have strategies in place for early detection through continued surveillance and prompt response to any rabid animals that could bypass vaccination zones and be introduced into Quebec by long-distance translocation. This is an important issue considering that the raccoon rabies outbreak in Hamilton, Ontario, that entered in 2015 was likely caused by a long-distance displacement of a raccoon (Trewby et  al., 2017; Lobo et  al., 2018). Strong collaborative work with neighbouring US states and provinces in pushing the epidemic front to the south is essential to prevent any northward return (Stevenson et al., 2016). Keeping knowledgeable resource people on the SC to maintain scientific expertise is also necessary to address any emerging issues regarding rabies. The SC has enlarged its mandate to arctic fox rabies to investigate new threats, such as the potential southward movement of arctic foxes cases. This will allow the SC to be a reference group for the Quebec government wherever the threat of rabies arises in Quebec.

The Future Challenges Associated with Success and the Duration of the Program With the elimination of raccoon strain from Quebec in four years (2006–2009), one of the greatest challenges is keeping citizens interested enough to report potential cases of rabies. Surveillance and readiness to resume field control operations after a positive case is identified are the cornerstones of a good control program, its evaluation through time, and the provision of information to provide risk evaluation for public health. Therefore, a sustainable program needs an appropriate and available budget, up-to-date communications, and diverse strategies to accommodate future threats. Furthermore, when a program extends over several years, it is highly probable that it will have to deal with government budget cuts. This implies that the SC will have to continue to review its strategies in order to have a rabies management program

Acknowledgments The authors would like to thank all the members of the scientific, operational, surveillance, communication, and interministerial committees who have worked jointly since 1996 to eliminate rabies in Quebec. With the expertise of all, teamwork made it possible. The authors recognize the help from the OMNR rabies unit, Artemis, New Brunswick DNR, and Dennis Slate and Martha Dunbar from the USDA, and thank Laura Bigler and Donald Lein from Cornell University for their great collaboration. In addition, several people must be mentioned for their time and involvement: Horacio Arruda (Directeur national de la santé publique, MSSS), Danielle Auger (MSSS, past member of the Interministerial Committee), Rhéaume Courtois (MRNF, retired, former president of the Interministerial Committee), Alain Messier (MSSS, who acted as coordinator of the Scientific Committee for several years), former project managers Julien Mainguy (MRNF) and Julie Picard (Agence de la santé publique de la Montérégie), and former members of the scientific committee: Hélène Bergeron (MAPAQ), Nathalie Côté (MAPAQ), Colette Gaulin (MSSS), René Lafond (MEF, retired), Fréderick Lelièvre (Ministère des Forêts de la Faune et des Parcs, MFFP), Suzanne Ménard (Direction de la santé publique de l’Estrie), Erin Rees (former researcher on the scientific committee), Gilles Rivard (CFIA, retired), Geneviève Toupin (CFIA), and Chantal Vincent (MAPAQ). We are also grateful to Kathleen Brown (Centre québécois sur la santé des animaux sauvages, Université de Montréal), Jacques Dancosse (Biodôme de Montréal), Christine Fehlner-Gardiner (CFIA), Hélène Jolicoeur (MRNF, retired), Marianne Gagnier (MFFP), Patrick Leighton (Université de Montréal), Isabelle Picard (MAPAQ), and Guillaume Tremblay (MFFP) for important contributions to Quebec’s rabies program. A special recognition goes to Louise Lambert (Institut national de santé publique du Québec), who has contributed significantly to the scientific committee since 1995, and to the trappers for their professionalism, as well as to wildlife and animal health technicians, biologists, veterinarians, and wildlife protection officers for their past and continuing work in rabies management in Quebec. Finally, the authors thank researchers and students from Université de Montréal, Université de Sherbrooke, and Université Laval, as well as the personnel of the OMRNF who contributed significantly with their applied research to the efficiency of Quebec’s control program.

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12 Maritime Provinces: Nova Scotia, Prince Edward Island, and New Brunswick James Goltz,1 Jacqueline Badcock,2 and Rowland R. Tinline3 1

New Brunswick Provincial Veterinary Laboratory, Department of Agriculture, Aquaculture and Fisheries, Fredericton, New Brunswick, Canada 2 Department of Health, Fredericton, New Brunswick, Canada 3 Professor Emeritus, Geography, Queen’s University, Kingston, Ontario, Canada

Place Three provinces on the east coast of Canada – New Brunswick, Prince Edward Island, and Nova Scotia, which includes Cape Breton Island – are collectively known as the Maritime provinces. They were the second area in Canada to be settled by Europeans after Newfoundland. French explorer Jacques Cartier made a detailed reconnaissance of the area and claimed the area for the King of France. The French immigrants who followed built small settlements in today’s Nova Scotia and New Brunswick, as well as Île-Saint-Jean (Prince Edward Island) and Île-Royale (Cape Breton Island), and called themselves Acadians. By 1713 France had ceded Acadia (Nova Scotia) to Britain and by 1763 had also ceded New France (to become Quebec and Ontario), Île-Royale (Cape Breton Island), and Île-Saint-Jean (Prince Edward Island) to Great Britain. In the same year, Great Britain re-annexed Cape Breton Island and Prince Edward Island to Nova Scotia. In 1784 Great Britain split Nova Scotia into three separate colonies: Cape Breton Island, New Brunswick, and peninsular Nova Scotia. By 1820 Cape Breton Island was once again annexed to Nova Scotia. The British North America Act, 1867 united New Brunswick, Nova Scotia, and Canada into the Dominion of Canada. At that time Canada was what is now Quebec (then called Lower Canada) and Ontario (then called Upper Canada). Under the Dominion Act of 1873, Prince Edward Island became Canada’s seventh province (see Overview, Part 3). The Maritimes front the Atlantic Ocean and its various sub-basins (e.g., Gulf of Maine, Bay of Fundy, and the Gulf of St Lawrence). Quebec’s Gaspé Peninsula lies to the

northwest; Newfoundland and Labrador, to the northeast; and the US state of Maine to the southwest. New Brunswick is sheltered from the Atlantic Ocean and has, for the most part, a continental climate. Its northwestern border is dominated by the Appalachian Mountains within the eastern Canadian forest ecosystem. Nova Scotia and Prince Edward Island are surrounded by water giving them a mid-temperate zone and maritime climate. The three Maritime provinces are the smallest in Canada, with a total population of only 1,813,606 (Table 12.1).

Rabies Cases The first recorded case of rabies was that of a dog in 1926 in Prince Edward Island. Thirty-five years later (1961) rabies was diagnosed in a horse in New Brunswick. Since then there have been three major outbreaks in the Maritimes, dominated by cases in foxes and raccoons. The outbreaks were the result of spread from neighbouring Quebec and Maine, respectively, and were limited to New Brunswick with no detectable spillover into the other two provinces (Figure 12.1, Tables 12.2 and 12.3). In 1966 rabies in a red fox was reported in the county Table 12.1  Maritime provinces’ statistics. New Brunswick 2

Area km Population Capital

70,250 747,101 Fredericton

Nova Scotia Prince Edward Island 55,283 923,598 Halifax

Data source: Statistics Canada, 2016.

5,660 142,907 Charlottetown

A History of Rabies Management in the Provinces and Territories

of Carleton in New Brunswick. Cases in red foxes were subsequently reported in the nearby counties of Madawaska York, Sunbury, Restigouche, and Northumberland. This outbreak was the extension of the arctic fox variant in red foxes (Vulpes vulpes) that swept through the fox population in Ontario and Quebec and moved east into the Gaspé Peninsula and the Saint John River Valley in New Brunswick. The typing of rabies virus in Canada was first undertaken in the mid-1980s (see Chapter 23). Hence, our statements about virus variants before virus typing are inferences based on the species involved and the nature of the outbreaks. This epizootic ended by 1973. The next incursion of wildlife rabies also occurred in New Brunswick in 2000–2002 as the northward extension of a raccoon (Procyon lotor) variant rabies epizootic that had been spreading up the east coast of the United States since the 1950s and moved through Maine into New Brunswick. A second incursion from Maine of raccoon variant rabies occurred in 2014–2017. Since 1984 a continuing small number of positive cases in bats appears to be independent of incidence in other species (Table 12.2). The sections that follow discuss these three major components of the rabies history of the Maritimes. These sections focus on New Brunswick as the outbreaks were only detected in that ­province and so were control efforts.

Fox Rabies The red fox outbreak that began in 1966 in New Brunswick appeared to have run its course by 1973, although isolated cases occurred until 1977 (a pig in 1975, two bovines in 1976, and a pet in 1977). Given that there were no reported rabies cases in foxes at that time, it is possible those isolated cases were caused by bat variants. Unfortunately, there is no way of confirming this. Table 12.3 clearly illustrates that rabies in foxes dominated the outbreak and spread to livestock, pets, and other wildlife, primarily skunks and raccoons. Similar trends occurred in Ontario and Quebec, where the fox was also the primary rabies vector. This epizootic never reached Prince Edward Island or Nova Scotia. Rabies cases that occurred in a red fox and a bovine from Bras d’Or on Cape Breton Island in 1989 and three red fox cases in Prince Edward Island in 1993 were shown to be bat variant rabies by monoclonal antibody analysis (Webster et al., 1989). Table 12.4 shows that the fox rabies outbreak in 1966– 1973 was concentrated in the counties in New Brunswick along the Saint John River Valley (Figure 12.2 shows counties in New Brunswick). Incidence was low along the Gulf of St Lawrence coast and absent in the counties

Figure 12.1: Rabies cases in the ­Maritimes, 1961 to 2017. Source: created from CFIA data.

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Nova Scotia, Prince Edward Island, and New Brunswick

Table 12.2  Rabies cases in the Maritime provinces, 1926 to 2017. Year 1926 1961 1962 1963 1964 1965 1966 1967 1968 1969 1970 1971 1972 1973 1974 1975 1976 1977 1978 1979 1980 1981 1982 1983 1984 1985 1986 1987 1988 1989 1990 1991 1992 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012 2013 2014 2015 2016 2017 Total % Total

Total

NB

NS

1 1 0 0 0 0 85 39 33 50 28 44 33 10 0 1 2 1 0 0 0 0 0 0 1 0 1 1 0 2 0 0 2 3 1 1 0 4 0 0 15 51 3 3 2 1 0 3 0 1 2 0 2 1 2 24 3 11

0 1 0 0 0 0 85 39 33 50 28 44 33 10 0 1 2 1 0 0 0 0 0 0 1 0 0 0 0 0 0 0 1 0 0 1 0 4 0 0 13 51 3 1 1 1 0 1 0 0 1 0 1 1 2 24 3 11

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 1 0 2 0 0 1 0 1 0 0 0 0 0 2 0 0 2 0 0 0 2 0 0 1 0 1 0 0 0 0 0

468

448 95.7

14 3.0

Table 12.3  Rabies cases by year and by species for the Maritime provinces, 1926 to 2017. No cases were reported from 1927 to 1960.

PE Year

1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 1 0 0 0 0 0 0 0 0

Total

1926 1 1961 1 1962 0 1963 0 1964 0 1965 0 1966 85 1967 39 1968 33 1969 50 1970 28 1971 44 1972 33 1973 10 1974 0 1975 1 1976 2 1977 1 1978 0 1979 0 1980 0 1981 0 1982 0 1983 0 1984 1 1985 0 1986 1 1987 1 1988 0 1989 2 1992 2 1993 3 1994 1 1995 1 1996 0 1997 4 1998 0 1999 0 2000 15 2001 51 2002 3 2003 3 2004 2 2005 1 2006 0 2007 3 2008 0 2009 1 2010 2 2011 0 2012 2 2013 1 2014 2 2015 24 2016 3 11 2017 Total 468 % Total

6 1.3

Fox 0 0 0 0 0 0 47 22 26 43 9 24 21 4 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 3 0 0 0 0 0 0 0 0 0 0 0 0 0 2 0 0 0 0 0 0 0 0 0 0

Rac Live

Dom Bat

0 0 0 0 0 0 2 1 0 1 2 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 6 46 3 0 0 0 0 0 0 0 0 0 0 0 1 23 1 1

1 0 0 0 0 0 12 3 1 2 2 5 1 1 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 2 1 0 0 0 0 0 0 0 1 0 0 0 0 0

0 1 0 0 0 0 14 10 5 4 15 14 10 5 0 1 2 0 0 0 0 0 0 0 0 0 0 0 0 1 2 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

202 87 84 43.2 18.6 17.9

33 7.1

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 1 1 0 0 0 0 1 1 0 4 0 0 4 1 0 1 0 1 0 1 0 1 2 0 1 1 0 0 2 7 31 6.6

Skunk

Other

0 0 0 0 0 0 6 3 1 0 0 1 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 5 4 0 0 1 0 0 0 0 0 0 0 0 0 1 1 0 3

0 0 0 0 0 0 4 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

27 5.8

4 0.9

The four cases in the Other column were three mice and one rat. Source: compiled from CFIA data.

Source: compiled from CFIA data.

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A History of Rabies Management in the Provinces and Territories

of Kent, Westmorland, and Albert in the east and along the border with Nova Scotia. Those counties are primarily maritime lowlands, in contrast to the rolling uplands on interior New Brunswick and the rich farmland of the Saint John River Valley. The lowland area appears to have acted as a barrier, preventing the spread of rabies into Nova Scotia.

Raccoon Rabies Rabies in raccoons had been detected in small numbers through the years in New Brunswick: two cases in 1966 (Gloucester and Sunbury County), one case in York County in 1967, one case in Carleton County in 1969, and two more in 1970. As far as is known, these cases were the arctic fox variant linked to the ongoing outbreak in the fox ­population in Quebec (see Chapter 11). In the 1990s the raccoon variant spread northward through the eastern states, reaching New Brunswick in 2000. The first three rabies cases in 2000 were reported in skunks (Mephitis mephitis) in St Stephen, Charlotte County. Subsequent monoclonal antibody analysis determined they were infected with the raccoon variant (Nadin-Davis, 2006). It is likely that the virus crossed the St Croix River from Maine and that the carriers were raccoons. The St Croix River is narrow and has several bridges. Cases in raccoons peaked in 2001, and all cases during this first incursion were confined to Charlotte County. Despite the relatively large number of raccoon submissions in counties adjacent to Charlotte County (Table 12.5), no additional cases of raccoon variant rabies were detected until 2014, when a rabid raccoon was diagnosed in late May and a rabid skunk was diagnosed in

Table 12.4  Rabies cases by species for counties reporting rabies in New Brunswick, 1966 to 1973. County

Total

Fox

Live

Carleton York Victoria Sunbury Madawaska Northumberland Restigouche Queens Charlotte Gloucester Saint John Total

151 94 35 14 9 7 5 3 2 1 1 322

90 64 22 5 3 4 2 3 2 0 1 196

43 11 9 7 4 1 2 0 0 0 0 77

Dom Skunk 9 10 3 1 2 1 1 0 0 0 0 27

2 8 1 0 0 1 0 0 0 0 0 12

Rac

Other

3 1 0 1 0 0 0 0 0 1 0 6

4 0 0 0 0 0 0 0 0 0 0 4

Live = livestock; Dom = cat/dog; Rac = raccoon, Other = rat/ mouse. See Figure 12.2 for locations. Source: created from CFIA data.

Figure 12.2:  Maritime ­provinces and counties. Source: created from a base map ­derived from Natural Resources ­Canada outlines.

182

Nova Scotia, Prince Edward Island, and New Brunswick

early October near St Stephen and near the previous cases. New Brunswick’s successful efforts to confine the outbreak to Charlotte County and then eliminate it for 12 years are discussed in more detail in the rabies management section later in this chapter. The incursion of raccoon variant rabies that began in 2014 spread farther eastward and northward (into York County) than did the 2000–2002 incursion and

peaked in 2015 but declined when control measures were implemented. Together, fox and raccoon cases dominated the temporal and spatial patterns of rabies in the Maritimes (Table 12.3, Figure 12.3) and rabies in all species has occurred primarily in the western and southwestern counties of New Brunswick.

Table 12.5  Raccoon submissions in New Brunswick by county, 1997 to 2010. Year County Charlotte Kings Westmorland York SaintJohn Carleton Kent Albert Restigouche Queens Sunbury Gloucester Victoria Madawaska Northumberland Total

1997

1998

1999

2000

2001

2002

2003

2004

2005

2006

2007

2008

2009

2010

Total

1 0 0 2 1 0 0 0 1 0 1 0 1 2 0 9

1 0 2 0 0 0 0 0 0 0 0 1 0 0 0 4

1 0 0 4 0 1 0 1 0 0 0 0 0 0 0 7

28 3 6 5 1 3 2 1 1 1 2 1 0 1 0 55

191 53 25 43 20 18 8 2 0 7 2 3 3 0 4 378

31 6 11 17 6 13 1 1 2 1 3 1 0 0 1 94

19 13 15 12 2 2 7 10 0 5 2 2 0 0 1 90

7 142 6 8 31 3 2 3 2 2 1 0 0 2 0 209

9 17 1 9 10 3 1 8 0 1 0 1 0 2 0 62

7 2 40 14 0 4 3 6 19 0 1 0 1 0 0 97

66 33 669 14 11 66 331 44 00 11 00 11 00 11 00 2334

5 3 18 2 2 7 2 0 2 0 0 1 0 0 0 42

0 0 0 0 0 1 0 1 0 0 0 0 0 0 0 2

0 5 0 0 0 1 0 0 0 0 1 1 0 0 0 8

348 247 193 130 74 62 56 37 27 18 13 12 5 8 6 1236

Source: compiled from CFIA data.

Figure 12.3: Rabies-positives by county, 1926 to 2012. Source: created from CFIA data.

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A History of Rabies Management in the Provinces and Territories

Bat Rabies

Island, a fox and bovine (already reported), were diagnosed as bat variants by monoclonal antibody analysis in 1989. In 1992, two horses, one each from New Brunswick and Nova Scotia, were also found to be infected with bat variant. As both specimens were formalin fixed, an in situ hybridization (ISH) method was used to determine that the horse from Truro, Nova Scotia, was infected with a viral variant associated with the silver-haired bat while the bat from Stanley, New Brunswick, was infected with the variant associated with the big brown bat (Eptesicus fuscus) (Nadin-Davis, 2003). The rabid horse from the Stanley area was an interesting case: the brain tested negative for rabies using the fluorescent antibody test, but one of this chapter’s authors (Goltz) found lesions in the thoracic spinal cord, and these tested positive for rabies by immunohistochemistry. This has been the Maritimes’ only case of spinal rabies. Between 1988 and 1993 no bats were reported as positive for rabies, though bat variant rabies was diagnosed in several terrestrial animals as already mentioned. In 1993 three foxes were diagnosed with rabies in Prince Edward Island. Two were identified with a bat variant associated with the northern long-eared bat (Myotis septentrionalis) (C. FehlnerGardiner, CFIA, personal communication, 6 August 2019). Since 1993 small numbers of rabid bats have been found in all the Maritime provinces and include the big brown bat, northern long-eared bat, and little brown bat (Myotis lucifugus). Most of the rabid bats were single cases except for three big brown bats that were found dead at Central Hampstead. A horse from Rogersville, New Brunswick, was diagnosed with bat variant rabies in 2004, shown to be a little brown bat variant by monoclonal antibody analysis. In 2012 a cat from Balmoral, New Brunswick, was

Since 1976 a small but continuing number of positive reports of bat cases have occurred in the Maritimes (Table 12.6). At least six of the seven known species of bats in the Maritimes have been submitted for testing (Table 12.7). The seven species of bats listed in Table 12.7 are reported from NB and NS. The species TCB, BBB, HRB, and SHB have no confirmed reports from PEI (D. McAlpine, ­personal communication, 16 August 2019). The earliest case of bat rabies confirmed by the Canadian Food Inspection Agency (CFIA) was a human-associated case. A Nova Scotia man was bitten on the hand by a bat in 1976 and died in 1977 (see Chapter 3b, Case 36). A diagnosis was not determined until 1978 by monoclonal antibody analysis (Agriculture Canada, 1977; see Chapter 3b; De Serres et al., 2008). It was not until 1984 that the next case, a silver-haired bat (Lasionycteris noctivagans), was diagnosed in New Brunswick. The bat was found in a tent at Canadian Forces Base Gagetown and it had bitten a soldier. Two additional rabid bat cases were reported in Nova Scotia in 1986 and 1987. Two rabies cases on Cape Breton Table 12.6  Rabies cases in bats, 1984 to 2017. Abbreviations are defined in Table 12.7. PROV

TOTAL

BBB

LBB

NLB

SHB

HRB

KEB

NB NS PE Total

23 7 1 31

16 0 0 16

4 6 0 10

0 1 1 2

1 0 0 1

1 0 0 1

1 0 0 1

Source: compiled from CFIA data. Table 12.7  Bat submissions, 1985 to 2017. Code

Name

Scientific Name

Total

NS

NB

PE

LBB BBB NLB HRB SHB TCB RDB BAT Total % Total

Little brown bat Big brown bat Northern long-eared bat Hoary bat Silver-haired bat Tricoloured bat Eastern red bat Unspecified

Myotis lucifugus Eptesicus fuscus Myotis septentrionalis Lasiurus cinereus Lasionycteris noctivagans Perimyotis subflavus Lasiurus borealis

922 101 55 4 2 0 0 27

487 12 27 1 1 0 0 2

358 83 20 2 1 0 0 2

77 6 8 1 0 0 0 23

1111

530 47.7

466 41.9

115 10.4

% Total 83.0 9.1 5.0 0.4 0.2 0.0 0.0 2.4 100

The northern long-eared bat was first reported on Prince Edward Island in 1988 (Brown et al., 2007). Note that eastern M. septentrionalis (NLB) were assigned to M. keenii (Keen’s little brown bat, KEB) before the mid-1980s, but the two species have been recognized as distinct since then, and the Canadian range of M. keenii is restricted to British Columbia (D. McAlpine, research curator and head, Zoology Section, New Brunswick Museum, personal communication, 23 September 2013). Unfortunately, laboratory reports refer inconsistently to NLB and KEB, so these species have been added together in this table. Note that the tricoloured bat was formerly called the eastern pipistrelle. Scientific names in the table are consistent with Naughton (2012). Source: compiled from CFIA data.

184

Nova Scotia, Prince Edward Island, and New Brunswick

also diagnosed with rabies. This is an interesting case since the last diagnosed case in cats in New Brunswick was in 1971. The cat was unvaccinated, went outdoors, seemed sick when it returned, bit the owner, and died the next day. Later, tests showed the virus was consistent with the profile found circulating in the little brown bat variant (C. FehlnerGardiner, CFIA, personal communication, 6 August 2019).

focused on information sharing, clarification of roles and responsibilities, communication, public education, and coordination of responses to the sporadic cases. The New Brunswick Rabies Committee developed and implemented the New Brunswick Rabies Management Plan in June 2001 (New Brunswick Department of Health, 2001). This plan provided a comprehensive program for the surveillance, prevention, and control of rabies. At that time, committee members included the New Brunswick departments of Health and Wellness; Agriculture, Fisheries and Aquaculture; Natural Resources and Energy; Education; Environment and Local Government; Transportation; and Business New Brunswick; CFIA; the New Brunswick Medical Society; and the New Brunswick Veterinary Medical Association. The main objectives of the plan were (1) to conduct effective wildlife rabies surveillance to identify where rabies had occurred and inform control efforts, (2) to monitor the disease’s geographic spread, (3) to identify which wildlife species were affected, and (4) to develop a wildlife rabies control program to reduce the numbers of cases and prevent spread. An integral part of the plan was international collaboration with the US state of Maine. Other components of the management plan were vaccination of domestic pets, stray animal control, public awareness and education, rabies pre-exposure vaccination for high-risk workers, and wildlife regulations that prohibited the relocation of live-trapped high-risk wildlife (see the sections below). The overall goals were to reduce the need for post-exposure prophylaxis (PEP) and reduce public anxiety. The New Brunswick Rabies Committee was revitalized in 2014 in response to the second incursion of raccoon variant rabies in the southwestern part of the province. Membership included the New Brunswick departments of Agriculture, Aquaculture and Fisheries; Energy and Resource Development; Health; and Environment and Local Government; the New Brunswick Veterinary Medical Association; the New Brunswick Medical Society; CFIA; and the New Brunswick Society for the Prevention of Cruelty to Animals.

Rabies Management Fox Rabies Outbreak Historically, rabies was mainly managed by Agriculture Canada (now CFIA), and this was the case during the fox epizootic of 1966 to 1973. Under its mandate, provided by the Health of Animals Act and Regulations, this management included investigating all suspect rabies cases in domestic animals or wildlife in contact with humans; submitting specimens to a federal laboratory for testing (the Sackville Laboratory between 1949 and 1995 and, ­subsequently, the Fallowfield laboratory in Ottawa); imposing quarantines when necessary; reporting positive diagnoses to the Maritime agencies, especially where humans were involved; paying indemnity; providing educational material (Department of Health, 1967); and conducting animal bite investigations. Free rabies vaccination clinics were established in heavily infected areas (Canada Department of Agriculture, 1968, p. 45). This was done in close cooperation with many other agencies involved in rabies management at the provincial level, such as the Medical Office of Health. Responses to outbreaks and sporadic cases of rabies, including prevention and control measures and media coverage, have been traditionally handled by provincial government agencies.

Raccoon Rabies Incursions Anticipating the invasion of raccoon rabies, the Government of New Brunswick established a Rabies Committee in 1993 to develop a protocol for monitoring and addressing sporadic outbreaks of rabies in the province. The committee included the New Brunswick departments of Health and Community Services; Agriculture and Rural Development; Natural Resources and Energy; Education; Municipalities; Culture and Housing; the federal government’s Agriculture and Agri-Food Canada; the New Brunswick Medical Society; and the New Brunswick Veterinary Medical Association. The committee initially

SURVEILLANCE

Surveillance for rabies in New Brunswick had historically concentrated on testing available wild and domestic animals that may be rabid and had come in direct contact with people or domestic animals. This is described as public health surveillance, which informs decisions regarding PEP for individuals exposed to rabies. This surveillance system, based only on public health exposures, lacked

185

A History of Rabies Management in the Provinces and Territories

sensitivity for rabies control efforts as it did not necessarily reflect the level of incidence or prevalence of disease in wild populations. To address the limitations of public health surveillance, the departments of Health; Agriculture, Fisheries and Aquaculture; and Natural Resources and Energy implemented targeted wildlife surveillance in summer 2000. This effort focused on testing raccoons, striped skunks, and red foxes that were acting abnormally. Surveillance was province wide, and the public reported suspected rabid animals to a toll-free, 24/7, bilingual rabies information phone line. The provincial Department of Health coordinated this surveillance and paid for the retrieval of suspect animals. Reports were screened based on surveillance criteria that included species and abnormal animal behaviour, such as staggering with non-coordinated movement, dragging one or more legs, lacking fear of humans, showing extreme excitement or aggression, and having porcupine quills or smelling of skunk (in species other than skunks). Targeted surveillance was effective in demonstrating the presence of rabies during the 2000–2002 epizootic, as shown in Table 12.8. Animals that met the criteria noted above were retrieved by licensed rabies response operators or the Department of Natural Resources and submitted to the Department of Agriculture, Fisheries and Aquaculture’s provincial veterinary laboratory. The laboratory processed specimens and forwarded them to the CFIA for diagnostic testing. Targeted wildlife rabies surveillance was discontinued in 2008 when rabies control efforts were also discontinued. In addition to testing wildlife that were acting abnormally, surveillance of road-killed wildlife was also conducted for a short period (2000–2003) in the counties where raccoon rabies cases were occurring. This surveillance was the

collection, submission, and testing of raccoons and striped skunks found dead along roads and highways. In spring 2011 the New Brunswick Provincial Veterinary Laboratory and the Canadian Wildlife Health Cooperative Centre at the Atlantic Veterinary College began to perform the direct rapid immunohistochemical test (dRIT) for rabies. CFIA would no longer test animals that did not have contact with humans or domestic animals. Given the lower cost of dRIT compared to sending specimens for laboratory testing at CFIA (see Chapter 24c) this was a way to increase wildlife surveillance for rabies and continue testing highrisk wild animals that did not have contact with humans or domestic animals. Targeted wildlife surveillance in New Brunswick was reactivated in 2014 in southern and western parts of the province, after the detection of the second incursion of raccoon variant rabies. The New Brunswick Department of Agriculture, Aquaculture and Fisheries assumed responsibility for rabies surveillance activities, with funding from the Department of Health. The reporting and response mechanism was mostly as previously described, but if a rabies response operator cannot be contacted then the Department of Energy and Resource Development will retrieve the specimen. In early February 2017, a skunk that was active in the daytime, heavily infested with porcupine quills, and not exhibiting any fear of humans was live-trapped near an abandoned barn at Waweig, New Brunswick, euthanized, and tested positive for rabies. Signs of activity of other mammals in and around this barn prompted a targeted surveillance effort using live-traps to humanely remove and test animals in the Waweig area in February and March. Fourteen animals were captured and tested: eight raccoons, four skunks, and two porcupines. In addition to the primary case, two other live-captured skunks tested positive for the rabies virus; all the other animals tested negative. All three rabid skunks came from the same barn.

Table 12.8  Wildlife surveillance rabies diagnostic results, New Brunswick, 2000 to 2008. Public Health Targeted Wildlife Surveillance Submissions Surveillance Submissions Year

Total

Positive

Total

Positive

2000 2001 2002 2003 2004 2005 2006 2007 2008

98 170 128 124 124 85 76 62 76

0 0 0 0 0 0 0 0 0

89 427 122 115 249 66 108 142 52

13 48 3 0 0 0 0 0 0

CONTROL IN WILDLIFE

New Brunswick’s wildlife rabies control program initially consisted of population reduction and trap-vaccinaterelease (TVR) activities (2001–2002) and was implemented 13 months after detection of the first rabies case. This was a modification of Ontario’s point infection control (PIC) strategy, which usually was implemented immediately following detection of a rabies case and traditionally used three tactics in concentric areas: population reduction, TVR, and oral rabies vaccination (Rosatte et al., 2001). Oral rabies vaccination was not initially done in New Brunswick because of funding constraints.

Source: compiled from data provided by the New Brunswick Provincial Veterinary Laboratory.

186

Nova Scotia, Prince Edward Island, and New Brunswick

Two years of intensive wildlife rabies control management actions reduced the spread and the number of rabies cases. The new goal was to prevent the reintroduction and subsequent spread of raccoon variant rabies in the province by maintaining a barrier of vaccinated animals. During 2003–2007 only TVR activities were used. The costs of TVR wildlife rabies control varied year to year depending on the size of the control area and equipment purchases, but on average were approximately $357/km2 (J. Badcock, New Brunswick Department of Health, personal communication, 23 September 2013). In 2008 the program was modified by implementing oral rabies vaccination (ORV). Wildlife rabies vaccination programs were discontinued between 2008 and 2014, but oral rabies vaccination using ONRAB vaccine baits recommenced in 2015. The targeted area was initially within a 30-kilometre radius of rabies cases in New Brunswick, but it expanded to include areas of New Brunswick close to where raccoon variant rabies cases are occurring in Maine. The annual cost of oral rabies vaccination in this expanded area was approximately $1.3 million. Wildlife rabies control activities generally occurred from late summer to early fall (August to mid-September). In New Brunswick raccoons and striped skunks are born in early spring, and by late summer to early fall they are old enough to respond to vaccination (Rosatte et  al., 1990). Raccoon and striped skunk activity declines during autumn as ambient temperatures fall and food becomes scarce. Choosing August/September maximized captures and vaccinations of more mobile adults and dispersing juveniles than later in autumn, for example, from ­mid-October to late November.

by mail to all residences within the wildlife rabies control areas. In addition, a toll-free, 24/7, bilingual rabies information line was implemented. Additional communications were provided for the oral rabies vaccination program. For 60 days after the start of bait distribution, inquiries from people who had found baits were monitored through reports to the information line. Information about the bait, the ORV program, and the vaccine was also provided to the Poison Control Centres, local Public Health and Natural Resource offices, physicians, and local veterinarians. Communication brochures in 2003 for New Brunswick included “Sophie Has No Idea That Her Dog Has Rabies,” “Are You at High Risk for Contracting Rabies?” and “Roger and Robert Have No Idea That This Animal Has Rabies.” A web page was included in the Office of the Chief Medical Officer of Health’s section of the Government of New Brunswick’s website. PROGRAM PARTICIPANTS

Fur harvesters (trappers) licensed by the Department of Natural Resources were key participants in the TVR program. For a fur harvester’s licence, individuals completed a firearm safety/hunter education course and a trapper education course under the Fish and Wildlife Act (SNB 1980, c. F-14.1) and associated regulations. The Department of Natural Resources provided trappers with permits for trapping during the wildlife rabies control program. Finally, individuals had to have proof of rabies pre-exposure vaccination. Trappers attended training sessions that provided information on rabies and other wildlife diseases, proper vaccination and ear tagging techniques, effective trapping methods and trapping regulations, record keeping, health and safety issues, humane treatment of animals, and program guidelines and protocols. Program guidelines and protocols, including proper safety equipment, were expected to be followed at all times. Trappers were encouraged to work together to be more efficient and safe while in the field. Volunteers in the wildlife rabies TVR control program had to have proof of rabies pre-exposure vaccination and included a CFIA veterinarian; a private veterinarian and a wildlife technician from the Canadian Cooperative Wildlife Health Centre, Atlantic Veterinary College, Prince Edward Island; and a field epidemiologist from the Canadian Field Epidemiology Program, Public Health Agency of Canada. Since 2015 the distribution of oral rabies vaccine baits has mainly been conducted by staff of the Department of Agriculture, Fisheries and Aquaculture, with assistance from the Department of Energy and  Resource

PUBLIC AWARENESS AND EDUCATION

Public messaging through press releases, brochures, posters, talks, and websites has focused on encouraging the public to enjoy wildlife from a distance, thereby preventing potential exposures, to keep rabies vaccination in pets up to date, to refrain from relocating wildlife from one jurisdiction to another, to report animals that are suspected to have rabies, and to seek medical attention if bitten or scratched by an animal. Each year during the control program, large-scale media campaigns informed the public about the wildlife rabies control activities and recommended that pets be kept indoors or leashed while the program was being conducted. Press releases were distributed, airtime was purchased on local radio, advertisements published in local newspapers, social media was utilized, and print information delivered

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A History of Rabies Management in the Provinces and Territories

Development (formerly Natural Resources and Energy), the Canadian Wildlife Health Cooperative, and students from the Atlantic Veterinary College. The Ontario Ministry of Natural Resources and Forestry has provided flight line planning, a crew, and plane to enable the aerial distribution of oral rabies vaccine baits.

included most of the previous wildlife rabies control areas and an extension northward. The area covered 893 km2 and was divided into 60 trapping cells (average 14.9 km2). In response to rabies cases in Maine in 2007, additional TVR cells were placed in the north and trapping cells with low raccoon and skunk catches were eliminated. The 2007 TVR area was approximately 900 km2 and was divided into 60 trapping cells, each averaging 15.0 km2. Raccoons and striped skunks vaccinated in previous years were identified by ear tag numbers and were revaccinated and released according to TVR animal processing protocols. Rabies vaccines are regulated by the CFIA under the legislative authority of the Health of Animals Act and Regulations. Permission to administer rabies vaccines by non-veterinarians under the supervision of a licensed veterinarian was provided by both the CFIA and the New Brunswick Veterinary Medical Association. Raccoons, striped skunks, and red foxes were vaccinated against rabies by intramuscular injection (hip or thigh) with Imrab 3, an inactivated rabies vaccine (Merial Inc., Athens, Georgia, United States). A single metal ear tag

POPULATION CONTROL AND TRAP-VACCINATE-RELEASE

In 2001 and 2002 population reduction (PR) was carried out five kilometres around rabies cases and TVR activities occurred a further 10 kilometres around rabies cases. The 2001 wildlife rabies control area was divided into 47 trapping cells (20 PR cells and 27 TVR cells), and the 2002 area was divided into 47 trapping cells (13 PR cells and 34 TVR cells) (Figures 12.4 and 12.5). Overall TVR efforts are shown in Table 12.9. Before the two cases that occurred in 2014, the last diagnosed case of raccoon variant rabies in New Brunswick was in May 2002. Population reduction was discontinued in 2002 and efforts focused on TVR. In 2003–2006 the TVR area

Figure 12.4: Wildlife rabies control areas (population reduction and trap-vaccinate-release) in New Brunswick, 2001 and 2002. Source: New Brunswick Department of Health, unpublished data.

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Nova Scotia, Prince Edward Island, and New Brunswick

with a unique serial number was placed on one ear using either size 2 or size 3 metal bands (National Band and Tag Company, Newport, Kentucky, United States). All captured feral domestic cats (without collars or owner identification) were also vaccinated against rabies by intramuscular injection (hip or thigh) with Imrab 3. Vaccinated feral and owned domestic cats (with collars or other owner identification) were identified by marking the inner side of the ear pinna with waterproof ink.

Animals exhibiting abnormal behaviours or other signs suggestive of rabies were submitted for rabies testing, as were all animals that had come in contact (e.g., bite or scratch) with any of the trappers. None of these animals tested positive for rabies. In 2001 PR cells were trapped for eight nights (23–31 October) and 103 raccoons and 17 skunks were humanely killed. In 2002 PR cells were trapped for 12 nights (23 August to 5 September) and 113 raccoons and 96 skunks were humanely killed.

Figure 12.5: Wildlife rabies control areas (trap-­vaccinaterelease) in New Brunswick, 2003 to 2007. Source: New Brunswick Department of Health, unpublished data.

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A History of Rabies Management in the Provinces and Territories

Table 12.9  Trap-vaccinate-release results in New Brunswick, 2001 to 2007. Raccoons Year 2001 2002 2003 2004 2005 2006 2007

Individuals Vaccinated

Striped Skunks

Individuals Vaccinated Previous Years

297 609 783 758 847 1221 1149

0 43 128 103 209 208 237

Individuals Vaccinated 98 183 281 311 342 537 589

Feral Domestic Cats

Individuals Vaccinated Previous Years 0 11 33 50 62 74 99

Individuals Vaccinated 148 137 209 217 183 198 268

Source: prepared by the New Brunswick Department of Health.

All TVR cells were trapped for a minimum of 12 nights. TVR activities ran from 15 October to 18 November 2001; 23 August to 19 September 2002; 14 August to 28 September 2003; 15 August to 29 September 2004; 11 August to 7 October 2005; 17 August to 15 October 2006; and 17 August to 17 October 2007. The numbers of incidental catches of non-target species varied each year. The seven-year averages (2001 to 2007) of incidental captures were as follows: snowshoe hares (41%), red squirrels (27%), and the following other animals (20%): bird, marten, porcupine, weasel, muskrat, domestic rat, mink, fisher, turtle, black bear, groundhog, beaver, bullfrog, chipmunk, domestic dog, coyote, and a red fox. ORAL RABIES VACCINATION

In 2008 in collaboration with the Ontario Ministry of Natural Resources and the CFIA, New Brunswick conducted field research to evaluate the efficacy of ONRAB, a live adenovirus recombinant oral vaccine, consisting of a human adenovirus-type five-vector encoding the Evelyn-RokitnickiAbelseth (ERA) rabies virus glycoprotein gene. At that time, ONRAB was under experimental permit and contained a tetracycline biomarker, and permission was granted to the New Brunswick Department of Health by the Veterinary Biologics Section of CFIA on 31 July 2008 (New Brunswick Department of Health, 2008; “Summary New Brunswick,” 2009). The area for study comprised two experimental plots (Figure 12.6): the north ORV plot (area 750 km2) and the south ORV plot (area 675 km2). Approximately 90,070 ONRAB ultralite baits were dropped in the plots from fixed-wing aircraft at a density of 75 baits/km2 and flight-line spacing of 1.0 kilometre on 25 and 26 August. The aircraft were provided by the Ontario Ministry of Natural Resources Aviation Services and Dynamic Aviation, a private US based contractor. ONRAB ultralite baits were also applied by hand in villages and towns

Figure 12.6: ORV wildlife rabies control area in New Brunswick, 2008. Source: New Brunswick Department of Health, unpublished data.

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Nova Scotia, Prince Edward Island, and New Brunswick

at a bait density of 150 baits/km2 on 28 August and 6, 8, and 9 October. A total of 10,553 baits were distributed by hand. Post-ORV sampling began approximately five weeks after bait distribution (6–16 October 2008). Each study plot had five individual trapping cells located at least five kilometres from the international border. Trapping cells were approximately 15–20 km2 and TVR trapping protocols were followed. Trappers brought captured raccoons and skunks to a central location for processing by veterinarians and wildlife technicians. Following immobilization, blood was collected and a second premolar tooth was removed from adults (raccoon and striped skunk), and a canine tooth from juveniles (raccoon only). Animals were vaccinated against rabies and ear tagged as per TVR animal processing protocols. All animals were returned and released at the site of capture upon recovery from anaesthesia. A total of 76 raccoons were captured; 60 in the north plot and 16 in the south plot. A total of 38 striped skunks were captured; 24 in the north plot and 14 in the south plot. Blood samples were analysed for evidence of seroconversion, indicative of bait consumption and vaccine efficacy. Samples were taken from 73 raccoons and 33 striped skunks. The Centre of Expertise for Rabies, CFIA, performed serum neutralization assays and competitive enzyme-linked immunosorbent assays (c-ELISA) for rabies antibodies. The Rabies Laboratory, Wadsworth Center, New York State Department of Health, performed the rabies rapid fluorescent focus inhibition test (RRFIT). A positive result for the rabies virus neutralization assays was a rabies antibody titre ≥ 0.05 IU/mL. There was no significant difference in the estimated proportion of antibody-positive animals among the three tests. The seropositivity of raccoons averaged 73.5%, and the seropositivity of skunks averaged 16.2%. Teeth collected were sent to Matson’s Laboratory LLC, Montana, for teeth cementum age determination and tetracycline biomarker analysis, indicative of bait consumption. Teeth from 71 raccoons were analysed, of which 21 (29.6%) were tetracycline positive. Only one (2.6%) of 38 skunk teeth analysed was positive. Tetracycline biomarker deposition may not be the best measure of vaccine uptake because bioavailable concentration of tetracycline within a bait can be less than half of stated concentration at manufacture. The deposition within premolar teeth is also less reliable than in canine teeth. In August 2015 New Brunswick implemented oral rabies vaccine bait distribution in response to the incursion of raccoon variant rabies that was detected in May 2014. ONRAB oral rabies vaccine baits were distributed by plane and by hand over 2430 km2 in Charlotte County with technical assistance from the Ontario Ministry of Natural Resources

and Forestry. The vaccine baits were distributed by air at 75 baits/km2 along flight lines spaced at 750 m intervals, and manually at 150 baits/km2. Following the bait distribution in August, a rabid raccoon was confirmed on 2 September 2015 in the village of McAdam in York County, just north of Charlotte County and north of the geographic area where the vaccine baits had been distributed. In response to the McAdam case, staff from the Department of Agriculture, Aquaculture and Fisheries and the Department of Natural Resources hand-distributed 600 oral rabies vaccine baits over a 3 km2 area in the village of McAdam, and they contracted Canadian Helicopters to assist with aerial distribution of approximately 36,000 oral rabies vaccine baits by helicopter over 510 km2 in the McAdam area. Approximately 4000 oral rabies vaccine baits were also distributed along the highway between McAdam and Harvey Station. No further cases have been reported in York County or outside of the Charlotte County oral rabies vaccine zone. The distribution of oral rabies vaccine baits was continued each summer from 2016 through 2019, through collaborative efforts led by the New Brunswick Department of Agriculture, Aquaculture and Fisheries, and involving the Department of Energy and Resource Development, the Department of Health, the Ontario Ministry of Natural Resources and Forestry, Forest Protection Limited, and volunteers from the Atlantic Veterinary College in Prince Edward Island and the University of New Brunswick. Approximately 539,000 ONRAB oral rabies vaccine baits were distributed annually in western New Brunswick by plane (477,000) and by hand (62,000) over 5700 km2. The aerial distribution was done at a density of 75 baits/km2 over much of Charlotte County and portions of York and Carleton Counties in 2016. In 2017 aerial vaccine bait distribution density in the targeted portion of Charlotte County was increased to 150 baits/km2 in response to raccoon variant rabies cases occurring in nearby Maine. The hand distribution of vaccine baits was done at densities between 150 and 300 baits/ km2 in areas unsuitable for aircraft bait delivery in parts of Carleton (Woodstock and Hwy 95 leading to the border and Woodstock First Nations), York (McAdam, Harvey, St Mary’s First Nations), and Charlotte Counties (Milltown, St Stephen, St Andrews, St George, Blacks Harbour, Elmsville, Waweig, Deer, and Campobello Islands), as well as Grand Bay-Westfield in Kings County (Figure 12.1). In 2017 and 2018 additional ORV baits were distributed by hand in the vicinity of Waweig and Milltown in response to the detection of rabies cases there in 2017, at a density of 300 baits/km2 to boost immunity of wildlife in those areas. Oral rabies vaccine baits were also distributed by hand in the cities of Fredericton and Saint John from 2016 through

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2018 as a preventive/proactive measure in case raccoon variant rabies were to jump the vaccine barrier and appear in the Saint John River Valley, since the risk of human-raccoon interactions is much higher in urban areas because of greater numbers of both people and raccoons there.

in the geographic areas where raccoon rabies occurred have held low-cost rabies vaccination clinics, and other low-cost clinics were organized elsewhere in the province. Some veterinarians continue to promote the vaccination of horses against rabies, since there have been two horses with bat variant rabies in New Brunswick. The Department of Environment and Local Government and most municipalities have made vaccination of dogs mandatory within their jurisdictions.

INTERNATIONAL COLLABORATION

Between 2003 and 2007 Maine and New Brunswick cooperated on wildlife rabies management efforts to implement and maintain a continuous barrier of vaccinated raccoons and striped skunks along the international border to prevent the re-emergence of raccoon rabies. New Brunswick continued its TVR program, and Maine, in conjunction with the University of Cornell, and the United States Department of Agriculture, Animal and Plant Health Inspection Service, Wildlife Services, implemented an ORV program using the vaccine bait RABORAL V-RG (a vaccinia-rabies glycoprotein recombinant oral vaccine in coated fishmeal sachet – Merial Inc., Athens, Georgia, United States). The baits were distributed by aircraft or by hand. In 2007 cases of raccoon variant rabies were detected in Maine north of the existing TVR barrier in New Brunswick and ORV barrier in Maine. In response both Maine and New Brunswick altered their barriers and continued joint efforts. By 2008 raccoon rabies was under control in New Brunswick, but it continued to spread in Maine. A case was detected near Houlton, Maine, in 2008. The Maine 2008 ORV zone was placed north of known cases to prevent the spread of raccoon rabies in northern Maine and east into New Brunswick. New Brunswick implemented ORV and the barrier was contiguous with Maine’s barrier. The vaccination zone in Maine continues to be located towards the northern limit of locations where rabies has been detected in the state. This zone borders on parts of New Brunswick where oral rabies vaccination has been occurring, but it does not include all areas where rabies has recently occurred in Maine close to the New Brunswick border.

Stray Animal Control

From 2000 through 2008, the Department of Health and Department of Environment and Local Government implemented a province-wide response to stray and suspect rabid domestic cats and dogs. The public was asked to report suspect animals to a toll-free, 24/7, bilingual rabies information line. Reports were screened based on response criteria that included the species, behaviour, and location of animal and were directed to provincial or municipal animal control services or to private animal control services. Animals with clinical signs suggestive of rabies were euthanized and submitted for diagnostic testing in collaboration with the CFIA. For human contact (i.e., bites) involving stray dogs and cats, animals could be placed under a 10-day observation period in an animal shelter. In addition, the Royal Canadian Mounted Police responded to circumstances involving domestic animals that were imminent and potentially life threatening to a person.

Rabies Pre-exposure Vaccination

From 2002 to 2009, the Department of Health provided pre-exposure rabies vaccination for people at potentially high risk of contact with rabid animals. This included both non-government individuals at occupational high risk of exposure to potentially infected animals at a reduced cost ($50 off the series) and individuals at non-profit animal shelter organizations with a charitable status ($50 for series).

Nuisance Wildlife Regulations

The Department of Energy and Resource Development (formerly Natural Resources) regulates wildlife under the New Brunswick Fish and Wildlife Act (SNB 1980, c. F-14.1) and Regulations. The department prohibits individuals from possessing wild animals as pets, including raccoons, skunks, foxes, and bats. The department does permit some individuals to possess wild animals during wildlife rehabilitation with a goal of eventual release. Individuals involved in wildlife rehabilitation are licensed and regulated by this department. The department defines nuisance

OTHER MANAGEMENT CONSIDERATIONS FOR RABIES MANAGEMENT IN NEW BRUNSWICK

Vaccination of Domestic Pets

Information on rabies, including updates on the numbers and locations of rabies cases, was distributed to all veterinarians in New Brunswick via the New Brunswick Veterinary Medical Association (NBVMA) newsletter and by email. The NBVMA promotes rabies vaccination of companion animals in the province. Several veterinarians

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Nova Scotia, Prince Edward Island, and New Brunswick

Sunbury, and Northumberland, CFIA positive rabies data indicates that the spread was limited. The counties of Kings, Kent, Westmorland, and Albert seemed to act as a buffer to the spread towards Nova Scotia as no positive cases were reported in these New Brunswick counties or Cumberland County in Nova Scotia. The raccoon outbreak in 2000 lasted under two years, expanding from its origin at St Stephen but as the data show, positives were found only in Charlotte County despite the large number of submissions from adjacent counties (Table 12.5). More importantly, the first three cases of raccoon variant rabies reported in New Brunswick were skunks, which also accounted for 8 of the first 16 cases reported in New Brunswick from September 2000 to January 2001; the skunk was the affected species for 50% of the specimens during that time (Nadin-Davis, 2006). A genetic characterization of 190 isolates from Ontario and New Brunswick by Nadin-Davis (2006), distinguished five isolates from New Brunswick, which do not cluster with the Ontario isolates, supporting the theory of independent incursion of the two viruses into Canada. The New Brunswick isolate clustered with high confidence with the Massachusetts and New Hampshire isolates (­Nadin-Davis, 2006). In the fox outbreak and the first raccoon incursion, the cases were contained within a small area, mostly in Carleton County for the foxes and only in Charlotte County for the raccoons. The counties of Albert, Westmorland, and Kent in New Brunswick, adjoining Cumberland in Nova Scotia, seemed to act as a buffer to incursion into Nova Scotia. Analysis of the submission data indicates that greater human population in areas support more submissions (Sackville, Moncton, and Saint John). Charlotte County, however, dominates the submission data. While the number of rabies cases in bats in the Maritimes is small, the risk of human contact is always present as shown by the increasing number of terrestrial animals with bat variant rabies and the increasing number of human/bat interactions. This suggests that surveillance for rabid animals, particularly bats, should be enhanced and ongoing in the Maritimes. The dRIT test is used in New Brunswick and Prince Edward Island for testing suspect rabid animals with confirmatory testing by CFIA. However, dRIT had not been validated for use in bats and often gave false positives and a sense of insecurity within the agencies using the test. Consequently, most bat specimens are sent to the CFIA rabies laboratory for the fluorescent antibody test. More recently, the Canadian Wildlife Health Cooperative at the Atlantic Veterinary College has developed greater confidence with the dRIT test methodology in bats.

Table 12.10  Estimated annual number of people starting postexposure prophylaxis in New Brunswick, 1995 to 2008. Year

Number

1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008

11 39 29 24 33 62 138 109 101 91 51 34 41 38

Source: compiled from New Brunswick Department of Health data.

wildlife as wildlife that is damaging property or posing a threat to human or animal health, and does permit private individuals to enact nuisance wildlife control on their own property. Nuisance wildlife control operators are licensed and regulated by this department. The department also prohibits relocation of raccoons and striped skunks by licensed nuisance wildlife control operators and wildlife rehabilitators. The arrival of raccoon rabies in the province caused tremendous public anxiety and resulted in an increase in the number of PEP treatments (Table 12.10). PEP is provided when a potential exposure to a rabid animal has occurred. Prophylaxis is highly effective at preventing rabies if given as soon as possible after exposure.

Discussion Rabies invaded the Maritimes in three separate events: foxes in 1966, raccoons in 2000 and again in 2014. It is likely that fox rabies died out because the area affected and population size weren’t large enough to allow rabies to persist after the initial invasion. It is also likely that the intensive efforts to control rabies in raccoons played a large part in the transient elimination of this variant of the virus from the Maritimes following the two outbreaks. Unfortunately, continuing cases in neighbouring Maine are a potential source of re-infection. An examination of available data shows that the fox rabies entered from Quebec and travelled down the Saint John River Valley to Carleton County. While the outbreak spread to the neighbouring counties of York, Victoria,

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References Agriculture Canada. (1977). Rabies – Nova Scotia: Memorandum from regional veterinarian. Halifax, NS: Agriculture Canada, Atlantic Provinces District Offices. Brown, J. A., McAlpine, D. F., & Curley, R. (2007). Northern long-eared bat, Myotis septentrionalis (Chiroptera: Vespertilionidae), on Prince Edward Island: First records of occurrence and over-wintering. Canadian Field-Naturalist, 121(2), 208–209. https://doi .org/10.22621/cfn.v121i2.448 Canada Department of Agriculture. (1968). Annual report for the year ending 31 March 1968. Ottawa, ON: Author. De Serres, G., Dallaire, F., Côte, M., & Skowronski, D. M. (2008). Bat rabies in the United States and Canada from 1950 through 2007: Human cases with and without bat contact. Clinical Infectious Diseases, 46(9), 1329–1337. https://doi.org/10.1086/586745 Nadin-Davis, S. A., Huang, W., Armstrong, J., Casey, G. A., Bahloul, C., Tordo, N., & Wandeler, A. I. (2001). Antigenic and genetic divergence of rabies viruses from bat species indigenous to Canada. Virus Research, 74(1–2), 139–156. https://doi.org/10.1016 /S0168-1702(00)00259-8 Nadin-Davis, S. A., Sheen, M., & Wandeler, A. I. (2003). Use of discriminatory probes for strain typing of formalin-fixed, r­ abies virus-infected tissues by in situ hybridization. Journal of Clinical Microbiology, 41(9), 4343–4352. https://doi.org/10.1128/ JCM.41.9.4343-4352.2003 Nadin-Davis, S. A., Muldoon, F., & Wandeler, A. I. (2006). A molecular epidemiological analysis of the incursion of the raccoon strain of rabies virus into Canada. Epidemiology and Infection, 134(3), 534–547. https://doi.org/10.1017/S0950268805005108 Naughton, D. (2012). Natural history of Canadian mammals. Toronto, ON: University of Toronto Press and Canadian Museum of Nature. New Brunswick Department of Health. (1967). Rabies! Important facts you should know about the disease [Brochure]. Fredericton, NB: Author. New Brunswick Department of Health. (2001). Rabies management plan. Fredericton: Author. New Brunswick Department of Health. (2008). New Brunswick proposal for ONRAB 2008 experimental design, study areas and field ­stations. Fredericton: Author. Rosatte, R. C., Howard, D. R., Campbell, J. B., & MacInnes, C. D. (1990). Intramuscular vaccination of skunks and raccoons against ­rabies. Journal of Wildlife Diseases, 26(2), 225–230. https://doi.org/10.7589/0090-3558-26.2.225 Rosatte, R., Donovan, D., Allan, M., Howes, L. A., Silver, A., Bennett, K., ... Radford, B. (2001). Emergency response to raccoon rabies introduction into Ontario. Journal of Wildlife Diseases, 37(2), 265–279. https://doi.org/10.7589/0090-3558-37.2.265 Summary New Brunswick 2008 oral rabies vaccination (ORV) program. (2009). Rabies Reporter, 20(2), 4–5. Retrieved from Legislative Assembly of Ontario website: http://www.ontla.on.ca/library/repository/ser/140213/2009//2009v20no02.pdf Webster, W. A., Casey, G. A., & Charlton, K. M. (1989). Bat-induced rabies in terrestrial mammals in Nova Scotia and Newfoundland. Cross-Canada Disease Report. Canadian Veterinary Journal, 30, 679.

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13 Newfoundland and Labrador David J. Gregory1 and Rowland R. Tinline2 1

Canadian Food Inspection Agency (Retired), Ottawa, Ontario, Canada Professor Emeritus, Geography, Queen’s University, Kingston, Ontario, Canada

2

Place History suggests that Norsemen from Greenland visited Newfoundland and Labrador as early as 1001 CE, and that sailors from the Channel Islands were blown to a strange land where the sea was full of fish. Evidence points to its discovery in 1497 after John Cabot was given a charter by Henry VII to sail to all parts, regions and coasts of the eastern, western and northern sea, under our banners, flags and ensigns, with five ships or vessels of whatsoever burden and quality they may be, and with so many and such mariners and men as they may wish to take with them in the said ships, at their own proper costs and charges, to find, discover and investigate whatsoever islands, countries, regions or provinces of heathens and infidels, in whatsoever part of the world placed, which before this time were unknown to all Christians. We have also granted to them and to any of them, and to the heirs and deputies of them and of any one of them, and have given licence to set up our aforesaid banners and ensigns in any town, city, castle, island or mainland whatsoever, newly found by them. (Biggar, 1911)

In 1583 Humphrey Gilbert sailed into St John’s for provisions and formerly took possession in the name of Queen Elizabeth. John Guy was perhaps the first to attempt to colonize the island in 1613 and establish a fishing industry. From 1662 to 1713 conflict was constant between the English settlers and the French. By 1713 the French relinquished their interests in Newfoundland to Great Britain except for the

fishing rights (Bélanger, 2004). Exploration by Moravian missionaries hoping to establish missions along the northern coast of Labrador improved the European knowledge of the area (Figure 13.1). The first mission station was established at Nain in 1772 (Hiller, 1998). In 1763 Britain enlarged Newfoundland by assigning the Labrador coast to it. However, by the Québec Act of 1774, Quebec was enlarged to include Labrador, Anticosti, and the Madeleine Islands. In 1809 by the Labrador Act, Britain re-annexed the Labrador coast and Anticosti Island to Newfoundland. By 1825 Lower Canada (or Quebec) had regained Anticosti Island and a part of the Labrador coast by changes to the Labrador Act. The British Imperial Order in Council of 1880 transferred all British islands in North America not already in Canada to Canada except Newfoundland. The boundary between Quebec and Labrador was redefined in 1927 by the Imperial Privy Council and in 1949, Newfoundland joined the Confederation and became the 10th province by the Newfoundland Act (“Territorial Evolution,” 2012; Overview, Part 3). In 2001 an amendment to the Constitution changed the name to Newfoundland and Labrador. The province of Newfoundland and Labrador (Figure 13.2) is made up of the island of Newfoundland and the mainland region of Labrador and has a total land area of 405,720 km2 (Government of Newfoundland and Labrador, 2011a). The capital of the province is St John’s. The population in 2017 was 528,817 (Government of Newfound and Labrador, 2017). The island has a population density of 4.6 per km2 while Labrador has a population of 27,484 and a population density of less than 0.1 per km2.

A History of Rabies Management in the Provinces and Territories

Figure 13.1: Inuit houses and dogs in Okak, 1913.

Note: The Mission stations were those of the German Moravian Protestants, invited to settle in Northern Labrador in the 1700s as a way of ­Christianizing the Inuit population, or to stop their attacks on European fishermen. Their written accounts helped detail this period. Source: Moravian Archives, Herrnhut, Germany, P0827. Labrador Inuit through Moravian Eyes, Collection.

History of Rabies in Newfoundland and Labrador

This is an important factor in considering surveillance and management of rabies. The province is divided into three main eco-regions: the cordillera, comprising the mountains in the northwest of Labrador; the northern forests, a moist subarctic coniferous forest area of spruce and fir covering Newfoundland and the southwest corner of Labrador; and the taiga covering the rest of Labrador (Figure 13.2). Most of the reported rabies cases occur in the northern forests in Labrador and the northwest coast of Newfoundland. The peninsula in the northwest of Newfoundland, called the Great Northern Peninsula (GNP), is about 220 kilometres long and 80  ­kilometres wide. This area, consisting of the high plateau of the Long Range Mountains and the coastal area with settlements, is where rabies is usually first reported on the island and is the primary location of control efforts in the province. The island has a marine climate modified by the cold Labrador Current, keeping the summers cool and producing low winter temperatures with extensive snow cover (Bélanger, 2004).

Pre-Confederation No documented cases of rabies have been found before 1949, but oral histories and memoirs help to fill in where science is absent (see Chapter 37). On the island, a report (Pedley, 1863) came out of St John’s in 1815 shows the tensions between the residents and the imperial government, and the class structure resembling so closely that left behind in Britain (Great Britain. Colonial Office, 1815). The affair apparently started when a case of rabies was reported “aboard a visiting ship” (Bumsted, 2000). In Labrador the most significant reports relate to “dog sickness,” most probably canine distemper. A summarized review (Saunders & Hearder, 1985) from 1803 until the late 1940s spoke of no rabies-like illnesses. One account (Hawkes, 1916) states that “in 1857 the dogs at the Mission stations were attacked by a mysterious

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Newfoundland and Labrador

Figure 13.2: Regions, features, and communities identified in this chapter. Dots show total number of rabies cases at each location from 1988 to 2017. Ten cases from 1955 to 1982 were missing locations. Another 14 cases between 1988 and 2017 were also missing locations. Source: created from CFIA data.

disease of the Arctic peculiar to canines, and many of them perished. Wild game was also infected, with caribou, foxes, wolves, and other animals dying in large numbers” (p. 20). One could attribute the canine deaths to distemper but it is hard to imagine the link to caribou, or understand how many other wild game species may have been affected. There is really not enough description to consider this to be rabies (Elton, 1931, p. 685). In the early 1990s, older members of Labrador communities were asked about their memories about rabies (Whitney, 1992a; see Chapter 37). Bella Lyall of Nain remembered a nine-year-old boy being bitten by a local dog in Hebron in 1919 (p. 41), after which he developed a fever and started biting his lip, dying shortly afterwards. Her uncle had to kill a lot of dogs that year (Figure 13.3).

Susie Andersen of Makkovik remembered living in Flowers Bay in the early 1920s and how, during the fall, a small dog tried to attack the window of their cabin. It was weak in the hind legs and dragged itself around. It had to be shot. In early 1934 she travelled from Mary’s Harbour to Makkovik by dog sled. A young dog attacked the team and couldn’t be beaten away, so it was shot. Susie’s husband, Jim, remembers that in late spring 1941, dogs were dying up and down the coast, some of them frothing and turning vicious (Whitney, 1992a, p. 41).

Confederation to 1980 Sir Wilfred Grenfell, an English medical missionary, first visited Labrador in 1892. In a memoir of his 20 years in southern Labrador (Grenfell et al., 1913), he states, “Indeed,

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A History of Rabies Management in the Provinces and Territories

Figure 13.3: Dogs being fed, Hebron, 1909.

Source: Moravian Archives, Herrnhut, Germany, P0800. Labrador Inuit through Moravian Eyes, Collection.

even distemper and mange are very rare among Eskimo dogs. Though every family keeps half a dozen at least, not a single case of hydrophobia has been known” (p. 280). Ten years later in North West River, Dr Harry Paddon (1923) stated that “before the end of November the settlements around the head of the bay had to be visited. But here a terrible tragedy occurred. Rabies appeared among our beautiful dogs and we lost about half of them” (p. 92). It is possible that Dr Paddon mistook distemper for rabies. On 5 June 1919 An Act to Prevent the Introduction of Rabies into Newfoundland was passed giving authority to the governor in council to prohibit or regulate “the importation of dogs into this Colony,” for the destruction of dogs as required, and for the imposition of penalties (Acts of the General Assembly, 1919). The debate over its passage included the following comment from the Honourable Mr Ellis that “in England at the present time, dogs are suffering from various diseases, and the desire is to give the Governor in Council the right to prohibit the importation of dogs and so protect us from having this disease rampant in this country” (Newfoundland. House of Assembly, 1919,

p. 107). Legislative measures had been taken in Britain since 1901 (Banyarda et al., 2010) to prevent the introduction of rabies into that island nation as well. As An Act to Prevent the Introduction or Spreading of Insects, Pests and Diseases Destructive to Vegetation was also passed in 1919, it was likely a carryover of general concerns over disease transmission from the mother country, not a direct concern over their past or imminent entry into Newfoundland. Canada’s history of rabies was consolidated in a 1974 article (Tabel et  al., 1974) identifying two cases of rabies in dogs in Labrador in 1954 and one on the island in 1955. The article discusses the large southern movement of rabies from the Arctic into southern Canada that occurred in the 1950s and considers that the 1954 cases were likely a part of this spread. Bella Lyall (Whitney 1992a, p. 41) said that in 1948–1950, rabid foxes were so common in Nutak (Okak Island) that the children had to be kept inside. Many dogs got sick and had to be shot. Nutak was known to have rabies, cycling every three to four years. If this was rabies, it suggests that the arctic wave also moved through Labrador.

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Newfoundland and Labrador

A further report describes cases of illness and death in dogs in both Hebron and Nain (1949–1950), attempting to distinguish between distemper and rabies and quoted below (“Arctic Dog Disease,” 1951):

was transferred to St John’s then to Sunnybrook Hospital in Toronto for further treatment where he remained until June 1956, after which he returned to active service. He was diagnosed with post-vaccination polyneuritis, a complication known to occur following vaccination with the vaccine in use at that time (Briggs et al., 2002). Strangely, there is no reference in the local or provincial newspapers of the day about the actual rabid dog. There is reference to the Mountie being transferred after contact with a dog that turned out to be rabies-negative. The article did state that the disease was “similar to the disease which afflicted dogs around Labrador and in other parts of Newfoundland last year” (“Dog Bites Mountie,” 1956, p. 1). The federal government records identify a laboratory diagnosis on 6 December 1955 of a dog from Lewisporte, but there is no local mention or reaction. The Town of Lewisporte has no record of this event or of a local reaction through the tying up, or muzzling, of dogs as would be expected. Rabies cases appeared sporadically in Labrador and likely reflected the attitudes towards this disease or the available infrastructure more than its prevalence. In 1965 a single dog near North West River was diagnosed through a US laboratory. The dog had bitten a US Air Force sergeant in the leg. Some details are available (“Epidemiological Bulletin,” 1965): the air force sergeant was working on a radar site in Northwest Point and when passing some “Indian mongrel dogs” was unexpectedly bitten on the leg. When he struck back he was bitten a second time. “All stray dogs in the area are being rounded up and destroyed” “Epidemiological Bulletin,” 1965). Perhaps the disease was well known to those with traditional attachments to the region, and unless there was significant human contact, there was no need to look for a diagnosis. Jim and Susie Andersen of Makkovik lost a dog around March 1956; it was frothing and dragging its legs (Whitney, 1992, p. 41). It was only in 1976 that a wild animal was actually diagnosed with the disease, an arctic fox (Vulpes lagopus) in Border Beacon, but no details are available other than that there was no human contact.

Hebron: During the early part of November we first heard of foxes dying of disease, and now and again all through the winter till March people were reporting that some were still being found. One even ran into a house porch here in Hebron one night and was killed and eaten by the dogs. The dogs first began to die of the disease shortly after the foxes were found; most likely they were infected from eating the diseased foxes. The sickness lasted in the dogs till May, and I should say at a rough estimate that over 50 died. Most of these had not been inoculated with Distemper Virus and so had no resistance built up. There is no doubt that the inoculation saved the rest of the dogs here in Hebron. Nain: From March to June, this year, some 20 to 30 dogs died in the Nain District. The disease was obviously, I think, not distemper because many of the dogs which died had been immunized against distemper with Canine Distemper Vaccine “Ferret Origin” (Green Method) ... the disease seems at first to have originated with dogs which had fought with a fox and were bitten by the fox ... there is abundant evidence of cerebral disturbance among the dogs affected, indeed the Eskimo claimed that some, but only some, of the dogs were mad.

The 1955 case on the island was of interest. The story involved a dog getting off a fishing boat in Lewisporte. It was unclear whether it was a fishing boat that had been to Labrador or whether it was a Portuguese vessel. On 14 December an RCMP officer (Powell, 2011) was asked to collect a four month old pup that had reportedly been drinking two weeks earlier out of the same water bowl as the dog confirmed with rabies. At the same time a federal veterinarian, Dr Button, was in Lewisporte vaccinating dogs. The pup was reportedly lazy and weak, had had a fit, and was frothing at the mouth. While euthanizing the pup, the officer received a minor claw scratch that didn’t break the exposed skin between his glove and sleeve. The pup’s head was sent for testing, and on 22 December an initial report stated that it was negative for Negri bodies. Mouse inoculations were initiated and on 23 December the officer received post-exposure prophylaxis. One week later he developed a reaction to this treatment of weakness in the muscles of his ankles and both arms, but it resulted in his collapse when answering the barracks phone one night. He

1980 to the Present LABRADOR

In 1981 the number of rabies cases increased, with one showing a number of interesting features. A wolf (Canis lupus) found dead and frozen outside Nain on 23 January was taken home to be skinned by a trapper (Newfoundland

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A History of Rabies Management in the Provinces and Territories

and Labrador Fisheries and Land Resources, 2019a). When it was noted that the wolf had bitten off and swallowed its own tail, they decided to have it tested. When it later came back positive, the trapper received post-exposure prophylaxis. This type of activity was very common among trappers, who typically held a suspended carcass with a bare hand by the mouth and skinned it with a sharp knife. The chances of having infected saliva contact an open wound would be significant, yet we see no reports in Canada of this type of contact resulting in human rabies. Four other animals were confirmed in 1981, three foxes and one wolf (Table 13.1). In 1982 there was one wolf in Churchill Falls and a red fox in Nain. Vaccination clinics against rabies were held throughout Labrador, provided jointly by Agriculture Canada and the provincial government. A veterinarian from each organization and a provincial employee from Labrador visited each community, vaccinating dogs and cats and speaking to the public about the importance of the disease. Clinics were held in community centres, fire halls or other convenient locations. To avoid conflict between animals, sled dogs were vaccinated at their owner’s residence or on islands where dogs were sometimes kept. These trips were usually held in late winter when there was still snow down, making flying and snowmobiling more predictable, and before school ended, when families often moved out to fishing grounds. Though cases of rabies were not found on the island during these years, there was concern about the risks of importation, both from Labrador and from mainland Canada. In the 1960s, rabies in foxes had moved into New Brunswick (see Chapters 2 and 12), and there was fear that it would cross onto the island via pets. The Livestock Health Act, passed in 1970, an echo of the 1919 concern, provided regulatory control on the importation of domestic animals including, through its regulations (Livestock Health Regulations, 1976), an obligation for rabies vaccination of all pets. An inspection station was established at the ferry terminal in North Sydney (Cape Breton Island) to verify that pets entering had met these restrictions (Whitney, 1988a).

Table 13.1  Rabies-positives between 1955 and 2017 in Labrador and the island of Newfoundland. Only years with cases are shown between 1955 and 1988. Reports before 1980 did not distinguish between arctic and red foxes so this table uses the code Fox. Six arctic foxes were reported (4 in 1988, 1 in 1989, and 1 in 1992). Labrador

Island

Year

Total

LLB Dog Cat Fox

Wolf Cat

Fox Sheep

1955 1965

1 1

0 0

1 1

0 0

0 0

0 0

0 0

0 0

0 0

1976

1

0

0

0

1

0

0

0

0

1981 1982 1988 1989 1990 1991 1992 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012 2013 2014 2015 2016 2017 Total

5 2 20 2 0 1 14 1 0 1 18 0 0 0 1 11 4 19 7 4 0 0 0 0 0 0 16 0 1 12 0 0 142

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 1

1 0 0 0 0 0 0 0 0 0 2 0 0 0 0 2 0 0 1 0 0 0 0 0 0 0 0 0 0 2 0 0 10

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 1

3 1 16 0 0 0 14 1 0 1 13 0 0 0 0 8 2 0 2 3 0 0 0 0 0 0 2 0 1 7 0 0 75

1 1 0 0 0 1 0 0 0 0 2 0 0 0 1 1 0 0 2 0 0 0 0 0 0 0 0 0 0 2 0 0 11

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1

0 0 4 2 0 0 0 0 0 0 1 0 0 0 0 0 2 15 1 1 0 0 0 0 0 0 14 0 0 0 0 0 40

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3

LLB = little brown bat Source: compiled from CFIA data

another dog in a shed. The fox was subsequently killed and confirmed as having arctic fox strain rabies; the first diagnosed case of rabies on the island in a wildlife species. Sea ice commonly blocks the narrow passageway (Strait of Belle Isle, 15 kilometres at its narrowest point) between southern Labrador and the Island in the springtime, providing a convenient bridge for arctic fox and polar bear (Ursus maritimus) to cross over, taking advantage of the large harp seal (Phoca groenlandica) whelping populations off the GNP for feeding (Johnston & Fong, 1992). Sightings of polar bear on the GNP and the discovery of a rabid arctic

ERADICATION PROGRAM, 1988

And cross it did, not with pets from the Maritimes but with foxes on the ice from Labrador. In February and March of 1988, 13 cases were confirmed in foxes in northern Labrador (Table 13.1). On 24 March, a red fox tried to break into a store to attack two dogs in the middle of the night in Roddickton (GNP) (Government of Newfoundland and Labrador, 1988). The owner went outside and thought he had killed the fox, only to find the next morning that it was attacking

200

Newfoundland and Labrador

fox in the community of Blanc Sablon (Quebec) neighbouring on southern Labrador, supported this theory. The red fox, however, is common throughout the island, supporting an annual fur harvest of up to 3000 animals with minimal trapping effort. This species’ numbers probably increased during the past century because of the introduction of several prey species onto the Island (Northcott, 1975). The question was raised as to whether rabies could persist or whether the prey density would be low enough that it would die out on its own once it had thinned out the fox population. There may have been other such introductions over the years which had not persisted. Two further cases in foxes were reported within nine kilometres of the 24 March case in Roddickton (Englee, 2 April; Bide Arm, 14 April), and clinically suspect cases were reported over a 300 km2 area, so secondary or tertiary transmission was likely occurring. Given the scattered human population in the peninsula, there was no way of knowing whether other cases had gone undetected over a wider area and whether the fox population was sufficient to sustain rabies. With the risk of further spread, it was decided to make an attempt at eradication even though attempts at rabies eradication elsewhere had been unsuccessful (World Health Organization, 1973). No other wild mammals known to be able to sustain an epizootic of rabies were found in sufficient numbers on the island, although the coyote (Canis latrans) had recently crossed on the ice from Cape Breton Island and had become established (Government of Newfoundland and Labrador, 2011b). This was the start of the province’s first rabies eradication program (Whitney, 1988b; Whitney, 1989). David Johnston from Ontario was contracted to provide professional guidance in this program, which was jointly directed by provincial wildlife and animal health officials, with the involvement of provincial public health, federal and provincial field veterinarians, and the rabies laboratory of Agriculture Canada in Ottawa. The control strategies included the identification of an eradication zone and a surrounding surveillance zone. The eradication zone was a 30-kilometre radius around Roddickton (approximately 2000 km2) and was established based on the locations where rabid foxes were found; the potential rate of spread through contiguous home ranges, assuming a red fox home range of 5.9 km2 (Voigt & Earle, 1983); an average incubation period of 21 days (Voigt & Tinline, 1980); and the time required to implement a population reduction program encompassing the entire area of potential spread. Within both zones, all potential rabies vectors were to be eliminated to prevent further spread. Surveillance was established to look for evidence of other

foci of infection, which might then require adjustments to the limits of each zone. To reduce the risk of further rabid fox introductions onto the island, a specimen reward of $150 for red fox and $250 for arctic fox (south of 52° N) was set to encourage the hunting and trapping of these target species. Domestic animals were vaccinated and stray dogs controlled in both zones. All unvaccinated domestic animals exposed to rabid foxes were destroyed. Extensive public education was carried out, of particular concern as there was no local experience with, or knowledge of, the disease. Post-exposure prophylaxis was provided to any people exposed to possibly rabid animals. Intensive media coverage helped to broadcast recommended precautions and to support the collection of information and specimens for rabies testing. In a number of remote suspect areas where rewards did not produce specimens, red fox were live trapped, held in captivity for six to eight weeks and observed for symptoms of rabies. Trapping was a feasible method of removing foxes from the eradication zone where roads permitted daily servicing of traps; however, 90% of the area is without road or water access. Because of the need to eradicate potential vectors as quickly as possible, poison bait stations were established in remote areas. Station sites were selected from helicopters, based on the presence of fresh fox tracks in the snow and availability of a landing site. Baits consisted of pieces of moose, seal, beef fat, or whole chicken hearts, treated with 150 milligrams of strychnine sulphate or 5 milligrams of monosodium fluoro-acetic acid (Compound 1080). At each station, three to five baits were buried approximately 6 centimetres deep at the base of 45-centimetre stakes made from dead tree branches. Cod oil and red fox urine were used as attractants. Five to 20 paces away, a tree or rock was marked with fluorescent orange paint to assist in relocation. Stations were not placed within two kilometres of a residence or one kilometre of a public road, or within the watershed of any community water supply. About 2595 strychnine baits were distributed at 865 stations, and 2715 monosodium fluoro-acetic acid baits at 587 stations. Five wild red foxes that had been held in captivity for six to eight weeks were fitted with radio collars (Kolenosky & Johnston, 1967) and released in the eradication zone to determine bait acceptance and potency. Three of the five were tracked and found dead with evidence of strychnine poisoning, an indication that the system worked. In the event that the outbreak spread outside the eradication zone, a contingency plan was formulated for a broad oral vaccination zone stretching across the GNP to limit further spread. There was, however, no proven oral vaccine baiting system available for arctic fox. Alaskan trials on captive

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A History of Rabies Management in the Provinces and Territories

arctic fox had shown that the SAD live-attenuated vaccine would immunize arctic fox (Follman et  al., 1988). Ontario had a vaccine-baiting system capable of immunizing red fox using ERA vaccine in sponge baits and ­blister pack tallow baits (Lawson et al., 1987). Because of the availability of the Ontario baiting system and the ­capability of aerial distribution (Johnston et al., 1988), a trial was undertaken to test the efficacy of the Ontario vaccine-bait on wild arctic fox. The Grey Islands, 15 kilometres off the GNP, was chosen as an isolated test site where arctic fox were known to come ashore hunting for seal whelping remains. On 9 October 1988, 300 baits containing ERA-BHK oral vaccine (Connaught Laboratories) were dropped by helicopter onto these islands. A trapper was stationed on the island for a month following the bait drop and caught three arctic fox within 33 to 44 days of the bait drop. These animals were tested for rabies and found to be negative but positive for the tetracycline marker, indicating that they had eaten baits. Serum samples revealed rabies antibody titres ranging from 1/16 to 1/1024, indicating that the ERA vaccine had been immunogenic for arctic foxes in field conditions (Johnston, 1990). This was the first successful oral rabies vaccination of arctic fox in the field. Following three initial positive cases in the eradication zone, 31 red and 1 arctic fox collected over the next year were negative. Outside the eradication zone, 2 of the 102 arctic foxes collected from Newfoundland were rabies-positive and 0 of 19 from Labrador were rabies-positive. One of the positive arctic foxes was found floating in the sea by a woman in a dory near Triton Island on 11 May 1988. On 3 December the second rabid arctic fox was submitted from Shoal Cove West but with no other positive foxes found in the area. Results of 295 red foxes collected from the GNP and 60 collected from the remainder of Newfoundland were negative (Tucker & Fong, 1989). On 18 January 1989 a red fox found dead on a snowbank in Grand Bruit and confirmed with rabies caused concern suggesting spread from the GNP to the south coast. The recent use of monoclonal antibody technology permitted the division of rabies virus into antigenic groups (Webster et al., 1986) such that a fox that died of bat rabies, as in this case (Webster et al., 1989), could be considered a dead-end oddity not requiring control action. Twenty-seven red fox trapped within 10 kilometres of the Grand Bruit site tested negative. Approximately 100 arctic and 300 coloured foxes were tested during this program, which cost about $2 million. The outbreak of rabies in Ontario and Quebec during the 1950s (Johnston & Beauregard, 1969), which subsequently spread south into the United States and New Brunswick in coloured fox, necessitated annual control programs, which in 1987 alone cost Ontario $19  million (Johnston

et al., 1988), suggesting the level of long-term costs to be expected if rabies became established. The Island’s vulnerability to uncontrolled entry of rabies by wildlife prompted reflection on a legislated barrier between the island and mainland Canada since fox rabies hadn’t been reported in the Maritimes since 1977. In 1991 the obligation to have prior vaccination of pets was dropped and free movement permitted between mainland Canada and the island (Whitney, 1991). BACK TO LABRADOR

Cases continued in Labrador with a single wolf confirmed in 1991and 14 foxes confirmed in 1992 (see Table 13.2). The 1992 cases were found throughout the region from Nain in the north, to Labrador City in the west, and Cartwright in the south. Cases were found in areas surrounding Labrador Table 13.2  Specimen submissions, 1986 to 2017.

Year

Total

Labrador Negative

Labrador Positive

1986 1987 1988 1989 1990 1991 1992 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012 2013 2014 2015 2016 2017 Total Neg/Pos

7 6 434 185 24 23 49 11 10 19 54 9 11 6 22 47 23 124 50 43 9 15 24 17 18 10 26 12 13 48 16 17 1382

4 4 19 13 6 8 20 2 1 6 22 3 7 0 13 22 3 7 20 3 1 6 5 5 7 1 4 6 2 10 4 5 239

0 0 16 0 0 1 14 1 0 1 18 0 0 0 1 11 2 0 7 4 0 0 0 0 0 0 11 0 1 10 0 0 98 2.4

Island Negative

Island Positive

3 2 395 170 18 14 15 8 9 12 14 6 4 6 8 14 16 98 23 36 8 9 19 12 11 9 6 6 10 22 7 11 1001

0 0 4 2 0 0 0 0 0 0 0 0 0 0 0 0 2 19 0 0 0 0 0 0 0 0 5 0 0 2 0 0 34 29.4

Note: Island = Island of Newfoundland. There are 10 submissions for 2015–2017 (4, 5, 1) for which the testing was inconclusive. Source: compiled from CFIA data.

202

Newfoundland and Labrador

as well (Whitney, 1992b). Two cases were seen, one in 1993, one in 1995, and 18 in 1996. The spread was farther than in the 1992 outbreak, being seen as far south as Capstan Island on the Strait of Belle Isle. The surrounding areas of Quebec had 31 confirmed cases, reaching from Kuujjuaq to Sept-Isles (Whitney, 1997). GNP officials were advised to look for possible cases crossing again, but sea ice was not as dense and none was present when the Capstan Island case was discovered. Where wild animal surveillance prior to the 1980s had been minimal, the accumulation of recent data suggested a cyclic pattern occurring every four years (1988, 1992, and 1996), usually starting around February and persisting into spring or sometimes fall (see Figure 13.4). The 1996 outbreak provided a correction to over-confidence in predictions. With no confirmed cases since July, a press release on 9 October suggested that the outbreak was over (Government of Newfoundland and Labrador, 1996). On 21 October a wolf provided the correction in a scene showing the drama that makes this disease the subject of popular literature. The case notes read: “1:30 am wolf jumping on hood of vehicles at gas station, people in vehicles. RNC [Royal Newfoundland Constabulary] investigated, wolf attacked front and rear bumpers of cruiser. One hour later reported chewing on bumper of pickup truck at Wabush Mines. 10 minutes later seen at intersection of 503, shot & wounded by RNC. Within 15 mins jumping at fence of dog

kennels in Wabush. Killed near 503 intersection after running at police car” (Newfoundland and Labrador Fisheries and Land Resources, 2019b). Four years later the disease was again seen in Labrador but in only a single wolf. By 2001, 10 cases were reported throughout Labrador, but in 2002 there were just two cases in Cartwright, until 9 December when a red fox attacked a dog in St Paul’s (Figure 13.2), an enclave inside Gros Morne National Park on the Island. ERADICATION PROGRAM, 2002 TO 2003

One month later a woman in St Paul’s was attacked by her cat after it came home dragging its hind legs. Such a condition in the middle of winter could easily have been caused by cat hiding under the hood of a parked vehicle, unable to escape when it started, or some other source of traumatic injury, but with the recent confirmation of rabies, she was immediately given post-exposure prophylaxis while waiting for the results to come back, which were positive. The original fox was confirmed with arctic fox strain, so  once again the Island faced an outbreak. Attempts to determine how it arrived were postponed while plans were made to start another eradication program. David Johnston was again contracted, and with the support of provincial Wildlife Division, for the logistics of aerial baiting; and provincial Ecosystem Management staff, for the coordination of carcass collection and follow-up on reports of errant

Figures 13.4: Fox submissions from Labrador (left) and Newfoundland (right), 1987 to 2017. Source: created from CFIA data.

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A History of Rabies Management in the Provinces and Territories

behaviour in wildlife, the provincial team was complete. Vaccination of domestic animals and public education programs were carried out by veterinary personnel. Public health officials dealt with human contacts or ­pre-exposure prophylaxis issues, and the Canadian Food Inspection Agency (CFIA) conducted the laboratory testing, this time on contract, as wildlife surveillance in cases without human contact was no longer its stated responsibility. The scene was set by the end of January 2003, with the crucial support of the Ontario Ministry of Natural Resources and Forestry and Artemis Technologies. The first task was to delimit the control area. Cases had been reported much further south than in 1988 and if rabies escaped from the peninsula, crossing the Trans-Canada Highway near Cormack (Figure 13.2) into the body of the island, the opportunity for eradication would be lost. Faced with the question of whether the outbreak would die out on its own, officials choose to err on the side of caution. Trappers were paid a specimen reward of $150 for foxes and coyotes collected within the Northern and Baie Verte Peninsulas (Government of Newfoundland and Labrador, 2003a). Later that year, the subsidy was reduced to $25 for fox, lynx, and coyote specimens but covered the entire island to broaden the scope of surveillance (Government of Newfoundland and Labrador, 2003b). This decreased the temptation to trap outside the surveillance area and sell within it, which would compromise the integrity of the program. The fee remained in place for the remainder of the trapping season, but by 17 December 2003 trappers were no longer paid for specimens from the eastern half of Newfoundland (Government of Newfoundland and Labrador, 2003c). ERA vaccine baits were diverted from Ontario to allow for an immediate drop in the control area, and after considering the choice of baiting machines in fixed-wing aircraft versus hand delivery in helicopters, helicopters were chosen, partially because of their greater manoeuvrability in mountainous terrain. A toll free number was placed on all baits, permitting the public to call in with any concerns that they might have. Not a single call was received during the baiting period. The public was well aware of the program through intensive media coverage, school talks, town meetings, and the involvement of local residents in the trapping program. One advantage of a low population density is a more rapid diffusion of information and achievement of consensus. Affected communities received first attention on 11 March 2002 using point infection control (Johnston & Tinline, 2002) to minimize risks of human exposure, and a southern baited containment zone to minimize the chances

of escape from the peninsula was completed on 16 March. One-kilometre grid lines were then set up, and the entire GNP baited (30–35 baits per square kilometre). As cases were also reported on the west side of White Bay (Jackson’s Arm), the Baie Verte Peninsula was also baited. All baiting was completed by 1 June 2002. Enhanced surveillance was conducted outside the baited area, to look for possible disease escapes. On 6 April 2002 a case was found in Cormack, outside of the baited zone, requiring an expansion of the baiting towards the critical limit of the Trans-Canada Highway, and an expansion of the enhanced surveillance zone. The last case was found on 6 May, resulting in a total of 21 positive cases (17 foxes, 3 sheep, and 1 cat). Surveillance continued for one more year with no further cases discovered. A total of 3743 carcasses were tested and 607,850 baits distributed over a 22,500 km2 area. This eradication program cost slightly more, at about $2.5 million, though it was carried out over a much larger area than the 1988 outbreak. This figure represents only the rabies-specific activities, such as bait purchase ($750,000), helicopter rental ($1 million), professional contracts, and specimen rewards, and did not include the cost of diverting existing salaried employees to the program. The eradication program had required that a significant number of people be diverted from their normal work for a very intensive activity. Approximately 500 thank you letters and pins were sent out to trappers, biologists, media, veterinarians, and public officials. Theories on the route of the disease’s entry onto the island included crossing on the ice from southern Labrador, as in 1988, or entering via an incubating pet. Crossing from Labrador could have happened around the time of the two cases in Cartwright in April–May 2002 as ice bridges had formed between Labrador and the northern tip of the GNP (Government of Canada, 2018a). It is difficult to confirm this contention since no cases were seen on the Island until seven months later in December at St Paul’s (see Figure 13.2) some 200 kilometres south of the ice bridge. Over the next six months 20 additional cases were reported within 100 kilometres of St Paul’s, suggesting that this was a recent introduction. Genetic studies supported this view (Nadin-Davis et al., 2008). No conclusion was reached on the actual source.

Discussion Rabies continues to circulate throughout Labrador with a sporadic incursion into Newfoundland. There is some evidence of cycling in Labrador but not in Newfoundland.

204

Newfoundland and Labrador

With such a large area and little understanding of patterns of fox movements and population changes, any predictions are based on a minimum of scientific knowledge. The absence of significant historical evidence of rabies in Labrador, followed by reports in the 1950s and then the 1980s, could suggest that, once introduced, it persists for a while then dies out until another introduction occurs from adjacent areas or even across the ice from Greenland. Research on variants of the virus that exist in Labrador provides supporting evidences that the virus can come from many directions (Nadin-Davis et al., 2008). On 12 January 2012 a red fox attacked some i­ nanimate objects in front of a residence in Wabush and was ­subsequently diagnosed with rabies. Confirmed cases in coloured foxes, arctic foxes, and dogs were also reported from neighbouring northern Quebec in 2011 and into 2012, in communities on Ungava Bay and Hudson Bay, showing that the virus was again active in the region. Throughout Labrador, red fox populations were high at the time. Arctic foxes, normally limited to northern Labrador, were seen much further south. Sea ice formed broadly along the coastline of Labrador and created bridges over to the island (Government of Canada, 2018b). All conditions necessary for a significant outbreak in Labrador and another extension onto the island of Newfoundland (as in 1988 and 2002) were in place, but no cases were reported. One problem associated with low human population densities in Newfoundland and even lower densities in Labrador is the detection of rabies in these remote areas since most reports of rabies are generally linked to human-animal interaction. Most of the population lives in isolated communities along the coast lines, leaving large interior areas uninhabited. In addition to lack of knowledge of the disease and treatment, isolation compounds the logistical problems dealing with the collection and movement of specimens to a laboratory for diagnosis. There are, however, striking differences in reporting between Labrador and the island of Newfoundland. These differences are seen in comparing submissions from Labrador and Newfoundland for foxes, the primary rabies vector (Figure 13.4). Almost half of the submissions from Labrador (49.7%) are positive, while only 4.5% of submissions from the island prove positive. This difference likely reflects three factors: (1) the long experience of rabies in Labrador spread from neighbouring Nunavik leads to more a discriminating view of what to submit; (2) the desire to keep the island free of rabies leads to a greater tendency to submit specimens for checking; and (3) rabies

cases in Labrador tend to lag one to two years behind cases in neighbouring Nunavik so there is, in effect, an early warning system in place. Three species of bats have been reported from the island, the little brown bat (Myotis lucifugus) (Table 13.1), the northern long-eared bat (Myotis septentriolis), and the hoary bat (Lasiurus cinereus), with only the little brown bat being found in Labrador. Only two cases of ­bat-related rabies have been reported in Newfoundland, that of a fox in 1989 at Grand Bruit on the island (Webster et  al., 1989) and a little brown bat in 2004 from Cartwright in Labrador (Newfoundland and Labrador Fisheries and Land Resources, 2019c). Following-up to the 1989 outbreak was the testing of 27 coloured fox trapped within 10 kilometres of the positive case, all with negative results. To better understand the bat populations, research in cooperation with Alyssia Park and Dr Hugh Broders of St Mary’s University (Park, 2010) was initiated in 2008. No further cases of bat rabies have emerged, but the understanding of these fascinating mammals has expanded with the hopes that more investigative work will follow. Further public education materials were published in 2012, including the production of a children’s story Uapikun Learns About Rabies and associated posters (Plate 2). The book was published in Innu-aimun (Sheshatshiu and Mushuau dialects) English, and French, and adapted into Inuttitut. Cree adaptations for northern Ontario are now being produced in cooperation with the Ontario government. The Chinook Project (chinookproject.ca), a veterinary outreach program for students at the Atlantic Veterinary College, has visited numerous northern Labrador communities in recent years (Government of Newfoundland and Labrador, 2018) to provide spay and neuter clinics and associated health checks to dogs that would otherwise never receive veterinary care. This is important in areas that do not have access to private veterinarians, such as Happy Valley Goose Bay and Labrador West Communities; vaccination may be provided by provincial staff, Innu band council, or the Nunatsiavut government. (Note that the Labrador Inuit Lands Claims Agreement set a precedent by including self-government provisions within the land claim. Nunaatsiavut is the first Inuit region in Canada to have achieved self-government.) The provincial government continues to support the Chinook Project both financially and logistically. The resultant decrease in stray dogs, the increased immunization status of these dogs and the increased sensitivity to animal care has helped reduce the risk of domestic animal rabies and associated risk to humans.

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A History of Rabies Management in the Provinces and Territories

Little is known about the movement of rabies in Labrador and in Canada’s north. Nadin-Davis et al. (2008) show that the region is open to movement of different viral isolates from the circumpolar region. Figure 13.5 shows that annual incidence in neighbouring Nunavik leads or coincides with incidence in Labrador. Simon et al. (2014) suggest that Labrador’s outbreaks are driven by the southeast movement of the disease through Nunavik. With the changes happening to the northern ice fields, there may be an increase in movement throughout this area. Breaking up of northern ice could increase the chances of the virus again moving across from Labrador to Newfoundland if ice bridges become more predictable and persistent. The historical record suggests that Labrador remains at the highest risk of rabies. The coastal areas of the island that had past intrusions from Labrador also remain at risk although the remainder of the island seems at low risk.

of specimens and risk assessment of specimens of animals with no human contact. Currently in Newfoundland and Labrador, any animal suspected of having rabies infection regardless of human exposure must be reported to the regional medical officer of health (RMOH) in the Department of Health and Community Services (DHCS), and the chief veterinary officer (CVO) in the Forestry and Agrifoods Agency (FAA), Animal Health Division (AHD). Reporting to the CVO is a requirement under the Animal Health and Protection Act (AHPA), while exposure to humans is reported to the RMOH or a designated member of the DHCS under the Communicable Disease Act (Government of Newfoundland and Labrador, 2018). Service Newfoundland and Labrador appoints and trains environmental health officers who are responsible for investigation of all suspect rabies exposure cases reported in humans. They work in collaboration with the RMOH and have the authority to issue quarantine orders. The FAA through its AHD and the Ecosystem Management Division are the agencies responsible for the surveillance and control of rabies in domestic and wild animals. Their responsibilities include enforcement of the AHPA; reporting all suspect cases of rabies to the CVO; training of field personnel in sample collection and the shipment of samples under the Transport of Dangerous Goods Regulations; identification of rabies in animals; laboratory diagnostics; public education; and research. Conservation

Rabies, 2014 to 2017 On 1 April 2014 the Canadian government withdrew all field services associated with rabies in Canada, that is, sample collection, submission, and control programs. While, by law, CFIA continues to test all specimens suspected of rabies that have had human or domestic animal contact, the provinces and territories are now responsible for collection

Figure 13.5: Annual rabies ­incidence in Nunavik and ­Labrador, 1986 to 2017.

Source: created from CFIA data.

206

Newfoundland and Labrador

officers (COs) are the field agents responsible for the enforcement, surveillance, and control of rabies. Veterinary and technical staff of AHD are involved in animal health assessment, euthanasia, sample collection, shipping of samples, laboratory testing at the Animal Health Laboratory, FAA, in St John’s, and carcass disposal. Bat submissions are sent to the Canadian Wildlife Health Cooperative at the Atlantic Veterinary College, Charlottetown, PE. ­Samples positive for rabies using the direct rapid immunohistochemical test (dRIT) are reported to and sent to Ottawa Laboratory Fallowfield (CFIA) for confirmation. Rabies test results are reported to the CVO, who relays the results to the RMOH/chief medical officer of health, Service Newfoundland and Labrador’s regional director and manager of operations, the director of population health in the regional Health Authority involved, the FAA regional compliance manager, and members of the Nunatsiavut Government (NG) as needed. The COs of the NG have the same authority and training as provincial COs. In the Innu communities, cooperation between the band councils, the AHD, provincial COs, public health nurses, and the Royal Canadian Mounted Police (RCMP) collectively supports the rabies education and control needs of the communities (Government of Newfoundland and Labrador, 2018). The provincial Department of Environment and Conservation is responsible for the Wildlife Act and actively

participates in or initiates wildlife research. Its knowledge of wildlife biology was crucial in the assessment of wildlife populations during disease control efforts against rabies. The RCMP and Royal Newfoundland Constabulary, as inspectors under the AHPA, can assist as required with suspect rabies cases. Municipal governments, either through their own city acts, by-laws under the Municipalities Act, or authority granted them under the AHPA, support the rabies program through control of stray animals or by assisting in the immediate needs of a the control program (Government of Newfoundland and Labrador, 2018). The development of the dRIT (Lembo et al., 2006) by the US Centers for Disease Control and Prevention, and the decision by the Canadian federal government to limit its involvement in wildlife surveillance testing, has prompted a number of provincial and territorial laboratories to consider the adoption of this technique. Had the dRIT test been available during the 2002–2003 outbreak, the 3743 tests could have been done in-house, rather than being prepared and shipped for analysis elsewhere, resulting in significant savings of time, effort, and cost. With the cautions placed around the transportation of potentially infectious substances, keeping transportation to a minimum improves diagnostic efficiency. Recent investments in laboratory infrastructure in this province have also expanded testing abilities and space that will make the practicalities of dealing with surge capacity much easier should another outbreak occur.

Acknowledgments The authors want to acknowledge the major contributions of Dr Hugh Whitney, Newfoundland and Labrador Department of Natural Resources (now retired), in describing the history of the province and the associated history of rabies. David Johnston, a pioneer in rabies control in Ontario and now retired from the Ontario Ministry of Natural Resources and Forestry, consulted with Dr Whitney to design and implement the early eradication and control programs in Newfoundland and Labrador. Together, they wrote the draft for the second and third major sections of this chapter. Although only a few other individuals are named in this chapter, the research, surveillance, and control activities for rabies in the province involved the efforts of hundreds of people. The authors thank them for the essential roles they have played and continue to play in rabies management in Newfoundland and Labrador.

References Acts of the General Assembly of Newfoundland passed in the ninth and tenth years of the reign of His Majesty King George V. (1919). St John’s, NL: J.W. Withers. Arctic dog disease and reports of Arctic dog disease. (1951). The Arctic Circular, 4(3), 47–49. Banyarda, A. C., Hartley, M., & Fooks. A. R. (2010). Reassessing the risk from rabies: A continuing threat to the UK? Virus Research, 152(1–2), 79–84. https://doi.org/10.1016/j.virusres.2010.06.007

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A History of Rabies Management in the Provinces and Territories Bélanger, C. (2004). Newfoundland history: Early colonization and settlement policy in Newfoundland. Retrieved from Marianopolis College website: http://faculty.marianopolis.edu/c.belanger/nfldhistory/NewfoundlandHistory-EarlyColonizationandSettlementof Newfoundland.htm Biggar, H. P. (Ed.). (1911). Patent granted by King Henry VII to John Cabot and his sons, March 1496. The precursors of Jacques ­Cartier, 1497–1534: A collection of documents relating to the early history of the Dominion of Canada. Ottawa, ON: Government Printing ­Bureau, 1911. Original document housed in the Public Record Office, London, England. Retrieved from Heritage Newfoundland and Labrador website: https://www.heritage.nf.ca/articles/exploration/1496-cabot-patent.php Briggs, D. J., Breesen, D. W., & Wunner, W. H. (2002). Vaccines. In A. C. Jackson & W. H. Wunner (Eds.), Rabies (pp. 371–400). San ­Diego, CA: Academic Press. Bumsted, J. M. (2000). Caesar Colclough. Dictionary of Canadian biography (Vol. 6). Retrieved from http://www.biographi.ca/en/bio /colclough_caesar_6E.html Dog bites Mountie. (1956, January 11). The Daily News, p. 1. Elton, C. (1931). Epidemics among sledge dogs in the Canadian Arctic and their relation to disease in the arctic fox. Canadian Journal of Research, 5, 673–692. Epidemiological bulletin. (1965). Canadian Medical Association Journal, 93, 889. Follman, E. H., Ritter, D. G., & Baer, G. M. (1988). Immunization of arctic foxes (Alopex lagopus) with oral rabies vaccine. Journal of Wildlife Diseases, 24(3), 477–483. https://doi.org/10.7589/0090-3558-24.3.477 Government of Canada. (2018a). 1: Daily ice chart – E/NE Newfoundland – WIS27 – 2002/04/26. Retrieved from Environment Canada Ice Archive website: https://iceweb1.cis.ec.gc.ca/Archive/page1.xhtml Government of Canada. (2018b). 1: Daily ice chart – E/NE Newfoundland – WIS27 – 2002/02/15. Retrieved from Environment ­Canada Ice Archive website: https://iceweb1.cis.ec.gc.ca/Archive/page1.xhtml Government of Newfoundland and Labrador. (1996, October 9). End of rabies outbreak in Labrador [Press release]. Retrieved from Newfoundland and Labrador Forest Resources and Agrifoods website: http://www.releases.gov.nl.ca/releases/1996/forest/1009n06.htm Government of Newfoundland and Labrador. (2003a, March 31). Trapping season extended for fox and coyote on Northern and Baie Verte peninsulas [Press release]. Retrieved from Newfoundland and Labrador Tourism, Culture and Recreation website: https://www .releases.gov.nl.ca/releases/2003/tcr/0321n02.htm Government of Newfoundland and Labrador. (2003b, October 16). Revised carcass collection program for fox, lynx and coyote [Press ­release]. Retrieved from Newfoundland and Labrador Tourism, Culture and Recreation website: https://www.releases.gov.nl.ca/ releases/2003/tcr/1016n03.htm Government of Newfoundland and Labrador. (2003c, December 2). Revised fox carcass collection – Rabies Eradication Program [Press release]. Retrieved from Newfoundland and Labrador Tourism, Culture and Recreation website: https://www.releases.gov.nl.ca /releases/2003/tcr/1202n05.htm Government of Newfoundland and Labrador. (2011a). About this place. Retrieved from Newfoundland and Labrador Tourism website: https://www.newfoundlandlabrador.com/about-this-place/nl-facts Government of Newfoundland and Labrador. (2011b). Eastern coyote in Newfoundland and Labrador. Retrieved from Department of Environment and Conservation, Wildlife Division website: https://www.flr.gov.nl.ca/publications/wildlife/coyote_harvest1.pdf Government of Newfoundland and Labrador. (2017). Government of Newfoundland and Labrador statistics, 1971–2017. Retrieved from https://www.stats.gov.nl.ca/Statistics/Population/PDF/Annual_Pop_Prov.PDF Government of Newfoundland and Labrador. (2018). Rabies policy manual for Newfoundland and Labrador. Retrieved from ­ewfoundland and Labrador Forestry and Agrifoods website: https://www.faa.gov.nl.ca/agrifoods/animals/health/pdf/Rabies_ policy_manual.pdf. Great Britain. Colonial Office. (1815). D’Alberti papers, Vol. 25, 1815 (Correspondence, incoming and outgoing, between the Colonial Office and the Governor’s Office in Newfoundland). Letter of 17 September 1815. London, England: Colonial Office. Retrieved from Memorial University of Newfoundland and Labrador, Centre for Newfoundland Studies Digital Archive Initiative website: http:// collections.mun.ca/PDFs/cns_colonia/A51_V25.pdf Grenfell, W. T., Daly, R. A., Delabarre, E. B., Townsend, C. W., Allen, G. M., Johnson, C. W., ... Rathbun, M. J. (1913). Labrador, the country and the people. New York, NY: Macmillan. Hawkes, E. W. (1916). The Labrador Eskimo, Memoir 91, No. 14, Anthropological Series, Geological Survey, Canada Department of Mines. Ottawa, ON: Government Printing Bureau. Hillier, J. K. (1998). Moravian voyages. Retrieved from Newfoundland and Labrador Heritage website: http://www.heritage.nf.ca /exploration/moravian_voyages.html Johnston, D. H. (1990, April). Wildlife rabies vaccine baiting trials in North America [Background paper 5]. In G. Hugoson (Chair), Workshop on Arctic rabies. Workshop conducted by World Health Organization/Department for Management of Noncommunicable Diseases, Disability, Violence and Injury Prevention (NVI), Uppsala, Sweden.

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Newfoundland and Labrador Johnston, D. H., & Beauregard. M. (1969). Rabies epidemiology in Ontario. Bulletin Wildlife Diseases Association, 5(3), 357–369. https://doi.org/10.7589/0090-3558-5.3.357 Johnston, D. H., & Fong, D. W. (1992). Epidemiology of arctic fox rabies. In K. Bögel, F.-X. Meslin, & M. Kaplan (Eds.), Wildlife rabies control (pp. 45–49). Kent, England: Wells Medical. Johnston, D. H., & Tinline, R. R. (2002). Rabies control in wildlife. In A. C. Jackson & W. H. Wunner (Eds.), Rabies (ch. 14). San Diego, CA: Academic Press. Johnston, D. H., Voigt, D. R., MacInnes, C. D., Bachmann, P., Lawson, K. F., & Rupprecht, C. E. (1988). An aerial baiting system for the distribution of attenuated or recombinant rabies vaccines for foxes, raccoons, and skunks. Review of Infectious Diseases, 10(4), S660–S664. https://doi.org/10.1093/clinids/10.Supplement_4.S660 Kolenosky, G. B., & Johnston, D. H. (1967). Radio-tracking timber wolves in Ontario. American Zoologist, 7(2), 289–303. https:// doi.org/10.1093/icb/7.2.289 Lawson, K. F., Black, J. G., Charlton, K. M., Johnston, D. H., & Rhodes. A. J. (1987). Safety and immunogenicity of a vaccine bait containing ERA strain of attenuated rabies virus. Canadian Journal of Veterinary Research, 51, 460–464. Lembo, T., Niezgoda, M., Velasco-Villa, A., Cleaveland, S., Eblate, E., & Rupprecht, C. E. (2006). Evaluation of a direct, rapid immunohistochemical test for rabies diagnosis. Emerging Infectious Diseases, 12(2), 310–313. https://doi.org/10.3201/eid1202.050812 Nadin-Davis, S., Muldoon, F., Whitney, H., & Wandeler, A. I. (2008). Origins of the rabies viruses associated with an outbreak in ­Newfoundland during 2002–2003. Journal of Wildlife Diseases, 44(1), 86–98. https://doi.org/10.7589/0090-3558-44.1.86 Newfoundland. House of Assembly. (1919). Proceedings of the House of Assembly and Legislative Council during the eight session of the twenty-third General Assembly of Newfoundland. St John’s, NL: Evening Herald. Retrieved from Memorial University of ­Newfoundland and Labrador, Centre for Newfoundland Studies Digital Archive Initiative website: http://collections.mun.ca /PDFs/h_assembly/ProceedingsoftheHouseofAssemblyandLegislativeCouncil1919.pdf Newfoundland and Labrador Fisheries and Land Resources. (2019a). Listing of all cases of rabies reported: 1981 Labrador only. ­Retrieved from Forestry and Agrifoods website: https://www.faa.gov.nl.ca/agrifoods/animals/health/pdf/rabies_1981.pdf Newfoundland and Labrador Fisheries and Land Resources. (2019b). Listing of all cases of rabies reported: 1996 Labrador only. ­Retrieved from Forestry and Agrifoods website: https://www.faa.gov.nl.ca/agrifoods/animals/health/pdf/rabies_1996.pdf Newfoundland and Labrador Fisheries and Land Resources. (2019c). Listing of all cases of rabies reported: 2004 Labrador only. ­Forestry and Agrifoods website: https://www.faa.gov.nl.ca/agrifoods/animals/health/pdf/rabies_2004.pdf Northcott, T. (1975). Long-distance movement of an arctic fox in Newfoundland. Canadian Field Naturalist, 89, 464–465. Paddon, H. (1923). Winter season at North West River. Among the Deep Sea Fishers, 21(3), p. 92. Retrieved from Memorial University of Newfoundland and Labrador, Centre for Newfoundland Studies Digital Archive Initiative website: http://collections.mun.ca /PDFs/hs_fisher/ADSF2103.pdf Park, A. P. (2010). Factors affecting the distribution and roost-site selection of bats on the Island of Newfoundland (Master’s thesis, Saint Mary’s University). Retrieved from http://library2.smu.ca/bitstream/handle/01/21888/park_allysia_c_masters_2010.PDF Pedley, C. (1863). The history of Newfoundland from the earliest times to the year 1860. London, England: Longman, Green, Longman, Roberts & Green. Powell, G. (2011, May). Conversation with retired RCMP officer George Powell and examination, with permission, of his personal files (H. Whitney, Interviewer). Saunders, D., & Hearder, V. (1985). Dog sickness. Them Days (Stories of Early Labrador), 11(2), 48–51. Simon, A., Bélanger, D., Leighton, P., Hurford, A., & Whitney, H. (2014). Mouvement du virus de la rage dans le nord du Québec et au Labrador: Preliminary report. St John’s: Government of Newfoundland and Labrador. Tabel, H., Corner, A. H., Webster, W. A., & Casey, C. A. (1974). History and epizootiology of rabies in Canada. Canadian Veterinary Journal, 15(10), 271–281. Territorial evolution, 1670–2001. (2012). Retrieved from Historical Atlas of Canada: Online Learning Project website: http://www .historicalatlas.ca/website/hacolp/national_perspectives/boundaries/UNIT_17/U17_Timeline/U17_timeline_1713.htm Tucker, B., & Fong, D. W. (1989). Rabies in Newfoundland. St John’s: Government of Newfoundland Wildlife Division. Voigt, D. R., & Earle, B. E. (1983). Avoidance of coyotes by red fox families. Journal of Wildlife Management, 47(3), 852–857. https://doi .org/10.2307/3808625 Voigt, D. R., & Tinline, R. R. (1980). Strategies for analyzing radio tracking data. In C. J. Amlaner & D. W. Macdonald (Eds.), A ­handbook of biotelemetry and radio tracking (pp. 387–404). Oxford, England: Pergamon Press. Webster, W. A., Casey, G. A., & Charlton, K. M. (1986). Major antigenic groups of rabies virus in Canada determined by anti-nucleocapsid monoclonal antibodies. Comparative Immunology and Microbiology Infectious Diseases, 9(1), 59–69. https://doi.org/10.1016/0147-9571(86) 90076-7 Webster, W. A., Casey, G. A., & Charlton, K. M. (1989). Bat-induced rabies in terrestrial mammals in Nova Scotia and Newfoundland. Canadian Veterinary Journal, 30, 679.

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A History of Rabies Management in the Provinces and Territories Whitney, H. G. (1988a). Rabies in Canada. Canadian Veterinary Journal, 29, 554. Whitney, H. G. (1988b). Newfoundland – Rabies outbreak. Canadian Veterinary Journal, 29, 665. Whitney, H. G. (1989). Newfoundland – Update on rabies. Canadian Veterinary Journal, 30, 522–523. Whitney, H. G. (1991). Regulations changed for animal movement. Canadian Veterinary Journal, 32, 520. Whitney, H. G. (1992a). Rabies in Labrador. Them Days (Stories of Early Labrador), 17(3), 39–44. Whitney, H. G. (1992b). Rabies epizootic in Labrador. Canadian Veterinary Journal, 33, 756. Whitney, H. G. (1997). Rabies in Labrador – 1996. Canadian Veterinary Journal, 38, 242–243. World Health Organization. (1973). Expert Committee on Rabies: 7th report (Technical Report Series 709). Geneva, Switzerland: Author

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14a Canada’s North YUKON

Mary Vanderkop,1 David J. Gregory,2 and Philip Merchant3 1

Chief Veterinary Officer, Whitehorse, Yukon, Canada Canadian Food Inspection Agency (Retired), Ottawa, Ontario, Canada 3 Laboratory Technician (Retired), Whitehorse, Yukon, Canada

2

Place Yukon is derived from the native word Yu-kun-ah meaning “Great River” or “Big Steam” in the Gwich’in dialect (Wonders, 2011). Originally, Yukon was a part of the Hudson’s Bay Company administered North-Western Territory. The Canadian government purchased the territory from the Hudson’s Bay Company in 1870, renaming the area the North-west Territories and in 1895 established districts within the territory named the Ungava, Mackenzie, Yukon, and Franklin districts. Yukon (Figure 14a.1) was established as a separate territory in 1898 by the Yukon Territory Act (“Territorial Evolution,” 2012; see Overview, Part 3). During the Klondike Gold Rush of 1897–1898, Dawson became the capital. When the gold was gone and after the Alaska Highway was built in 1942, Whitehorse became the capital in 1953 (Wonders, 2011). With a total land mass of 482,443 km2, or about 4.8% of Canada’s total land mass, Yukon is the smallest of the three territories in Canada. It is located in the northwest of Canada and bounded on the east by the Northwest Territories, British Columbia to the south, the US state of Alaska to the west, and the Beaufort Sea to the north. Most of Yukon is boreal forest with the exception of a small strip of tundra on the north coast. In general, the climate is dry, subarctic, protected from the Arctic by northern mountains and sheltered from the Pacific by the coastal mountains. In the south, adjacent to the British Columbia border, the climate is humid continental.

Yukon has a population of 38,455 (Yukon Bureau of Statistics, 2018), 87% of whom live in the three largest communities: Whitehorse (pop. 38,455), Dawson (pop. 2226), and Watson Lake (pop. 1464). The remainder live in small settlements scattered along the major highways. Old Crow, beyond the reach of highways in the north, has a population of only 257. The territory is officially bilingual (English and French), although English is the mother tongue of 83.4% of the population and French is the mother tongue of only 4.4% of the population. Although there are 14 First Nations speaking eight languages, only 1.9% of the population listed themselves as Indigenous speakers; 10% report other languages as their mother tongue, and 90.7% report that English is the language spoken most often at home (Yukon Bureau of Statistics, 2016).

Rabies in Yukon One of the earliest reported outbreaks of rabies in Yukon occurred at the time of the Klondike Gold Rush. The outbreak probably started in 1898 during the influx of people and their animals at the time of the Gold Rush. The outbreak was reported by the Toronto Daily Star on 9 March 1901 (“Epidemics of Rabies in Dawson,” 1901). Also reported as an epidemic of rabies in Dawson, describing it as “dumb rabies,” with the North-West Mounted Police issuing an order to tie up all dogs (“Dogs Must Be Tied or Shot,” 1901). This outbreak resulted in the slaughter of many valuable dogs, the value placed on a malamute or

A History of Rabies Management in the Provinces and Territories

Figure 14a.1: Yukon Territory. Source: compiled from Natural ­Resources Canada maps.

husky dog at that time was $300 (“Mad Dogs Increasing,” 1901); the death of at least one man (“Did Rabies Kill Ewing?,” 1901; “A Fatal Case,” 1901); and speculation as to the cause of the outbreak (“Poison or Hydrophobia?,” 1900) (see also Chapter 3b). The case of a man bitten by a wolf in Whitehorse in 1904 and dying in British Columbia in 1905 is related in Chapter 3b. Williams (1949) describes possible rabies in a red fox in Yukon, the result of an epizootic in Alaska in 1945– 1947 that spread from the area of the Yukon River, up through the Yukon Flats, into the upper reaches of the

Porcupine, Black and Salmon Fork Rivers, and into Old Crow in Yukon. The red fox specimen reported on was in a state of autolysis and did not demonstrate Negri bodies. Presumably this incursion from Alaska went no farther. Several small outbreaks of rabies occurred during 1952 to 1975 (Table 14a.1). These outbreaks were, possibly, the result of incursions of arctic fox rabies from the neighbouring Northwest Territories, which experienced outbreaks in Aklavik, Inuvik, Tuktoyaktuk, and Fort McPherson during 1952, and in Tuktoyaktuk and Sachs Harbour in 1963, 1965, and 1975 (see Chapter 14c). While the Northwest

212

Yukon

Table 14a.1  Total positives for Yukon, 1952 to 2017. Year

Total

1952

Table 14a.2  Submissions for rabies testing from Yukon, 1985 to 2009.

Dog

Cat

1

 

 

1

1964

1

 

 

1

1970

2

1

1973

1

 

 

1

1975

1

1

 

 

1

Arctic Fox

 

Note: only years with positives are shown. Source: compiled from CFIA data.

Territories experienced large outbreaks of arctic fox rabies in 1974, 1978, and 1982 (see Chapter 14b), these were not detected in Yukon. The cases of a dog and cat in 1970 at Whitehorse and Pelly Crossing are difficult to explain but may be remnants of earlier incursions or may reflect contact with wildlife reservoirs such as bats. It is also possible that the locations recorded were those of the human patient and not the location of the interaction with the animal. Since 1975, no positive rabies cases have been reported in Yukon. Submissions data has been available since 1985, and submissions have primarily been in dogs (Table 14a.2). Most submissions were from the Whitehorse area or areas south of the town, with the exception of submissions from Old Crow and Dawson City. Interestingly, there were two bats submitted: one whose species was unspecified and one yuma bat (Myotis yumanensis). Although there were no submissions in 2012, a coyote that bit a child was killed by conservation officers and tested by the direct rapid immunohistochemical test (dRIT) (see Chapter 24c) by the Ontario Ministry of Natural Resources and Forestry. The result was negative. This test was used because the bite didn’t break the skin, and the animal appeared to have been habituated to humans but was stalking people before the bite. Thus, the incident did not meet the criteria of the Canadian Food Inspection Agency (CFIA) for rabies testing that included bite severity and potential for human exposure.

Species

Total

Dog

19

Cat

3

Arctic fox

2

Coyote

2

Ferret

1

Grizzly bear

1

Little brown bat

1

Lynx

1

Mouse

1

Red fox

1

Wolf

1

Yuma bat

1

Total

34

Source: compiled from CFIA data.

vectors in other northern jurisdictions, the number of these species received by the Yukon Environment laboratory was historically low. An established wolverine health monitoring program that examined skinned wolverines submitted by trappers throughout Yukon offered an opportunity to sample the whole brain or a portion of the brain (Barrat, 1996) for rabies surveillance. The 45 brains tested in the first year were all negative for rabies. In 2012, the rabies surveillance sampling was expanded to include any opportunistically collected, road-killed, or trapper submitted carnivores and bears that were killed for human contact. Only wolverines from the trappers in the most northern zones of Yukon and any wolverines that had evidence of porcupine quills when the carcass was examined were selected for testing. Opportunistic sampling of wildlife has continued and there have been no positive fluorescent antibody tests from surveillance samples to date. The numbers of each species tested between 2010 and 2017 are summarized in Table 14a.3.

Active Surveillance In late 2010 an active rabies program was initiated within the Animal Health Unit of the Yukon Department of Environment, and the CFIA agreed to support rabies surveillance testing of opportunistic samples from wild carnivores. While arctic and red fox populations were the most desirable species to monitor because they are the primary

Wildlife Management Programs Since the 1980s, Yukon has produced six comprehensive predator management programs that have included wolf

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A History of Rabies Management in the Provinces and Territories

This large land mass and small, widely distributed populations has challenged rabies management in terms of education, surveillance, specimen collection, and delivery, as well as treatment of human rabies contacts. Most of the population is located at Dawson City; which to the south and is surrounded by mountains; the Selwyn Mountains to the east bordering Alberta, the Pelly Mountains to the south along the BC border, Kluane National Park Reserve to the southwest, and the Ogilvie and Wernecke Mountain ranges to the north. These barriers may limit movement of animals that can spread rabies and make any surveillance activities difficult. Conversely, the lack of any rabies cases may induce apathy or indifference to the management measures in place. Historically (Table 14a.1) there have been relatively few instances when rabies was a threat. The wildlife species most often responsible for transmitting rabies to domestic animals and humans in other provinces – the skunk (Mephitis mephitis) and raccoon (Procyon lotor), are not found in Yukon. Foxes and bats are present, however, and may represent a potential reservoir. A lingering concern is the occurrence of rabies in arctic foxes in Alaska and the neighbouring Northwest Territories. Currently, there is also concern that climate change may favour the expansion of the range of red foxes (Vulpes vulpes) and an overlap with arctic fox (Alopex lagopus) populations, increasing the risk of rabies spreading to red foxes, which are more likely to inhabit urban centres and have contact with domestic animals. Fortunately, the very small human population does mean that there have been few encounters between people and wildlife and correspondingly few submissions from Yukon for rabies testing.

Table 14a.3  Negatives by CFIA fluorescent antibody test, 2010 to 2017. Species

Negatives

American marten

1

Arctic fox

4

Black bear

30

Coyote

31

Grizzly bear

13

Little brown bat

13

Lynx

102

Red fox

43

Wolf

80

Wolverine

82

Total

399

Source: compiled from CFIA data.

control to support caribou and moose populations in Yukon. From 1992 Yukon functioned under a wolf conservation and management plan that was renewed in 2012 (Yukon Wolf Conservation and Management Plan Review Committee, 2012). The plan has several goals that provide ethical and scientific guidelines for managing wolves and includes conditions for carrying out wolf control. At least 58 wolves have tested negative since 2010, many carcasses sourced from trappers participating in wolf control programs, so this does provide for a means of surveillance action for wolves and other wildlife in Yukon.

Early Rabies Management

Management of Rabies in Yukon

ROYAL CANADIAN MOUNTED POLICE

The early history of the Royal Canadian Mounted Police (RCMP) involvement with rabies management is discussed in Chapter 14b for the Northwest Territories. This police force was important in dog control during the outbreak of canine rabies during the Klondike Gold Rush (“Looks Like Mad Dogs,” 1900). Typically, the role of the RCMP included dog control and dissemination of information on rabies. Dog control in isolated communities meant restraining strays, muzzling them, or destroying them (see Figure 14a.2). After 1950 a rabies vaccine became available, and the RCMP provided vaccination clinics for the communities. The vaccine was provided to the designated officers under the Health of

General Considerations While the smallest of the three territories in Canada, Yukon is still a very large land mass with a sparse population mostly located in Whitehorse, the capital. It is a land of many rivers, lakes, and mountain ranges, mostly inaccessible except by the Alaska Klondike, Dempster, and Campbell Highways (Figure 14a.1). Besides these highways, transport of goods and people is by air, with an international airport at Whitehorse; regional airfields at Old Crow, Dawson City, and Watson Lake; and airstrips or water access in many of the other smaller communities.

214

Yukon

Figure 14a.2: Advertisement in the Semi-Weekly Klondike Nugget, 29 May 1901.

Animals Act and Regulations and sent to the Northwest Territories and Yukon. Agriculture Canada records show that between 1961 and 1964, some 2500 doses of vaccine were shipped to Yukon. Earlier records show nearly 2000 animals vaccinated by the RCMP between 1955 and 1960, and 885 in 1976. This was the period of rabies outbreaks in the Arctic and two cases occurred in the Northwest Territories during 1952 and 1964. The RCMP was also responsible for the collection and transport of specimens to the nearest laboratory for diagnosis. The RCMP withdrew their services from this non-police function in 1995 because of limited resources.

of the Environmental Health Services (EHS). Patients requiring rabies treatment are dealt with through Yukon’s two hospitals or 13 health centres in the major communities (Government of Yukon, 2019a). The Health centres may have physicians or nurses on staff. Disease monitoring in wild and domestic animals is the mandate of the AHU, with oversight by the chief veterinary officer (CVO) and staff of the AHU.

Risk Assessment and Management

The decision to test animals that contact or bite people and the decision on administration of post-exposure prophylaxis (PEP) was historically delegated to the staff in Environmental Health or Communicable Disease at Yukon HSS. Local RCMP, conservation officers, or animal control officers were at times asked to provide local support for animal control when a bite from a wild or domestic animal occurred, especially in the smaller, remote communities in Yukon. This resulted in concern about shared responsibility and how to ensure personal protective measures, including vaccination, were implemented for individuals dealing with animals. There was considerable inconsistency as to how rabies suspect animals were managed, and remote communities have limited facilities available to provide for secure holding and observation of either wild or domestic animals. In August 2011 Yukon government departments with shared responsibility for rabies management developed a manual that provided rabies risk management guidelines. This document has been updated and is available online (Government of Yukon, 2019a). The updated version guides the decision-making process for rabies risk assessment. Inservice training sessions are provided for primary health care providers, as are updates for other partners, guided by standardized presentations and delivered by the staff of

Present Day Rabies Management CANADIAN FOOD INSPECTION AGENCY (CFIA)

Rabies is named in the federal Health of Animals Act and Regulations, and any suspect case must be reported to and ultimately diagnosed by the CFIA. In the absence of a CFIA district office in Yukon, and because of size of the territory combined with the low population density, CFIA veterinarians have not been traditionally available to provide oversight to animal management or sample collection and transport for testing. The district veterinarian in Dawson Creek, BC, has been available for consultation and has been responsible for decision making and advice from that office. TERRITORIAL RABIES MANAGEMENT

The management of rabies in Yukon is through two Yukon government departments: Health and Social Services (HSS) and the Animal Health Unit (AHU) within the Department of Environment. Within HSS, rabies is under the control of the chief medical officer of health (CMOH), Yukon Communicable Disease Control staff, and the staff

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A History of Rabies Management in the Provinces and Territories

EHS, the CMOH, and the CVO to assist in consistent implementation. The guideline was shared with the district veterinarian (CFIA) during development and has been shared with regional CFIA staff since it was first published.

the CVO has had the authority to quarantine or order destruction of animals that are a hazard to human or animal health. In addition, staff within EHS may order a rabies suspect animal to be held for observation or to be killed for testing. The AHU supports animal capture and containment and advises on the recommended procedures for animal handling, euthanasia, and carcass handling. Animals may be contained or killed by AHU staff or in cooperation with local veterinarians, animal control officers, or conservations officers, but the responsibility for the animal management remains with the AHU, currently in consultation with the district veterinarian of the CFIA. When the animal involved is a wildlife species, conservation officers will facilitate capture or killing the animal for testing, recognizing that identifying a wild suspect animal may not be possible. When no local animal control officer or veterinarian is available, the CVO or program veterinarian provides direct support to the community by travelling to the location and working with RCMP and local officials to confine and quarantine or kill the animal and obtain samples for testing. The CVO may liaise with the district veterinarian in Dawson Creek, BC, to expedite rabies submissions involving animal/human contact. The cost of specimen submission is borne by AHU.

Rabies Risk Evaluation

The primary health care providers located at the community health centres are requested to complete a rabies risk investigation form for any person seeking medical attention for an animal bite or exposure to a possible rabid animal. They also provide the patient with copies of a fact sheet that outlines treatment of bite wounds, rabies risk, what happens to an animal that bites, and what the animal owner can expect. The criteria for reporting incidents with domestic animals are broad, and the form documents whether the animal’s owner can be identified, its rabies vaccination status, and if the animal had contact with any wildlife. The form also includes information specific to the patient. The EHS coordinates the rabies risk evaluation under the authority of the Yukon Public Health and Safety Act, and gathers additional information on the details of the animal contact, including the circumstances of the animal’s behaviour to confirm whether the encounter was provoked, confirmation of vaccination status, and whether the animal can be observed for 10 days after the encounter. This information is relayed to the CVO, who makes a recommendation with respect to the risk of rabies based on details of the encounter. The CMOH receives all information and decides whether rabies PEP is required and informs the primary health care provider of this decision within 48 hours.

Transportation of Samples

Transportation of diagnostic specimens to the CFIA laboratory in Lethbridge, Alberta, is hampered by limited direct air cargo services between Whitehorse and Lethbridge. Courier transport out of Yukon is usually required, with delivery to Lethbridge within 48 hours of when the samples were shipped, at a cost of $300 to $400 per shipment. Diagnostic samples are sometimes transported between remote communities and Whitehorse by the AHU staff that have driven to the community to euthanize the animal and collect the sample, or they may be shipped by direct flight if AHU staff have been able to contract with a local veterinarian or government official to manage the sample collection in the community. These issues of sample delivery can result in delays in excess of a week between the time of the incident and when the sample arrives in Lethbridge for testing.

Animal Health Unit Responsibility

Yukon AHU and CVO are responsible to coordinate and manage the Yukon government’s response to any animals suspected of having rabies. With a decision by the CMOH to initiate PEP for the patient, the CVO contacts the CFIA district veterinarian in Dawson and provides them with all supporting documentation. Based on this documentation and in consultation with the CVO, the district veterinarian decides whether the circumstances of the animal encounter meet the criteria for rabies testing by the CFIA. If a rabies test is authorized, the AHU takes responsibility to coordinate sample collection and submission for rabies testing. Rabies specimen collection containers are provided by CFIA, and a quantity are maintained at the AHU in Whitehorse as well as in several of the remote communities. The remote location of Yukon communities requires a locally coordinated response in a timely manner. Since a revised Animal Health Act came into effect in January 2014,

Non-vaccinated Animals

The CMOH does not initiate PEP when the risk of rabies in the animal involved is assessed as negligible or minimal. This has been the case with the vast majority of instances since 2011, typically because it is almost invariably determined that the bite was provoked from the perspective of the animal. In circumstances involving domestic animals that

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Yukon

do not have current vaccination status, the CVO and EHS recommend that the animal be observed for 10 days and any abnormal clinical signs or illness be reported to the CVO immediately. This is not an official quarantine but provides an increased level of confidence that the risk evaluation is valid. In all instances thus far, the animals have remained normal. It is recommended that the animal receive vaccination for rabies after the observation period in all these instances.

Discussion Wildlife rabies appears to be very low or absent in Yukon. A total of 43 domestic animals from Yukon were tested by the CFIA laboratories for rabies between 1985 and 2017, and all were negative for rabies virus. These results have recently been supplemented by negative results from testing of over 200 wildlife samples (Table 14a.2). While rabies is known to occur in Alaska along the Beaufort Sea coast in foxes and in other species in the interior (“Animal Rabies,” 2000; “Animal Rabies,” 2011) the intervening mountain ranges may be a sufficient barrier to limit vector movement into Yukon. Rabies is also known from the Mackenzie Delta to the east of Yukon’s north coast into the Northwest Territories. Again, mountains along the northern and eastern borders of Yukon may inhibit spread from the Mackenzie Delta and the Northwest Territories. There is also little tradition of arctic fox trapping in Yukon, which may limit potential exposure to a higher risk species. It is important to continue targeted surveillance to determine if and when rabies does occur, and to support a risk-based approach to decision making for human health care in cases where animal encounters occur. The submission of the yuma bat for rabies testing was a first for Yukon. The yuma bat is difficult to differentiate from the little brown bat except by genetic means, but is quite possibly the species identified in Table 14a.2. A recent review of bat specimens in the Alaska museum has shown that the yuma bat is in southeast Alaska (Olsen et  al., 2014). With further research into species differentiation and the climate changes which are occurring, these bats, and others may yet be found in Yukon (Government of Yukon, 2019b). For example, the western long-eared bat (Myotis evotis) lives in northern BC while the California bat (Myotis califonicus) is found in southeast Alaska. The long-legged bat (Myotis volans), Keen’s bat (Myotis keenii), and the silver-haired bat (Lasionycteris noctivagans) have been found in northern BC and Alaska. Audio recordings indicate some of these species may be moving into southern Yukon. On the east side of the territory, five species of bats have been found in the Nahanni River drainage, close to Yukon’s southeast border, and include the western long-eared bat, the long-legged bat, the little brown bat (Myotis lucifugus), the northern long-eared bat (Myotis septenrionalis), and the big brown bat (Eptesicus fuscus). These bat species and others maybe an important event for Yukon given the possibility of rabies in these species as seen in BC (see Table 6.3 and Chapter 27).

Rabies Confirmation

If rabies is confirmed from an animal submission, the CVO has authority to issue quarantines, order destruction of animals, and coordinate testing of animals that are known or suspected to have been in contact with the positive animal. The CMOH and EHS have primary responsibility for the communication and risk mitigation for people who were in contact or within the affected community. The AHU currently supports EHS with communication plans to advise the public in the event of a rabies positive animal in a community. The AHU also provides local logistical support for further surveillance, sampling, and transport of samples to CFIA testing laboratories.

Vaccination

Rabies vaccination is not mandated for any domestic species in Yukon. While veterinary services for companion animals are available in major Yukon centres, such as Whitehorse, Dawson City and Haines Junction, the smaller and more remote communities are not consistently serviced by private veterinary practitioners. Although lay vaccination programs have been used in other jurisdictions in the Arctic, this type of program has not been offered in Yukon to date. A low level of general concern about rabies may relate to the relative lack of confirmed rabies cases historically in Yukon. The Yukon government has coordinated several pet neutering clinics in remote communities in Yukon in the past several years, and in some instances remote communities have contacted volunteer organizations to provide local veterinary care. The clinics sponsored by the Yukon government have included rabies vaccination for all animals neutered, but the total number of pets that are immunized in this manner is not known and likely to be a small percentage of the population. Yukon humane societies require vaccination and neutering of all animals that are adopted, approximately 200 per year. The city of Whitehorse Animal Control by-law has a provision to seize and quarantine for 14 days any animal that is not vaccinated for rabies and bites a person, and this authority is exercised for any dog bite reported in the city.

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References Animal rabies: 1998–February 2000. (2000). State of Alaska Epidemiology Bulletin, 5. Retrieved from Alaska Department of Health and Social Services website: http://www.epi.hss.state.ak.us/bulletins/docs/b2000_05.pdf Animal rabies in Northwestern Alaska. (2011). State of Alaska Epidemiology Bulletin, 6. Retrieved from Alaska Department of Health and Social Services website: http://epibulletins.dhss.alaska.gov/Document/Display?DocumentId=157 Barrat, J. (1996). Simple technique for the collection and shipment of brain specimens for rabies diagnosis. In OIE Monograph-Laboratory Techniques in Rabies (4th ed., Appendix 1). Geneva, Switzerland: World Health Organization. Retrieved from WHO website: https://www.who.int/rabies/en/simplified_technique_collection_brain_specim_rabies_diagnosis.pdf Did rabies kill Ewing? (1901, May 5). Semi-Weekly Klondike Nugget, col. 3, p. 3. Library and Archives Canada, Textual Documents, Reference Number AN 7502197 and AN 7502202. Dogs must be tied or shot. (1901, May 9). Semi-Weekly Yukon Nugget, p. 1. Library and Archives Canada. Textual Documents. Reference Number AN 7502197 and AN 7502207. Epidemics of rabies in Dawson, Yukon. (1901, March 9). Toronto Daily Star, p. 11. A fatal case of hydrophobia is reported in Dawson. (1901, May 11). The Globe and Mail, p. 5. Government of Yukon. (2019a). Yukon communicable diseases control: Rabies. Retrieved from Department of Health and Social Services website: http://www.hss.gov.yk.ca/pdf/ycdcrabies.pdf Government of Yukon. (2019b). A guide to Yukon bats. Retrieved from https://yukon.ca/sites/yukon.ca/files/env/env-yukon-bats.pdf Looks like mad dogs – Mad dog shot. (1900, December 16). Semi-Weekly Klondike Nugget, col. 2, p. 6. Library and Archives Canada. Textual Documents, Reference Number: AN 7502197 and AN 7502207. Mad dogs increasing – Police killed valuable malamute Saturday afternoon. (1901, December 25). Semi-Weekly Klondike Nugget, p. 5. Library and Archives Canada. Textual Documents. Reference Number AN 7502197 and AN 7502207. Olson, L., Gunderson, A., MacDonald, S. O., & Blejwas, K. (2014). First records of yuma myotis (Myotis yumanensis) in Alaska. Northwestern Naturalist, 95(3), 228–235. .https://doi.org/10.1898/13-29.1 Poison or hydrophobia? (1900, November 22). Semi-Weekly Klondike Nugget, p. 2. Library and Archives Canada, Textual Documents. Reference Number AN 7502197 and AN 7502207. Territorial evolution, 1670–2001. (2012). Retrieved from Historical Atlas of Canada: Online Learning Project website: http://www.historicalatlas.ca/website/hacolp/national_perspectives/boundaries/UNIT_17/U17_Timeline/U17_timeline_1713.htm Williams, R. B. (1949). Rabies in Alaska. Canadian Journal of Comparative Medicine and Veterinary Science, 13(6), 136–143. Wonders, W. C. (2011). Yukon. Retrieved from The Canadian Encyclopedia website: https://www.thecanadianencyclopedia.ca/en/ article/yukon Yukon Bureau of Statistics. (2016). Language census, 2016. Retrieved from Executive Council Office website: http://www.eco.gov.yk.ca /stats/pdf/Language.pdf Yukon Bureau of Statistics. (2018). Yukon statistical review, 2017. Retrieved from Executive Council Office website: http://www.eco.gov .yk.ca/stats/pdf/2017_Annual_Stats_Review.pdf Yukon Wolf Conservation and Management Plan Review Committee. (2012). Yukon wolf conservation and management plan. Retrieved from Yukon Fish and Wildlife Management Board website: http://yfwmb.ca/wp-content/uploads/2013/08/Yukon-Wolf-Conservationn-and-Management-Plan.pdf

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14b Canada’s North NORTHWEST TERRITORIES

Kami Kandola1 and Brett Elkin2 1

Department of Health and Social Services, Yellowknife, Northwest Territories, Canada 2 Environment and Natural Resources, Yellowknife, Northwest Territories, Canada

Place The North-Western Territory was the name initially assigned by the British Government to all the lands held and traded by the Hudson’s Bay Company. A royal charter from King Charles II in 1670 granted the Hudson’s Bay Company trading rights to all the area whose rivers and streams emptied into the Hudson Bay, an area known as Rupert’s Land (see Overview, Part 3). This area included present-day Manitoba, the northern parts of Ontario and Quebec, most of Saskatchewan, southern Alberta, southern Nunavut, parts of Minnesota and North Dakota, and small parts of Montana and South Dakota. By 1870 Canada had gained control of Rupert’s Land and the North-Western Territory from the Hudson’s Bay Company (see Overview, Part 3). A small part of Rupert’s Land became Manitoba, and the rest of the area was merged and renamed the North-west Territories. In 1906 the hyphen was removed from the name and, until 1999, the Northwest Territories included all Canada north of the 60th parallel, except for Yukon, Quebec, and Newfoundland. On 1 April 1999, the Northwest Territories was officially split into two territories, with the eastern part becoming Nunavut. The western part remained as the Northwest Territories. Throughout this chapter we generally use Northwest Territories referring to the territory before 1999 and Northwest Territories or Nunavut as required after that date. Note that some data tables span periods before and after 1999. In those cases we show data extracted for the current administrative units in Northwest Territories or Nunavut.

The Northwest Territories is bordered on the north by the Arctic Ocean and the Beaufort Sea; on the east by Nunavut; on the south by Saskatchewan, Alberta, and British Columbia, and on the west by Yukon. The Northwest Territories covers 1,346,106 km2 including the Great Bear and Great Slave Lakes, the northern islands, Banks Island, Prince Patrick Island, the eastern portions of Victoria Island, and Melville Island (Figure 14b.1). Most settlements lie along or near the Mackenzie River, Great Slave Lake, and Great Bear Lake. The Northwest Territories had an estimated population in 2017 of 45,520, with 20,824 people living in Yellowknife, the capital and largest city (Government of the Northwest Territories, 2017), the so-called diamond capital of North America. The Northwest Territories is divided into two climatic zones, subarctic and Arctic, and two major geographical regions: the taiga (a boreal forest belt that encompasses the subarctic and is resident to pine, aspen, poplar, and birch trees), which covers most of the Northwest Territories; and a smaller area of tundra (a rocky Arctic region where vegetation is stunted by the cold climate) bordering Nunavut. The division between these regions, the treeline (Figure 14b.1), roughly parallels the border between the Northwest Territories and Nunavut. The two geographic regions also represent two climatic zones, with average temperatures ranging from −23°C in January for the subarctic zone to −27°C in the Arctic zone, and 21°C and 10°C, respectively, in July.

A History of Rabies Management in the Provinces and Territories

Figure 14b.1: Northwest Territories. Source: compiled from various sources.

disease killed a number of “Esquimaux” dogs, putting the North Pole expedition in danger at that time. Reports in the 1900s noted disease in dogs and wildlife that, in some instances, decimated the dog population and caused economic hardship to the Indigenous communities. The 1918– 1919 outbreak at Baker Lake, Nunavut (Elton, 1931), and further outbreaks during the 1920s led the Hudson’s Bay Company to distribute a questionnaire to their posts in the Arctic regions of Nunavut and Northern Quebec to try and understand fluctuations in the wildlife populations. Elton (1931) describes the results of this survey (see Chapter 14c). Freuchen (1935) also describes the occurrence of rabies among sled dogs, arctic foxes (Vulpes lagopus), wolves (Canis lupis), and ermine (Mustela artcia) during 1922 in the

Rabies in the Northwest Territories Early Rabies Rabies outbreaks in the Arctic lie within a very large area that includes the Kamchatka Peninsula, Alaska, Yukon, the Northwest Territories, Nunavut, Nouveau Quebec, Labrador, the Queen Elizabeth Islands, and Greenland. Rabies is thought to have entered from Kamchatka, Russia, across the Bering Strait to Alaska and into Canada’s Arctic some 30,000 to 75,000 years ago (Walker & Elkin, 2005; see Chapters 2, 29, and 37 for the origin of rabies in Canada). Early reports of rabies in the Arctic come from Greenland (Fleming, 1875; Colan, 1881) where a rabies-like

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Northwest Territories

Northwest Territories. This was followed by Plummer’s (1954) report describing the outbreaks of “arctic dog disease” in dogs and wildlife during the 1930s.

Rabies, 1947 to 2017 The first laboratory-diagnosed cases of rabies reported in the Northwest Territories were a wolf and dog at Aklavik in 1947 (Plummer, 1954; see Table 14b.1). Diagnosis was done microscopically (Negri bodies) and by animal inoculation. Previously, rabies had been diagnosed in a dog, a wolf, and a fox in Baker Lake, Nunavut (Plummer, 1954), and a dog in Frobisher Bay, Nunavut (Plummer, 1954), establishing the presence of rabies in the western, central, and eastern regions of Northwest Territories. Rabies was not diagnosed again until 1951 in Northwest Territories with a wolf, a red fox, and a dog in Aklavik, and a dog in Fort Smith. By 1952, 21 cases of rabies had been diagnosed throughout northern, central, and southern Northwest Territories in foxes, dogs, and wolves. This outbreak continued until 1955. Rabies reappeared in 1959 and has waxed and waned since (Figure 14b.2). There is evidence of a four-year cycle in time series of annual ­incidence for foxes (Figure 14b.3). Over this time, arctic and red foxes were the major vectors, composing 72% of all diagnosed cases. Dogs accounted for almost 23% of cases. Thus, foxes and dogs made up 95% of recorded cases, with wolves being most of the remaining cases. Of the 254 foxes listed in Table 14b.1, 117 (46%) were arctic foxes, 52 (20%) were red foxes (this includes one silver fox – a colour variant of the red fox), and the remaining foxes were not differentiated. There were seven cases in other species: caribou in Sachs Harbour in 1968 and 1987, and in Silence Bay in 1953; a lynx in Inuvik in 2001; a grizzly bear in Paulatuk in 2002; and cats in Inuvik in 1969 and Hay River in 1971. Table 14b.1  Positive rabies cases in the Northwest Territories, 1947 to 2017. Year

Total

1947 1948 1949 1950 1951 1952 1953 1954 1955 1956 1957

2 0 0 0 4 21 18 1 2 6 0

Fox 0 0 0 0 1 14 8 1 0 1 0

Dog

Wolf

Other

1 0 0 0 2 5 7 0 2 5 0

1 0 0 0 1 2 2 0 0 0 0

0 0 0 0 0 0 1 0 0 0 0

1958 1959 1960 1961 1962 1963 1964 1965 1966 1967 1968 1969 1970 1971 1972 1973 1974 1975 1976 1977 1978 1979 1980 1981 1982 1983 1984 1985 1986 1987 1988 1989 1990 1991 1992 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012 2013 2014 2015 2016 2017

0 7 0 0 1 5 0 6 2 7 1 0 8 0 13 3 27 2 0 1 50 2 2 5 5 1 7 7 1 1 6 8 3 5 2 2 2 2 0 4 3 1 11 12 6 0 0 3 8 6 4 7 1 6 6 12 6 1 4 4

0 1 0 0 1 2 0 2 0 2 0 0 6 0 11 2 26 1 0 1 48 2 2 2 4 0 5 6 1 1 5 5 0 3 2 2 1 2 0 2 3 1 10 9 4 0 0 1 6 4 4 3 1 6 5 11 4 1 4 4

0 6 0 0 0 3 0 4 2 5 0 0 2 0 2 0 1 1 0 0 1 0 0 2 1 1 1 1 0 0 1 3 3 1 0 0 1 0 0 2 0 0 0 2 1 0 0 2 2 2 0 2 0 0 1 1 1 0 0 0

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 1 0 0 1 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 2 0 0 0 0 1 0 0 0

 Total

353

254 72.0

80 22.7

14 4.0

  % Total

0 0 0 0 0 0 0 0 0 0 1 1 0 1 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 7 2.0

Source: compiled from CFIA data. Fox = AFX and RFX; Other = 1 lynx, 3 caribou, 1 grizzly bear, 2 cats.

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A History of Rabies Management in the Provinces and Territories

Figure 14b.2: Rabies in foxes and dogs in Northwest Territories (current boundaries), 1947 to 2017. Source: created from CFIA data.

Figure 14b.3: Times series analysis of annual fox incidence from Table 14b.1. The peak at lag 4 shows a four year cycle that is statistically significant (Pearson r = 0.35, p = .05). Since foxes are the dominant vector, the time series analysis for total incidence shows the same pattern. Source: authors.

The large spike in cases between 1972 and 1978 led to the surveys in the coastal areas of Northwest Territories and Nunavut from 1977 to 1985 that are discussed in the next section. The arctic fox is the primary rabies vector in the Northwest Territories, closely followed by the red fox (Walker & Elkin, 2005). As evidenced by the location of reported cases of rabies (Table 14b.2), the spatial distribution of the

two species differs. The red fox is a highly adaptable species occurring through most of North America, and its home range can be extensive in its search for food (Government of Northwest Territories, 2019b). On the mainland almost 66% of the reported cases are red fox, whereas on the islands 98% of reported cases are in the arctic fox. Although the red fox is thought to have crossed to Banks Island, Victoria Island, Melville Island, and Baffin Island in the 1940s

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Active Surveillance for Rabies

Table 14b.2  Location of fox rabies cases, 1951 to 2017. Of the 254 cases reported in foxes only 169 were differentiated by species (RFX = red fox, AFX = arctic fox). Location

RFX

AFX

Total

Mainland Islands

50 2

24 93

74 95

Total

52

117

169

Data used in Table 14b.1 and Figures 14b.2 and 14b.3 are from passive surveillance: contact is reported with a suspected rabid animal and, subsequently, a submission is sent to the CFIA laboratory for diagnosis. Active surveillance is the direct collection of samples to determine the incidence of rabies and is further discussed in Part 5, Chapter 24a of this book. Beak Consultants (1975) carried out the earliest active surveillance for rabies in the arctic fox from 1973 to 1974. Panarctic Oils Ltd. commissioned these consultants to undertake studies on various aspects of arctic fox biology on Banks Island. Panarctic was drilling in the area at that time and several personnel had been attacked by foxes. The study involved the use of trap-line returns in the areas around the drilling platforms. A total of 259 brains from arctic foxes were submitted to Lethbridge, Alberta, for diagnosis (Table 14b.3). Of these, 14 (or 5.4%) were positive on the fluorescent antibody test (FAT). These results are not included in the CFIA database. Further surveillance for rabies in arctic foxes was carried out in 1978 in Northwest Territories at Sachs Harbour and Banks Island and included three areas from Nunavut: Cambridge Bay, Gjoa Haven, and Spence Bay. This study investigated the presence of rabies virus in the brain and parotid salivary gland of trapped foxes, each being tested by the FAT and mouse inoculation (MI) tests. The results of the tests on 522 submissions showed 44 arctic fox brains and 43 glands as positive in the Sachs Harbour area and four brains and two salivary glands positive from Cambridge Bay (Table 14b.3). Subsequent surveys carried out between 1979 and 1985 showed spikes of rabies-positives in 1978 and 1982, coincident with the reported incidence information from passive surveillance (Table 14b.1). This active surveillance demonstrated that the passive surveillance system did capture the extent of rabies incidence in the study areas. The patterns of annual incidence revealed by active surveillance mirror the patterns shown by passive surveillance. Similar results have been demonstrated in other provinces (e.g., Alberta, see Chapter 7; Quebec, see Chapter 11). Secord et al. (1980) argue that active surveillance is most useful to gauge the magnitude of rabies over large enzootic areas. Ontario’s recent massive use of active surveillance (see Chapter 10) demonstrates its value in planning and evaluating control programs.

Source: compiled from CFIA data.

(Government of Nunavut, 2012), there have only been two red fox rabies cases in those areas (Banks Island in 1988 and Rea Point in 1975). Cases of arctic fox on the mainland primarily occur on the coastline above the treeline (Figure 14b.1). Almost 80% of all reported arctic fox cases occur on Banks or Holman Island and, of those, 85% are from Banks Island. Traditionally, Banks Island yields high numbers of fox catches for the fur industry, with yearly fluctuations; yields of 7000 to 11,000 catches have been recorded (Usher, 1970). The lowland area of western Banks Island provides ideal habitat for arctic foxes and their prey, with suitable terrain for denning, an abundance and variety of food, and few predators or competitors. It provides the sandy, well-drained, and vegetated areas the foxes are known to prefer (Macpherson, 1969), with a southern exposure and abundant streams for water. The Northwest Territories has never had a documented case of rabies in bats. Before 2006 only three species of bats were recorded in the Northwest Territories: the little brown bat (Myotis lucifugus), the northern long-eared bat (Myotis septentrionalis), and the hoary bat (Lasiurus cinereus). Since then an additional four species have been confirmed: the long-eared bat (Myotis evotis), the longlegged bat (Myotis volans), the big brown bat (Eptesicus fuscus), and the silver-haired bat (Lasionycteris noctivagans). One more species is suspected, the eastern red bat (Lasiurus borealis), for a total of eight species (Government of the Northwest Territories, 2019a). Canadian Food Inspection Agency (CFIA) records show some bat submissions over the years, usually from the Fort Smith and Hay River areas. Little brown bat submissions were made in 1974 (8), 1987 (6), 1994 (1), 2005 (4), and 2010 (1). In 1986 there was a big brown bat submission from Grise Fjord (which is now in Nunavut); in 1987 there were five submissions from the South Slave region, and in 2014 there was a northern long-eared bat submission from Fort Smith.

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Table 14b.3  Survey results for rabies in arctic (AFX) and red fox (RFX) rabies in Northwest Territories, 1973 to 1985. Brain

Salivary gland

Positives

Positives

Year

Location

Samples FAT

MI

FAT

MI

Species

1973–1974

Banks Island Banks Island Cambridge Bay Gjoa Haven Spence Bay  (Taloyoak) Banks Island Cambridge Bay Gjoa Haven Banks Island Cambridge Bay Gjoa Haven Banks Island Gjoa Haven Banks Island Cambridge Bay Gjoa Haven Spence Bay Banks Island Cambridge Bay Gjoa Haven Spence Bay Cambridge Bay Gjoa Haven Spence Bay Coppermine (Kugluktuk) Deer Pass Bay McGill Bay Great Bear Lake Cambridge Bay Gjoa Haven Spence Bay Coppermine

259 202 127 100 93

14 44 0 0 0

0 44 0 0 0

0 42 0 0 0

0 43 0 0 0

AFX AFX AFX AFX AFX

204 198 100 256 150 67 312 96 316 202 92 101 201 106 99 100 73 50 51 7 1 1 1 50 50 54 71

1 2 0 0 0 0 0 2 14 9 1 5 1 0 0 0 1 0 0 0 0 0 0 0 1 0 1

1 2 0 0 0 0 0 2 10 0 1 5 1 0 0 0 1 0 0 0 0 0 0 0 1 0 1

1 2 0 0 0 0 0 1 0 1 1 5 0 0 0 0 1 0 0 0 0 0 0 0 1 0 1

1 2 0 0 0 0 0 1 0 0 1 5 0 0 0 0 1 0 0 0 0 0 0 0 1 0 1

AFX AFX AFX AFX AFX AFX AFX AFX AFX AFX AFX AFX AFX AFX AFX AFX AFX AFX AFX RFX RFX RFX RFX AFX AFX AFX AFX

1978 1979 1980 1981 1982

1983

1984

1985

FAT = fluorescent antibody test; MIT = mouse inoculation test Source: compiled from CFIA data.

Rabies Management

1939 the Yellowknife administrative district was formed. In 1953 Yellowknife became a municipal district and has been the capitol since 1967. Managing rabies in the Canadian Arctic has considerable challenges, including the vastness of the area; its lack of infrastructure and its low human population living in scattered settlements; inclement weather; and the wildlife vectors and reservoirs of rabies and their cycles. Further, diagnosis of rabies depends on laboratories in southern Canada with the attendant difficulties of obtaining a specimen and transporting it to the nearest community where personnel and facilities are available to ship samples for testing. The winter temperatures present a challenge to both human and wild life populations in terms of food, security, survival, and rabies management.

General Considerations Northwest Territories has a very large surface area and yet only 0.1% of the Canadian population live there. While about 46% of the population lives in Yellowknife, the remaining population is spread among 33 widely separated communities (Figure 14b.1). Indigenous peoples (Dene, Métis, and Inuit) compose over 50% of this population (Statistics Canada, 2019). Until 1898 the Hudson’s Bay Company maintained the only administrative infrastructure when the federal government began organizing provinces and territories administered out of Ottawa. The Yellowknife Dene began moving into the Yellowknife area, and by

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Northwest Territories

From 1947 to the present, the main reservoir of rabies has been the arctic fox and red fox. As foragers and scavengers, both fox species can be found north and south of the treeline with a normal home range of between 5 and 35 km2. Both are omnivorous, feeding on whatever is available, which may include carrion, birds, lemmings, and other small mammals, as well as fish and seaweed for the arctic fox on the islands (Macpherson, 1969). The fox cycles appear to peak every four years depending on lemming cycles, especially for arctic foxes. Incidence in other wild animals and domestic dogs (working sled dogs and pets) tends to follow incidence in foxes. How an epizootic starts and how the virus is maintained in a population is not known. The contact rate – that is, the number of animals that can become infected by one infected ­animal – depends on the population density, social interaction, denning, and when the animal migrates (Mork & Prestrud, 2004). The arctic fox is known to migrate long distances. Migration typically starts in the fall when the young adults leave their dens and disperse. A long incubation period, long periods of virus excretion, and oral infection through eating a frozen, infected carcass where the virus has been maintained have been suggested (Mork & Prestrud, 2004; see Chapter 14d). Kantorovitch (1964) reported on work carried out between 1957 and 1962 in which clinically normal arctic foxes were found to be carrying the rabies virus.

from the United States. While the NWMP dealt with the health of their own horses and the imported cattle from the United States, they were involved with dog control during rabies outbreaks in the Yukon and the Northwest Territories. Since most outbreaks of rabies at that time involved dogs, dogs were at risk of being shot if found loose. With isolated communities to service and a lack of understanding and knowledge of rabies at the time, rabies control provided by the NWMP was essentially that of dog control and dissemination of information. Most of the communities tied their sled dogs outside of their homes, which allowed rabid wildlife an opportunity to disseminate the disease. Freuchen (1935) describes the decision by some Inuit to keep sick animals, leading to the infection being carried from one place to another. This could have been a lack of understanding of the disease and its transmission, or a need to keep the dogs, their main system of transport. Dog control meant restraining strays for a time, muzzling them, or destroying them. The RCMP was responsible for collection and transport of specimens to the nearest laboratory as diagnostic services and transportation means improved. After 1950, when rabies vaccines became available for domestic animals, the RCMP provided vaccination clinics for the local communities. The number of vaccines shipped to the Arctic, including the Northwest Territories, Yukon, and Nunavut, was about 5000 doses yearly starting in 1956. In 1995 the RCMP withdrew its services from the rabies vaccination program for community dogs, citing a need to eliminate this non-police function given limited resources and because it was not part of its mandate. This decision may have arisen from allegations concerning the slaughter of Inuit sled dogs between 1950 and 1970 by the RCMP. A report in 2006 suggested that Inuit were turning their dogs loose and using snowmobiles in the 1960s. The report found no blame with the RCMP or Inuit and suggested a reconciliation (Royal Canadian Mounted Police, 2006). A desire by Agriculture Canada and territorial partners to see vaccination efforts continue led to the implementation of a community lay vaccinator program discussed later in this chapter. Also, responsibility for dog control in Northwest Territories primarily rests with municipalities. RCMP officers will respond to emergencies on occasion but have largely removed themselves from this role (Northwest Territories Dog Act, 2013, amended).

Early Rabies Management Despite the concerns noted in the previous section, Northwest Territories has developed a rabies management process that has evolved through many agencies and through improvements in its educational, diagnostic, and transportation methods. These are discussed in the sections that follow. ROYAL CANADIAN MOUNTED POLICE

The North-West Mounted Police (NWMP) was established in 1873 to bring Canadian authority to the North-west ­Territories, mostly present-day Alberta and Saskatchewan. Its jurisdiction grew to include the Yukon in 1895, the Arctic Coast in 1903, and northern Manitoba in 1912 (North West Mounted Police, 2012). Its name changed in 1904 to the Royal North-West Mounted Police, and after the force absorbed the Dominion Police in 1920, it became known as the Royal Canadian Mounted Police (RCMP). Besides establishing law and order in the areas, general duties included fighting fires, disease, and destitution, and being the arm of the federal government responsible for enforcing disease control in domestic animals arriving with settlers

POPULATION CONTROL

A wolf control program was implemented in the 1950s in Northwest Territories to increase the prey populations for human consumption (Russell, 2010), though no report was

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A History of Rabies Management in the Provinces and Territories

published to substantiate its success. This was discontinued in 1977–1978. Harvesting of wolves by trappers does occur as part of the traditional fur economy. There are an estimated 10,000 wolves in Northwest Territories and Nunavut, with a reported trapping and harvesting of less than 200 wolves per year. Northwest Territories has no management plan for wolves currently in place (Russell, 2010). Historically, the communities of the Arctic depended on hunting and trapping as a means of survival. The Hudson’s Bay Company paid for pelts to supply a demand for fur in Europe. The fur harvest of arctic fox and red fox varied with the price paid for the pelt. For example, the average price paid for a red fox pelt between 1991 and 2006 varied between $16 and $83 in Northwest Territories, with a high in 2003–2004 of $83 per pelt (Government of Nunavut, 2012). In general, trapping is influenced by the pelt price and the cost of hunting and trapping. Rabies in the fox population may make hunting more accessible but may also reduce the fox population. Not only do the trappers provide a local and traditional knowledge on fox population trends, but they also act as a front-line information base about an outbreak of rabies in their area. An annual wildlife conservation questionnaire allows trappers to provide information on wildlife populations. Their traditional knowledge and experience related to important vegetation and habitat areas provided input to help understand the environmental impact of the proposed Mackenzie Valley Pipeline (Fur Institute, 2003).

program in the Northwest Territories is administered by the regional office in Calgary. The CFIA has used the Edmonton district office to provide direction and supervision to any rabies management program in Northwest Territories through the territorial Environmental Health officers (in Health and Social Services) and officials with the Department of Environment and Natural Resources (ENR). CFIA actions include communicating with the appropriate wildlife and human health personnel in the Northwest Territories, including Health and Social Services (HSS) Environmental Health officers; updating policies by taking into account the physical, logistical, and cultural environment; providing rabies cans to ship specimens to the CFIA laboratory in Lethbridge; updating CFIA’s manual of procedures on rabies; ensuring the delivery of specimens to Lethbridge; communicating diagnostic results back to the Government of Northwest Territories Chief Public Health Officer; and disseminating data as needed. TERRITORIAL RABIES MANAGEMENT ORGANIZATIONS

Given the vastness of the region, rabies control depends on dividing the area into manageable parts. The Northwest Territories is divided into five administrative regions (Table 14b.4). Three Health and Social Services Authorities (HSSAs) service 33 communities: Hay River HSSA, Tłįchǫ Community Services Agency, and Northwest Territories HSSA (NTHSSA) which services the majority of the region. They provide a full program of community and facility-based services for health care and social services. HRHSSA and NTHSSA are governed by Regional Wellness Councils (RWCs), which are composed of a group of residents within each geographic region of the Northwest Territories. Their purpose is to serve as an advisory body to the territorial HSSA. RWCs provide advice to the Northwest Territories HSS Leadership Council respecting health and social services, the priorities under the territorial plan, and the promotion of health and wellness. In addition, RWCs may also seek opinions and information from residents of the respective region about health and social services. The chair of each RWC sits on the Northwest Territories HSS Leadership Council. The chair of the Tłįchǫ Community Services Agency is also a member of the Leadership Council (Government of the Northwest Territories, 2019c). Domestic animal health services in the communities are dependent on accessibility, availability, and cost of primary veterinary services, their acceptance by the community and knowledge of animal health education as it relates to zoonoses (Brook et al., 2010).

Rabies Management Today Since the 1950s animal and human health services provided in Northwest Territories for rabies management and its diagnosis have gradually increased. Improvements include a CFIA office in Edmonton dedicated to helping the regions of the Northwest Territories and Nunavut; better organization of government services leading to improved diagnostic and disease management capabilities; improved communications with isolated communities; and community clinics and local controls. CANADIAN FOOD INSPECTION AGENCY

Rabies has been a reportable disease under the Health of Animals Act and Regulations of the CFIA since 1905. As such, all suspected cases of rabies in animals or contact with possibly rabid animals must be reported to the nearest inspector of CFIA. Since CFIA had no personnel in Northwest Territories, any action taken was by a person designated by the ­department, usually from the RCMP. The rabies management

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Northwest Territories

Table 14b.4  Administrative Regions and Health and Social Service Authorities in the Northwest Territories Administrative Region

Health and Social Service Authority (HSS)

Regional Office

Communities

Inuvik Region Dehcho Region Sahtu Region

NTHSSA Beaufort-Delta region NTHSSA Dehcho region NTHSSA Sahtu region NTHSSA Fort Smith region Hay River HSSA NTHSSA Yellowknife region NTHSSA Stanton Territorial Hospital Tłı̨chǫ Community Services Agency

Inuvik Fort Simpson Norman Wells Fort Smith Hay River

8 6 5

South Slave Region North Slave Region

Yellowknife Behchoko

7 8

Source: authors.

Veterinary practices provide full-time resident services in only one community: Yellowknife. Regional centres and some smaller communities receive regular visiting veterinarians who provide a full range of services on a feefor-service basis, and some remote small communities have received one-time or periodic visits by non-profit veterinary providers (e.g. Vets Without Borders). In some more remote Arctic communities, a government-coordinated lay vaccinator program exists to provide rabies vaccine because of the lack of any veterinary service. In several small isolated communities, no services are available because of the lack of private veterinary services and the logistical challenges of delivering the lay vaccinator program. In a case of suspect rabies with human contact, it is the territorial government’s responsibility to facilitate rabies reporting and to take appropriate action. The CFIA disease control manual of procedures provides the basic established policies for dealing with all animals suspected of being rabid or contact with rabid animals. In each case of a bite or an animal attack, the health care provider in the community, usually a nurse practitioner or community health nurse, reports the incident to the regional Environmental Health Officer (EHO), who then passes an investigation report to the Office of the Chief Public Health Officer for a decision about post-exposure prophylaxis (PEP) for the individual contacted or actions to deal with the animal in terms of observation, quarantine, or euthanasia and a specimen being sent for laboratory diagnosis (Mitchell & Kandola, 2005). In the larger communities, animal bite victims usually present to the hospital emergency room for care. In that scenario, the physician typically calls the Office of the Chief Public Health Officer to speak directly to the public health physician or communicable disease nurse for advice on PEP. If the animal is killed before the end of an observation period, the diagnostic specimen, if available and intact, is transported to the nearest airport facility by road or snowmobile, flown to Inuvik or Yellowknife, then flown to CFIA Edmonton, and then sent by bus to the CFIA Lethbridge

laboratory. The results are reported back to the Office of the Chief Public Health Officer for the appropriate action. The Office of the Chief Public Health Officer strongly recommends pre-exposure vaccination of at-risk individuals, including dog mushers, hunters, trappers, wildlife officers, by-law officers, veterinarians, and lay vaccinators. The regional EHOs encourage the vaccination of domestic animals, the prompt reporting of all animal bites by local health personnel, community dog control efforts, and recognition by the public of animals with abnormal behaviour. COMMUNITY LAY VACCINATOR PROGRAM

Following the decision to discontinue vaccination of dogs by the RCMP in 1995, discussions were held between Agriculture Canada and the Government of the Northwest Territories to find a way to continue this important animal and public health program. HSS, with the former Department of Renewable Resources (now known as the Department of Environment and Natural Resources), in collaboration with and with the support of Agriculture Canada Animal Health staff, created a community-based volunteer lay vaccinator program. Individuals were approved in each community to provide rabies vaccination to the local dogs. Under the Health of Animals Act and Regulations, rabies vaccines maybe administered by trained personnel in remote areas where veterinary services are not readily available. Using this mandate, trained EHOs, by-law officers, and local nurses also can perform this function. The lay vaccinator program is administered jointly by the HSS and the ENR; ENR personnel provide training, vaccines, and support materials to the EHOs and lay vaccinators. The training includes vaccination techniques; vaccine integrity; the handling of animals; adverse reactions; record keeping; the Health of Animals Act and Regulations; and the proper shipment of specimens to the appropriate laboratory (Wrathwell & Breadmore, 1996). However, the number of communities involved and the total number of dogs vaccinated under this program has decreased over time.

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A History of Rabies Management in the Provinces and Territories

In part, this is the result of challenges with high turnover of lay vaccinators in small, isolated communities. From a positive perspective, part of this decrease is the result of an increase in veterinary services available in more communities across the Northwest Territories. Currently, only the smallest northern Arctic communities in the Beaufort Delta, which do not have any resident or visiting veterinary service, continue to have coverage under the lay vaccinator program. Veterinary services in Northwest Territories are regulated under the Northwest Territories Veterinary Professional Act, 1988, which outlines the qualifications needed to practice, the licensing requirements, and the complaints review process. All veterinarians are licensed under the veterinary registrar of the HSS and the Canadian Veterinary Medical Association (Brook et  al., 2010). Presently, there are two veterinary practices in Northwest Territories, both based in Yellowknife, providing animal health care to the communities on a permanent basis. In addition, visiting veterinarians from other Canadian jurisdictions provide regularly scheduled clinics in a number of communities across the Northwest Territories. By-law officers are present in the larger communities, such as Inuvik, Yellowknife, Hay River, and Fort Smith, enforcing animal control by-laws and dog control. Smaller communities may employ dog control officers (Northwest Territories Dog Act, 2013, amended). They provide licencing of all dogs over five months of age, encouraging residents to keep their dogs tied and shooting stray dogs if necessary (Brook et al., 2010).

rabies and other diseases were given, and the animals were dewormed. During 2009 surgical castrations and ovariohysterectomies were offered. Questionnaires were handed out to students at school to try to assess the health status and care given to their animals (Brook et  al., 2010). Vets Without Borders also visited Inuvik in spring 2012 to provide one week of veterinary services when the local veterinary office was temporarily closed. Veterinary services offered through benevolent organizations and researchers have also been provided in other communities within Northwest Territories periodically.

Discussion Rabies reports for Nunavut, the eastern neighbour of the Northwest Territories, are somewhat similar to those in Northwest Territories: foxes account for 73.4% of all cases (72% in Northwest Territories), dogs for 22% (almost 23% in Northwest Territories), with wolves accounting for most of the remaining cases. There are, however, differences in incidence between these two Arctic territories: (1) arctic foxes in Nunavut account for the majority of rabies cases in foxes (over 83%); (2) there is no cycle evident in the data for Nunavut; (3) since 1985 a steady trickle of red foxes cases (11 to date) have been reported on the islands in Nunavut; (4) most cases (83%) occur on the islands or coastline above the treeline rather than in the interior mainland. These differences probably reflect the very different landscapes in the two regions: taiga below the treeline in mainland Northwest Territories, and tundra over much of Nunavut. Nunavut is a much larger area dispersed over many islands in addition to a very large mainland – a spatial pattern that would mask any evidence of the four-year cycle in rabies incidence seen in the much smaller area of high rabies incidence in Northwest Territories: Banks Island, Holman Island, the Mackenzie River Delta, and the northern coastline. No reported cases of rabies in bats have occurred in Northwest Territories and only three species reported in submissions to CFIA. As mentioned previously, seven species of bats have been confirmed in the Northwest Territories (see the section “Rabies, 1947–2017”) and an eight species, the Eastern Red Bat, was also suspected. Given climate change and further research into bat species and locations, it is possible the Northwest Territories will find rabies in additional species. It is surprising that no human case of rabies has been documented in the north given the often close contact between community members, their dogs, and wildlife. A

VACCINATION CLINICS

There are a number of visiting veterinary services in Northwest Territories. One such example is the Sahtu Veterinary Service Program, which was initiated in 2008 through the collaborative effort between the Faculty of Veterinary Medicine, University of Calgary, the ENR, Sahtu Settlement Area, and the Government of Northwest Territories (Sahtu Veterinary Services Program Report, 2011). The veterinary services provided were to the communities of Norman Wells, Colville Lake, Fort Good Hope, Deline, and Tulita. With the exception of Norman Wells, which receives annual services itself, veterinary clinics have been provided to the Sahtu Settlement Area since 2008. Resources for the clinics were provided by a number of external sources (Brook et al., 2010). The clinics were advertised through the media of public meetings, posters, and radio announcements, and to students at schools. For 2008 physical examinations were conducted on dogs, histories were taken, vaccinations for

228

Northwest Territories

reduced pathogenicity of the rabies virus to humans has been proposed but not proven (Kuzmin et  al., 2008; see Chapter 37). Given northern resident’s activities of hunting and trapping, there is potential risk from minor skin abrasions and exposure to salivary secretions from handling or skinning fox pelts. The risk, however, seems low. In Alaska, for example, only three human rabies cases associated with exposures have been reported. However, in one reported case, a man from the former Soviet Union, severely bitten on his face, shin, and hands by a rabid wolf, died of rabies within 24 days despite treatment (Kuzmin et al., 2008). The isolate was shown to belong to the Arctic-3 group of rabies Arctic viruses (see Chapter 29). Before a report by Follmann (1994), cases of idiopathic rabies titres had been published in the Canada Diseases Weekly Report (“Idiopathic Rabies Titre,” 1982). One report involved a rabies vaccine trial in which 15 of 226 (6.6%) students and faculty members tested at a veterinary college had neutralizing antibodies in their sera. None of the participants reported a history of exposure to or contact with rabies vaccines.

must be given. The main elements relevant to the Northwest Territories context are as follows. • Pre-exposure vaccination: Northwest Territories veterinary services need to build on expanding their program to meet the needs of the smaller communities not benefiting from the lay vaccinator program. Domestic animals requiring vaccination should have some means to access these services, regardless of the community of residence. Animals should have a visible tag showing their vaccination status at all times. • Animal control: the Northwest Territories Dog Act needs to be enforced. Dogs need to be registered and effectively restrained in public. Stray dog populations need to be controlled. Local municipalities should incorporate education covering responsible pet ownership, bite prevention, and appropriate veterinary care in their programs. • Animal bite investigation: all animal bites should be investigated appropriately and forms transmitted promptly to the regional EHO for follow-up with the office of the chief public health officer for final assessment. Regardless of rabies vaccination status, a domestic animal that potentially exposes a person through a bite should be confined and observed daily for 10 days from the time of the exposure. In Northwest Territories confinement is typically at the place of residence. • Post-exposure management: any illness in an animal that has been exposed to rabies should be reported immediately to the regional EHO. If signs suggestive of rabies develop (e.g., paralysis or seizures), the animal should be euthanized and the head shipped for testing to the CFIA Lethbridge, Alberta, laboratory. PEP should be given to those considered at risk following contact with suspect rabid animals. • Ongoing education: education of the public, especially children, is required on (1) avoiding animals acting strangely and reporting this behaviour immediately to an authority, and (2) understanding the importance of reporting animal bites to the appropriate authorities. • Continued surveillance: surveillance is essential for both terrestrial mammals and bats. Given the warming trend globally, it is possible that bat bite incidents will increase. • Wildlife vaccination: in terms of active vaccination of wildlife, some thought has been given to the use of bait drops to vaccinate wildlife. This will be very difficult given the vast areas to be baited. It would be more effective if baits could be used in areas attracting wildlife, such as garbage dumps, but must depend on agreements from all agencies and communities involved.

Next Steps Rabies remains an issue of ongoing concern in the Northwest Territories, with the arctic fox and red fox acting as the main reservoirs for the virus. Rabies is also a reportable disease under the federal Health of Animals Act and ­Regulations. Until 2014, the CFIA rabies management program was aimed at reducing or eliminating the disease in domestic animals and investigating all human or domestic animal exposures to rabies, suspect or confirmed, in domestic animals. In April 2014, however, the CFIA withdrew its field services program, downloading it to the provinces’ and territories’ agencies but keeping the diagnostic and reporting capabilities for samples from animals suspected of being rabid and contacting human or domestic animals. Samples are submitted to CFIA Lethbridge only after an assessment of the case as to the possibility of rabies. Unlike several other provinces, the direct rapid immunohistochemical test (dRIT) test is not used by the Northwest Territories. The territorial government has been working closely with CFIA in all suspect rabies investigations. With the responsibility for maintaining an effective rabies program now vested in the territorial government, renewed consideration of areas such as those referenced in the Compendium of Animal Rabies Prevention and Control (National Association of State Public Health Veterinarians, 2011)

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A History of Rabies Management in the Provinces and Territories

References Beak Consultants. (1975). Banks Island arctic fox studies: Age structure and rabies infection from 1973 to 1974: Trap line returns. Calgary, AB: Panarctic Oils. Brook, R. K., Kutz, S. J., Millins, C., Veitch, A. M., Elkin, B. T., & Leighton, T. (2010). Evaluation and delivery of domestic animal health services in remote communities in the Northwest Territories: A case study of status and needs. Canadian Veterinary Journal, 51(10), 1115–1122. Colan, T. (1881). The dog disease, or canine madness of the Arctic regions, viewed in connection with hydrophobia; together with the measures used and suggested for its extinction, from information collected and observations made in the country. Veterinary Journal and Annals of Comparative Pathology, 13(11), 324–325. https://doi.org/10.1016/S2543-3377(17)43026-3 Elton, C. (1931). Epidemics among sledge dogs in the Canadian Arctic and their relation to disease in the arctic fox. Canadian Journal Research, 5(6), 673–692. https://doi.org/10.1139/cjr31-106 Fleming, G. (1875). The Arctic expedition and the sledge dogs of Greenland. Veterinary Journal and Annals of Comparative Pathology, 1, 277–278. Follmann, E. H., Ritter, D. G., & Beller, M. (1994). Survey of fox trappers in northern Alaska for rabies antibody. Epidemiology and Infection, 113(1), 137–141. https://doi.org/10.1017/s0950268800051554 Freuchen, M. (1935). Mammals – Part II: Field notes and biological observations. In Report of the Fifth Thule Expedition, 1921–24 (pp. ­137–139, 184, 185, Vol. 2). Copenhagen, Demark: Nordisk Forlag. Fur Institute of Canada. (2003). Trappers: Stewards of the land. Ottawa, ON: Author. Government of the Northwest Territories. (2017). Yellowknife statistical profile. Retrieved from https://www.statsnwt.ca/community-data/Profile-PDF/Yellowknife.pdf Government of the Northwest Territories. (2019a). Bats. Retrieved from Environment and Natural Resources website: https://www.enr.gov.nt.ca/en/services/bats Government of the Northwest Territories. (2019b). Red fox. Retrieved from Environment and Natural Resources website: https://www .enr.gov.nt.ca/en/services/red-fox Government of the Northwest Territories. (2019c). Governance. Retrieved from Health and Social Services Authority website: https:// www.nthssa.ca/en/governance Government of Nunavut. (2012). Wildlife fact sheets: Red fox, Vulpes vulpes. Retrieved from https://www.gov.nu.ca/sites/default/files/ Red%20Fox.pdf Government of Yukon. (2011). A guide to Yukon bats. Retrieved from Environment Yukon Wildlife Viewing Program website: http:// www.wildlifeviewing.gov.yk.ca Idiopathic rabies titer. (1982). Canada Diseases Weekly Report, 8(17), 7. Kantorovich, R. A. (1964). Natural foci of a rabies-like infection in the far north. Journal of Hygiene, Epidemiology, Microbiology and Immunology, 8, 100–110. Kuzmin, I. V., Hughes, G. J., Botvinkin, A. D., Gribencha, S. G., & Rupprecht, C. E. (2008). Arctic and Arctic-like rabies viruses: Distribution, phylogeny and evolutionary history. Epidemiology and Infection, 136(4), 509–519. https://doi.org/10.1017 /S095026880700903X Macpherson, A. H. (1969). The dynamics of Canadian Arctic fox populations (Canadian Wildlife Service Report Series, Number 8). ­Ottawa, ON: Department of Indian Affairs and Northern Development. Mitchell, R., & Kandola, K. (2005). Rabies in the Northwest Territories – Part 2: Rabies surveillance in Northwest Territories. Epinorth, 17(1), 4–6. Mork, T., & Prestrud, P. (2004). Arctic rabies – A review. Acta Veterinaria Scandinavica, 45(1), 1–9. https://doi.org/10.1186/ 1751-0147-45-1 National Association of State Public Health Veterinarians. (2011). Compendium of animal rabies prevention and control. Retrieved from the Centers for Disease Control and Prevention website: https://www.cdc.gov/mmwr/pdf/rr/rr6006.pdf North West Mounted Police. (2012). Personnel records, 1873–1904. Retrieved from the Library and Archives Canada website: http:// www.bac-lac.gc.ca/eng/discover/nwmp-personnel-records/Pages/north-west-mounted-police.aspx Northwest Territories Dog Act. (2013). RSNWT 1988, c.D-7, amended 2013. https://www.justice.gov.nt.ca/en/files/legislation/dog /dog.a.pdf Plummer, P. J. G. (1954). Rabies in Canada, with special reference to wildlife reservoirs. Bulletin World Health Organisation, 10, 767–774. Royal Canadian Mounted Police. (2006). Final report: RCMP review of allegations concerning Inuit sled dogs. Retrieved from Government of Canada Publications website: http://publications.gc.ca/collections/collection_2011/grc-rcmp/PS64-84-2006-eng.pdf

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Northwest Territories Russell, D. (2010). A review of wolf management programs in Alaska, Yukon, British Columbia, Alberta, and Northwest Territories for Yukon Wolf Conservation and Management Plan Review Committee. Retrieved from the Yukon Co-operative Fish & ­Wildlife Management website: http://www.yfwcm.ca/YukonWolfPlanReview/going/documents/WolfmgmtprogramreviewNov62010 .pdf Sahtu Veterinary Services Program. (2011). Summary, March 2011. Yellowknife: Northwest Territories Department of Environment and Natural Resources. Statistics Canada. (2019). Census profile, 2016 census, Northwest Territories. Retrieved from https://www12.statcan.gc.ca/censusrecensement/2016/dp-pd/prof/details/Page.cfm?Lang=E&Geo1=PR&Code1=61&Geo2=&Code2=&Data=Count &SearchText=Northwest%20Territories&SearchType=Begins&SearchPR=01&B1=All&GeoLevel=PR&GeoCode=61 Secord, D. C., Bradley, J. A., Eaton, R. D., & Mitchell, D. (1980). Prevalence of rabies virus in foxes trapped in the Canadian Arctic. ­Canadian Veterinary Journal, 21(11), 297–300. Usher, P. J. (1970). The Bankslanders: Economy and ecology of a frontier trapping community: Report of the Northern Science Research Group (Vol. 2). Ottawa, ON: Department of Indian Affairs and Northern Development. Walker, J., & Elkin, B. (2005). Rabies in the Northwest Territories – Part 1: A historical overview of Rabies in the Northwest Territories. Epinorth, 17(1), 1–3. Wrathwell, B., & Breadmore, R. (1996). Rabies control in the Northwest Territories. Environmental Health Review, Spring, 17–19.

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14c Canada’s North NUNAVUT

Darcia Kostiuk,1 Peter Workman,2 and Stephen Atkinson3 1

Public Health Veterinarian, Government of Alberta, Canada 2 Department of Health, Nunavut, Canada 3 Consultant, Wildlife Research and Management, Winnipeg, Manitoba, Canada

Place

Rabies in Nunavut

Nunavut, “our land” in the Inuktitut language and originally part of Rupert’s Land and the North-Western Territory (see Overview, Part 3), separated from the Northwest Territories on 1 April 1999 via the Nunavut Land Claims Agreement Act and the Nunavut Act. The largest and newest territory, it is bordered on the west by the mainland Northwest Territories and its Victoria and Melville Islands, by Manitoba to the south, by a small part of Saskatchewan to the southwest, and by Newfoundland and Labrador through Killiniq Island; shares the same coastline with Manitoba, Ontario, and Quebec; and has Greenland as a close neighbour through Ellesmere Island to the north (Figure 14c.1). Nunavut covers 1,877,787 km2 of land and 160,935 km2 of water in northern Canada and had a population estimated at 33,588 people in 2012, with 83.6% identifying as Inuit. Its capital, Iqaluit (originally Frobisher Bay), is located on Baffin Island and Nunavut has four official languages: Inuktitut (the most commonly used language), Inuinnaqtun, French, and English (Government of Nunavut, 2012). Nunavut has two climatic zones: subarctic and Arctic. There are also two major geographical regions: the taiga, a boreal forest belt located south of Baker Lake and resident to pine, aspen, poplar, and birch trees; and tundra, which covers a majority of Nunavut (the mainland and islands), a rocky region where vegetation is stunted by the cold climate. Baker Lake (Qamani’tuaq, meaning a “big lake joined by a river at both ends”) is the Nunavut’s sole inland community and is near the geographical centre of the territory.

Early Rabies As with the Northwest Territories, the origin of the rabies in Nunavut is clouded in folklore but probably followed the same path as that of the Northwest Territories (see Chapter 14b). Some of the earliest reports of a rabies-like disease came from a report written by Elton (1931) who had been commissioned by the Hudson’s Bay Company to determine the reason for fluctuations of wildlife numbers in the Arctic areas of Baffin Island, Hudson Strait, and Hudson Bay. While not completely accurate in detail, his report brings together the results of a questionnaire delivered by the Hudson’s Bay Company to some of their posts in the North to determine as much as possible about the sled dog and fox disease (Elton, 1931). His report says nothing of actual rabies cases diagnosed but rather gives first-hand accounts of outbreaks in and around the Hudson Bay area. The first of these accounts was from the Pond Inlet Post (Mittimatalik) in 1909 and again in 1927. He reported numerous attacks on sled dogs by foxes in the Baker Lake Post area during 1916–1920, as well as 1929, although the disease on this last date might have been distemper (Elton, 1931). Similar attacks on dogs were reported at Chesterfield Post in 1922 and 1925–1928; Eskimo Point Post (Arviat) in 1927 and 1928; Frobisher Bay Post (Iqaluit) in 1924 and 1927; Lake Harbour Post (Kimmirut); every year in Repulse Bay Post (Naujaat) after 1926 (perhaps distemper), and Wager Inlet Post in 1929 (now Ukkusiksalik National Park of Canada).

Nunavut

Figure 14c.1: Nunavut communities using current names.

Source: Nunavut Department of the Environment. Note: Refer to Table 14c.1 for English, Inuktitut, and Syllabics spellings.

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A History of Rabies Management in the Provinces and Territories

communities of Baker Lake, Aklavik, and Frobisher Bay, thus confirming the presence of rabies in the western, central, and eastern Arctic. Table 14c.2 shows the rabies-positive cases for Nunavut from 1947 to 2017. Rabies was not diagnosed in Nunavut in 1949, 1950, 1951, or 1952. Three cases were reported in 1953 one of which was a caribou at Spence Bay, in the Central Arctic Region of Nunavut. Between 1953 and 1975, few positive cases of rabies were reported. However, in 1976, 13 foxes were diagnosed in the Cambridge Bay area of Victoria Island, leading to the inclusion of this community along with Gjoa Haven and Spence Bay in the 1978 surveillance for rabies (Secord et al., 1980). No rabies was found in 127 arctic fox specimens submitted for diagnosis for that year (see Chapter 14b, Table 14b.3). A large outbreak occurred in 1981 in Nunavut with 19 cases: 13 arctic foxes, 4 dogs, 1 caribou, and 1 wolf. This was followed by an even larger outbreak in 1982 in arctic foxes, one dog, and a caribou in the Cambridge Bay area (Table 14c.2). From 1982 onwards, rabies-positive cases remained high, mostly in arctic foxes and a few wolves. Rabies peaked again in the early 1990s, with most cases in arctic foxes, some red foxes and dogs, and the occasional wolf (Table 14c.2). Rabies cases in Nunavut have remained relatively high since then. Incidence was primarily in foxes. Over 73% of all diagnosed cases were in arctic foxes, red foxes, and foxes whose species were not differentiated. Of those cases over 83% were arctic foxes and 9% were red foxes. Unlike its neighbour Northwest Territories, there was no evidence that incidence in red foxes was concentrated inland. Approximately 23% of cases were in dogs, and the remaining cases were in wolves (18 cases) or caribou (2 cases). Table 14c.3 examines the species composition of submissions of specimens for rabies testing. In relative terms, diagnosing rabies in foxes is more efficient than in domestic animals (dogs and cats). About 66% of all submitted fox specimens test positive while only about 21% of submitted domestic specimens test positive. Since the surveillance system’s first priority is to protect humans, the additional submissions of domestic specimens simply reflects that human contact with domestic animals in rabies-suspicious circumstances is more likely. Interestingly, until 1976, more positive dog cases were reported than fox cases. Then fox positives increased and have since surpassed cases diagnosed in dogs. Whether this represents a shift in reporting priorities or less reliance on sled dogs with the introduction of the snowmobile is not known.

Table 14c.1  Nunavut community names. English

Inuktitut

Syllabics

South Camp*

Sanikiluaq

ᓴᓂᑭᓗᐊᖅ

Eskimo Point

Arviat

ᐊᕐᕕᐊᑦ

Whale Cove

Tikirarjuaq

ᑎᑭᕋᕐᔪᐊᖅ

Rankin Inlet

Kangiqliniq

ᑲᖏᕐᑭᓂᖅ

Baker Lake

Qamani’tuaq

ᕐᑲᒪᓂᑦᑐᐊᖅ

Coral Harbour

Salliq

ᓱᓪᓕᖅ

Chesterfield Inlet

Igluligaarjuk

ᐃᒡᓗᓕᒑᕐᔪᒃ

Kugluktuk

Qurluqtuq

ᕐᑯᕐᓗᖅᑐᖅ

Cambridge Bay

Iqaluktuuttiaq

ᐃᕐᑲᓗᒃᑑᑦᑎᐊᖅ

Gjoa Haven

Uqsuqtuuq

ᐅᕐᒃᓱᕐᒃᑑᖅ

Taloyoak

Talurjuaq

ᑕᓗᕐᔪᐅᕐᒃ

Pelly Bay*

Kugaaruk

ᑰᒑᕐᔪᒃ

Repulse Bay

Naujaat

ᓇᐅᔮᑦ

Hall Beach

Sanirajak

ᓴᓂᕋᔭᒃ

Igloolik

Iglulik

ᐃᒡᓗᓕᒃ

Cape Dorset

Kinngait

ᑭᙵᐃᑦ

Lake Harbour

Kimmirut

ᑭᒻᒥᕈᑦ

Frobisher Bay

Iqaluit

ᐃᕐᑲᓗᐃᑦ

Pangnirtung

Pangniqtuuq

ᐸᖕᓂᖅᑑᖅ

Broughton Island*

Qikiqtarjuaq

ᕐᑭᑭᕐᒃᑕᕐᔪᐊᖅ

Clyde River

Kangiqtugaapik

ᑲᖏᕐᒃᑐᒑᐱᒃ

Pond Inlet

Mittimatalik

ᒥᑦᑎᒪᑕᓕᒃ

Arctic Bay

Ikpiarjuk

ᐃᒃᐱᐊᕐᔪᒃ

Resolute

Qausuittuq

ᖃᐅᓱᐃᑦᑐᕐᒃ

Grise Fiord

Aujuittuq

ᐊᐅᔪᐃᑦᑐᖅ

Source: Nunavut Department of Environment. * Names are no longer used.

Rabies, 1947 to 2012 The Hudson’s Bay Company reported that a disease of dogs resembling rabies had developed at Creswell Bay on Somerset Island in 1945 and that 23 of 39 dogs had died of the disease (Tabel et  al., 1974). The disease was then reported in 1946 at Arctic Bay (Ikpiarjuk), Pond Inlet (Mittimatalik), Clyde River (Kangiqtugaapik), Pangnirtung (Panniqtuuq), and Lake Harbour (Kimmirut) on Baffin Island. The reports indicated that the epizootic spread among the arctic foxes and was then transmitted to the sled dogs by the foxes. In October 1946 a rabies-like disease was reported at Eskimo Point on Baker Lake (Tabel et al., 1974). By 1947 rabies had been diagnosed by Plummer both histologically and later by virus isolation in the three

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Nunavut

Table 14c.2  Rabies cases by species, Nunavut, 1947 to 2017. These data excludes all cases in the old Northwest Territories. Arctic (AFX) and red (RFX) foxes are not differentiated. Until the early 1970s submission reports were simply coded as FOX, after which the species of fox was usually noted.

Year

Total

Fox

Dog

Wolf

1993

28

23

5

0

Caribou 0

1994

15

10

5

0

0

1995

7

2

3

2

0

Year

Total

Fox

Dog

Wolf

1996

0

0

0

0

0

1947

4

1

2

1

0

1997

2

2

0

0

0

1948

4

0

4

0

0

1998

7

6

1

0

0

1954

2

1

1

0

0

1999

5

4

0

1

0

5

5

0

0

0

Caribou

1955

2

1

1

0

0

2000

1956

4

0

4

0

0

2001

13

10

3

0

0

12

10

2

0

0

1957

0

0

0

0

0

2002

1958

1

0

1

0

0

2003

0

0

0

0

0

1959

0

0

0

0

0

2004

4

4

0

0

0

1960

0

0

0

0

0

2005

7

3

2

2

0

1961

0

0

0

0

0

2006

10

6

4

0

0

1962

0

0

0

0

0

2007

6

5

1

0

0

1963

2

2

0

0

0

2008

14

8

5

1

0

5

4

0

1

0

1964

5

3

2

0

0

2009

1965

0

0

0

0

0

2010

5

5

0

0

0

4

3

0

1

0

1966

1

0

1

0

0

2011

1967

3

2

1

0

0

2012

10

8

2

0

0

1968

2

0

2

0

0

2013

10

6

4

0

0

1969

3

1

2

0

0

2014

10

7

3

0

0

1970

0

0

0

0

0

2015

17

15

2

0

0

2016

5

5

0

0

0

1971

0

0

0

0

0

1972

4

2

2

0

0

2017

13

10

3

0

0

458

336

102

18

2

73.4

22.3

3.9

0.4

1973

2

1

1

0

0

 Total

1974

5

3

2

0

0

  % Total

1975

4

0

4

0

0

1976

13

12

1

0

0

1977

11

10

1

0

0

1978

2

2

0

0

0

1979

1

1

0

0

0

1980

4

3

1

0

0

1981

17

11

4

1

1

1982

8

6

1

0

1

1983

4

4

0

0

0

1984

1

1

0

0

0

1985

11

10

0

1

0

1986

15

14

0

1

0

1987

7

6

1

0

0

1988

18

15

2

1

0

1989

13

11

2

0

0

1990

22

16

5

1

0

1991

33

24

5

4

0

1992

16

12

4

0

0

Source: compiled from CFIA data.

Unlike in the Northwest Territories there is no evidence of any cycling in foxes in Nunavut despite the early comments that fox populations follow a three- to fiveyear lemming cycle and that rabies incidence follows fox populations (Elton, 1931; Angerbjörn, 1999). Given the large size of the area, the low numbers of rabies cases reported, and the scattered locations of observers, cycling would be difficult to detect with CFIA data. This question is further discussed in the section “Fluctuations in Fox Populations.”

Active Surveillance The active surveillance undertaken by Secord (1980) from 1978 until 1985 was discussed in Chapter 14b. The active

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A History of Rabies Management in the Provinces and Territories

on Banks Island, concluded that 1973–1974 was a peak year for fox populations on Banks Island, with fur export returns indicating 6024 skins sold. Previous years had shown a harvest of less than 3000 pelts. The report suggests that while trapping success is dependent on fox abundance and effort (Usher, 1971), for the 1973–1974 season, fur prices were at record high levels, perhaps offering an inducement for trapping by the Bankslanders (Beak Consultants, 1975). On the other hand, Elton (1931) examined the fur records of the Hudson’s Bay company and concluded that the average population for lemmings and foxes peaked about every four years, with the lemming’s peaking a year before the fox population. This lag time was similar to that reported by Angerbjörn (1999) in his study on arctic foxes on the north Arctic coast of Russia from the Kola Peninsula to Wrangel Island (Ostrov Vrangelya). Although there were annual variations in incidence (Figure 14c.2), time series analysis similar to that done in Chapter 14b did not show any periodicity in the annual rabies record for Nunavut. The size of the area, its island geography, and the relatively low number of observers confound any effort to detect any periodicity in the case records for Nunavut.

Table 14c.3  Submissions by species, 1978 to 2017, for Nunavut. Submissions were only available from 1978 onwards. Test Species

Total

Negative

Positive

% Positive

Fox

483

171

312

64.6

Dog/Cat

344

271

73

21.2

36

16

20

55.6

Wolf Other

26

24

2

7.7

 Total

889

482

407

45.8

Source: compiled from CFIA data.

surveillance carried out between 1973 and 1985 used trap lines to target the arctic and red fox but ignored other wildlife rabies vectors, such as the wolf. The number of submissions from Nunavut communities was about half that from the Northwest Territories, perhaps because of better organization of trapping in the Banks Island area or the shorter distances from the main survey station in Northwest Territories. Overall, the number of positives in the active surveillance samples was low, except for the results in 1979 for arctic foxes in Banks Island (44 of 202).

Fluctuations in Fox Populations

Rabies Management in Nunavut

Macpherson (1969) undertook a study between 1958 and 1963 in the Baker Lake, Keewatin, and Resolute Bay, Franklin, areas to determine the cause of the fluctuations occurring in the arctic fox populations. Trapping arctic foxes for their fur at that time was an important source of revenue. The author investigated the biology of the arctic fox, with annual surveys of fox dens, analyses of fox diets, estimation of lemming numbers, and a count of weaned fox litters. Lemmings (Lemmus and Dicrostonyx) were found to be the major prey animals of the arctic foxes, with mice, birds, and carrion when lemmings were scarce. When lemming numbers decreased, fewer whelps survived. The main interest of the author was to identify factors important in determining arctic fox numbers in the wild, to then try to predict trapping harvests. The years of highest lemming population were also the years of highest whelp production. Adapting to the Arctic environment, the fox may produce larger litters for survival of the species (Macpherson, 1969). A relationship between the lemming and fox populations, the number of arctic fox pelts taken, the fur price paid for the pelt in a particular year, and the link to rabies in the fox populations is debatable given the confounding variables of fur prices and trapper effort. A 1975 report by Beak Consultants

General Considerations Nunavut faces similar challenges to those of the Northwest Territories in its programs to manage rabies. Nunavut’s Indigenous population is situated in 25 isolated communities widespread over a huge land mass (see Overview, Part 3), its wildlife vectors and reservoirs are spread over a vast tundra area, and it is often faced with inclement weather. Compounding this is the fact that diagnosis of rabies occurs in laboratories much farther south, with the difficulties of obtaining a specimen and transporting it to the nearest collection facility for shipping by air to a federal diagnostic laboratory. As a new territory, Nunavut has the advantage of lessons learnt about rabies management by its neighbour the Northwest Territories and from the administrative experience of the Hudson’s Bay Company until 1898, when control of the area was organized out of Ottawa, the nation’s capital. Aboriginal Affairs and Northern Development Canada (AANDC) transferred responsibility and control over the lands, resources, and environment to the Indigenous peoples and northerners through land claims and self-government agreements and devolution to territorial governments.

236

Nunavut

Figure 14c.2: Rabies cases by year for Nunavut, 1954–2017. Source: created from CFIA data.

their superiors in Nunavut. Help with the submission of specimens is minimal. Additional information on the duties of the RCMP can be found in Chapter 14b.

AANDC also helps in developing the area’s natural resources and protecting the environment in most First Nations communities and their territories (Aboriginal Affairs and Northern Development Canada, 2012). As mentioned, the arctic fox is the primary rabies vector in Nunavut (see Chapter 26b). The primary exposure risk for humans, however, is the dog. Despite the transition in the north from dog sleds to snowmobiles, communities across Nunavut have large numbers of dogs. Sled dogs are generally tied in specific areas in winter and summer, often two different areas. There are stray dogs in most communities and pet dogs tied near the houses. Since arctic foxes are often attracted to areas around communities and camps where there are good opportunities for scavenging (i.e., landfills or garbage, food caches, drying hides around houses) and that all Nunavut communities have open pit dumps, with the dumps located very close (within one or two kilometres) to communities, many opportunities exist for fox and dog interactions and the transmission of rabies.

WILDLIFE MANAGEMENT

During the mid-1900s, a wolf control program was initiated in Nunavut and the Northwest Territories in an attempt to increase the prey populations for human consumption. No report came from this program, and it was discontinued in 1977–1978. At that time, Nunavut was a part of Northwest Territories and they shared an estimated population of 10,000 wolves. Since the territories’ separation in 1999, wildlife management in Nunavut has come under the jurisdiction of wildlife management boards established by the Nunavut Land Claims Agreement, which provides for the Wildlife Management division of the Department of Environment (DoE) to recommend appropriate total allowable harvest (TAH) levels for some wildlife species in Nunavut. These species include the two groups of wolves found in Nunavut: the tundra or timber wolf (Canis lupus occidentalis) and the high arctic wolf (Canis lupus arctos). In its report of 2007, the DoE recommended no TAH for the tundra or timber wolf, as it was in no danger of extermination because of its relatively large population, high intrinsic rates of natural population growth, complete lack of barriers to movement, and large source populations in Northwest Territories, Saskatchewan, and Manitoba (Wildlife Research Section, 2007). There is conflicting evidence that the discontinuation of the wolf control program has affected rabies incidence in wolves. Table 14c.2 shows that there was only 1 diagnosed

Early Rabies Management ROYAL CANADIAN MOUNTED POLICE

The early history and involvement of the Royal Canadian Mounted Police (RCMP) in rabies control is discussed in Chapter 14b. As in Northwest Territories, the RCMP has not been involved with vaccination of domestic pets since 1995. Today, RCMP officers assist as necessary when there is no wildlife officer or by-law officer in the community, and the employees of the Health Centre are unable to assist with animal quarantines. This assistance is negotiated with

237

A History of Rabies Management in the Provinces and Territories

case of rabies in wolves before 1980 and 17 cases since then. Table 14c.3, which includes some active surveillance submissions, shows 20 cases since 1980. Eight of those cases were in the Baker Lake District, which has experienced population growth since 1980 with exploration, mining, and development in the area. Increased population means increased contact with wildlife and, therefore, more reporting. Recently, for example, a rabid wolf attacked a worker at Peregrine Diamond’s Ltd, Nanuq site, near Wager Bay (“Mining Camp Worker Shot,” 2011, pp. 1–3) some 280 kilometres northeast of Rankin Inlet. This resulted in medical treatment for the worker.

Environment, 2012). This includes humane euthanasia of diseased wildlife, collection of samples, receipt of samples submitted by the public, and collection and submission of samples for testing and, in the case of rabies, submission of samples to the CFIA laboratory. When samples submitted to the Canadian Cooperative Wildlife Centres at the Western College of Veterinary Medicine in Saskatoon or the Ontario Veterinary College in Guelph are reported to be positive for rabies on a differential diagnosis, these are forwarded to CFIA in Ottawa for confirmation.

Rabies Management Today

The chief medical officer of health (CMOH) of the Department of Health leads the investigation of all potential human exposures to rabies. Located in Iqaluit, the CMOH and staff are responsible to their minister for delivery of programs. Health has five regional Environmental Health officers (EHOs) who assist in coordinating a response to rabies in the territory: three officers in the Baffin region (Qikiqtaaluk); one officer in the Kitikmeot region; and one in the Kivalliq region (Keewatin). Iqaluit has two full-time territorial environmental health specialists, a position akin to a territorial EHO. The EHOs respond to and investigate all human and animal exposures to ensure that the risk to humans of rabies is mitigated through consultation between the CMOH and the medical staff in the communities (M. Baikie, personal communication, 19 April 2014). The local by-law officer or CO often assist the EHOs in the investigation and quarantine of animals in the communities. The DoE provides the sampling services for submission of rabies samples for analysis and arranges the transport of the sample to the CFIA laboratories with the help of the regional EHO. Twenty-five communities have health centres, each with between one and five nurses, either nurse practitioners or expanded duty nurses. Iqaluit has a hospital and an emergency department that receives the rabies animal contact incident victims. All other community health centres provide the emergency treatment for animal contact victims. No one department is responsible for sled dogs and dog teams or animal health in the communities (P. Workman, personal communication, 21 and 24 April 2012).

Department of Health

CANADIAN FOOD INSPECTION AGENCY PRESENCE

As of 2014, the Canadian Food Inspection Agency (CFIA) downloaded the tasks of collection and transportation of suspect rabies cases to the provincial and territorial governments. However, rabies testing still occurs at the federal government laboratories. Nunavut pays for the shipment of specimens from the northern Arctic communities of Baffin Region (Qikiqtaalak) to Iqaluit and then to Nepean, Ottawa, and specimens from the Kitikmeot and Kivalliq Regions are flown to Edmonton and then shipped by bus to Lethbridge, Alberta. TERRITORIAL RABIES MANAGEMENT

With no regional health authorities in Nunavut (compared with the Northwest Territories), the Nunavut Department of Community and Government Services has three regional offices with a headquarters in Iqaluit, the capital. The Kitikmeot Office in the central Arctic region has a headquarters at Cambridge Bay and administers six other communities. The Kivalliq region (Keewatin), with its headquarters at Rankin Inlet, also administers six other communities. Baffin Region (Qikiqtaaluk), headquartered at Cape Dorset, administers 12 other communities, including Iqaluit. Rabies management in Nunavut is through two departments: the DoE and the Department of Health.

Department of Environment

The Wildlife Management division of the Nunavut DoE is responsible for the delivery of wildlife management at the community level through a network of conservation officers (COs). The COs ensure compliance with wildlife laws and regulations; as part of their duties, they deal with emergency wildlife issues affecting public safety and animal welfare, such as diseases of wildlife, including rabies, near communities and camps (Nunavut Department of

LAY VACCINATION PROGRAMS

A lay vaccinator program existed in the Northwest Territories before the creation of Nunavut in 1999 (see Chapter 14b) and was supported by the departments of Sustainable Development, Environment, and Health. Health continues to provide the program, with vaccination 238

Nunavut

of the dogs in community being another layer of human rabies prevention and management. Training is minimal for vaccinators, each being given instructions, the equipment, and vaccines to vaccinate community dogs. The program exists in all Nunavut communities, with Health purchasing approximately 6000 vaccine doses per year and associated supplies (syringes, needles, etc.) under a special permit from the CFIA. A pamphlet on rabies provided by the DoE in several languages gives information on rabies and its signs, as well as contacts after bites from a possibly rabid animal.

semi-generalists, living mostly on fluctuating populations of Microtine rodents (see Chapter 26b). This observation was confirmed in a Swedish report that compared the Microtine diet of in-land foxes to the generalist foxes in coastal areas whose diet included inland prey, seal carcasses, sea birds, fish, and other assorted vertebrate carcasses (Elmhagen et  al., 2006). This generalist foraging behaviour allows the fox to inhabit a variety of home ranges, be widely distributed, and be able to reach high population densities in and near human communities or camps. It also allows for a very rapid recovery of populations decimated by disease or culling. Given the need to scavenge, the foxes are able to travel long distances in search of food, perhaps carrying living rabies virus with them (Tarroux et al., 2010). Recent movement studies illustrate how arctic foxes can play a major role in epizootic rabies events across Nunavut. During 2008 reproductively active adult arctic foxes fitted with satellite tracking collars travelled up to 90 kilometres per day and travelled as far as 4599 kilometres away and returned several times to their original location on Bylot Island (Tarroux et al., 2010). One of the authors (Atkinson) noted that a fox tagged at Cambridge Bay was subsequently trapped at the dump in Resolute Bay, the same year, a distance of over 600 kilometres. The relatively low level of vaccination in pets and working dogs, the origin of services available for rabies vaccination, and the limited geographic coverage provides for poor vaccination in Nunavut. Given that there are lay clinics for vaccination, one veterinary clinic in Iqaluit servicing local needs and pets in the surrounding areas, and several visiting veterinary teams serving a few communities periodically, the level of pet vaccination is low. The proportion of rabies-vaccinated animals with protective immunity in Nunavut is unknown, but it is certainly less than other parts of Canada. What role this level of immunity plays in rabies in the north is unknown but should be a concern for public health officials.

VETERINARY CLINICS

A community clinic, sponsored by the Rotary Club, provides veterinary care for dogs, cats, and other animals on a yearly basis in Iqaluit. It provides spay and neuter surgery for pets, other minor surgery, rabies vaccination, and veterinary medications. More recently, a veterinary graduate established a clinic in Iqaluit, providing the first veterinary health care clinic in Nunavut (Rogers, 2011). Veterinarians must register with the professional practice unit in Kugluktuk to practice in Nunavut. OUTSIDER VACCINATION CLINICS

A recent development in rabies management in Nunavut has been the arrival of veterinary assistance teams providing veterinary care to communities in Nunavut. The Canadian Animal Assistance Team (CAAT), staffed by volunteers, has provided sterilization and vaccination services to some Nunavut communities since 2007. The team also educates community members on animal health issues. CAAT moved its focus on veterinary care and population control by sterilization from Iglulik to Baker Lake in 2009 and has provided vaccinations for pets including distemper, parvovirus, and rabies. CAAT is a non-profit registered Canadian charity and does not charge for its services. The team comprises a team leader, veterinarians, veterinary assistants, and technicians (C. Robinson, March 9 and 10, 2012).

Future Developments

Discussion

In the future, we might see higher reported rabies incidence as a result of increased human and pet populations and population expansions into previously uninhabited areas. These changes will result in higher encounter rates and, therefore, increased incidence and prevalence rates, particularly if the disease ecology and human land use favour the transmission or maintenance of the disease. In the north rabies is more of an emerging problem. There are no regulations requiring rabies vaccination of

How the rabies virus is maintained in the Arctic is not known (see Chapter 37). The length of its incubation period is known to vary widely, which perhaps ensures that some animals survive any period of minimal inter- and intra-specific contact during spring and summer and provide for a source of the virus later, when the young adults are moving away from their dens (see Chapter 26b). arctic foxes tend, for the most part, to be specialists or 239

A History of Rabies Management in the Provinces and Territories

domestic animals. The lack of licensing programs for dogs and cats makes it difficult to monitor the vaccination status of pets. Improvement requires developing and implementing legislation governing rabies vaccination, licensing companion animals, monitoring levels of vaccination, addressing the critical waste management issues in communities, and developing more a formal control strategy or policy for management and mitigation of risks. Finally, more research is needed on the ecology of the arctic fox and the expanding range of the red fox. This will

require surveying the animal populations and related work on prey species. These surveys will also provide a means of evaluating the role of active surveillance and passive surveillance in rabies monitoring. Finally, the surveys will help provide parameter estimates on animal populations and the ecology of rabies that will aid in the development of models to explore the interactions of animal movement, variations in incubation period, cycling in prey species, and levels of population immunity in the persistence of rabies in the north.

Acknowledgments The authors would like to acknowledge the useful update edits of Wanda Joy, BSc, BTech, CPHI(C), territorial environmental health specialist, from the Department of Health in Nunavut.

References Aboriginal Affairs and Northern Development Canada. 2012. Environment and natural resources. Retrieved from https://www .aadnc-aandc.gc.ca/eng/1100100034243/1100100034247 Angerbjörn, A., Tannerfeldt, M., & S. Erlinge. (1999). Predator-prey relationships: Arctic foxes and lemmings. Journal of Animal Ecology, 68(1), 34–49. https://doi.org/10.1046/j.1365-2656.1999.00258.x Beak Consultants. (1975). Banks Island arctic fox studies: Age structure and rabies infection from 1973–1974 trap-line returns (Project: C6038). Calgary, AB: Panarctic Oils. Elmhagen, B., Tannerfeldt, M., Verucci, P., & Angerbjösrn, A. (2006). The arctic fox (Alopex lagopus): An opportunistic specialist. ­Journal of Zoology, 251, 139–149. https://doi.org/10.1111/j.1469-7998.2000.tb00599.x Elton, C. (1931). Epidemics among sledge dogs in the Canadian Arctic and their relation to disease in the arctic fox. Canadian Journal of Research, 5(6), 673–692. https://doi.org/10.1139/cjr31-106 Government of Nunavut. (2012). Government of Nunavut. Retrieved from https://www.gov.nu.ca/eia Macpherson, A. H. (1969). The dynamics of Canadian arctic fox populations (Canadian Wildlife Service Report Series, Number 8). ­Ottawa, ON: Department of Indian Affairs and Northern Development. Mining camp worker shot in rabid wolf mishap. (2011, July 14). Nunatsiaq News, pp. 1–3. Retrieved from https://nunatsiaq.com/stories /article/65674_fending_off_rabid_wolf_causes_camp_shooting_injury/ Rogers, S. (2011, December 2). Iqaluit-raised vet moves mobile vet service back home. Nunatsiaq News. Retrieved from https:// nunatsiaq.com/stories/article/65674iqaluit-raised_vet_moves_mobile_vet_service_back_home/ Secord, D. C., Bradley, J. A., Eaton, R. D., & Mitchell, D. (1980). Prevalence of rabies virus in foxes trapped in the Canadian Arctic. ­Canadian Veterinary Journal, 21, 297–300. Tabel, H., Corner, A. H., Webster, W. A., & Casey, C. A. (1974). History and epizootiology of rabies in Canada. Canadian Veterinary Journal, 15(10), 271–281. Tarroux, A., Berteaux, D., & Bety, J. (2010). Northern nomads: ability for extensive movements in adult arctic foxes. Polar Biology, 33, 1021–1026. https://doi.org/10.1007/s00300-010-0780-5 Usher, P. J. (1971). The Bankslanders: Economy and ecology of a frontier trapping community. Vol. 2: Economy and ecology. Ottawa, ON: Department of Indian Affairs and Northern Development. Retrieved from http://publications.gc.ca/collections/collection_2017 /aanc-inac/R42-4-1971-2-eng.pdf Wildlife Research Section. (2007). Recommendations on total allowable harvest (TAH) rates for the terrestrial wildlife populations in Nunavut (Final Wildlife Report No. 4). Iqaluit, NU: Nunavut Department of Environment. Retrieved from http://www.gov.nu.ca/sites /default/files/recommendations_on_total_allowable_harvest_tah_rates_for_the_terrestrial_wildlife_populations_in_nunavut ._final_wildlife_report_no.4_2007.pdf

240

14d Canada’s North NUNAVIK

David J. Gregory1 and Manon Simard2 1

Canadian Food Inspection Agency (Retired), Ottawa, Ontario, Canada Nunavik Research Centre, Makivik Corporation (2003–2014), Kuujjuaq, Quebec, Canada

2

Introduction Nunavik, meaning “great land” in the Inuktitut dialect, comprises a land area of 443,685 km2 north of the 55th parallel and is home to Inuit of Quebec, whose 12,090 inhabitants call themselves Nunavimmiut and live in coastal communities and municipalities (Kativik Regional Government, 2019). Kuujjuaq is considered the regional capital of Nunavik. Before 1912 the most northerly part of the region was known as Ungava District of the Northwest Territories and, until 1987, was referred to as Nouveau-Québec or New Quebec (see Overview, Part 3). It is bordered by Hudson Bay and James Bay in the west, Hudson Strait and Ungava Bay in the north, Labrador in the northeast, and the administrative regions of Abitibi-Témiscamingue, Mauricie, Saguenay–Lac-Saint-Jean, and Côte-Nord in the south and southeast. This region now known as Nord-du-Québec is divided into three territories: Nunavik, north of the 55th parallel, which became part of Quebec in 1912 and is predominately Inuit; Jamésie, south of the 55th parallel; and Eeyou Istchee, scattered enclaves within the first two with a predominately Cree population. Eeyou Istchee had been a part of Jamésie territory until made into a separate territory on 30 November 2007. On 24 July 2012 the Quebec government signed an accord with the Cree, combining the two territories and creating a new regional government known as Eeyou Istchee James Bay Territory (Government of Quebec, 2010). Following negotiations between Inuit, Cree, Canada, and Quebec, the James Bay and Northern Quebec Agreement

(JBNQA) was signed in 1975 (Secretariat aux affaires autochtones, 1998). This provided for compensation funds to the territory and the Makivik Corporation was created to receive and invest the compensation money intended for Inuit as provided by the JBNQA allowing for economic development to promote the welfare and education of Inuit and preserve the Inuit way of life, values, and traditions (Savoie, 2008; Makivik, 2019). Negotiations for the formation of an autonomous region within Quebec for Nunavik are under way following the settlement of outstanding land claims in 2011. This chapter deals with rabies management in Nunavik and, for purposes of this book, Nunavik is treated separately from Quebec. Rabies data for this area is maintained, however, by the federal government and is stored as part of the database for Quebec.

Rabies in Nunavik Early Rabies Like its neighbouring territories of Nunavut and the Northwest Territories, the origin of rabies in Nunavik is wrapped in legend and stories handed down from generation to generation (see Chapters 14b and 14c). The report by Elton (1931), commissioned by the Hudson’s Bay Company to determine the reason behind the fluctuations in wildlife populations in the Arctic regions of Baffin Island, Hudson Strait, and Hudson Bay, gives the first insight of

A History of Rabies Management in the Provinces and Territories

a rabies-like disease in foxes and sled dogs. While lacking detail of the disease outbreaks or diagnosis of actual rabies cases, the report gives an account of the attacks on dogs by foxes and the resultant death of many dogs. The first accounts, derived from Elton’s questionnaire, reported that many signs of rabies were seen by respondents and that the disease was a constant menace in many communities for years. Great Whale Post (Poste-de-la-Baleine), now Kuujjuarapik, had seen many outbreaks in dogs over the years. George’s River Post or Kangiqsualujjuaq experienced an outbreak among its dogs in March and April 1921, followed by a further outbreak in 1928. Fort Chimo Post, now Kuujjuaq, reported four white foxes dying of the disease in 1922 and community dogs affected during the spring and summer of 1929. South of the 55th parallel, Fort George Post, or Chisasibi in the Eeyou Istychee James Bay Territory of Nouveau Québec, noted disease outbreaks in dogs and foxes in 1925 and 1926. Stupart’s Bay Post or Kangiqsujuaq reported a disease that killed 90% of their dogs in 1927–1928. Between 1928 and 1930, the communities at Leaf River Post, Tasiujaq, and Wolstenholme Post or Ivujivik reported disease in their dog populations (Elton, 1931). These outbreaks were all probably a continuation of outbreaks occurring at the same time in Nunavut.

Table 14d.1  Rabies positives in Nunavik, 1953 to 2017. Only years with cases are included. Arctic foxes were entered as a submission code only from 1985 onwards. Hence, totals and percentages are shown for both 1953 to 2017 and 1985 to 2017. Year

Rabies, 1953–2014 Elton’s report was published in 1931, but it was not until 1947 that a laboratory diagnosis, using Negri body demonstration of rabies in a fox, was published by Plummer (1947). The stories of rabies in the Arctic coming from Elton’s report and the diagnosis of rabies by Plummer indicated a widespread occurrence of rabies in the north, central, and eastern parts of the Northwest Territories. These reports were all probably a result of an epizootic originating in Alaska’s North Slope area around Point Lay and Barrow in 1945–1947 (Williams, 1949) and continuing through 1949–1957 in Alaska (Rausch, 1958) and eventually spreading through Canada’s territories and provinces. Table 14d.1 shows rabies positives from 1953 to 2017 for Nunavik. The data for Nunavik is derived from the Canadian Food Inspection Agency (CFIA) records for Quebec and has been separated from the provincial data based on place names for the reported location of the incident. Those names have changed over time (Table 14d.2) and in a few cases there was missing or incomplete location data. As a result, we made best guesses in some 10 instances as to whether the reported case was inside or outside the

Total

Red Fox

Arctic Fox

Dog

Wolf

Caribou

1953

2

0

n/a

2

0

0

1962

3

0

n/a

3

0

0

1964

3

0

n/a

3

0

0

1965

1

0

n/a

1

0

0

1967

4

3

n/a

1

0

0

1968

1

0

n/a

1

0

0

1975

1

1

n/a

0

0

0

1979

1

1

n/a

0

0

0

1982

1

0

n/a

0

1

0

1983

3

2

0

1

0

0

1986

2

1

1

0

0

0

1987

15

6

6

1

1

1

1988

11

1

7

1

1

1

1990

2

0

1

0

1

0

1991

9

5

2

1

1

0

1992

7

1

2

4

0

0

1993

1

0

1

0

0

0

1995

1

1

0

0

0

0

1996

13

11

1

1

0

0

1999

2

1

1

0

0

0

2000

3

2

0

1

0

0

2001

3

3

0

0

0

0

2002

2

1

1

0

0

0

2003

4

2

0

2

0

0

2004

3

3

0

0

0

0

2005

2

0

1

1

0

0

2006

1

0

0

1

0

0

2007

1

0

1

0

0

0

2008

1

0

0

0

1

0

2009

4

1

0

2

1

0

2011

5

1

3

1

0

0

2012

11

3

5

2

1

0

2014

1

0

1

0

0

0

2015

4

1

1

2

0

0

2016

1

1

0

0

0

0

2017  Total

4

0

3

1

0

0

133

52

38

33

8

2

39.1

28.6

24.8

6.0

1.5

45

38

21

7

2

39.8

33.6

18.6

6.2

1.8

  % Total 1985– 2017   % Total

113

Source: compiled from CFIA data.

242

Nunavik

jurisdictions: Nunavut and the Northwest Territories. As expected, given the considerable distance between them, no statistically significant relationship existed between the time series for Nunavik and the Northwest Territories. There was, however, a statistically significant relationship (r = 0.43, p = .05) between Nunavik and Nunavut at lag 4. Hence, the Nunavik time series appear to lag the peaks in the Nunavut time series by four years (Figure 14d.4). Several considerations arise from the observed four-year cycle in Nunavik and the time series correlation between Nunavut and Nunavik. First, as suggested by Elton (1931), fox populations appear to follow the lemming cycle, which is about four years long. The four-year cycle in Nunavik supports this notion. The lead and lag relationship between the time series in Nunavut and Nunavik appears to contradict the notion that fox populations in the Arctic are driven by area-wide variations in climate that affect food sources for foxes. If it were so, variations in incidence should be similar over adjacent areas. More likely, however, there is enough variation in climate between the two areas that the lemming cycles are out of phase in each area. The third possibility is that there is movement of arctic foxes between the two areas during the winter freeze when pack ice covers Hudson Bay, the Hudson Strait, and Ungava Bay. There is documentation supporting long-distance movements of arctic foxes in other areas of the north (Tarroux & Bertaux, 2010). If indeed the two areas are linked in winter, the corollary of these arguments is that there should be an in-phase fouryear cycle in both areas. Movement across the ice, however, would likely be sporadic given variable conditions throughout the year. As well, long distances are involved. Hence, the weak linkage between the regions could lead to incidence being out of phase. A similar out-of-phase relationship between rabies incidences in neighbouring areas separated by physiographic barriers was reported in Ontario (Tinline & MacInnes, 2004). That a regular cycle is not seen in Nunavut could simply be an artefact of a sparse dataset collated over a very large area, which makes it difficult to detect any signal in the data and affect any conclusions drawn from the data.

Table 14d.2  Hudson’s Bay Posts about 1930, with modern day names in Inuktitut and Syllabics. Post Names

Inuit Names

Syllabics

Georges River Post

Kangiqsualujjuaq

ᑲᖏᕐᓱᐊᓗᒃᔦᐊᕐᒃ

Fort Chimo

Kuujjuaq

ᑰᒃᔦᐊᕐᒃ

Leaf River Post

Tasiujaq

ᑕᓯᐅᔭᕐᒃ

Aupaluk

ᐊᑯᓕᕕᒃ

Kangirsuk

ᑲᖏᕐᓱᕐᒃ

Quaqtaq

ᕐᑯᐊᕐᑕᕐᒃ

Kangiqsujuaq

ᑲᖏᕐᓱᔪᐊᕐᒃ

Salluit

ᓴᓪᓗᐃᑦ

Ivujivik

ᐃᕗᔨᕕᒃ

Payne Bay or Bellin Stuart’s Bay Post Wolstenholme Post

Akulivik

ᓯᓵᓯᐱ

Povungnituk Bay

Puvirnituq

ᐳᕕᕐᓂᑐᕐᒃ

Port Harrison

Inukjuak

ᐊᐅᐸᓗᒃ

Umiujaq

ᐅᒥᐅᔭᕐᒃ

Kuujjuarapik

ᑰᒃᔦᐊᕌᐱᒃ

Great Whale Post

Whapmagoostui (Cree community) Fort George Post

Chisasibi

ᓯᓵᓯᐱ

Source: Manon Simard.

southern boundary of Nunavik. Since 2013, however, this problem has been virtually eliminated as entries in the CFIA data for Quebec include latitude and longitude co­ ordinates for almost all submissions. Dogs were the most diagnosed animal in the 1950s and 1960s. Since then arctic and red foxes have dominated. Unlike in neighbouring Nunavut, the red fox has been diagnosed more often than the arctic fox (Table 14d.1). Over 50% (27) of all red fox cases, however, have been located in Kuujjuaq (Fort Chimo) and Kuujjuarapik (Great Whale Post), the two major communities south of the treeline (Figure 14d.1). In contrast, almost 79% of diagnosed arctic fox cases were located in the coastal communities above the treeline. Since the numbers are small and the distribution of observers (settlements) is scattered, it is not possible to make definitive statements about the patterns of rabies incidence in Nunavik. The relative levels of arctic and red fox incidence, however, seem more like those in the Northwest Territories than in Nunavut. The graph of rabies incidence (Figure 14d.2) shows evidence of cycling. Times series analysis (Figure 14d.3) suggests evidence of a statistically significant four- to five-year cycle. A four-year cycle was also observed in the Northwest Territories. The times series of positives for Nunavik (Figure 14d.2) was compared to the time series of the other northern

Rabies Management General Considerations With its large land mass and sparse landscape; a population located in 14 small Inuit communities accessed only by air, and by water in the summer; and no regional

243

A History of Rabies Management in the Provinces and Territories

Figure 14d.1: Nunavik, the northern portion of Nord-du-Québec. There are no road links between Nunavik communities and southern Quebec. All communities shown are served by airports. Map source: compiled by R. Tinline, Queen’s University, from publically available maps produced by Natural Resources Canada.

government, Nunavik faces many problems in managing rabies. Compounding this is a people steeped in tradition and folklore who often lack an understanding of rabies, and a low level of carcass identity, where sending a specimen for diagnosis means a long trip from Kuujjuaq or other communities in Nunavik to Dorval Airport, Montreal, and then on to the federal laboratory in Ottawa. Furthermore, the long distances separating communities makes surveillance difficult. Added to this is the severe weather associated with Nunavik’s Arctic and subarctic climates where Hudson Bay,

Hudson Strait, and Ungava Bay freeze over providing a potential corridor for animals with rabies to move between Nunavut and Nunavik.

Early Rabies Management ROYAL CANADIAN MOUNTED POLICE

A history of involvement by the Royal Canadian Mounted Police (RCMP) in rabies management is found in Chapter 14a. For Nunavik, this has included rabies vaccination, dog control,

244

Nunavik

Figure 14d.2: Rabies positives in Nunavik, 1962 to 2017. Source: created from CFIA data.

Figure 14d.3: Time series analysis of rabies positives for Nunavik, 1971 to 2017. The peak in the graph at lag 4 (r = 0.33) is statistically significant (95% level). The graph shows a period of 4 to 5 years. The secondary peak at lag 8–9 years emphasizes the significance of the observed cycle. Source: created from CFIA data.

elimination of stray dogs, and the collection and shipment of specimens to Ottawa for rabies diagnosis. Between 1950 and 1970 the RCMP was involved in allegations of the slaughter of Inuit dogs, which were later cleared in 2006 (RCMP, 2006). The immunization of dogs in Nunavik has not been supported by the RCMP or federal agencies since the 1980s, following the signing of the JBNQA. The Ministère de l’Agriculture, des Pêcheries et de l’Alimentation du Québec (MAPAQ) has taken over this support to Nunavik communities.

the Département de Santé Communautaire du Centre hospitalier de l’université Laval (CHUL). In 1983 MAPAQ joined the group, setting objectives for the program to prevent rabies in humans by vaccinating dogs, training local people to carry out vaccination, and providing an intervention protocol for human post-exposure to the virus. Also, a protocol was established by the Public Health Department and the CFIA for sending specimens of potentially rabid animals to the OLF-CFIA diagnostic laboratory in Ottawa, Ontario. Although CFIA had a legal mandate on this issue, it also needed the volunteer involvement of other regional and local organizations such as municipalities, the two hospitals, the Nunavik Research Centre, and the Kativik Regional Government. The protocol included (1) procedures following exposure to a suspected rabid animal, (2) roles and responsibilities of each organization, (3) dog

Rabies Management Today The regional program of rabies control in dogs in Nunavik was established in the 1980s under the collaboration of the CFIA (then Agriculture Canada) and the Nunavik Regional Board of Health and Social Services (NRBHSS) then called

245

A History of Rabies Management in the Provinces and Territories

Figure 14d.4: Annual rabies incidence in Nunavut and Nunavik, 1962 to 2017. Incidence in Nunavik appears to lag incidence in Nunavut by four years, especially since the early 1970s. Source: created from CFIA data.

Nunavik Regional Board of Health and Social Services (NRBHSS)

vaccination and technical aid for Inuit and Cree to protect dogs against rabies and control of stray dogs, (4) education about the main characteristics of the disease in animals, (5) the ways rabies affects people, (6) a vaccination protocol, and (7) procedures for shipping specimens to Ottawa.

The NRBHSS (2019) was instituted by the JBNQA and has the mandate for providing clinical and public health services to the population of Nunavik. It is part of the Quebec network of organizations and institutions working towards the population’s health and safety. With its head office in Kuujjuaq, its principal partners are the Ministère de la Santé et des Services sociaux (MSSS), the 17 other regional boards of health and social services, the two regional health centres of Inuulisivik in Puvirtnituq and Tulattavik in Kuujjuaq, the community organizations, the Kativik Regional Government, the Kativik School Board, and Makivik Corporation. The NRBHSS’s responsibilities are to document and inform the Nunavik population about all health risks, including that of rabies, through education and to support regional programs and service delivery systems. For rabies, it has developed and maintained a protocol and trains health professionals on management of potential human exposure to rabid animals. The NRBHSS also maintains a supply of vaccines and immunoglobulin in both health centres. There are Centres locaux de services communautaires of health (CLSC) in each of the 14 communities. A risk assessment determines whether the contact patient will be treated for rabies and whether an animal specimen will be submitted for diagnosis. This is done in consultation with the Public Health Department professionals at the Health Board, the MAPAQ, the Ministère des Forêts, de la Faune et des Parcs (MFFP), and CFIA. The CLSC contacts the Council of Northern Villages (CNV), one in each

CANADIAN FOOD INSPECTION AGENCY

With no offices in Nunavik, CFIA, through its Health of Animals Act and Regulations, provides mandated direction to Nunavik organizations involved in rabies management through requiring reporting and investigation of all incidents involving contact of people or domestic animals with a suspected rabid animal. Where the contact involves humans, the medical authorities are informed and a specimen submission to Ottawa is authorized. Provision of general information on rabies is a coordinated effort with Nunavik authorities through conferences, newspapers, or phone consultations. As an example: On February 23, 1983, Dr. Eric Forest, a veterinarian from the Veterinary Inspection Directorate in Montreal, travelled to Akulivik to investigate a case of rabies in a dog. He provided information on rabies and its prevention to all local officials, peace officers, doctors and nurses, organizing anti-rabies clinics and ensuring that all village dogs were vaccinated. (Communication, 1983)

RABIES MANAGEMENT NUNAVIK

Nunavik’s regional agencies that are involved in rabies management are discussed below.

246

Nunavik

community, and the person delegated collects the specimen and ships the specimen from the CLSC, alerting the CFIA Montreal office when the flight will arrive in Dorval. Flights occur between most villages and Dorval once a day.

Table 14d.3  Dogs vaccinated per year by MAPAQ in Nord-duQuébec, 2002 to 2013. Villages

Animals

Visited

Vaccinated

2002–2003

15

661

2003–2004

16

669

2004–2005

15

558

2005–2006

16

916

2006–2007

5

290

2007–2008

16

611

2008–2009

6

269

2009–2010

15

282

2010–2011

14

420

2011–2012

15

344

2012–2013

14

393

Year

Innulitsivik and Tulattavik Health Centres

The responsibility of the Inuulisivik and Tulattavik health centres and its professionals is to evaluate the risk of rabies, provide treatment to people exposed to the rabies virus, and provide local management and administration with vaccines and immunoglobulin.

Kativik Regional Government

The Kativik Regional Government encompasses most of the Nunavik region of Quebec. Nunavik is the northern half of the Nord-du-Québec, has 14 municipalities and the Kativik police force under its jurisdiction, and is responsible for creating municipal by-laws to prevent rabies by controlling stray or aggressive dogs. The administrative capital is Kuujjuaq on the Koksoak River.

Source: compiled from MAPAQ data.

Ministère de l’Agriculture, des Pêcheries et de l’Alimentation du Québec

in the data. MAPAQ visits include the training of lay vaccinators.

In the absence of veterinary services in northern Quebec, MAPAQ provides technical and material assistance to the 14 Inuit villages, 9 Cree communities, and the Naskapi community of Kawawachikamach for rabies protection in local dog populations through vaccination as requested (MAPAQ, 2019). This vaccination program by MAPAQ began in 1983 and continues today. Information on the main signs of rabies and ways to protect their animals is provided to the local residents. Training for individuals designated in each community on vaccination procedures; vaccine, syringe, and needle use; and recordkeeping is provided. Travel to the areas to vaccinate dogs is on an annual basis as communities ask for the service. Since 2012 MAPAQ has received all calls about suspected rabid dog cases in Nunavik, evaluated the situation, and relayed the information to CFIA as needed (I. Picard, personal communication, 23 April 2013). Visits to the communities are arranged by the Kativik Regional Government and usually occur in June or September. Dogs are vaccinated for rabies, distemper, and parvovirus disease. Table 14d.3 shows the number of animals vaccinated by MAPAQ per year. While CLSC keeps vaccine on hand, additional vaccine is made available on an as needed basis, and this is not shown

Vaccination Programs

The plan to vaccinate dogs over three months of age by MAPAQ and other organizations had logistical problems. In March 2008 MAPAQ called a meeting of all organizations, known as the Network, to find solutions. The Faculté de Médecine Vétérinaire de Sainte-Hyacinthe (FMV) (University of Montreal) also proposed to help by involving its students in Nunavik’s dog health issues and providing other veterinary services for dogs, including vaccinations. In 2009 FMV started a service called “Free veterinary advice for dogs and cats” for all of Nunavik. This service is given free by phone or by e-mail by the veterinarians at FMV. People can call and ask for advice on their domestic animals. Over the years, veterinary students have come to Kuujjuaq for internships; providing vaccinations, examining dog sled teams for diseases, and providing first aid kits for dogs and first aid training classes to a few interested communities. It is hoped that this cooperative Network service will be accepted by all of Nunavik’s communities and will expand, but it depends on the budget available. In May 2011 a Network called Santé publique vétérinaire au Nunavik was created to inform the public about activities in Nunavik and provide updates on rabies cases as they occur.

247

A History of Rabies Management in the Provinces and Territories

Discussion

Rabies Management, 2014 to 2017

Effective 1 April 2014, the CFIA withdrew from rabies management programs. CFIA no longer assumes responsibility for sampling, specimen submission, or case management of animals suspected of rabies. However, the service of diagnosis of rabies and reporting data was retained. In Quebec, rabies management is now based on a coordinated responsibility shared with animal owners, veterinary practitioners, the Ministry of Forests, Wildlife and Parks (Ministère des Forêts, de la Faune et des Parcs, MFFP), the Ministry of Health and Social Services (Ministère de la Santé et des Services sociaux, MSSS) and the Department of Agriculture, Fisheries and Food (Ministère de l’Agriculture, des Pêcheries et de l’Alimentation du Québec, MAPAQ). The authorities of the northern villages may be involved in the identification of a local resource, particularly for the observation of biting animals or for the preparation and submission of specimens for analysis. In Kuujjuaq the Nunavik Research Centre staff is also responsible. The assessment of the risk of exposure to rabies for humans and the management of significant exposures are supervised in all regions of Quebec, including Nunavik, by a provincial response guidebook and a decision support line (Santé et des Services sociaux Quebec, 2019). Front-line workers in the health network can obtain help from the Public Health Department of Nunavik at any time via the 24-hour medical care system. A bite reporting centre has been set up by MAPAQ and the MSSS to allow the evaluation and observation of biting domestic animals, while the MFFP assumes the responsibility for wild animals. In the event of human exposure to a suspect rabid domestic animal, the protocol dictates that MAPAQ in Nunavik takes the lead role in the case management. In the case of wild animals suspected of having rabies, the office of the MFFP takes responsibility. The local health centre in collaboration with the Nunavik Public Health Department conducts an assessment of human risk. The MFFP and MAPAQ collaborate closely to send specimens from wild animals that have been exposed to human or domestic animals for rabies testing at CFIA. When no human or domestic animal contact is involved, the wild animal specimen can be sent to the Centre québécois pour la santé des animaux sauvages at FMV. In 2018 an agreement was reached between MAPAQ and the authorities of the FMV of the University of Montreal to take charge of the domestic animal vaccination program.

Overall Coordination Despite the lack of a veterinary service in Nunavik, there is a protocol to limit rabies infections in humans that works well. Still, more work needs to be done in regards to dog control, rabies education, dog health care education, training of vaccinators, and maintenance of municipal by-laws. Lack of funding is an issue that falls between several jurisdictions. No regional organization has the expertise or the mandate to provide a veterinarian in Nunavik since this would require funding for infrastructure (personal housing, an office, and a proper laboratory). Municipal by-laws need to be created for some municipalities, and money is required to put them into effect. Currently, there is no legal mandate for health officials to work on zoonotic diseases in dogs and wildlife in Nunavik. The Nunavik Research Centre (part of the Makivik Corporation) is fulfilling part of this role, conducting research on zoonotic diseases in wildlife that may affect the outcome of subsistence hunting. Unfortunately, the JBNQA makes no mention of domestic dog issues in its mandate. The Nunavik Research Centre is involved in the Network because Makivik Corporation hosts the Ivakkak race (dog team race) and has the laboratory facilities to handle potentially rabid animals.

Submissions and Surveillance From 1986 to 2017, some 241 specimens were collected for rabies diagnosis in Nunavik, a relatively small number compared to the Northwest Territories (756) and Nunavut (567) for the same period. These differences probably reflect the size of these regions and the distribution of settlements. The surveillance problem is compounded in Nunavik given its recently developing infrastructure and limited air and water accessibility. This compounds the logistics of specimen collection and often resulted in poor recording of specimen location, lessening the value of the collected data. Active surveillance is essential for good rabies management in terms of anticipating and being prepared for future outbreaks and monitoring their progress. We have already suggested a lag relationship with incidence in Nunavut (Figure 14d.4), an observation that can potentially be used to improve Nunavik’s response to rabies.

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Rabies Resurgence

fox carcasses (see Chapter 37). Scavenging foxes will prey on dead animals of any species or those dying from rabies, thus perpetuating a new cycle. An example of this is given in an RCMP report of 1951 in which eyewitnesses reported that feeding dead rabid fox carcasses to sled dogs resulted in further deaths from rabies. The report, from G Division in Port Harrison (now known as Inukjuak), details events occurring in and around Sugluk (now known as Salluit), Cape Smith (now known as Akulivik) and Puvirnituq during 1951. The report also gives details of the signs demonstrated by the foxes and dogs and on the number of submissions at that time. The full report is in the appendix on pages 250–251.

While data are often sparse from Canada’s north, CFIA data over the past two decades has shown that the arctic fox strain of rabies persists in wildlife, circulating in northern Canada and over time reappearing and spreading south into Quebec and Labrador, as it did in 2012–2013. In 1992 a red fox in the Jamésie region of northern Quebec was diagnosed with the AFX variant of rabies. During 1993, 1996, and 1999 the AFX strain of rabies was isolated from single arctic foxes, typed to arctic strain antigenically. The AFX strain was also isolated from red foxes in 2000, 2002, 2003 (two foxes), and 2004 (three foxes) in Nunavik. All these virus isolates typed to the A3 branch of the arctic fox lineage (S. Nadin-Davis, personal communication, 24 July 2019; see Chapter 2). Of greater interest is the isolation of the AFX strain from a wolf in 2004 in Radisson and three dogs in 2009 from Kangirsuk and Puvirnituq of Nunavik. Isolation of the AFX variant in arctic fox occurred in 1993, 1996, 1999, and 2002. These data indicate that the arctic fox strain remains in the Arctic and has the potential to spread south given the right circumstances. Why the AFX strain continues to recycle and resurge in Canada’s north is not completely understood, but it is probably a combination of many factors, including the fox population density, the available prey as the foxes move through a territory, and the survival of the virus in dead

Future Considerations Future considerations for rabies management in Nunavik include neutering dogs – an idea that needs to be accepted by the Inuit and provided at low cost; using vaccine baits around communities, which could be problematic and needs more research because of the closeness of wildlife, dogs, and humans in the communities; and developing a better understanding of the behaviour and biology of red and arctic foxes in the subarctic (M. Simard, personal communication, 2012). Increasing dog vaccination and public awareness about rabies are also key factors that will contribute to improve rabies management in Nunavik.

Acknowledgments The authors would like to acknowledge the assistance of Dr Mario Brisson, Public Health Department of Nunavik and Dr Jean-François Proulx, Regional Board of Health and Social Services, Nunavik, in editing and updating sections of this chapter. Our thanks to Dr Ariane Massé, biologist with Ministère des Forêts, de la Faune et des Parcs for her assistance with editing sections of this chapter.

References Communication. (1983). Rabies in Northern Québec. Agriculture Canada, Food Production and Inspection Branch, Communication # 36. The document is available upon request from Canadian Agriculture Library, [email protected]. Elton, C. (1931). Epidemics among sledge dogs in the Canadian Arctic and their relation to disease in the arctic fox. Canadian Journal of Research, 5(6), 673–692. https://doi.org/10.1139/cjr31-106 Government of Quebec. (2010). Territorial Profile: Nord-du-Québec. Retrieved from Energy and Natural Resources website: https:// mern.gouv.qc.ca/english/publications/nord-du-quebec/profile-nord-du-quebec.pdf Kativik Regional Government. (2019). General information. Retrieved from https://www.krg.ca/en-CA/general-information Makivik Corporation. (2019). Mandate. Retrieved from https://www.makivik.org/corporate/makivik-mandate/

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A History of Rabies Management in the Provinces and Territories Ministère de l’Agriculture, des Pêcheries et de l’Alimentation du Québec. (2019). Technical assistance to northern communities for the protection of dogs against rabies. Retrieved from Ministry of Agriculture, Fisheries and Food website: https://www.mapaq.gouv. qc.ca/SiteCollectionDocuments/Santeanimale/Maladies%20animales%20sous%20surveillance/Rage/Programmeaidetechnique_anglais.pdf Nunavik Regional Board of Health and Social Services. (2019). About us. Retrieved from http://nrbhss.ca/en/nrbhss/about-us Plummer, P. J. G. (1947). Preliminary note on arctic dog disease and its relationship to rabies. Canadian Journal of Comparative Medicine, 11, 154–160. Rausch, R. L. (1958). Some observations on rabies in Alaska, with special reference to wild Canidae. Journal of Wildlife Management, 22(3), 246–260. https://doi.org/10.2307/3796457 Royal Canadian Mounted Police. (2006). Final report: RCMP review of allegations concerning Inuit sled dogs. Retrieved from Government of Canada Publications website: http://publications.gc.ca/collections/collection_2011/grc-rcmp/PS64-84-2006-eng.pdf Santé et des Services sociaux Quebec. (2019). Aide à la décision – Gestion des expositions à risque de rage. Retrieved from http://www. msss.gouv.qc.ca/aide-decision/etape.php?situation=Rage Savoie, D. (2008). Self-government in the Canadian north: Creation of the Nunavik Regional Government: Innovative project and challenges. Presentation by the former chief federal (Canada) negotiator for Nunavik, Inuit, Arctic and Circumpolar Affairs. Retrieved from Henry M. Jackson School of International Studies, University of Washington, website: https://jsis.washington.edu/wordpress/ wp-content/uploads/sites/20/2018/07/NUNAVIK-GOVERNMENT-ENGLISH.pdf Secretariat aux affaires autochtones. (1998). James Bay and Northern Québec agreement and complementary agreements. Sainte-Foy, QC: Les Publications du Québec. Retrieved from http://www.aenq.org/fileadmin/user_upload/syndicats/z77/Stock/English/Documents/ James_Bay_agreement/JamesBayAgreementComplete.pdf Tarroux, A., & Berteaux, D. (2010). Northern nomads: Ability for extensive movements in adult arctic foxes. Polar Biology, 33(8), 1021– 1026. https://doi.org/10.1007/s00300-010-0780-5 Tinline, R., & MacInnes, C. (2004). Ecogeographic patterns of rabies in southern Ontario based on time series analysis. Journal of Wildlife Diseases, 40(2), 212–221. https://doi.org/10.7589/0090-3558-40.2.212 Williams, R. B. (1949). Epizootic of rabies in interior Alaska, 1945–1947. Canadian Journal of Comparative Medicine, 13(6), 136–143.

Appendix: Royal Canadian Mounted Police Division File 49G 1074-4-2-M1 Division Subdivision Detachment “G” Port Harrison Province P.Q. Date 10-3-51 Dog Diseases in Northern Quebec, Rabies.

3. The following was received from G. G. Sinclair, Director, Resources and Development on the 29-12-50: 4. Quote: Rerutel data Dec 19th regarding dog disease stop Research Institute state that evidence is insufficient to give advice and if the affected dogs present nervous symptoms the condition would almost certainly be rabies stop Would appreciate further information regarding affected dogs and if symptoms are other than nervous please ship out on first available flight a few frozen specimens so that precise examination can be made. Unquote. 5. The various post managers were requested to assist in giving a general synopsis of the symptoms of the disease and in supplying specimens for examination. From the information received it would appear that the affected dogs did show nervous symptoms and it is very likely that the disease is rabies. However, during the course of the investigation it was found that the disease in the dogs seemed to bear some sort of connection with the foxes in the district and it is thought that this might be of interest. For instance, at Sugluk during the winter of 1949–50 due to a shortage of dog food and a very heavy fox catch, the dogs there were

1. During last fall and this winter there have been a number of outbreaks of dog disease amongst the Eskimo dogs in the Port Harrison district. The largest number of cases were in the vicinity of Sugluk with only a few scattered cases in the vicinity of Port Harrison Povungnituk and Cape Smith. In view of the circumstances, on the 18-12-50 the following radio telegram was sent to the Deputy Commissioner of the N. W.T. with a copy to the O.C. “G” Division: 2. Quote: Reference file dog disease northern Quebec stop Disease has appeared in this district with outbreaks at Sugluk Capesmith and Povungnituk stop Most cases reported from Sugluk but not considered of epidemic proportions yet stop All posts taking whatever precautions possible to confine disease Unquote.

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fed on fox carcasses for a good part of the winter and it as at Sugluk that the disease first appeared early in the fall of 1950. In the vicinity of Povungnituk, during the present winter there have been several cases of apparently “crazy” foxes attacking dogs and dog teams and as far as can be ascertained, in every case a Povungnituk where dog teams have developed the disease, it is know that they have eaten part of the carcass of one of these “crazy” foxes. 6. In view of the above, five specimens are being forward direct to the Dominion Animal Pathologist, Hull, P.Q. Two of the specimens, labelled no. 1. and 2. are from Sugluk, P.Q. and are heads of dogs which were killed after contracting the disease. Specimen labelled no. 3. is the head of a fox that entered the porch of an igloo in the Povungnituk district and started fighting with the dogs in the porch. The fox was killed with a stick and the dogs ate the carcass. Five of the dogs from this group died of the disease and specimen labelled no. 4. Is the head of one of the young dogs in this group. Specimen labelled no. 5. is the head of a dog that ate part of the carcass of a “crazy” fox that attacked the dog team in which it was working. A copy of this report is being enclosed with the specimens for the information of the Dominion Pathologist. 7. The following is a synopsis of the symptoms of the disease in the dogs at Sugluk, P.Q as supplies by the H.B.Co. postmanager at that point. 8. The most common form of the disease seems to be that the dog loses its appetite, and then shortly afterwards loses control of his senses; and then appears about fifty percent crazy. There is no discharge from the mouth or nose, eyes appear fairly bright but have a tendency to roll now and then. Dog tries to bite other dogs but does

not have the power to bite properly. Does not appear to be dangerous to humans at this stage. 9. In the second form of the disease there is first loss of appetite, dog would appear normal even then but within a few hours would be difficult to handle as it would be biting at other dogs and trying to bite humans too. Even in this case there is no discharge at the mouth or nose. 10. In the third form of the disease there was the usual loss of appetite, dull look in the eyes, dogs would run from other dogs and humans and would run around in an erratic fashion. Finally they would have a prolonged bout of shivering and lose all control of their limbs and go around as if intoxicated. They do not appear to be dangerous in this form. 11. The postmanager at Sugluk also reported that as of the 20-1-51, roughly 34% of the fall dog population at Sugluk had either died or been shot due to the disease. The symptoms as noted above seem to apply generally throughout this district but the natives in the vicinity of Port Harrison and Povungnituk also report a foamy watery discharge from the mouth. 12. The writer has incurred expenses in connection with these specimens to the extent of $6.00. $3.00 was paid to E-9-921, Philiposie for bring them from Povungnituk to Post Harrison and $3.00 is being authorized for E-9-1452, T...IE for obtaining the head of the “crazy” fox. These two amounts will be charged to the Department of Resources and Development. Concluded here. Cpl. (G. A. Mansell) 13150 i/c Port Harrison Detachment.

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PART 4

The Development of Vaccines and Delivery Systems

Overview Part 4 describes the history behind vaccine development for human (Chapter 15a) and animal use (Chapter 15b) and the use of those vaccines in the treatment and prevention of rabies. Canada was a pioneer in both areas, producing vaccines that became world standards. As Chapter 15b notes, Canada hesitated to use mass vaccination of domestic animals until the massive outbreaks in wildlife in the 1950s forced changes in Canada’s control policy and spurred further research. Vaccine and bait development was carefully regulated (Chapter 16) and it culminated in the development of oral rabies vaccines (Chapter 17) via the early work of Campbell and Previc (Chapter 17a); Lawson’s research in conjunction with the Ontario Ministry of Natural Resources and Forestry (Chapters 17b) in creating a bait that is attractive to vector species, suitable for aerial delivery, and containing enough vaccine to immunize an animal; and an innovative Canadian company, Artemis Technologies (Chapter 17c), which developed the machinery both to mass produce various baits and to produce the unique Canadian ONRAB vaccine (using an adenovirus vector AdRG1.3), which has proven successful for immunizing raccoons and skunks, as well as foxes. Vaccines and baits underwent a rigorous testing regime (Chapter 18). The final part of the story was the development of an airborne delivery system, including the flight planning and management software and organization structure required for a complete baiting system (Chapter 19). The work by various Canadians outlined in these chapters pioneered aerial baiting in North America and has produced, over 50 years, vaccines superior to all other vaccines in current use.

15a Rabies Vaccines in Canada HUMAN VACCINES

Paul Varughese Senior Science Advisor, Public Health Agency of Canada (Retired), Ottawa, Ontario, Canada

Introduction Immunoprophylaxis plays an important role in the human rabies prevention strategy in Canada. Although human rabies is rare (see Chapter 3b) in Canada, post-exposure treatments for rabies are common; thousands of Canadians receive rabies immunization every year (see Chapter 34). An estimated 34,000 doses of vaccines are used in Canada each year for both pre- and post-exposure prophylaxis, this number varying from year to year. Post-exposure prophylaxis (PEP) in Canada began over one hundred years ago, and undoubtedly immunoprophylaxis has saved many lives from this invariably fatal disease. Pre-exposure immunization in Canada was introduced in 1965 and since then it has been recommended for people at high risk of exposure to rabid animals or rabies virus. Potential risk of human exposure to rabies continues, as rabies is endemic in Canadian wildlife, especially in bats, skunks, foxes, and raccoons. Rabies biologics (vaccines and immune globulins or antiserum) for PEP are distributed through the provincial, ­territorial, and local public health systems, and is provided free. This chapter provides a brief account on the development of various types of human rabies biologics, the Canadian experience, its impact on human rabies, and the evolution of recommendations and immunization practices.

Rabies Immunoprophylactic Agents: Effectiveness More than 130 years ago, Louis Pasteur and his colleagues developed the first rabies vaccine, Pasteur vaccine (PV), crude by current standards, for PEP, which was based on

attenuated virus in dried nerve tissue. Until 1965 only nerve-tissue-based vaccines (NTV), which were less immunogenic and more reactogenic, were available in Canada, and NTVs were not ideal for pre-exposure immunization. Between 1965 and 1980 Canadians had access to safer vaccines, such as duck embryo vaccine (DEV) and hamster kidney cell culture vaccine (HKV). Since 1980 more immunogenic and even safer human diploid cell vaccines (HDCV) and purified chick embryo cell vaccine (PCECV) have become available. Each vaccine product will be discussed in detail in this chapter. There are two types of immunoprophylactic agents for human rabies prevention: (1) vaccines for active immunization, which contain inactivated virus that induces an immune response beginning in 7 to 10 days and persisting for several years; and (2) rabies-specific immune globulins (RIG) or antiserum for passive immunization, which gives rapid protection that persists for only a short time (half-life about 21 days) (National Advisory Committee on Immunization [NACI], 1993). Unlike vaccines, passive immunization is administered only once, at the beginning of immunoprophylaxis to previously unvaccinated persons, to provide immediate rabies virus neutralizing antibody until the patient responds to effective vaccines (HDCV or PCECV) by actively producing antibodies. The effectiveness of rabies vaccines is measured by their ability to protect the person exposed to rabies and to induce antibodies to rabies virus. Efficacy and effectiveness data for the biologicals come from both human and animal studies (US Advisory Committee on Immunization Practices [US ACIP], 1984). Because controlled human trials cannot be performed for rabies vaccines, studies describing extensive

The Development of Vaccines and Delivery Systems

field experience and immunogenicity studies from around the world are reviewed by expert advisory bodies, such as Canada’s National Advisory Committee on Immunization (NACI), US Advisory Committee on Immunization (US ACIP), and World Health Organization (WHO), to develop their own recommendations. It is well established that PEP that combines prompt wound treatment, local infiltration of rabies immunoglobulin (RIG), and vaccination is uniformly effective when appropriately administered. Currently used vaccines, HDCV and PCECV, are very effective and safe, and both provide adequate immunity to rabies when administered as pre-exposure immunization, boosters, or PEP.

available cell cultured vaccines (HDCV or PCECV) are safer and more immunogenic. The most recent Canadian recommendation for pre-exposure immunization is three 1.0 millilitre intramuscular (IM) or 0.1 millilitre intradermal (ID) doses of rabies vaccine given on days 0 and 7 and any time between days 21 to 28 (NACI, 2012). Each millilitre of HDCV or PCECV should contain at least 2.5 international units (IU) of rabies antigen, which is the WHO standard. A 10-year follow-up study of individuals who received three doses of HDCV followed by a booster dose at one year has shown the maintenance of sero-conversion up to five years is 96.2% (NACI, 2012). Both HDCV and PCECV vaccines are comparable in terms of antibody induction, and the level and persistence of antibody response (NACI, 2006). When these vaccines are used, post-vaccination serological assessment is not needed for healthy people unless vaccinated by ID route. Although IM (intramuscular) is the gold standard, the ID (intradermal) route of administration is an economical and widely accepted alternative to IM vaccination, and uses only one-tenth of the IM dose or 0.1 millilitre of vaccine for rabies pre-exposure immunization (NACI, 2006). Following a short supply of HDCV in 1982, both NACI in Canada and the US ACIP recommended a 0.1 millilitre ID regimen of HDCV for pre-exposure immunization (NACI, 1982). Since improper ID administration can result in a suboptimal dose delivery of the vaccine, ID vaccines should only be given by well-trained staff. Moreover, post-vaccination antibody assessment is recommended to ensure that an acceptable sero-protection level has been achieved. A sero-conversion rate of 95.1% was demonstrated in travellers who received three ID injections of HDCV or PCECV with a booster after 12 months (NACI, 2012). Pre-exposure immunization is an elective procedure and is generally given in physician’s offices or travel health clinics, and in some jurisdictions or institutions that are publicly funded. The number of Canadians receiving pre-exposure vaccinations annually is unknown, but about one-third of the annual doses of rabies vaccine used in Canada in recent years is for pre- exposure immunizations.

Human Rabies Immunization in Canada Rabies Pre-exposure Immunization Pre-exposure rabies immunization is recommended to high-risk individuals, such as certain laboratory workers, veterinarians, and animal control and wildlife workers, for several reasons. Although pre-exposure vaccination does not eliminate the need for post-exposure treatment, it simplifies the post-exposure management of cases by eliminating the need for RIG and decreasing the number of doses of rabies vaccine. An important use of rabies p ­ re-exposure immunization is to prime the immune response to enable a rapid anamnestic response to post-exposure vaccinations. It provides partial immunity to individuals whose post-exposure treatment is delayed, and it might provide some protection to those at risk for unrecognized or ­in-apparent exposures (US ACIP, 2008; NACI, 2012). Periodic booster doses are recommended for people who are at continual risk of rabies virus exposure. Before 1965 only NTVs were available, and these were not ideal for pre-exposure immunization. Following the introduction of non-NTVs, such as DEV in 1965 and HKV in 1968, these were recommended for pre-exposure rabies immunizations to high-risk groups. Since 1980, following the licensure of HDCV, Canadian travellers to certain high-risk endemic areas, where adequate and safe post-exposure management may not be available or is lacking, are also offered pre-exposure rabies vaccine. The number of recommended doses varies depending on the type and or the immunogenicity of vaccine products available. For example, DEV and HKV, which were less immunogenic, required four doses, and post-vaccination serological assessment and additional doses were recommended, if necessary, to ensure continued protection. Currently,

Rabies Post-Exposure Management: Immunoprophylaxis in Canada Administration of rabies PEP is considered as a medical urgency, and the decision to treat for rabies exposure must be made rapidly and judiciously. Delays in starting vaccine treatment reduces its effectiveness, and once established, the disease is almost always fatal. A risk assessment is made

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by the health care provider to determine if the individual has been exposed to rabid or potentially rabid animals. Rabies PEP is considered if rabies is present in the local area animal population, and the risk assessment includes consultation with the local public health and veterinary officials. Other considerations for risk assessment include the species of animal involved, type of exposure (bite, nonbite, or direct contact with a bat), circumstances (provoked, unprovoked), vaccination status and behaviour of a domestic animal, age of the exposed person, and location and severity of the bite (NACI, 2012). The health care provider needs to weigh the potential adverse consequences associated with administering PEP along with their severity and likelihood versus the actual risk of the person acquiring rabies in each situation (US ACIP, 2008). Another important consideration is that rabies biologics (vaccines and RIG) are traditionally expensive and valuably scarce resources that are periodically in short supply in Canada. Post-exposure management of cases has two components: immediate local treatment of the wound and prompt immunoprophylaxis. Local treatment is aimed at immediate removal of rabies virus from the exposed site (usually a bite wound or scratch) by chemical and physical means through washing and flushing with soap and water. PEP for people who have never been vaccinated against rabies include concurrent administration of both passive antibody (i.e. RIG) and an effective rabies vaccine, such as HDCV or PCECV. The passive administration of RIG (previously antiserum, equine) is intended to provide an immediate supply of virus neutralizing antibodies to bridge the gap until the production of vaccine-induced immunity. NACI’s recent rabies post-exposure management and treatment guidelines and updates are available on the Public Health Agency of Canada (PHAC) website or in print form (NACI, 2006, 2009, 2012). The most recent recommendation for rabies PEP of previously unimmunized individuals is four IM doses of 1.0 millilitres each of HDCV or PCECV, as soon as possible after exposure at day 0, concurrently with an appropriate dose of RIG, and at 3, 7, and 14 days; for those previously immunized, only two doses at day 0 (without RIG), and three days later is recommended (NACI, 2012). Over the years, there have been some changes in the number of doses of vaccine for PEP. Canada has been using a five-dose HDCV schedule for PEP since 1980, although WHO recommends a six-dose series initially (NACI, 1980). The change from a five- to a four-dose schedule recommended by US ACIP in 2010 (ACIP, 2010) was based on the cumulative evidence in several areas, including rabies

virus pathogenesis, experimental animal models, human immunogenicity studies, prophylaxis effectiveness in humans, documented failures of prophylaxis in humans, and vaccine safety. After US ACIP and NACI reviews, the four-dose reduced schedule was recommended by NACI (NACI, 2012). However, for those who have not previously been immunized or are immuno-compromised or are taking anti-malarial drugs, a fifth dose of vaccine is recommended on day 28. HDCV was first licensed in Canada in 1980 and has been used since, and PCECV has been used since 2005. Unlike the previous rabies vaccines (Semple type and DEV), systemic reactions are rare and are similar with both HDCV and PCECV. There have been no post-exposure treatment failures in Canada or in the United States when the recommended procedures are followed.

Epidemiology of Rabies Post-Exposure Prophylaxis Animal rabies surveillance data from the Canadian Food Inspection Agency indicate that control of rabies in pet animals (dogs and cats) has been achieved for some time through successful preventive programs (beginning in the 1950s; see Chapter 15b). Because of the wide distribution of rabid animals across Canada and spillover to domestic animals, human exposures are frequent, resulting in a large number of people receiving post-exposure treatment (Varughese, 1988; see Chapters 33b and 34). Contact by children and adults with unsuspectedly rabid stray young pets or other animals at times has resulted in multiple exposures and a large number of people treated with PEP, creating excessive demand for the vaccine and RIG in a short time. There are numerous cases of clustered human exposures to rabies. For example, in November 1980, 125 Ontario children and adults from Simcoe County received PEP following exposure to a rabid kitten: 110 received a course of Semple vaccine; 15 received a combined Semple vaccine and human RIG. All received an additional three dose course of HKV boosters (Carlson, 1981). This episode occurred just before HDCV became available to the Ontario Ministry of Health. In another incident a seemingly harmless act of taking two puppies to a seniors’ home to comfort residents in Ontario in fall 1986 turned into a nightmare when a puppy died of rabies. All the seniors in the facility, the families who owned the puppies, and anyone known to have contacted the puppies received rabies vaccination (Radkewycz, 1986). Multiple

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exposures among health care staff also can occur when an unsuspected human rabies case is attended. Human exposure to rabid or potentially rabid animals are not routinely monitored nationally. A time-limited epidemiologic study of PEP conducted in collaboration with the provincial and territorial ministries of health in the 1980s, following the availability of HDCV, indicated that the trend in human PEP and laboratory-confirmed animal rabies in Canada followed a similar pattern (Varughese, 1988); an increasing number of Canadians in that period were receiving rabies PEP; and it was attributed in part to safer vaccines. However, in 1986, 4669 Canadians received post-exposure treatments, the highest number ever recorded nationally (Varughese, 1988). This is a rate of 18 treated people per 100,000 persons or 1 in 5500 Canadians. At least 17 species of animals were identified, and many were not laboratory confirmed for rabies. By 1988 only 2281 PEPs were reported, a rate of 11 per 100,000 p ­ ersons, and at least 30 species of animals were implicated. Of these, only 50% had exposure to confirmed rabid animals (Varughese & Carter, 1990). It is well known that over-treatment for rabies exposure occurs frequently. Since real rabies risk is difficult to assess in some cases, and since prompt PEP prevents this invariably fatal disease, some people needlessly receive PEP as a precautionary treatment. The decision of a health care provider not to provide immunoprophylaxis has been often difficult. A US study suggested that for medico-legal reasons or to reduce patient anxiety, many physicians administer rabies PEP when exposure clearly carried no risk. Half of the PEP patients who receive PEP after exposure had not been bitten and the risk of rabies is non-existent in these patients (Helmic, 1983).

care providers for the use of licensed immunizing agents of public health significance. This is based on the up-to-date and best available scientific and clinical knowledge (see Chapter 5). In fact, rabies and rabies biologics (vaccines and antiserum or RIG) were often a topics on the NACI agenda beginning in 1964. NACI traditionally focuses on routine vaccine-preventable diseases affecting children and adults, such as polio, measles, diphtheria, influenza. However, the Committee has been providing issue-specific recommendations on aspects of human rabies prevention, including when a new vaccine is licensed, when there is a change in the epidemiology of the disease, when there is shortage of rabies biologics, and when limited stock of vaccines needs to be prioritized. Because the epidemiology and pathogenesis of rabies are complex, national recommendations cannot be specific for every possible situation in the field. Health care providers are reminded to seek assistance from local or provincial/territorial public health officials for assessing potential rabies exposures or determining the need for post-exposure management. NACI recommendations are disseminated through various media: the federal health department’s publications – such as the former Canada Diseases Weekly Report (CDWR), Canada Communicable Diseases Report (CCDR), or Canadian Immunization Guide – and various Health Canada and PHAC websites. The Committee to Advise on Tropical Medicine and Travel (CATMAT), another national advisory committee, also provides guidelines and recommendations pertinent to international travellers for certain endemic areas (Committee to Advise on Tropical Medicine and Travel [CATMAT], 2002).

Human Rabies Vaccine Development and Vaccination

National Recommendations for Human Rabies Prophylaxis

First Rabies Vaccine

Role of National Advisory Committee on Immunization and Committee to Advise on Tropical Medicine and Travel

Human rabies immunoprophylaxis began in 1885 in Paris with the administration of Pasteur’s rabies vaccine (PV), the first rabies vaccine ever administered to humans. The vaccine was crude by current standards and the treatment was empirical. The original PV was first prepared in Canada in 1913 at the Ontario Provincial Laboratory by Dr John G. FitzGerald and his assistant, William Fenton (Rutty, 2008). FitzGerald was associate professor of hygiene at the University of Toronto. Before a significant rabies outbreak in southern Ontario in 1910, victims of rabid animal bites had to travel to New York City to receive the PV as it could

The number of doses and the route of administration of vaccine product are generally based on the manufacturer’s instructions or the package insert. However, since the formation of the NACI in the early 1960s as an expert advisory committee of the federal health department, the committee has been providing additional recommendations or developing clinical or public health guidelines for health

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not be exported. However, an arrangement was made possible during the 1910 outbreak after the Provincial Board of Health secured $1000 to have the PV specially delivered from the New York City Health Department to enable rabies treatment clinics at Toronto General Hospital and the Hospital for Sick Children. FitzGerald learned how to prepare the PV at the Pasteur Institute in Brussels while studying there in the summer of 1910, and by 1913 he was able to start preparing it at the Provincial Laboratory, although he was hopeful that a Pasteur Institute could be established at the University of Toronto. By May 1914 FitzGerald had established something similar, but quite distinctive, at the University of Toronto, originally known as the Antitoxin Laboratory in the Department of Hygiene and in 1917 christened the Connaught Antitoxin Laboratories. While the production of diphtheria, and later tetanus, antitoxin were the primary focus of the Antitoxin Laboratory during its initial years, the PV and smallpox vaccine were also critical products prepared for national distribution (Rutty, 2008). Until the mid-1960s, human rabies vaccines used were exclusively for PEP, and only NTVs, such as Semple type or its variations, were available. Since then, safer vaccines, such as DEV, hamster kidney cells (HKV), human diploid cell culture vaccine (HDCV), and purified chick embryo cell culture vaccine (PCECV) have become available. As the number of different rabies vaccine products available in Canada increased in the 1960s and 1970s, there was confusion among Canadian clinical practitioners and public health officials regarding the choice of rabies vaccine products. HDCV and PCECV are the two vaccines used currently in Canada, and they are used for both pre- and post-exposure treatment.

his rabies vaccine, a suspension of rabbit spinal cord, on a human being before he had finished animal (dog) studies (Turner, 1977). The first patient was Joseph Meister, a nine-year-old boy, who had multiple bite wounds on hands, legs, and thighs, having been bitten by a rabid dog some 60 hours previously. His wounds had been cauterized with carbolic acid (phenol) by his local doctor before his parents took him to Pasteur’s laboratory in Paris as a last resort, and he received the first rabies vaccination in humans on 6 July 1885. A series of 13 subcutaneous injections over 10 days was administered, and the boy survived. In the following year (1886), some 2500 people were treated with PV (Kaplan et al., 1986). The Pasteur Institute of Paris was founded in 1888, and within a decade there were Pasteur Institutes in many parts of the world providing rabies vaccines. In the preparation of vaccine in various locations, Pasteur’s procedure was followed, sometimes with minor modifications. Treatment failures were encountered by Pasteur himself and by others who followed the procedure (Bahmanyar, 1979). The original rabies vaccines were suspensions of infected rabbit brain or spinal cord that had been dried over potassium hydroxide for approximately two weeks to make the virus non-infectious. Some of the difficulties encountered initially included inadequate inactivation of the rabies virus and the presence of large amount of myelin, resulting in severe adverse reactions in some patients. Major modifications in the NTV preparations were introduced by many researchers in the early part of the twentieth century, including Fermi (1908) and Semple (1911). Phenol was generally used for partial or full inactivation of rabies virus. SEMPLE TYPE VACCINE

Semple rabies vaccine was named for its developer, Dr  David Semple, a British army officer in the Indian Medical Service. In 1911 Semple, working in India, developed a phenol-inactivated rabies vaccine derived from rabbit brain tissue (Semple, 1911). Induction of virus-neutralizing antibodies (VNAs) and lack of failures after prompt post exposure vaccination had been used as the markers of protection. Connaught Laboratories at the University of Toronto, began producing the Semple-type rabies vaccine for Canadians, incorporating minor modifications in the production process periodically (Defries, 1968; see Chapter 15b). For the inactivation of rabies virus, both phenol and ultraviolet irradiation were used. However, the production details or product monographs for the earlier preparations from 1914 to 1952, or the year of

Active Immunizing Agents-Vaccines and Evolution Vaccine Derived from Nerve Tissue PASTEUR VACCINE

Louis Pasteur’s group in France established in 1881 that the central nervous system is the principal site of rabies virus replication. Subsequently, Emile Roux and other scientists observed that the virulence of rabies virus in infected rabbit spinal cords decreased rapidly by drying in air and was extinguished completely in 15 days. Based on this observation, in 1885, Louis Pasteur developed an NTV using an attenuated strain (fixed) of rabies virus, weakened by desiccation. In July 1885 Pasteur was persuaded to try

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formal licensing in Canada, are not readily available. The Semple human rabies vaccine was licensed in 1914 by the United States. In the early 1950s a modified Semple vaccine, prepared by Connaught Medical Research Laboratories, was available for human use in Canada (Wilson, 1952). The vaccine was a 4% suspension of fixed rabies virus prepared from the brains of rabbits and inactivated by ultraviolet irradiation, with merthiolate (thimerosal) added as a preservative. The vaccine was administered subcutaneously in the abdominal area. Two schedules were recommended, depending on the severity of the wound: for non-severe bite exposure, one dose of two millilitres daily for 14 days; and for severe bite exposures, two doses of two millilitres each twice daily for the first seven days, followed by a single two millilitre dose daily for the remaining seven days, for a total of 21 doses. By 1957 a minor modification was made in the preparation by adding 1% phenol for the inactivation of the virus (Wilson, 1957).

All Semple-type vaccine products were used only for PEP, and they were widely used in Canada until 1980, with a limited number of doses available until 1984 in some regions, depending on the local availability of the newer vaccines derived from non-nerve tissue.

Duck Embryo Rabies Vaccine DEV, developed in the United States, was the first human rabies vaccine used in Canada for both pre-exposure immunizations and PEP. DEV was introduced in the United States in 1956 (“Rabies Vaccination in Man,” 1974) and licensed and became commercially available in the United States in 1957 (Kaplan et al., 1986; US ACIP, 1976). DEV was prepared from embryonated duck eggs, infected with fixed rabies virus and inactivated with b ­ etapropilolactone. DEV had not been evaluated for efficacy in clinical trials, but accumulated patient evidence showed that the vaccine was effective. DEV was supplied in Canada by Eli Lilly as 1.0 millilitre single-dose vials of lyophilized vaccine with a diluent. Following DEV’s licensure in Canada in 1965, it was widely used until 1980, and in limited doses to 1984, when HDCV was unavailable (Varughese, 1983). Because of the lower incidence of neurologic reactions, DEV became the preferred vaccine of choice for post-exposure treatments in some provinces in Canada, while others continued to use the Semple-type vaccine.

REPORTED ADVERSE REACTIONS

Reported adverse reactions to the earlier Semple-type vaccines included local areas of redness, tenderness and soreness, and these were most marked from the fifth to the eighth day of injections with fewer reactions occurring before and after this period. The vaccination of approximately 9000 persons given a 14-dose course of Semple vaccination was studied in Ontario over 10 years (1957–1967). The estimated frequency of neuro-paralytic sequelae was 1 per 1400 vaccinated, with all persons recovering (McWilliam & Penistan, 1967). Because of the unique nature of rabies, the efficacy of rabies vaccines in humans has not been evaluated by controlled studies. The reported efficacy of the Sempletype vaccine to protect from rabies has varied and was estimated to be around 84% in India (Veeraraghaven & Subrahmanyan, 1958), although protection was lower after severe exposure. At least two vaccine treatment failures of Semple-type vaccine have been documented in Canada, one in 1967 involving a four-year-old, and the other, 40 years previously. Both involved children with severe bite wounds on the face inflicted by a rabid cat or a dog, and both had received the recommended doses of Sempletype vaccine therapy (Bell, 1967). Vaccine treatment alone (without RIG) is not adequate for total prevention of rabies, especially after severe exposure, and documentation is lacking as to whether the 1967 case, in fact, received combined vaccine and RIG therapy.

IMMUNOGENICITY

Antibody response following DEV was reported to be comparable to that of Semple-type vaccine, with antibodies appearing 7 to 10 days after the first dose of a 14-day course (McWilliam & Penistan, 1967); however, the immunogenicity of DEV was lower than with the Semple vaccine in experimental animals but both had approved potency test requirements, and treatment failures elsewhere were similar in frequency (NACI, 1979b). Studies have shown that more than 80% of persons given a course of DEV (or HKV) develop detectable serum antibody and are presumed to be protected against rabies. Post-vaccination serological assessment is recommended, usually one month after the last dose, and those who failed to develop antibody were given additional doses. DEV was not recommended for persons allergic to eggs, particularly duck eggs. DOSES

Recommended treatment with DEV for pre-exposure immunization was four doses, given at days 0, 7, and 14,

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and 5 to 6 months after the third dose (NACI, 1980). For post-exposure treatment, 21 daily doses were recommended, with additional doses given, if needed, on days 31 and 41. Either one dose of anti-rabies serum (ARS) equine or one dose of human RIG (since it became available) was given on day 1. Serum antibody titres were checked on about day 60. If no adequate antibody was detected, three doses of HDCV at seven-day intervals were recommended after HDCV became available. By 1977 DEV was the most frequently used human rabies vaccine in North America: approximately 80% to 90% of North Americans receiving rabies vaccines, were treated with DEV while the remaining 10% to 20% were treated with the Semple vaccine (Ferguson & Callcott-Stevens, 1977). By 1980, following the introduction of HDCV, DEV was recommended only for PEP, and then only if HDCV was unavailable (NACI, 1980). Since 1983 DEV has not been manufactured but smaller quantities were available in Canada until 1984 (Varughese, 1983).

to DEV) and were presumed to be protective against rabies. This vaccine was commonly known in Canada as rabies vaccine – tissue culture origin. HKV is a purified, concentrated suspension of fixed rabies virus adapted to and prepared in monolayers of baby hamster kidney cells and inactivated with formalin. Aluminum phosphate (one milligram per one millilitre dose) was added as an adjuvant (Connaught Medical Research Laboratories, 1972, p. 51; NACI 1979b). The fixed rabies virus strain CL-60 (derived from the Street alabama Dufferin rabies virus isolate) was used for the vaccine preparation (Sureau, 1987; Rhodes, 1981). The vaccine did not contain neural tissue but had a protein content of 0.1%. DOSE FOR IMMUNIZATION

Following a review in 1972, NACI recommended four doses of HKV for pre-exposure rabies immunization for high-risk groups: three IM one-millilitre doses near the insertion of deltoid muscle, three to four weeks apart, followed by a fourth (booster) three to six months later, followed by antibody assessment three to four weeks after the last dose. If no antibodies were detected, one or two additional doses, followed by annual doses for those at continual risk, were recommended (NACI, 1979b). In 1980, the specific recommendation by NACI for HKV was four doses given at days 0, 28, and 56, and three to six months after the third dose (NACI, 1980). Adequate protective antibody levels were reported after four doses in 80% to 95% of the HKV patients (Aoki, 1979). Annual recall or a booster dose of one millilitre HKV was recommended for those at continual risk. Serological assessment one month after the last dose was recommended, and supplementary doses were recommended for those who failed to develop adequate antibodies. Antibody determination was carried out at Connaught Laboratories at a nominal cost. Since 1975 the Ontario Public Health Service, Ontario Ministry of Health, has conducted rabies antibody testing at no charge for all Canadians. An antibody titre of 1:16 or greater by rapid fluorescent focus inhibition test is considered adequate response to vaccination. A booster dose every two years or as needed is recommended for high-risk groups. Although HKV is primarily used for pre-exposure treatment, in 1972, it was recommended (Wilson, 1972) for post-exposure booster doses: two one-millilitre doses HKV at day 10, and 20 or more days after the last dose following a 14-dose daily course of Semple vaccine; if ARS or human RIG is used with Semple vaccine, then three booster doses at 10, 20, and 90 days after the last daily dose of Semple vaccine (NACI, 1979b).

ADVERSE EVENTS

Most persons receiving DEV developed local reactions during therapy and up to one-third developed mild systemic reactions as well. Local reactions included pain, erythema, induration, and itching at the injection site for most patients. Severe reactions following DEV requiring cessation of treatment were rare but reported in Canada (Nelson, 1975). Systemic symptoms, including fever, malaise, and myalgia, were reported in one-third (33%) of recipients, usually after the fifth to eighth doses. Anaphylaxis occurred in less than 1% of patients, usually after the first dose, particularly in persons previously sensitized with vaccines containing avian tissue. Neuro-paralytic reactions were rare and reported at a rate of approximately 1 in 24,000 recipients (NACI, 1980). In fact, Semple vaccine caused a 20-fold greater frequency of neuro-paralytic reactions (Aoki, 1979).

Hamster Kidney Cell Culture Vaccine In 1965, scientists from Connaught Medical Research Laboratories (CMRL) of the University of Toronto, informed NACI on the potential development of a tissue culture rabies vaccine for humans using primary hamster kidney cells (HKV) and the company’s planned p ­re-exposure human clinical trials. Following the clinical trials in Canada, HKV was licensed in 1968 (Fenje, 1974; Sureau, 1987). Studies had shown that more than 80% of persons given a course of HKV develop detectable serum antibody (similar

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made the recommendation for its use. Initially, under SAP these doses were recommended for persons with serious hypersensitivity to either DEV or Semple vaccine (NACI, 1979a). For pre-exposure vaccination three o ­ ne-millilitre doses were given at days 0, 7, and 21, intramuscularly. Booster doses are recommended for persons with continuing risk of exposure every two years, or they should have their serum tested for rabies antibody every two years. Persons working with live rabies virus in laboratories or in vaccine production facilities at risk of in-apparent exposure should have the antibody titre determined every six months, and booster doses of vaccine given as needed. The recommended post-exposure regimen for HDCV initially is five doses, at days 0, 3, 7, 14, and 28. Although the WHO recommended a routine sixth dose on day 90, in 1980 NACI recommended a serological assessment two to three weeks after the fifth dose, before the sixth dose. However, based on the accumulated evidence by 1982, NACI recommended that when HDCV was used, after pre-exposure immunization or PEP, no serological testing was required (NACI, 1982).

ADVERSE REACTIONS

Local and other systemic reactions following HKV use were uncommon. Of the approximately 35,000 doses of HKV administered in Canada between 1971 and 1978, there were only seven (one per 5000 doses) non-fatal anaphylactoid reactions reported (Aoki, 1979). Neuro-paralytic reactions have not been reported because of the absence of myelin, which is found in the Semple vaccine. HKV is contraindicated in persons who are sensitive to bovine serum.

Human Diploid Cell Culture Vaccine Manufactured by Institut Merieux, Lyon, France, and distributed in Canada by Rhone-Poulenc Pharma, Montreal, Quebec, HDCV and its introduction represented a major breakthrough in the prevention of human rabies. Adaptation of rabies virus to human diploid cell culture in 1963 led to the development of a highly immunogenic and much safer vaccine than had been previously available (Bernard et al., 1982). Further studies have confirmed that rabies virus grown in human diploid cell strains containing concentrated and purified rabies virus elicited a higher immune response than did the previous vaccines. HDCV was first licensed in Europe for pre-exposure immunization and PEP of humans in 1976 (Plotkin et  al., 2008). Subsequently, HDCV was licensed in Canada and the United States simultaneously in June 1980 (NACI, 1980; Plotkin et al., 2008). The vaccine was prepared from rabies virus grown in W-38 or MRC-5 human diploid cell culture, concentrated by ultrafiltration, and then inactivated with beta-propiolactone. HDCV contains less foreign protein than DEV and more antigen per dose; and a booster dose induces a quick antibody response. Not only are the number of doses for PEP reduced to 5 from 14 to 23, but HDCV is also superior in creating immunogenicity, producing early antibodies, creating substantially fewer adverse reactions, and containing less foreign protein content. The average peak titre of rabies antibody after vaccination with HDCV was more than 10 times that after DEV (NACI, 1980). In Canada HDCV was the vaccine of choice until the licensure of PCECV in 2005. However, between 1980 and 1984, both Semple and DEV had to be used when HDCV was unavailable. For PEP Canada began using HDCV in 1979, before its formal licensing by Health Canada, because of its superior immunogenicity and safety profiles compared to DEV and Semple-type vaccines. A limited quantity of HDCV was available for use in this country through Health Canada’s Special Access Program (SAP), and NACI

Purified Chick Embryo Cell Vaccine In 2005 PCECV, known as RabAvert and manufactured by Chiron Corporation, was approved for use in Canada. PCECV had been available in the United States since 1997 (Dreesen et al., 1989). PCECV is produced by growing the fixed-virus strain Flury low-egg passage in primary cultures of chicken fibroblasts, and the virus is then inactivated with beta-propiolactone and processed by zonal centrifugation. Sterile diluent is supplied for reconstitution into a single 1.0 millilitre. PCECV, similar to HDCV, is safe, effective, and well tolerated for pre-exposure immunization, including boosters, and PEP against rabies, and is considered interchangeable in terms of indications for use, immunogenicity, efficacy, and safety (NACI, 2005). Three IM doses of either HDCV or PCECV given over 21 to 28 days have produced protective antibodies in 100% of individuals in all age groups. Virus neutralizing antibodies develop seven days after immunization and persist for at least two years.

Passive Immunizing Agents The efficacy of the combined use of vaccine and rabies serum was established from both human and animal studies and thoroughly reviewed by the WHO Expert Committee on Rabies. The addition of rabies hyper-immune serum to

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the human vaccination regimen started in 1954. The halflife is approximately 21 days.

pathogen clearance. Similar to ARS, RIG is administered only once at day 0, IM, and preferably directly into the edges surrounding the wound. The dose is 20 IU per kilogram body weight, the volume being thoroughly infiltrated into the wound and surrounding area, and the remainder given IM at a distant site. After administration of RIG, serum neutralizing antibodies can be detected within 24 hours, reach a level of about 0.1 IU at three days, and decay with a half-life of about 21 days. Ideally, RIG should be given immediately, but, if for any reason it is delayed, it may be given up to the seventh day after exposure, by which time an active response to vaccination should begin. Currently two human RIG products are approved in Canada for passive immunization. The safety profile of RIG is excellent; adverse reactions are minimal. Occasional pain and low grade fever have been reported. No transmission of adventitious agents has been documented after administration of RIG licensed in Canada or the United States (US ACIP 2008). This is due to extensive screening of plasma donors for previous exposure to certain viruses, by testing for the presence of certain current virus infections, and by inactivating or removing certain viruses.

Anti-rabies Serum For post-exposure treatment, the first preparation of ARS used in Canada was of equine origin. ARS, is a refined concentrated serum obtained from hyper-immunized horses and was used from 1957 to 1975. A dose of ARS (40 IU/kg) is used in Canada, along with various available rabies vaccines (Semple and DEV). It became commercially available in Canada and was distributed through Lederle Laboratories, Montreal, Quebec (McWilliam & Penistan, 1967). Initially, ARS was used in severe exposures, especially wounds to the head and neck. Approximately 40% of adult recipients developed serum sickness. ARS was also used when human RIG was in short supply.

Human Rabies Immune Globulin In 1977 the WHO recommended a regimen of RIG and six doses of HDCV over 90 days, based on studies in Germany and Iran. RIG (manufactured by Cutter Laboratories) was licensed in Canada on 29 August 1975, and since then it has essentially replaced ARS. With the increased availability of RIG, and safety, its usage in Canada increased by eight-fold by 1976 (Waters, 1977). In 1982 a usage survey indicated that 20,708 millilitres of RIG was administered to approximately 2700 Canadians (Aoki & Eadie, 1983). RIG is made from the plasma of hyper-immunized human donors. It is concentrated by cold ethanol fractionation and undergoes multiple procedures for human viral

Conclusion Total prevention of human rabies, an almost always fatal human disease, continues to be a public health challenge, especially in areas where rabies is endemic in many animals. Although control of rabies in domestic and certain wild animals is now feasible, eradication of rabies in bats will continue to remain extremely difficult.

References Aoki, F. Y. (1979). Human diploid cell culture vaccine for rabies prophylaxis. Canadian Medical Association Journal, 120, 1044–1047. Retrieved from National Center for Biotechnology Information website: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1819290/ pdf/canmedaj01445-0012.pdf Aoki, F. Y., & Eadie, J. A. (1983). Human rabies immune globulin (HRIG) used in Canada in 1982. Canada Diseases Weekly Report, 9(35), 140. Retrieved from Government of Canada Publications website: http://publications.gc.ca/collections/collection_2016/ aspc-phac/H12-21-1-9-35.pdf Bahmanyar, M. (1979). Benefit versus risk factors in prophylactic vaccination against rabies. Developments in Biological Standardization, 43, 305–307. Retrieved from National Center for Biotechnology Information website: https://www.ncbi.nlm.nih.gov/pubmed/520677 Bell, J. S. (1967). Surveillance reports. Epidemiology Bulletin, 17, 7. This source can be ordered from Library and Archives Canada website: http://central.bac-lac.gc.ca/.redirect?app=fonandcol&id=1458644&lang=eng Bernard, K. W., Smith, P. W., Kader, F. J., & Moran, M. J. (1982). Neuroparalytic illness and human diploid cell rabies vaccine. Journal of American Medical Association, 248(23), 3136–3138. https://doi.org/10.1001/jama.248.23.3136

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Vaccine, 7(5), 397–400. https://doi.org/ 10.1016/0264-410X(89)90152-7 Fenje, P. (1974). Rabies vaccine for human use. In R. H. Regamey, W. Hennessen, & F. T. Perkins (Eds.). International Symposium on Rabies, II. Symposia Series in Immunobiological Standardization, 21, 148–156. Ferguson, K. G., & Callcott-Stevens, V. A. (1977). Prophylaxis for exposure to rabies in humans. Canadian Medical Association Journal, 117, 12–13. Fermi, C. (1908). Uber die Immunisierung gegen. Wutkrankheitet. Zeitschrift fur Hygiene und Infectionskrankheiten, 58(1), 233–276. https://doi.org/10.1007/BF02142869 Helmic, C. G. (1983). The epidemiology of human rabies post exposure prophylaxis, 1980–1981. Journal of the American Medical ­Association, 250(15), 1990–1996. https://doi.org/10.1001/jama.1983.03340150032022 Kaplan, C., Turner, G. S., & Warrell, D. A. (1986). Rabies vaccine and immunity to rabies. In C. Kaplan, G. S. Turner, & D. A. Warrell (Eds.), Rabies – The facts (Rev ed., pp. 8–20). Oxford, England: Oxford Press. McWilliam, R. S., & Penistan, J. L. (1967). Immunization against rabies. Canadian Medical Association Journal, 96, 153–157. National Advisory Committee on Immunization. (1979a). Statement on human diploid cell strain vaccines. Canadian Diseases Weekly Report, 5, 37. Retrieved from Government of Canada Publications website: http://publications.gc.ca/collections/collection_2016/ aspc-phac/H12-21-1-5-10.pdf National Advisory Committee on Immunization. (1979b). A guide to immunization for Canadians, 1979. Ottawa, ON: Health Canada. Retrieved from Government of Canada Publications website: http://publications.gc.ca/collections/collection_2014/aspc-phac/HP403-1-2014-eng.pdf National Advisory Committee on Immunization. (1980). Statement on rabies prophylaxis. Canada Diseases Weekly Report, 6, 125–132. 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Retrieved from Government of Canada Publications website: http://publications.gc.ca/collections/Collection/HP40-32006E.pdf National Advisory Committee on Immunization. (2009). Recommendations regarding the management of bat exposures to prevent human rabies. Canada Communicable Disease Report, 35(7). Retrieved from Public Health of Canada website: http://www.phac-aspc. gc.ca/publicat/ccdr-rmtc/09vol35/acs-dcc-7/index-eng.php National Advisory Committee on Immunization. (2012). Part 4, Active vaccines: Rabies vaccine. In Canadian immunization guide. ­Retrieved from Public Health of Canada website: http://www.phac-aspc.gc.ca/publicat/cig-gci/p04-rabi-rage-eng.php Nelson, R. F. (1975). Meningoencephalitis secondary to duck embryo vaccine. Canada Diseases Weekly Report, 1, 37–38. Retrieved from Government of Canada website: http://publications.gc.ca/collections/collection_2016/aspc-phac/H12-21-1-1-10.pdf Plotkin, S., Koprowski, H., & Rupprecht, C. (2008). Rabies vaccines. In S. Plotkin, W. A. Orenstein, & P. A. Offit (Eds.), Vaccines (5th ed., pp. 686–714). Philadelphia, PA: Saunders/Elsevier. Rabies vaccination in man. (1974). British Medical Association Journal, 5897(January), 45–46. https://doi.org/10.1136/bmj.1.5897.45 Radkewycz, A. (1986, 8 September). Two pups died of rabies, Brampton residents are warned. The Globe and Mail, p. 13. Rhodes, A. J. (1981). Strains of rabies virus available for preparation of sylvatic rabies vaccines with special reference to vaccines ­prepared in cell culture. Canadian Veterinary Journal, 22, 262–266.

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Human Vaccines Rutty, C. J. (2008). Personality, politics and public health: The origins of Connaught Medical Research Laboratories, 1888–1917. In E. A. Heaman, A. Li, & S. McKellar. Essays in honour of Michael Bliss: Figuring the social (pp. 273–303). Toronto, ON: University of Toronto Press. Semple, D. (1911). The preparation of a safe and efficient anti-rabic vaccine: Scientific memoirs by officers of the Medical and Sanitary ­Departments of Government of India (No. 44). Calcutta, India: Superintendent Government Printing. Sureau, P. (1987). Rabies vaccine production in animal cell cultures. vertebrate cell culture. Advances in Bioclinical Engineering ­Biotechnology, 34: 111–128. Turner, G. S. (1977). Rabies vaccine and immunity to rabies. In C. Kaplan (Ed.), Rabies – The facts (pp. 104–113). Oxford, England: Oxford Press. US Advisory Committee on Immunization. (1976).Rabies recommendations of the Public Health Service. Morbidity and Mortality Weekly Report, 25, 403–406. US Advisory Committee on Immunization. (1984). Rabies prevention – United States, 1984. Morbidity and Mortality Weekly ­Report, 33, 393–403. Retrieved from Centers for Disease Control and Prevention website https://www.cdc.gov/mmwr/preview/ mmwrhtml/00022791.htm US Advisory Committee on Immunization. (2008). Recommendations: Human rabies prevention – United States, 2008. Morbidity and Mortality Weekly Report, 57, 1–26, 28. Retrieved from Centers for Disease Control and Prevention website: https://www.cdc.gov/ mmwr/preview/mmwrhtml/rr57e507a1.htm US Advisory Committee on Immunization. (2010). Recommendations and reports: Use of a reduced (4-dose) vaccine schedule for post-exposure prophylaxis to prevent human rabies. Morbidity and Mortality Weekly Report, 59(RR02), 1–9. Retrieved from Centers for Disease Control and Prevention website: https://www.cdc.gov/mmwr/preview/mmwrhtml/mm5901a7.htm Varughese, P. (1983). Rabies in Canada. Canada Diseases Weekly Report, 9: 137–140. Retrieved from Government of Canada ­Publications website: http://publications.gc.ca/collections/collection_2016/aspc-phac/H12-21-1-9-35.pdf Varughese, P. (1988). Rabies and post-exposure rabies prophylaxis in Canada. Canada Diseases Weekly Report, 14, 89–94. Retrieved from Government of Canada Publications website: http://publications.gc.ca/collections/collection_2016/aspc-phac/H12-21-1-14-21. pdf Varughese, P., & Carter, A. (1990). Rabies and rabies post-exposure prophylaxis in Canada. Canada Diseases Weekly Report, 16, 131–136. Retrieved from Government of Canada Publications website: http://publications.gc.ca/collections/collection_2016/aspc-phac/H1221-1-16-28.pdf Veeraraghaven, N., & Subrahmanyan, T. P. (1958). The value of 5 percent Semple vaccine prepared in distilled water in human treatment: Comparative mortality among the treated and untreated. Indian Journal of Medical Research, 46, 518–524. Waters, J. R. (1977). Rabies prevention program, 1972–1976, Manitoba. Canada Diseases Weekly Report, 3, 177. Retrieved from ­Government of Canada Publications website: http://publications.gc.ca/collections/collection_2016/aspc-phac/H12-21-1-3-45.pdf Wilson, R. J. (Ed.). (1952). Biological products for human use (2nd ed.). Toronto, ON: University of Toronto, Connaught Medical ­Research Laboratories. Wilson, R. J. (Ed.). (1957). Biological products for human use (3rd ed.). Toronto, ON: University of Toronto, Connaught Medical ­Research Laboratories.

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15b Rabies Vaccines in Canada DOMESTIC ANIMAL VACCINES

Christopher J. Rutty Professional Medical and Public Health Historian, Health Heritage Research Services, Toronto, Adjunct Professor, Dalla Lana School of Public Health, University of Toronto, Ontario, Canada

Introduction The control and prevention of rabies among animals – domestic pets, livestock, and wild animals of all types – has been a complex challenge internationally for most of the past century. The option of animal rabies prevention through vaccination, which first emerged in the late 1910s, clearly added to the available strategies against the disease, but it also added to the complexities of its control. While the challenges have been scientific and technical, they have also often been practical, political, and associated with traditions of strong policing and regulation of domestic pets and stray dogs among local and national government authorities, and hesitancy among farmers, veterinarians. and agricultural authorities to undertake large-scale livestock vaccination programs. Key factors to shaping national and local strategies against animal rabies, particularly domestic animals, have stemmed from the basic facts of geography. On the island of Japan, for example, rabies incidence among dogs was very high by the first decades of the twentieth century. Serious concerns there about the threat to human health fuelled the development and use of one of the first rabies vaccines for dogs based on adapting the original human Pasteur rabies treatment. However, in Great Britain, strong government control over the importation of animals effectively kept rabies off the island, and thus there was little interest in vaccines; the same was true in Australia. In Canada, with limited control over the flow of wild animals or stray dogs across its immense southern and northern borders, the federal Department of Agriculture, Health of

Animals Division, as well as local authorities, approached rabies control by using public health quarantine and animal policing strategies and did not include vaccines until the late 1930s and early 1940s. Vaccines were initially used for cattle and then for dogs when rabies emerged as a serious threat in northern Canada. Vaccination of domestic dogs in Canada by veterinary practitioners did not begin until 1953, although immunization of dogs was implemented in the United States starting in the early 1920s, but more systematically in the late 1940s, in response to persistently high rabies incidence in many areas of the country. Policy decisions regarding the use of vaccines against animal rabies have also been driven by the changing epidemiology and incidence of the disease, particularly among wild animals and their perceived threat of spreading it to livestock, stray dogs, and domestic pets, and in turn to humans. The spread of rabies from Northern Canada from wild foxes to dogs to coyotes and then to cattle in Alberta in the early 1950s and more generally in other provinces, especially Ontario, by the mid-1950s and into the 1960s, fuelled, if not forced, federal and provincial animal and human health authorities to innovate in their response in what became an increasingly desperate effort to keep up with the disease. Within this context, the growing rabies crisis also prompted pioneering Canadian innovations in rabies vaccine development, particularly from the late 1950s through the early 1970s, based at Connaught Medical Research Laboratories (CMRL) within the University of Toronto, to prevent the disease not only in animals but also in humans. Such innovation, most notably with the development of

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Doi (1921) at the Kitasoto Institute for Infectious Diseases in Tokyo. They developed a vaccine based on earlier comparative studies between standard fixed rabies virus and calf lymph vaccine used to prevent smallpox, and found that they had a close resemblance, especially in their resistance against physico-chemical action. This was important in vaccine preparation because the fixed rabies virus must be dried, heated, or diluted to sufficiently diminish its virulence. Umeno and Doi’s (1921) rabies vaccine for dogs was prepared using the brain and spinal cord of a rabbit seven days after inoculation with the fixed virus; the tissues were collected and ground up together, to which was added phenolized glycerine water in a proportion of four times the tissue mass. This mixture was then stored at room temperature for two weeks or in the ice chamber for 30 days, and then further diluted before its injection into the animals. An initial group of 500 dogs received the vaccine by September 1918, the encouraging results leading to further tests with larger numbers of dogs in several Japanese cities. As Umeno and Doi’s 1921 paper concluded, a total of 31,307 dogs had been immunized, with only one case of vaccination loss and one case where the vaccine appeared to be ineffective. At the same time, as they noted, there were “quite a number of rabid dogs among the non-vaccinated dogs. Thus, we see the great importance of the vaccination of dogs in order to prevent the spread of rabies among dogs” (Umeno & Doi, 1921, p. 108). By the early 1920s, it was clear that rabies incidence in the United States among animals, especially domestic dogs, as well as livestock, was rising sharply in several parts of the country, driven by new outbreaks among predatory animals in the west, particularly coyotes, and prairie dogs. At the time, a range of local and state dog control measures and specific laws and regulations existed in the United States, but no national quarantine regulations were in place. Such local laws included muzzle, leash, and quarantine requirements, but limited enforcement, popular resistance from dog owners, and general public indifference and apathy undercut their effectiveness in controlling the disease. Yet as a 1923 article summarizing the US rabies situation concluded, “It is too soon to anticipate the practical value of the new project of dog vaccination by means of the Japanese method” (Sellers, 1923, p. 747; Corwin, 1924). However, according to the leading US pioneer of rabies vaccines of the period, Dr A. Eichhorn, a further statistical analysis of more than 100,000 dog vaccinations in Japan conducted in practice “would convince even the skeptics of the value of the procedure.” Beginning in August 1921,

vaccines based on Connaught’s ERA (Evelyn-RokitnickiAbelseth) strain of rabies virus, later proved critical to the evolution and deployment of oral rabies vaccines to control the disease among wildlife.

Animal Vaccine Pioneers Louis Pasteur was quite familiar with how rabies could spread from dog to dog and the danger it thus posed to ­humans; the first recipient of his rabies vaccine treatment in 1885 was a young boy who had been bitten by a rabid dog. However, it was not until the latter 1910s that research efforts began to focus on minimizing human exposure to rabies by preventing the disease through the immunization of dogs. The leading edge of this work, driven by sharply rising rabies incidence, was focused in Japan, as well as in Hungary. Hungary was the home of Dr Endre Hőgyes, a close follower of Pasteur’s. Hőgyes had isolated a fixed strain of rabies virus from a Hungarian street virus that was different from the strain originally isolated by Pasteur. By 1890 Hőgyes led in the establishment of the Hungarian Pasteur Institute, which became the focus of work on a different type of human rabies vaccine. This work was also adapted to prepare a rabies vaccine for dogs based on Hőgyes’s strain and to a simpler dilution method of production, which required fewer vaccinations. This vaccine had been used in Bulgaria on about 6000 dogs with some success, while a vaccine based on a modified Hőgyes technique, requiring only six vaccinations, was used in the United States on over 15,000 domestic animals, although with a 1.5% failure rate (“Endre Hőgyes,” n.d.). Hungary suffered from the worst rabies incidence in Europe after the First World War, the situation expediting the experimental use of a one-dose, glycerol-phenolized emulsion vaccine based on Hőgyes strain and prepared from sheep brain. This initial use involved 17,000 dogs, the favourable results prompting the obligatory immunization of sheep dogs in many parts of the country (“The Etiology and Prevention of Rabies,” 1924; Meyer, 1954). The Hungarian experience, however, was soon eclipsed by the development and scientific evaluation work undertaken in Japan on another single-dose rabies vaccine for dogs. The number of rabid dogs reported in Japan rose sharply from 570 in 1911 to 856 in 1913 to 1424 in 1914, with the alarming toll of people bitten by rabid dogs reaching 3230 in 1914. Initial research into a rabies vaccine for dogs was completed in 1916 by the team of Umeno and

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the disease to other dogs and animals in southern Ontario (Higgins, 1910). Such a situation developed in early 1910, prompting a significant rabies scare as reflected in the Toronto press (“Muzzle All Dogs,” 1910; “Rabies Scare,” 1910), Canadian medical journals, and the political response it generated, which focused on better facilitating the public provision of Pasteur rabies vaccine in Canada (“A Pasteur Institute,” 1910; “The Rabies Outbreak,” 1910; “Rabies in Canada,” 1910). At the time, the human rabies vaccine could not be imported and victims of bites from suspected rabid animals had to travel to New York City for the long series of ­anti-rabies shots. In particular, the 1910 rabies crisis highlighted the need to build a capacity for the production of biological products in Canada to ensure a domestic supply of the Pasteur rabies treatment, among other vital public health products, such as diphtheria antitoxin. Starting in the summer of 1913, the Ontario Provincial Laboratory began preparing the Pasteur rabies vaccine, and in 1914, production was transferred to Connaught Antitoxin Laboratories within the University of Toronto for distribution to provincial laboratories as needed (Rutty, 2008a). Fortunately, demand was minimal for human rabies vaccine in Canada for most of the next decade, as was discussion about dog immunization, until a significant rabies outbreak began in the Ottawa area in late 1925. By early 1926 it had spread into Quebec, particularly the Gatineau area, and then into Montreal (see Chapter 3b). The outbreak began after two rabies-infected dogs were brought into the area from New York State, and soon a large number of cattle and sheep had been bitten, along with five young boys. According to an international survey of rabies incidence published in 1928, a total of 41 rabies-positive brains from infected animals were examined in Ontario in 1926. Despite the prompt and “extremely vigorous” control measures taken by local health authorities in Montreal (muzzling orders made, thousands of stray dogs and cats destroyed on the streets, clinics established at hospitals to provide anti-rabies treatment, and federal authorities called in to assist), the situation in the city became quite alarming (“Rabies in Quebec Province,” 1926, p. 1014). Although considerable numbers of infected cattle were destroyed, and fortunately no human deaths occurred from rabies, no serious attention was given to the idea of immunizing dogs against rabies (“Rabies in Quebec Province,” 1926; Rice & Beatty, 1928). At the end of a Canadian Medical Association Journal report on the 1926 rabies outbreak, it was briefly mentioned that the new dog immunization method developed in Japan “has been tried with apparent success”

Eichhorn and B. M. Lyon worked together to confirm the Japanese experience through a carefully controlled series of laboratory experiments, as did a number of others in the United States and elsewhere. For example, in Uruguay, the government charged the country’s Bacteriological Institute to prepare such a vaccine and passed a bill in Parliament requiring compulsory vaccination of all dogs (Eichorn, 1926, p. 645). In the United States by 1924, more than 25,000 dogs has been vaccinated, with no reported failures, although there was no record of how many dogs were exposed to the disease. While Connecticut was the first state to officially recommend dog vaccination during a major rabies outbreak in 1922, in Los Angeles County, California, facing a severe rabies outbreak in 1923, with 808 positive cases and nine human rabies deaths, the local government took the further step of instituting a compulsory dog vaccination scheme (“The Etiology and Prevention of Rabies,” 1924).

Canadian Hesitations In Canada, limited attention was paid to the developments in Japan and the United States with the immunization of dogs to prevent rabies. This was not unlike the incidence of the disease in Canada before the mid-1920s among dogs or other animals, or suspected or confirmed human rabies cases. While official laboratory confirmation of rabies cases in dogs or other animals was not always made, or even possible, there were certainly a number of outbreaks, individual cases and public scares of what appeared to be rabies in several parts of Canada prior to the mid-1920s (see Chapter 3b). Federal regulations for the control of rabies in Canada were first established in 1905, requiring the quarantine of all imported dogs. The first officially confirmed cases in Canada were not reported until 1907 and marked the start of a five-year period of localized outbreaks in Saskatchewan and Manitoba, and especially in southern Ontario, where it spread “in a territory overrun with dogs, and in which numberless strays were running around” (Hilton, 1930, p. 233). An article in the January 1910 issue of the Montreal Medical Monthly, “Rabies in Canada,” by Charles H. Higgins, pathologist to the federal Department of Agriculture, highlights Canadian experience with the disease up to that time. Almost all such cases were traceable to rabid dogs that had been illegally imported from the United States or strays that had simply wandered over the border, particularly from New York, and then spread

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(Malone, 1926, p. 292). However, the article said nothing else about the vaccine or where it had been used, before stressing how the disease appeared to be spreading rapidly across the United States. Canadian rabies cases continued to occur during the next few years, especially in eastern Ontario. A notable outbreak occurred in the Kingston area in 1927–1928, sparked by a strangely behaving dog that appeared on a farm and was seen fighting with other dogs. One child was bitten and was given 21 doses of rabies post-exposure rabies vaccine supplied by Connaught Laboratories (Hay, 1928). Prompted by the higher incidence in the late 1920s, Connaught began preparing a newer type of post-exposure rabies vaccine, which had been first developed in 1911 by Dr David Semple, a British Army Officer who established a Pasteur Institute in India. The Semple type of rabies vaccine (see Chapter 15a), based on inactivation of the rabies virus by phenol treatment, could be easily distributed to physicians throughout Canada, making it no longer necessary for patients to be treated at a central laboratory, as was the case with the traditional Pasteur treatment (Defries, 1968). During the Kingston outbreak, 31 positive heads of dogs and cattle were examined in provincial or federal laboratories, although, as emphasized by A. G. Nicholls (1928) in a Canadian Medical Association Journal editorial, this was “only a small percentage of the animals which actually died of the disease ... [Nevertheless] in dealing with the situation, efficient vaccination of dogs on a large scale was found to be impracticable” (pp. 88–89). Nicholls concluded that “preventive measures resolve themselves into muzzling all ‘respectable’ dogs, tying them up, and destroying the vagrants, the latter being particularly liable to disseminate the disease among their kind. The remedy, therefore, is simple and has proved sufficient to stamp out the disease” (pp. 88–89). The official Canadian attitude towards dog vaccination changed little during the 1930s. The veterinary director general of the Department of Agriculture in Ottawa, George Hilton, explained in 1930 that while “much attention has for a number of years been given to the vaccination of dogs,” and “much excellent work” done on “the suitable attenuation of the virus with a view to simplifying the immunization of animals,” vaccination was “undoubtedly of value as an accessory measure, but only as such, as the only way to get rid of this disease is to adequately ­prevent dogs from biting” (Hilton, 1930, p. 232). By this time, some two million doses of rabies vaccine for dogs had been prepared in the United States by commercial producers operating under a federal veterinary licence. The vaccine in most use was now a killed-virus

vaccine that was rendered avirulent using chemicals to such an extent as to be incapable of producing the disease when injected into rabbits in the laboratory. The original Japanese vaccine contained an attenuated virus that was still living and thus theoretically capable of producing the disease. As pointed out in a 1931 article prepared by a veterinarian of the Pathological Division of the U.S. Bureau of Animal Industry, this was “a feature highly objectionable in a prophylactic vaccine” (Schoening, 1931, p. 637). The focus of interest in commercial vaccine production shifted to whether phenol, or the more recently available chloroform treatment, was the most effective in preparing a killed, or avirulent vaccine. By early 1934, about 3,700,000 doses had been produced in the United States, and the US Bureau of Animal Industry had undertaken experimental investigations into the efficacy of the vaccine (Schoening, 1936). Such dog rabies vaccines produced in the United States, however, were not available in Canada, as they were not licensed north of the border. Indeed, no commercial laboratories in Canada at the time were preparing serums and vaccines for veterinary use. As it had with human biological health products since being established within the University of Toronto in 1914, Connaught Laboratories would soon serve as Canada’s only producer of veterinary biologicals, at least for most of the next two decades, providing such vaccines and serums as a public service through the provincial and federal governments. Connaught began its work with veterinary products in 1933 by responding, on a request from the Canadian government, to a serious rabies outbreak in cattle in Trinidad by producing a Semple-type rabies vaccine prepared in calf-brain tissue. With rabies continuing to be a challenge in that Caribbean country through the 1930s, Connaught prepared large quantities of this type of vaccine in an effort to control its impact, with some 500 calves required to prepare the vaccine in 1939. By this time, a significant rabies outbreak among cattle in Alberta prompted similar requests from the Alberta government, as well as the federal Department of Agriculture, for Connaught to supply its rabies vaccine. Preparation of a rabies vaccine on this scale was a difficult and hazardous job, the work led by Dr Neil E. McKinnon and Dr E. G. Kerslake. By 1940 a growing demand for a number of animal health biological products, such as rabies vaccine, particularly from the Canadian agricultural community during the Second World War, and a desire not to rely on imports, prompted the extension of Connaught’s biological production and research scope into the veterinary field (Defries, 1968).

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During the late 1930s and into the early 1940s, the focus on dog rabies in Canada remained on the problem of the disease being brought north across the border, such as occurred in western Ontario. Rabies also developed among a group of high-class hunting dogs from the southern United States that had been brought into Saskatchewan for training. Nevertheless, at a 1941 lecture on veterinary public health, A. E. Cameron, veterinary director general of Canada, concluded, “At present there is no rabies in Canada,” and “while vaccination may be an aid in control, the rabies vaccines used for the single inoculation of dogs are not standardized and all dogs inoculated are not immune. In Canada, where the disease has always been successfully eradicated, rabies vaccine is not licensed into Canada for use on dogs” (Cameron, 1941, p. 103). Such concerns about dog immunization and the real effectiveness of the vaccine grew during this period, prompting renewed research efforts in the United States. Studies were focused on developing methods to evaluate and standardize existing vaccines, such as through a mouse test, and to prepare a vaccine based on rabies virus cultivated in tissue cultures with minimal brain tissues (Webster, 1938; Habel, 1940). This work intensified during the war years under the leadership of the International Division of the Rockefeller Foundation, and with close cooperation of the Alabama State Board of Health and the U.S. Public Health Service, to establish a scientific basis for adequate rabies control measures. The field experience of the U.S. War Department in controlling rabies among dogs, coupled with more systematic field studies in Alabama, clearly established that a 5 cc dose of a potent phenol or chloroform-treated vaccine would produce a high degree of immunity that would last for one year. During the early post-war years, this new confidence prompted seven US states to establish rabies control laws that required annual dog vaccination. Nevertheless, the diversity of state and local rabies control regulations, and the absence of national legislation in the United States, had the effect of drawing attention north to the apparent effectiveness of Canada’s national quarantine regulations for imported dogs, which had been strengthened in September 1944 (Committee of Public Health Relations of the New York Academy of Medicine, 1947).

immunization efforts to bring the disease under control. This was especially true in Hungary, where after very high rabies incidence during the war, a step-by-step and vigorously enforced canine vaccine program across the country brought the number of rabies cases down to 0 in 1948. In 1950, the entire dog population of the country, some seven million, was vaccinated, prompting the delegates to a rabies conference in Budapest to recommend that authorities of all countries plagued by rabies follow the example set by Hungary. Yugoslavia was another country to institute compulsory immunization of dogs during 1946–1950, using three types of rabies vaccines, which brought about a steady decrease in rabies incidence after wolves had brought the disease into the country from Romania (Meyer, 1954). A similar situation developed in Canada during the late 1940s when the incidence of rabies among wild animals, such as wolves and foxes, spread to dogs. Yet, these were not domestic pets or stray dogs threatened by rabid animals moving north from the United States, but rather dogs in the northern Arctic region of Canada that played an important transportation role as sled dogs. Some of the rabid wolves and foxes came across the border from Alaska, likely originating in animals crossing the Bering Strait from Russia. Rabies had also existed among wild animals across the Canadian Arctic since the end of the nineteenth century, according to reports from northern Indigenous peoples and others familiar with the region (see Chapter 37). However, increased contact from people from the south during the war, particularly the military, increased development and travel in the north and thus increased opportunities for contact between a growing working dog population and wild animals infected with rabies. In 1947 such contact led to a significant rabies outbreak among dogs in the Baker Lake area in the Northwest Territories, 2000 miles north of Winnipeg. An emergency call was made to Connaught Laboratories by the federal government for supplies of rabies vaccine to protect the working dogs (Wells, 1954; Defries, 1968). During the next several years, Connaught supplied large quantities of rabies vaccine to the Department of Agriculture to combat the northern Canadian rabies outbreaks (Connaught Medical Research Laboratories [CMRL], 1948–1952). Such efforts, however, were unable to prevent the spread of the disease to the south by way of infected wildlife, first in northern Alberta, where serious outbreaks among cattle and other livestock began in June 1952. The first cases occurred in Fort FitzGerald after a wild fox bit a trapper’s dog, which later developed rabies. Other cases then followed caused by foxes biting hogs, dogs, cattle, and horses

New Northern Threats The early years after the end of the Second World War saw a significant resurgence of rabies incidence in many parts of the world, coupled with often very aggressive national dog

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(Central Rabies Control Committee, 1953). By the fall of 1952, after rabies had rapidly spread among wildlife and livestock across Alberta and into British Columbia, Saskatchewan, and Manitoba, the first major change in Canadian rabies control policy was implemented, which authorized the mass vaccination of dogs. However, such an immunization program, which used more than 100,000 doses of vaccine, was conducted entirely by, and at the expense of, the Health of Animals Division Veterinarians of the federal Department of Agriculture. At the same time, as described by K. F. Wells, of the Health of Animals Division of the Department of Agriculture in his 1954 Control of Rabies report, the entire affected area was placed under a tight quarantine and all dogs ordered kept under strict confinement as the vaccination program “was considered as an adjunct and does in no way replace absolute dog control” (p. 307). The severity of the northern and western Canadian rabies outbreak during 1952–1953 “raised the human exposure to heretofore unknown heights,” prompting 180 people to be given Pasteur rabies treatment following probable exposure to infected animals. In February 1953 this serious and unpredictable animal and human public health situation in Canada prompted “a second major change in the rabies control policy,” under which “rabies vaccine was for the first time made available for use by veterinary practitioners.” However, it was again stressed, “that vaccine is the second line of defense and does not replace dog control” (Wells, 1954, pp. 307–309). In contrast, in the United States, the Communicable Disease Centre of the U.S. Public Health Service, as outlined in an October 1950 CDC Bulletin, annual anti-rabies vaccination of all dogs was the primary tool for the control of the disease. Such efforts, pioneered in such cities as Memphis, St Louis, Denver, and Spokane, required w ­ ell-organized public education campaigns to facilitate the rapid vaccination of at least 70% of the dog population. However, as vaccination did not reach stray animals, the second priority for rabies control was impoundment and the destruction of all stray and ownerless dogs (Tierkel, 1950). By the early 1950s the greater reliance on dog vaccination in the United States reflected greater experience with the practice, compared to Canada, and also growing confidence in the quality and effectiveness of the vaccines that were available. As discussed at the 1953 Annual Meeting of the American Veterinary Medical Association, which was held in Toronto, confidence was high in the existing phenolized vaccine and the substantial one-year protection it provided after one dose. However, there was also excitement about the newer tissue culture-based vaccine that used the Flury strain of

rabies virus adapted to the developing chick embryo and pioneered by Hilary Koprowski and Herald Cox at Lederle Laboratories (Tierkel et al., 1953). Their work began in 1948, with the goal of preparing a single-injection rabies vaccine that would confer immunity to an animal that would last its normal lifespan while also reducing the occurrence of post-vaccinal paralytic accidents associated with vaccines based on animal brain or nervous tissue. In addition to initial use in the United States, mass ­vaccinations of dogs using the Flury live vaccine were undertaken in the early 1950s in Malaya and in Israel, where the jackal was the main wild animal vector threatening dogs. In Israel, a country surrounded by rabies-infected countries, rabies was eliminated after all dogs were vaccinated and the numbers of jackals were reduced by a poisoning campaign. Malaya had tried unsuccessfully to get rid of rabies using the phenolized killed vaccine, but after carrying out a well-organized national campaign using the Flury vaccine, rabies was wiped out (Committee of Public Health Relations of the New York Academy of Medicine, 1955). In a 1954 article in the Bulletin of the World Health Organization, P. J. G. Plummer of the Department of Agriculture, after summarizing Canada’s rabies experience, especially the current enzootic of rabies that was the most extensive ever known in Canada, noted that “Canada has not taken kindly to control measures that are not aimed at stamping out a disease.” But the “tried and successful” methods that had been followed in the south were “totally inapplicable to the wilderness country.” While active campaigns were undertaken to reduce wild animal populations by various means, including poisoned baits, “one might be inclined to wish that a vaccine which would be active by the oral route might be devised” (Plummer, 1954, pp. 772–773). In 1953, when the federal government permitted veterinarians in Canada to immunize dogs against rabies, Connaught Laboratories was able to supply the Flury chick embryo type live vaccine. Connaught had already provided this type of vaccine to the Department of Agriculture for use in controlling the rabies outbreaks in western Canada, as well as for similar use in Trinidad to control rabies among cattle. As was noted in Connaught’s Annual Report for 1953–1954, some 500,000 cc of veterinary rabies vaccine was prepared for the prevention of hydrophobia, much of the Flury vaccine production work led by Dr John Crawley (Defries, 1968; CMRL, 1954, p. 13). The severity of rabies reached a new level in Canada during the second half of the 1950s, extending its spread through wild animals, especially foxes, beginning in the

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north and the western provinces and moving into northern half and then the highly populated southern half of Ontario (Wells, 1957; see Chapter 2). During the fall and winter of 1955, the resultant public alarm prompted a dramatic increase in demand for animal and human rabies vaccines at Connaught, a demand it met at a time when supplies from other sources were insufficient to manage the emergency (CMRL, 1956, p. 9). During the summer of 1958, Connaught supplied over 120,000 doses of Flury rabies vaccine. The Health of Animals Division of the Department of Agriculture vaccinated for free 92,000 dogs in 333 special immunization clinics across Ontario from April 1958 through January 1959. The rabies threat also struck Connaught directly, with two rabid foxes killed on the Lab’s Dufferin Division property in north Toronto and several others caught within metropolitan Toronto (see Plate 3). Some 3000 people in Ontario were treated with rabies vaccine (Semple type) prepared by Connaught after bites from suspected rabid animals, although there were no reports of confirmed human cases. However, by the end of 1959 there had been two fatal human rabies cases (CMRL, 1958, pp. 5–6; Bator, 1995; see Chapter 3b).

the question of rabies virus strain variation, especially between the Arctic and southern regions and its relationship to the increasing animal rabies incidence in the south but relatively low human infection, and the effectiveness of rabies vaccines. Fenje’s human rabies vaccine work quickly bore fruit in 1960 when he was the first to report success in preparing a formalin-inactivated rabies vaccine based on non-nervous tissue cultures and using a distinctive SAD (Street, Alabama, Dufferin) rabies virus strain. Fenje found that hamster kidney was the most suitable tissue for a pre-exposure vaccine that would be of most value to animal workers. Also of interest to Fenje was the need for increased thoroughness in rabies immunization of farm animals. As he noted in an article co-written with Aimes, “The Problem of Rabies in Canada,” to the epidemiologist, at least, it seemed wrong to pay farmers compensation for animals that died of a disease that was easily preventable by vaccination (Fenje & Amies, 1960, p. 244; Bator, 1995). Fenje’s substantial progress with human rabies vaccine development proved of practical and inspirational value to his colleagues at Connaught who were focused on improving rabies vaccines for animals. Indeed, based on the rabies virus grown by Fenje in hamster kidney cells, Dr Melvin Abelseth was able to develop a unique rabies virus strain, known as ERA, that grew vigorously in pig kidney cells, a larger source of tissues, and would be suitable as an attenuated live rabies vaccine for a wide range of domestic pets and animals, not just dogs. Unlike the HEP Flury vaccine, the new ERA strain vaccine, first available in 1964 and administered in a single 2 cc dose, was highly antigenic and of particular value for cattle and other livestock immunization, as well as wildlife, especially foxes; it provided three years of immunity protection in cattle and two years in dogs and horses. The ERA strain vaccine, available as a freezedried product reconstituted just before administration, was named after the three key members of Connaught’s research staff involved in its development: (E) Evelyn Gaynor (technician), (R) Alex Rokitnicki (technician), and (A) Dr Abelseth (veterinary scientist). Overseeing the ERA project were Dr John F. Crawley, Dr J. D. Black, and Dr Kenneth F. Lawson, who, beginning in the late 1960s, were also responsible for pioneering the concept and application of oral immunization of wildlife using ERA rabies vaccine administered through carefully packaged baits dropped from aircraft (Bator, 1995; Abelseth, 1964; “Rabies Vaccine Modified,” 1965; see Chapter 17). A notable addition to the rabies control arsenal, by the 1970s and into the 1980s, the ERA rabies vaccine achieved

Canadian Rabies Vaccine Innovation, 1960s–1970s The alarming rise in rabies incidence, especially in c­ entral Canada, prompted an intensified rabies research program at Connaught that focused on improving animal ­pre-exposure vaccines and human post-exposure rabies vaccines, with more immediate success with the former than the latter. Starting in 1958, efforts to improve the human rabies vaccine were led by Dr Charles R. Amies, who first investigated preparing the vaccine in eggs, as was the method for the Flury animal vaccine (CMRL, 1959, p. 6). Connaught had pioneered the development and production of the high-egg-passage (HEP) Flury vaccine as a safer alternative to the original Flury vaccine, which was based on a low-egg-passage (LEP) production process. The LEP vaccine was safe for dogs but not for cattle and other susceptible animals, and there was thus a danger of its possible misuse. The HEP vaccine was acceptable for general animal use and became the standard animal rabies vaccine in Canada in 1956–1957 (Walker & Crawley, 1959). In 1960 Dr Paul Fenje, after assisting Aimes, assumed leadership of Connaught’s rabies research effort, as well as its smallpox vaccine research and production program (Rutty, 2008b). Of particular interest to Fenje was

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increasing acceptance among international veterinary circles as the best vaccine for animal rabies immunization. It was not long, however, before a number of other tissue culture rabies vaccines became available in Canada, mostly imported, as was discussed during the 1967 Rabies Conference hosted by the Toronto Academy of Veterinary Medicine. The other new live tissue vaccines included Endural from the Norden Company, and vaccines from Lederle and Dow Chemical. Several inactivated tissueculture-based rabies vaccines were also available, such as BarRab from Fort Dodge and Rabvac and Raboid from Fromm Laboratories, although their use in Canada became increasingly restricted. While increasing suburbanization during this period brought domestic pets into closer proximity to wild animals, of growing concern was rabies spreading among domestic cats and the threat posed by rabies in bats, which had become chronic carriers of the virus (Moynihan, 1966). Still, a general public lethargy about rabies persisted because human cases were rare. When such cases did occur, however, as happened in late 1968 when a rabid bat attacked two young boys in the Toronto area and a four-year-old girl died in Richmond, Ontario, after being attacked by a rabid cat, the media focus on the disease became quite intense (see Chapter 3b). Such a pattern was consistent with previous rabies outbreaks, each episode providing an opportunity to highlight ongoing issues with rabies prevention and control, as well as new developments. The 1968–1969 rabies media coverage, in particular, pointed out how farm animal vaccination had not been encouraged in Canada since financial compensation remained too easy when livestock became infected. However, farmers and veterinarians were left increasingly vulnerable. Media reports, nevertheless, stressed that without a doubt Canada had one of the best diagnostic and reporting services in the world facilitated

through the efforts of the Health of Animals Branch of the Department of Agriculture (Walker, 1969).

Conclusion After several decades of hesitation, by the end of the 1960s, vaccination had become the cornerstone strategy in Canada for rabies prevention in household domestic animals. Vaccination of livestock, however, especially cattle, remained an unresolved challenge. As we have seen, the changing epidemiology of rabies and its growing domestic threat, coupled with advances in vaccine effectiveness and safety, drove the evolution of a more accepting attitude towards rabies immunization in Canada. This was in contrast to what had occurred in the United States, where rabies vaccination was broadly accepted much earlier. After considerable leadership in rabies vaccine innovation for both domestic animals and for humans, especially during the 1950s and 1960s, Canadian involvement in this field declined, not unlike the incidence of the disease in the country. In 1969, however, after more than 11 years of development work, Connaught Laboratories was granted a licence for a pre-exposure human rabies vaccine designed primarily for veterinarians and others who work directly with potentially rabid animals, especially wildlife (CMRL, 1970, p. 9). By this time, the focus of Connaught’s animal rabies research program had shifted to the prevention of rabies in wildlife through oral immunization, rather than direct injection. The effectiveness of this method, which targeted the oral cavity with a vaccine based on the ERA strain, was first demonstrated in a 1970 paper by the research team of Black and Lawson (1970) (Bator, 1995). The story behind the development and pioneering use of oral rabies vaccine in Canada is the subject of Chapters 17, 18, and 19 in this book.

References Abelseth, M. K. (1964). An alternative rabies vaccine for domestic animals produced in tissue culture. The Canadian Veterinary ­Journal, 5, 279–286. Retrieved from National Center for Biotechnology Information website: https://www.ncbi.nlm.nih.gov/pmc/articles /PMC1695899/ Bator, P. A. (1995). Within reach of everyone: A history of the University of Toronto School of Hygiene and Connaught Laboratories ­Limited, Vol. II, 1955–75. Ottawa: Canadian Public Health Association. Black, J. G., & Lawson, K. F. (1970). Sylvatic rabies studies in the silver fox (Vulpes vulpes): Susceptibility and response. Canadian ­Journal of Comparative Medicine, 34, 309–311. Retrieved from National Center for Biotechnology Information website: https://www .ncbi.nlm.nih.gov/pmc/articles/PMC1319471/

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The Development of Vaccines and Delivery Systems Cameron, A. E. (1941). Public health. Canadian Journal of Comparative Medicine, 5, 102–103. Retrieved from National Center for ­Biotechnology Information website: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1583956/ Central Rabies Control Committee. (1953). Rabies. Alberta Department of Agriculture Bulletin, 89. Committee of Public Health Relations of the New York Academy of Medicine. (1947). Control of rabies. Public Health Reports, 62, 1215–37. Retrieved from National Center for Biotechnology Information website: https://www.ncbi.nlm.nih.gov/pmc/articles /PMC1995265/ Committee of Public Health Relations of the New York Academy of Medicine. (1955). Practical problems in rabies control. Public Health Reports, 70, 566. Retrieved from National Center for Biotechnology Information website: https://www.ncbi.nlm.nih.gov/pmc /articles/PMC2024576/ Connaught Medical Research Laboratories. (1948–1952). Annual reports. Sanofi Pasteur Limited (Connaught Campus) Archives, ­Toronto, ON. Connaught Medical Research Laboratories. (1954). Annual report, 1953–54. Sanofi Pasteur Limited (Connaught Campus) Archives, Toronto, ON. Connaught Medical Research Laboratories. (1956). Annual report, 1955–56. Sanofi Pasteur Limited (Connaught Campus) Archives, Toronto, ON. Connaught Medical Research Laboratories. (1959). Annual report, 1958–59. Sanofi Pasteur Limited (Connaught Campus) Archives, Toronto, ON. Connaught Medical Research Laboratories. (1960). Annual report, 1959–60. Sanofi Pasteur Limited (Connaught Campus) Archives, Toronto, ON. Connaught Medical Research Laboratories. (1970). Annual report, 1969–70. Sanofi Pasteur Limited (Connaught Campus) Archives, Toronto, ON. Corwin, G. E. (1924). The control of rabies in Connecticut. American Journal of Public Health, 14(8), 688–692. https://doi.org/10.2105 /AJPH.14.8.688 Defries, R. D. (1968). The first forty years, 1914–1955: Connaught Medical Research Laboratories, University of Toronto. Toronto, ON: University of Toronto Press. Eichorn, A. (1926). The present status of prophylactic rabies vaccination in dogs. American Journal of Public Health, 16(6), 644–647. https://doi.org/10.2105/AJPH.16.6.644 Endre Hőgyes. (n.d.). In Whonamedit? A dictionary of medical eponyms. Retrieved from http://www.whonamedit.con/doctor.cfm /3362.html The etiology and prevention of rabies. (1924). British Medical Journal, 1, 1059–1060. https://doi.org/10.1136/bmj.1.3311.1059 Fenje, P., & Amies, C. R. (1960). The problem of rabies in Canada. Canadian Medical Association Journal, 82, 243–245. Retrieved from National Center for Biotechnology Information website: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1937728/ Habel, K. (1940). Evaluation of a mouse test for the standardization of the immunization power of anti-rabies vaccine. Public Health ­Reports, 55(33), 1473–1487. Retrieved from National Center for Biotechnology Information website: https://www.ncbi.nlm.nih.gov /pmc/articles/PMC1996044/ Hay, W. D. (1928). A note on the outbreak of rabies in the Kingston District. Canadian Medical Association Journal, 19, 73. Retrieved from National Center for Biotechnology Information website: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1709767/ Higgins, C. H. (1910). Rabies in Canada. Montreal Medical Journal, 39(1), 15–19. Retrieved from Canadiana Online website: http://eco .canadiana.ca/view/oocihm.8_05178_259/18?r=0&s=1 Hilton, G. (1930). The control of rabies. Canadian Public Health Journal, 21, 226–234. Malone, R. H. (1926). Rabies. Canadian Medical Association Journal, 16, 288–292. Retrieved from National Center for Biotechnology Information website: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1708734/ Meyer, K. F. (1954). Can man be protected against rabies? Bulletin of the World Health Organization, 10(5), 845–866. Retrieved from National Center for Biotechnology Information website: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2542171/ Moynihan, W. A. (1966). Rabies in Ontario. Canadian Journal of Public Health, 57, 243–248. Muzzle all dogs in Ontario. (1910, February 3). Toronto Star, p. 1. Nicholls, A. G. (1928). Rabies in Ontario. Canadian Medical Association Journal, 19, 88–89. Retrieved from National Center for ­Biotechnology Information website: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1709744/ A Pasteur Institute. (1910). Canada Lancet, 43(7), 554. Retrieved from Canadiana Online website: http://eco.canadiana.ca/view /oocihm.8_05199_475/74?r=0&s=1 Plummer, P. J. G. (1954). Rabies in Canada, with special reference to wildlife reservoirs. Bulletin of the World Health Organization, 10, 772–73. Retrieved from National Center for Biotechnology Information website: https://www.ncbi.nlm.nih.gov/pmc/articles/ PMC2542158/

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Domestic Animal Vaccines Rabies scare is general. (1910, February 19). Toronto Star, pp. 1, 5. Rabies in Canada. (1910). Dominion Medical Monthly, 35(3), 128. Retrieved from Canadiana Online website: http://eco.canadiana.ca /view/oocihm.8_06539_177/34?r=0&s=1 Rabies in Quebec province. (1926). British Medical Journal, 2, 1014. https://doi.org/10.1136/bmj.2.3438.1014 The rabies outbreak. (1910). Canadian Journal of Medicine and Surgery, 27(4), 222–226. Retrieved from Canadiana Online website: http://eco.canadiana.ca/view/oocihm.8_05193_160/18?r=0&s=1 Rabies vaccine modified live virus tissue culture origin. (1965). Rabies vaccine modified live virus tissue culture origin. Canadian ­Journal of Comparative Medicine and Veterinary Science, 29, 81. Retrieved from National Center for Biotechnology Information ­website: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1494376/ Rice, T. B., & Beatty, N. (1928). The prevalence of rabies in the United States and the world. American Journal of Public Health, 18, 424. Retrieved from National Center for Biotechnology Information website: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1580648/ Rutty, C. J. (2008a). Personality, politics and public health: The origins of Connaught Medical Research Laboratories, 1888–1917. In E. A. Heaman, A. Li, & S. McKellar (Eds.), Essays in honour of Michael Bliss: Figuring the social. (pp. 273–303). Toronto, ON: ­University of Toronto Press. Rutty, C. J. (2008b). Canadian vaccine research, production and international regulation: Connaught Laboratories and smallpox vaccine, 1962–1980. In K. Kroker, J. Keelan, & P. M. H. Mazumdar (Eds.), Crafting immunity: Working histories of clinical immunology (pp. 273–300). Burlington, VT: Ashgate. Schoening, H. W. (1931). Immunization of dogs against rabies by the on-injection method. American journal of Public Health, 21(6), 637–640. https://doi.org/10.2105/AJPH.21.6.637 Schoening, H. W. (1936). Can the health officer safely utilize prophylactic immunization as the sole means to control canine rabies? American Journal of Public Health, 26(3), 265–267. https://doi.org/10.2105/AJPH.26.3.265 Sellers, T. F. (1923). Status of rabies in the United States in 1921. American Journal of Public Health, 13(9), 742–747. https://doi. org/10.2105/AJPH.13.9.742 Tierkel, E. S. (1950). The theory and practice of rabies control. CDC Bulletin, October, 1–3. Tierkel, E. S., Kissling, R. E., Eidson, M., & Habel, K. (1953). A brief survey and progress report of controlled comparative experiments in canine rabies immunization. In Proceedings Book, Annual Meeting of American Veterinary Medical Association (pp. 443–445). ­Philadelphia, PA: American Veterinary Medical Association Umeno, S., & Doi, Y. (1921). A study of the anti-rabic inoculation of dogs and the results of its practical application. The Kitasato ­Archives of Experimental Medicine, 4(2), 108. Walker, V. C. R. (1969). Rabies today: Man and animals. Canadian Veterinary Journal, 10, 11–17. Retrieved from National Center for Biotechnology Information website: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1697394/ Walker, V. C. R., & Crawley, J. F. (1959). The immunizing value of high egg-passage Flury rabies virus and its use in combination with the virus of canine distemper. Canadian Journal of Comparative Medicine, 23, 50–55. Retrieved from National Center for ­Biotechnology Information website: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1581491/ Webster, L. T. (1938). Experiments on anarabic vaccination with tissue culture virus. American Journal of Public Health, 28(1), 44–46. https://doi.org/10.2105/AJPH.28.1.44 Wells, K. F. (1954). Control of rabies. Canadian Journal of Comparative Medicine, 18, 302–309. Retrieved from National Center for ­Biotechnology Information website: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1791738/ Wells, K. F. (1957). The rabies menace in Canada. Canadian Journal of Public Health, 46, 239–243. Retrieved from https://www.jstor .org/stable/41981083?seq=1

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16 Regulation of Rabies Vaccines in Canada Carolyn Cooper,1 Tara da Costa,1 and Oksana Yarosh1 1

Canadian Centre for Veterinary Biologics, Canadian Food Inspection Agency, Ottawa, Ontario, Canada

Veterinary Biologics in Canada History of the Legislative Authority for Regulation Agriculture has long been an important driver of the ­Canadian economy. In recognition of this fact, legislation safeguarding the health of Canadian animals, in the form of the Animal Contagious Diseases Act, 1869, was one of the first pieces of legislation passed after Confederation (Dukes & McAninch, 1992). The Animal Contagious Diseases Act, amended in 1903, 1906, 1927, and 1952, remained in force until 1977 when it was replaced by the Animal Disease and Protection Act. This was subsequently replaced by the Health of Animals Act in 1990 (Dukes & McAninch, 1992; see Chapter 4). The need to create regulations to control the importation and manufacture of veterinary biologics (which include vaccines, diagnostic test kits, antibody products, and colostrum) in Canada was first recognized in 1921 by producers in the prairie provinces who wanted some control over the quality of veterinary biologics available on the Canadian market. The deputy minister of agriculture, J. H. Grisdale, then wrote to Dr Fred Torrance, veterinary director general, and asked him to promulgate regulations pertaining specifically to veterinary biologics (Health of Animals Branch, 1921). While the Department of Justice felt that the current Animal Contagious Diseases Act would support such regulations, Dr Torrance believed that this would be a difficult task because of a lack of adequate staff in the Health of Animals Branch (Health of Animals Branch, 1921). He succeeded, however, and regulations relating to veterinary

biologics were established on 12 May 1934, as the Regulations Relating to the Importation, Manufacture, Sale and Use of Veterinary Biologics, under the Animal Contagious Diseases Act, RSC 1927 (“Regulations Governing the Importation,” 1934). These regulations pertained both to the manufacture and to the importation of veterinary biologics (Alexander, 1989). They remained essentially unchanged even as they were incorporated into the Animal Contagious Disease Regulations in 1949 (“Animal Contagious Disease,” 1949). Rabies vaccines for domestic animals, as veterinary biologics, were regulated through this legislation. Legislation specific to rabies vaccines was not introduced until 1977, with the establishment of the Animal Disease and Protection Regulations (CRC c. 296). It was illegal to sell rabies vaccines to non-veterinarians, and this clause remains unchanged in the current Health of Animals Regulations (CRC, c. 296). Some exceptions are made for rabies vaccination in remote areas or where there is an absence of veterinarians, usually administered by local medical personnel or trained lay vaccinators, or for ­trap-vaccinate-release programs run by provincial wildlife officials. Eight amendments were made to Part XI of the Animal Disease and Protection Regulations between their establishment in 1977 and their replacement in 1990 by the Health of Animals Regulations. The Animal Disease and Protection Act was combined with the Livestock and ­Livestock Products Act in 1990 to establish the current Health of Animals Act. This legislation remains in force today, and the text relating to veterinary biologics is essentially unchanged from that drafted in 1977 for the Animal Disease and Protection Act.

Regulation of Vaccines in Canada

The current Health of Animals Act (1990) is an act r­especting diseases and toxic substances that may affect ­animals or that may be transmitted by animals to persons and respecting the protection of animals. Veterinary ­biologics are covered by this act as per the following:

Agency (CFIA) on 1 April 1997 (Canadian Food Inspection Agency Act, 1997). Although veterinary biologics have been regulated in Canada since 1934, the Veterinary Biologics Committee of the Health of Animals Branch of Agriculture ­Canada was formed only in 1976. It was headed by Dr Peter H. Langer and was composed of representatives from Agriculture, Health and Welfare, Industry Trade and Commerce, ­Treasury Board, and Supply and Services. The committee was formed in response to issues identified by both the branch and domestic veterinary biologics manufacturers, most notably insufficient supply of domestic veterinary ­biologics and concerns regarding adverse reactions associated with foreign-manufactured veterinary biologics. Rabies vaccines were undoubtedly implicated in these ­concerns as cases of vaccine-induced rabies had been ­previously identified in several species subsequent to the use of modified live rabies vaccines. The initial objectives of the committee included determining the status of veterinary biologics in Canada and making recommendations to provide reliable supplies of pure, potent, safe, and efficacious veterinary biologics for Canadian livestock. These objectives were to be accomplished through such activities as determining the domestic and foreign sources of veterinary biologics used in Canada, identifying problems faced by domestic veterinary biologics manufacturers, investigating problems with foreign veterinary biologics, and examining the regulatory approach of other national governments with respect to veterinary biologics. The Health of Animals Branch of Agriculture Canada began drafting guidelines for procedures related to the regulation of veterinary biologics. The committee was part of the Contagious Diseases ­Division of the Health of Animals Branch of ­Agriculture Canada and was located at Billings Bridge Plaza in ­Ottawa. The committee became Veterinary Biologics, Health of ­ Animals Division in the late 1970s, and remained as such until 1990, when it underwent a name change to the V ­ eterinary Biologics and Biotechnology Section. The ­section became part of the CFIA when the agency was e­ stablished in 1997, and subsequently became the ­Veterinary Biologics Section by 2000 and the Canadian Centre for Veterinary Biologics (CCVB) in 2010. The CCVB continues to be an integral part of the veterinary biologics regulatory program in Canada, in ­ conjunction with other facets of the CFIA. Currently, the ­responsibilities of CFIA-CCVB include licensing veterinary biologics (domestically and foreign produced); i­ssuing import permits and export certificates for veterinary biologics, including those for emergency or research use; issuing

64. (1) The Governor in Council may make regulations for the purpose of protecting human and animal health through the control or elimination of diseases and toxic substances and generally for carrying out the purposes and provisions of this Act, including regulations (s) prohibiting or regulating the importation, preparation, manufacturing, preserving, packing, labelling, storing, testing, transportation, sale, conditions of sale, advertising for sale, use and disposal of veterinary biologics and regulating their purity, potency, efficacy and safety. (Health of Animals Act, 1990)

The current Health of Animals Regulations (CRC, c. 296), under the Health of Animals Act, include regulations specific to veterinary biologics in Part XI, sections 120 to 135.1. These sections cover the following topics: permits to release veterinary biologics, information requirements, ­issuance of permits, new information requirements, permits to import, establishment licences and product licences, and requirements of operation in a licensed establishment (Health of Animal Regulations, CRC, c. 296). The regulations pertaining to vaccination of domestic animals vary across jurisdictions in Canada. Although rabies vaccination of domestic animals is not universally applied across Canada, it is strongly recommended. Since rabies vaccination of pets is important to protect people from rabies as well as to protect their pets, many provinces have legislation that require pets be certified as vaccinated against rabies by a veterinarian.

History of the Regulatory Program The Health of Animals Branch was founded in April 1902 as part of a reorganization of Agriculture Canada. Although originally located on Queen Street in downtown Ottawa, its offices were moved to the Experimental Farm in December 1902 (Higgins, 1943; see Chapter 20). The branch was divided into three divisions, with the regulatory responsibilities falling to the Contagious Diseases Division (Dukes & McAninch, 1992). In 1979, the Health of Animals Branch was renamed the Health of Animals Division and became part of the Food Production and Inspection Branch (Dukes & McAninch, 1992). It remained this way until the foundation of the Canadian Food Inspection

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establishment licences for manufacturers; inspecting domestic and foreign manufacturers; investigating suspected adverse reactions, complaints, or deficiencies; developing a Canadian veterinary biologics regulatory framework (regulations, guidelines, policies); providing advice to regulated parties and other stakeholders; and releasing veterinary biologics, among others. An important activity for wildlife rabies control is the ability of CCVB to complete environmental risk assessments and to issue permits to release veterinary biologics before, and in support of, the use of licensed and experimental rabies vaccines in field campaigns under specified conditions. At the time of the initial formation of the Veterinary Biologics Committee in the late 1970s, plans to develop a veterinary biologics laboratory facility at the Animal Disease Research Institute (ADRI, now CFIA Ottawa Laboratory, Fallowfield) were initiated, with a target implementation date of 1979–1980. The Biologics Evaluation Laboratory (BEL) was established in 1985 as part of Agriculture Canada, with the mandate to develop and conduct a quality assurance (QA) monitoring program for the purity, potency, safety, and efficacy of veterinary biologics licensed Canada (Thomas, 1989). BEL’s laboratory was located at the Animal Diseases Research Institute-Nepean, and scientists at BEL collaborated with scientists in other laboratories at ADRI if circumstances dictated that a given biologic needed specialized testing (such as by the rabies lab or brucellosis lab) because human safety issues, foreign animal disease status, or needed expertise. The main personnel of BEL were in place by October 1987, and routine testing of selected veterinary biologics for purity and potency commenced around this time (Thomas, 1989). Vaccine efficacy and safety testing tended to be limited to novel products and products with identified problems. During its operation, BEL developed and validated QA monitoring protocols for vet biologics licensed in Canada (including those for novel biotechnologically derived products), provided ongoing scientific advice to the veterinary biologics program, and collaborated with industry and university groups on technical and scientific matters. With its achieved goal of increasing QA of vet biologics in Canada, BEL served, in its time, to benefit Canadian clients, consumers, and industry (Thomas, 1989). BEL became part of the CFIA when the Agency was formed in 1997 and continued to operate until early 2011, when BEL was closed through program restructuring. The CFIA recognized the need for inspectors supporting the veterinary biologics program to be in place in each of the

four areas of Canada (East, West, Ontario, and Quebec), and thus Veterinary Biologics Operations (VBO) was formed in 2003. VBO’s roles include providing advice and guidance to regulated parties, universities, other governments and agencies, and the public regarding the veterinary biologics program; inspecting veterinary biologics manufacturers and importers; investigating suspected adverse reactions and complaints; and monitoring veterinary biologics manufacturers’ laboratory and field safety and efficacy trials.

Current Licensing Process for Veterinary Biologics in Canada To meet the requirements for licensure, a veterinary biologic must be shown to be pure, potent, safe, and effective when used in the target species according to the manufacturer’s label recommendations (Silva et al., 1995). Purity of a vaccine is the condition of being free from contaminating micro-organisms and substances. Potency measures the relative strength of a vaccine and correlates with its efficacy. Efficacy is a measure of the specific protective capacity of the vaccine when used according to label recommendations. Vaccines must also be safe and not cause undue local or systemic reactions when used as recommended. To be considered for licensing in Canada, a novel product must also be supported by data demonstrating that it can be manufactured and used without adversely affecting animal health, human health, food safety, or the environment. A risk-based approach is used to evaluate the efficacy and safety of the product in the target species, as well as its potential effects on non-target species, humans, and the environment. Manufacturers (domestic or foreign) wanting to license a veterinary biologic in Canada must submit a dossier to CFIA-CCVB, including, but not limited to, an outline of production, describing in detail how the product is manufactured; proposed labels; data on the preparation and characterization of the master seed; and data to support efficacy (usually vaccination/challenge studies), safety (usually large-scale field safety studies), and potency. If the vaccine is novel and live or to be distributed in the environment, such as wildlife rabies vaccine, an environmental assessment is carried out, a risk assessment document is prepared, and it is made available on the CCVB website. Currently, Canada has a small but growing capacity for veterinary biologic manufacturers. Canadian manufacturers of veterinary biologics are required to hold a valid Canadian veterinary biologics establishment licence and a corresponding Canadian veterinary biologics product ­licence

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Code of Federal Regulations, Title 9 (9 CFR) – Animals and Animal Products, Parts 101 to 123. Part 113 of 9 CFR ­describes the general requirements for veterinary biologics. Sections 209 and 312 are those sections in Part 113 that pertain specifically to rabies vaccines. Historically, annual administration of rabies vaccines has been recommended to ensure the protective titre did not wane in vaccinated animals. However, with more recent concerns regarding over-vaccination of companion animals, some rabies vaccines are labelled for use every three years, based on duration of immunity data, while others are available in combination with other core antigens. In Canada, rabies can be found in populations of wild animals, most notably bats, foxes, raccoons, and skunks. To combat this challenge, the CCVB has worked closely over the years with industry and provincial and territorial governments to ensure that appropriate oral vaccines are available to protect against this threat. Some of the vaccines that were used in the past include ERA (Evelyn-Rokitnicki-Abelseth), a modified live rabies virus vaccine that is no longer licensed in Canada, and V-RG, a live vaccinia virus that expresses the rabies glycoprotein (see Chapters 17 and 18). The vaccine that is currently used to control terrestrial wildlife rabies in Canada, ONRAB, is a recombinant live type 5 human adenovirus vector that expresses the rabies glycoprotein. The product is licensed for restricted use by government officials only. The CCVB has worked closely with provincial and territorial authorities who conduct the wildlife rabies control programs to assess the field efficacy of wildlife rabies vaccines. ONRAB vaccine has been instrumental in the recent sharp decrease in terrestrial rabies cases in Ontario, New Brunswick, and Quebec. The United States began incorporating ONRAB in its wildlife rabies control program in 2011, and the CCVB has worked with Artemis Technologies Inc. of Guelph, Ontario (see Chapter 17c for photographs of the Artemis Laboratory) and the United States Department of Agriculture to facilitate the vaccine’s use both in Canada and the United.

listing all products produced for sale or distribution. Manufacturers are inspected on an annual basis to ensure compliance with the Health of Animals Regulations. The majority of veterinary biologics used in Canada are manufactured in foreign countries (largely the United States) and imported into Canada after completing the Canadian licensing process. If all requirements for the Canadian ­licensing of the foreign manufactured veterinary biologic are met, then the designated Canadian importer is issued a permit to import veterinary biologics to allow the importation of the product into Canada from the manufacturer’s facility. For a Canadian-manufactured veterinary biologic to be eligible for licensing in Canada, samples of the product must be submitted for testing. Generally, a wildlife rabies vaccine, for example, would be tested for purity and for ­expression of the rabies (glycoprotein) antigen. This testing must be completed before field use of the vaccine, and sufficient time must be allotted for the possibility of re-tests, which may be required before release. The manufacturer’s serial release test report (MSRTR) is also submitted to the CCVB at this time for review and release authorization. As part of an ongoing quality control monitoring ­program, serials of licensed veterinary biologics may be selected at random for testing. The safety and e­fficacy of licensed veterinary biologics are also monitored post-licensing through an analysis of reported suspected adverse events. All Canadian manufacturers and designated importers are required to report suspected adverse events to the CCVB within 15 days of receiving the report.

Current Licensing of Rabies Vaccines in Canada Since all 35 of the rabies vaccines currently licensed in ­Canada for use in domestic animals are manufactured in the United States, they conform to the US standards (which are equivalent to the Canadian licensing standards). These standards are described in the United States Department of Agriculture, Animal and Plant Health Inspection S­ ervice

References Alexander, D. C. (1989). Regulation of veterinary biologics in Canada. Canadian Veterinary Journal, 30(4), 298. Retrieved from https:// www.ncbi.nlm.nih.gov/pmc/articles/PMC1681215/pdf/canvetj00557-0024.pdf Animal contagious diseases regulations [Order in Council]. (1949, March 1). Canada Gazette II, 83(10), 841–877. Retrieved from ­Collections Canada website: http://www.collectionscanada.gc.ca/databases/canada-gazette/093/001060-119.01-e.php?document _id_nbr=9987&image_id_nbr=380663&f=g&phpsessid=irb8mnnisjgr0fq17no4midvat3

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The Development of Vaccines and Delivery Systems Canadian Food Inspection Agency Act. SC 1997, c. 6. Current to 21 June 2019 and last amended on 17 June 2019. Retrieved from Justice Laws website: https://laws-lois.justice.gc.ca/eng/acts/c-16.5/FullText.html#h-67978 Dukes, T., & McAninch, N. (1992). Health of Animals Branch, Agriculture Canada: Look at the past. Canadian Veterinary Journal, 33(1), 58–64. Retrieved from http://www.ncbi.nlm.nih.gov/pmc/articles/PMC1481176/pdf/canvetj0005-0060.pdf Health of Animals Act. SC 1990, c. 21. Current to 6 June 2019 and last amended on 15 January 2019. Retrieved from Justice Laws ­website: http://laws-lois.justice.gc.ca/eng/acts/H-3.3 Health of Animals Branch. (1921). Veterinary biologics. [Draft of proposed regulations for control of serums, vaccines, toxins]. (File no. 5-15, Vol. 2862, microfilm reel T-7011, FIND017/90995). Library and Archives Canada, Ottawa, ON. Health of Animals Regulations. CRC, c. 296. Current to 6 June 2019 and last amended on 15 April 2019. Retrieved from Justice Laws website: https://laws-lois.justice.gc.ca/eng/regulations/C.R.C.,_c._296/ Higgins, C. H. (1943). Reminiscences of events: Before and after formation of the Health of Animals Branch. Canadian Journal of ­Comparative Medicine and Veterinary Science, 7(1), 3–6. Retrieved from https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1584179 /pdf/vetsci00115-0007.pdf Regulations governing the importation, manufacture, sale and use of veterinary biologics [Order in Council]. (1934, May 12). Canada Gazette II, 6(48), 2314–2316, http://www.collectionscanada.gc.ca/databases/canada-gazette/093/001060-119.01-e. php?image_idd_nbr=926965&document_id_ngr=14723&f=PHPSESSID=irb8mnisjgr0fq17no4midvat3 Silva, S. V. P. S., Samagh, B. S., & Morley, R. S. (1995). Risk analysis for veterinary biologicals released into the environment. Revue ­Scientifique et Technique (International Office of Epizootics), 14(4), 1043–1059. https://doi.org/10.20506/rst.14.4.897 Thomas, F. C. (1989). A new biologics evaluation laboratory. Canadian Veterinary Journal, 30(4), 299. Retrieved from http://www.ncbi .nlm.nih.gov/pmc/articles/PMC1681200/pdf/canvetj00557-0025a.pdf

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17a Oral Vaccine Development in Canada ORAL VACCINES

James B. Campbell1 and Ludvik Prevec2 1

Faculty of Medicine, Department of Microbiology and Immunology, University of Toronto (Retired), Ontario, Canada 2 Professor Emeritus, Department of Biology, McMaster University, Hamilton, Ontario, Canada

Introduction Although a decade of work in the 1970s by rabies research groups in North America and Europe had demonstrated the possibility of using the oral route to immunize certain wildlife species against rabies, most of these studies had used modified-live rabies vaccines (Campbell & Zhang, 1993). While these provided the basis for later field trials using vaccine-laced baits for the oral immunization of wildlife (Wandeler, 1988; Campbell, 1994), particularly foxes, there were concerns about the safety of using live rabies vaccine orally, some of which were known to cause clinical rabies in certain animal species, particularly rodents (MacInnes, 1988). As an alternative, while the use of inactivated rabies vaccine orally had not provided very encouraging results, a few studies had shown that if inactivated virus could bypass the stomach and duodenum, some animals would seroconvert (Lawson et al., 1982). The University of Toronto contracted Campbell in 1979 to participate in the Ontario Ministry of Natural Resources (OMNR) Wildlife Rabies Immunization Program. The original senior investigators were Campbell (vaccine development), Eugene Zalan (antibody testing) and Graham Nairn (vaccine formulations). Until the university’s level 3 bio-containment laboratory became available in 1981, much of the virus work was carried out in the Laboratory Services Branch, Ontario Ministry of Health, in Toronto. Following the untimely death of Dr Zalan, Campbell took responsibility for all serum antibody testing of the OMNR Program. The method initially used was the florescent inhibition microtest (FIMT) (Zalan et al., 1979), a

miniaturized version of the widely used rapid fluorescent focus inhibition test (Barton & Campbell, 1988). However, this test required highly trained operators and level 3 facilities, since live virus was involved. Lynda Barton, a master’s student in the laboratory, circumvented this by developing and validating an indirect enzyme-linked immunosorbent assay (ELISA) suitable for assaying rabies antibody in all target wildlife species (fox, skunk, raccoon), using cross-reacting anti-canine IgG and purified rabies glycoprotein (Campbell & Barton, 1988). This ELISA technique was simple and inexpensive, and produced results that correlated well with the FIMT. It was used for assaying most of the field serum samples until 1992, when antibody testing was taken over by the Animal Disease Research Laboratory, Nepean.

Studies on Oral Inactivated Rabies Vaccines The first few years of the program focused on attempts to develop an inactivated rabies vaccine formulation that could be used for the oral vaccination of wild foxes. Studies showed that inactivated vaccines directly instilled deep into the lumen of the duodenum of foxes by means of a catheterized gastrointestinal endoscope or an indwelling catheter resulted in seroconversion in about 30% of animals (Lawson et al., 1982; Lawson et al., 1989). For the most part, however, the resulting serological responses were low and of short duration. Similar results were found with raccoons (Rupprecht et al., 1992). Clearly, if inactivated vaccines were ever to provide a practicable approach to immunizing wild

The Development of Vaccines and Delivery Systems

animals, methods had to be found to enhance this ­response and to permit a more natural uptake of vaccine.

vaccine following solubilization at pH7, even after storage at 4°C for six months. In one experiment, 14 of 16 guinea pigs force-fed microspheres containing inactivated vaccine developed significant rabies antibody responses within 21 days, and all responded with increased titres after a booster dose. ­Further studies, however, showed that oral administration of liquid inactivated vaccine itself (i.e., without CAP coating) stimulated protective antibody responses in both guinea pigs and mice (Campbell et al., 1985; Maharaj, 1987). Once again, however, foxes fed vaccine-containing microspheres failed to respond. Nevertheless, these experiments clearly showed that the microspheres had the potential to deliver rabies antigen into the intestine in an immunogenically active form.

Cellulose Acetate Phthalate Cellulose acetate phthalate (CAP) is widely used in the pharmaceutical industry for enteric (acid-resistant) coatings. This chemical is insoluble in the acidic environment of the stomach but dissolves above pH6. Radiographic studies showed that CAP-coated gelatin capsules containing radio-opaque barium sulphate, force-fed to foxes, were able to withstand stomach conditions for at least five hours, and disintegrated rapidly after passage into the intestine (Figure 17a.1). Unfortunately, foxes fed capsules containing either live or inactivated lyophilized rabies vaccine failed to induce any measurable immunological responses (Maharaj, 1987). While this work was in progress, David Johnston and other members of the OMNRF Rabies Research Unit were testing different bait formulations. An early version consisted of 25 gram meatballs. Although CAP-coated capsules could be concealed within these baits, they were rejected in tests with captive foxes. The gelatin capsule approach was therefore abandoned in favour of a formulation that would be less easily detected by foxes in baits. After much experimentation, graduate student Indar Maharaj developed a rapid and simple method for preparing inactivated vaccine in quasi-spherical sucrose particles, one to three millimetres in diameter, embedded in CAP (Figure 17a.2) (Maharaj et al., 1986). These microspheres were stable under simulated stomach conditions and retained most of the Immunogenic activity of the original

Saponins Even when inactivated vaccines are given parenterally they generally require the addition of adjuvants to stimulate an effective immune response. Campbell turned his attention to finding a way to potentiate the weak responses of foxes observed when vaccine was introduced directly into the intestine. Of a number of immunostimulants tested, saponins (triterpenoid and steroidal glycosides) from the South American soap bark tree Quillaja saponaria were found to have the greatest promise (see Figure 17a.3). Quillaja saponins had already been used very effectively for decades in parenterally administered veterinary vaccines, such as for foot-and-mouth disease. Nevertheless, although potent immunostimulators, they were considered too cytotoxic for most vaccine applications, and their immunological activities by the oral route had not been investigated. Administered orally to mice along with inactivated rabies vaccine, however, Quillaja saponin preparations were found to be well tolerated at levels that markedly ­potentiated specific antibody responses and provided protection against lethal rabies challenge (Maharaj et al., 1986). This potentiating effect appeared to be mediated through several mechanisms, including inhibition of digestive enzyme activity and increased permeability of the intestinal mucosa, thereby permitting increased uptake of the viral antigen. The effect was enhanced when the saponins were given in advance (up to at least 16 hours) of the oral vaccine. These encouraging results led to a more detailed investigation on the immunostimulatory mechanisms of saponins by Siva Chavali, a post-doc in Campbell’s laboratory, resulting in a series of publications (Chavali & Campbell, 1987a, 1987b; Chavali et al., 1987; Chavali et al., 1988; Campbell & Chavali, 1989; Campbell, 1995). Results showed that Quillaja saponins administered orally to mice stimulated a

Figure 17a.1: Twenty CAP-coated barium sulphate capsules in the intestine of a fox, 5 hours 20 minutes post-feeding. Two intact capsules are still in the stomach: the remaining 18 have passed into the duodenum and disintegrated. Source: OMNRF.

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Figure 17a.2: Left, ­CAP-sucrose microspheres; right, H&E stained section of part of two microspheres showing the CAP matrix and the pockets that ­contained sucrose/vaccine. Source: J. Campbell.

inactivated vaccine were promising, would further research have been justified? Again the answer is no. Even if foxes had been induced to respond effectively when fed inactivated vaccine baits with saponin, the large amounts of antigen required per dose would probably have made their manufacture economically impracticable. Perhaps with today’s technology using, for example, DNA vaccines, there might have been more of a chance. But by the mid-1980s, when concerns about live vaccine safety had become less of an issue, live vaccines presented a much more attractive alternative. Was this research time wasted? Not at all! The early studies on saponins as oral adjuvants were intellectually rewarding and may have contributed to an increasing awareness of the potential value of these naturally occurring compounds in the development of mucosally targeted vaccines ­(Pickering et al., 2006).

Figure 17a.3: Common basic structure for Quillaja saponins. R and R’ = H or an oligosaccharide. Source: authors.

significant increase in lymphocyte proliferation in vivo and promoted helper (Th) cell and B-cell cooperation, resulting in markedly increased antibody production. Natural killer cell activity in mice fed saponins alone was greatly enhanced and persisted for an extended time, with induction of active soluble factors (presumably cytokines).

Adenovirus Recombinant Rabies Vaccine Considerations

Discussion

Although Prevec had worked with rhabdoviruses since 1959, the circumstances that led to his involvement in the development of an adenovirus-rabies recombinant were determined in large part by two relatively unrelated yet essential circumstances. The first of these, and by far the most important, was the fact that Frank Graham, the scientist who developed the calcium technique for introducing DNA into mammalian cells (Graham & van de Eb, 1973) and subsequently used this technique to produce the 293 cell line ­(Graham et al., 1977), was a friend and worked in the same laboratory. The 293 cell line, which is derived from human kidney cells, carries that portion of human adenovirus type 5 (Ad5) DNA which is responsible for expressing the E1 (early r­ egion 1) (Figure 17a.4) genes. This cell line not only allows growth

The above mouse studies were not extended to include foxes. Successive European field trials to control rabies in wildlife during the 1980s had shown the feasibility of this approach and had provided reassurance about the safety of using live rabies vaccines (Wandeler, 1988). The R ­ abies ­Advisory ­Committee directing the Ontario program decided to terminate work on inactivated vaccines and to follow the lead of the European groups by developing live vaccine baiting systems. With the termination of the inactivated vaccine research, questions remained. Did the five or six years spent on it accomplish anything? In terms of development of a practicable vaccine-bait system, the answer is clearly no. Given that the mouse studies using saponin as an adjuvant for an oral

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glycoprotein Prevec expressed within an Ad5 recombinant was the G protein of VSV. A student in his laboratory, Mary Schneider, rescued the G gene into the E3 region of Ad5 (Schneider et  al., 1989). To determine the role of exogenous promoters on the expression of this gene, Schneider ­inserted the G gene between a herpesvirus thymidine ­kinase (TK) promoter and its polyA addition sequence and then, using the Graham technology, inserted this cassette in both orientations in the Ad5 E3 region. Subsequent infection of HeLa cells with these recombinants demonstrated that, while the exogenous TK promoter was functional in this situation, readily detectable amounts of VSV glycoprotein were synthesized only when the G gene was inserted in an E3 parallel orientation. This, coupled with the fact that synthesis of this protein was unaffected by a DNA synthesis inhibitor, suggested that synthesis was driven by the E3 promoter. With the assistance of Brian Derbyshire in Guelph and Ken Rosenthal at McMaster, Prevec showed that immunization of mice (intraperitoneal), calves (intranasal or subcutaneous), pigs (intranasal or subcutaneous), and dogs (intranasal or subcutaneous) with the E3 parallel Ad-VSV G recombinant, produced good levels of VSV neutralizing antibodies (Prevec et  al., 1989). This gave them the confidence that the Ad-recombinant approach might be useful for more clinically significant vaccine purposes. Through his contact with Jim Campbell, Prevec learned of the Rabies Advisory Committee that had been set up in ­Ontario. Steve Smith, who chaired that committee, was ­invited to give a seminar at McMaster and his enthusiasm and ­encouragement played a significant part in getting the authors committed to the wildlife rabies vaccine project. Through Jim Campbell, Prevec arranged to get a rabies glycoprotein gene for insertion into an Ad5 vector.

Figure 17a.4: Transcription regions of Ad5. This figure shows the four early transcription regions (prior to viral DNA ­synthesis), E1, E2, E3, and E4. The major late promoter (MLP) drives late transcription across the region shown. Transcription of ­foreign gene inserts which replace the E3 structural genes may be driven by exogenous promoters or by E3 or ML promoters. Source: authors.

of Ad5 mutants from which the E1 region has been altered or deleted but also serves as a better substrate for the growth of adenoviruses than many other available human cell lines. When Martha Ruben in his laboratory discovered that circular forms of virus DNA were produced in some infected cell lines, Frank Graham cloned these in bacterial cells and isolated some that were infectious (Graham, 1984). Starting with these infectious adenovirus circles into which a bacterial plasmid had been inserted, Graham and his department produced a series of shuttle plasmids that could be used to create recombinant adenovirus that carried other foreign genes (Bett et  al., 1994; Graham & ­Prevec, 1995). Foreign genes could be inserted in place of the non-essential E3 region of Ad5 to produce replication competent Ad5-recombinant viruses, or they could be inserted in place of the E1 region of Ad5 to produce Ad5-recombinants which could only be grown on 293 cells or their equivalent. Since the Ad5 recombinant of current interest is a replication competent E3 insert, Prevec confined his description to that category though many E1 insertion rabies recombinants have been produced both by his laboratory and by others. The second important factor in this enterprise was the fact that Prevec had spent two years at the Wistar Institute in Philadelphia working next to Tad Wiktor’s rabies virus group. Though Prevec had worked on reovirus with A ­ ngus Graham, Wiktor’s group included Jim Campbell. When Prevec moved to McMaster, Campbell subsequently came to Toronto to continue his work on rabies. By the time Prevec became interested in this project, Campbell was ­actively involved in the Ontario rabies control program; his friendship and collaboration were invaluable to the success with the Ad-rabies recombinant.

Ad5-Rabies Recombinant The first useful Ad5-rabies recombinant made was AdRG1, which contained the rabies glycoprotein gene b ­ etween an SV40 early region promoter and polyA addition ­sequence in the E3 parallel orientation. With the help of Larry B ­ elbeck at McMaster to inoculate dogs (intranasal and subcutaneous) and mice (oral and intraperitoneal), and of Jim Campbell who assayed the sera and tested the r­ecombinant for protection against rabies infection in mice, ­Prevec was able to show the potential usefulness of this type of vector (Prevec et al., 1990). In collaboration with Ken Charlton, Alex Wandeler, their colleagues at Animal Diseases Research Institute (Nepean) and Jim Campbell, Prevec showed that AdRG1 could vaccinate skunks and foxes by the oral route

Adenovirus Recombinant Rabies Viral Studies With his background of 30 years working with rhabdoviruses, particularly vesicular stomatitis virus (VSV), the first

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(Charlton et al., 1992; see Chapter 18). Despite the success of AdRG1, Prevec was concerned by the fact that the level of rabies glycoprotein production by this vector in HeLa cells was difficult to detect. For this reason he sought to find a recombinant with a higher level of expression in vitro and possibly a better in vivo response at lower doses. All the vectors that had been constructed to this point were accompanied into the Ad5 E3 region by exogenous promoters and polyA addition sequences. Though many experiments with various genes had suggested that the most effective transcripts originated at adenovirus promoters, there was still the possibility that some exogenous sequence might at the very least act as a splice acceptor site to allow translation of the inserted foreign gene. Grace Martins in Prevec’s laboratory did some experiments with a beta-galactosidase reporter gene inserted in the E3 ­region to determine if expression was dependent on early or late adenovirus transcripts in permissive (human) and semi-permissive or non-permissive host species, such as bovine, canine, and mouse cells. Martins showed that Ad5 replicated less efficiently in bovine cells than in human and to very low levels in canine or mouse cells. Martins then went on to show that Ad DNA was produced not only in infected bovine cells but also to a lesser extent in canine cells and barely detectably in mouse cells (Martins, 1991). For a recombinant adenovirus to be a useful vaccine, the rabies gene must be expressed even in those species that are non-permissive for human adenovirus replication. Since it was known that the antigen was expressed in non-permissive mice, the authors were confident that many potential species, whether permissive or not, could be vaccinated with

this type of vector. Martins showed that the beta-galactosidase gene was expressed from both early and late adenovirus promoters in permissive human cells and from early adenovirus promoters in bovine, canine, and even mouse cells. Armed with this information, Prevec’s laboratory staff were confident that they could make a recombinant that would be useful at reasonable doses in a variety of host species. With Oksana Yarosh in his laboratory, Prevec designed an infectious adenovirus-rabies recombinant vector that carried as few exogenous sequences as they thought necessary and in which the rabies glycoprotein might be expressed to higher levels in vitro than was the case with AdRG1. To this end, all exogenous promoter sequences were deleted but retained the SV40 polyA addition sequence. They also altered the sequence around the rabies translation initiation site to conform to the consensus sequence defined by Kozak (1989). The resultant virus, AdRG1.3, had the desired property of producing readily detectable amounts of rabies glycoprotein in infected HeLa cells (Yarosh, 1996). With the assistance of Jim Campbell for the mouse studies and of Alex Wandeler for the skunk immunizations and analyses, Prevec clearly showed that AdRG1.3 was even more effective at inducing immunity in these target animals than AdRG1 had been (Yarosh, 1994). At this point further animal studies with the vectors were carried out by Alex Wandeler and his colleagues in Ottawa and by Artemis T ­ echnologies Inc. in Guelph. Some of these studies are presented in other chapters of this book (see Chapter 18). In 2008 Prevec and his colleagues were informed that Ontario had adopted AdRG1.3 as its vector of choice for the oral immunization of foxes, skunks, and raccoons and had renamed it ONRAB.

References Barton, L. D., & Campbell, J. B. (1988). Measurement of rabies-specific antibodies in carnivores by an enzyme-linked immunosorbent assay. Journal of Wildlife Diseases, 24(2), 246–258. https://doi.org/10.7589/0090-3558-24.2.246 Bett, A. J., Haddara, W., Prevec, L., & Graham, F. L. (1994). An efficient and flexible system for construction of adenovirus vectors with insertions or deletions in early regions 1 and 3. Proceedings of National Academy of Science, USA, 91(19), 8802–8806. https://doi .org/10.1073/pnas.91.19.8802 Campbell, J. B. (1994). Oral rabies immunization of wildlife and dogs: Challenges to the Americas. In E. Rupprecht, B. Dietzschold, & H. Koprowski (Eds.), Current topics in microbiology and immunology, vol. 187c. Lyssaviruses (pp. 245–266). New York: Springer Verlag. Campbell, J. B. (1995). Saponins. In D. E. S. Stewart-Tull (Ed.), Adjuvants: Theory and practical applications (pp. 95–127). Chichester, England: John Wiley. Campbell, J. B., & Barton, L. D. (1988). Serodiagnosis of rabies: Antibody tests. In J. B. Campbell & K. M. Charlton (Eds.), Rabies (pp. 223–241). Boston, MA: Kluwer Academic Publishers. Campbell, J. B., & Chavali, S. R. (1989). Saponins as oral immunopotentiators of rabies vaccines. In O. Thraenhart, H. Koprowski, K. Bögel, & P. Sureau (Eds.), Progress in rabies control (pp. 263–273). Royal Tunbridge Wells, England: Wells Medical.

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The Development of Vaccines and Delivery Systems Campbell, J. B., & Zhang, Y. (1993). Rabies virus infection: new vaccines and strategies in immunization. In E. Kurstak (Ed.), Control of virus diseases (2nd ed., pp. 267–305). New York: Marcel Dekker. Campbell, J. B., Maharaj, I., & Roith, J. (1985). In E. Kuwert, C. Mérieux, H. Koprowski, & H. Bögel (Eds.), Rabies in the tropics (pp. 285–293). Berlin, Germany: Springer Verlag. Charlton, K. M., Artois, M., Prevec, L., Campbell, J. B., Casey, G. A., Wandeler, A. I., & Armstrong, J. (1992). Oral rabies vaccination of skunks and foxes with a recombinant human adenovirus vaccine. Archives of Virology, 123(1–2), 169–179. https://doi.org/10.1007/BF01317147 Chavali, S. R., & Campbell, J. B. (1987a). Adjuvant effects of orally administered saponins on humoral and cellular immune responses in mice. Immunobiology, 174(3), 347–359. https://doi.org/10.1016/S0171-2985(87)80009-8 Chavali, S. R., & Campbell, J. B. (1987b). Immunomodulatory effects of orally administered saponins and nonspecific resistance against rabies infection. International Archives of Allergy and Applied Immunology, 84(2), 129–134. https://doi.org/10.1159/000234411 Chavali, S. R., Francis, T., & Campbell, J. B. (1987). An in vitro study of immunomodulatory effects of some saponins. International Journal of Immunopharmacology, 9(6), 675–683. https://doi.org/10.1016/0192-0561(87)90038-5 Chavali, S. R., Barton, L. D., & Campbell, J. B. (1988). Immunopotentiation by orally-administered Quillaja saponins: effects in mice vaccinated intraperitoneally against rabies. Clinical and Experimental Immunology, 74, 339–343. Graham, F. L. (1984). Covalently closed circles of human adenovirus DNA are infectious. EMBO Journal, 3(12), 2917–2922. https://doi .org/10.1002/j.1460-2075.1984.tb02232.x Graham, F. L., & Prevec, L. (1995). Methods for construction of adenovirus vectors. Molecular Biotechnology, 3(3), 207–220. https://doi .org/10.1007/BF02789331 Graham, F. L., & van der Eb, A. J. (1973). A new technique for the assay of infectivity of adenovirus 5 DNA. Virology, 52(2), 456–467. https://doi.org/10.1016/0042-6822(73)90341-3 Graham, F. L., Smiley, J., Russell, W. C., & Nairn, R. (1977). Characteristics of a human cell line transformed by DNA from human ­adenovirus type 5. Journal of General Virology, 36(1), 59–72. https://doi.org/10.1099/0022-1317-36-1-59 Kozak, M. (1989). The scanning model for translation: An update. Journal of Cell Biology, 108(2), 229–241. https://doi.org/10.1083/jcb.108.2.229 Lawson, K. F., Johnston, D. H., Patterson, J. M., Black, J. G., Rhodes, A. J., & Zalan, E. (1982). Immunization of foxes Vulpes vulpes by the oral and intramuscular routes with inactivated rabies vaccines. Canadian Journal of Comparative Medicine, 46, 382–385. ­Retrieved from https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1320299/ Lawson, K. H., Johnston, D. H., Patterson, J. M., Hertler, R., Campbell, J. B., & Rhodes, A. J. (1989). Immunization of foxes by the intestinal route using an inactivated rabies vaccine. Canadian Journal of Veterinary Research, 53, 56–61. MacInnes, C. D. (1988). Control of wildlife rabies: the Americas. In J. B. Campbell & K. M. Charlton (Eds.), Rabies (pp. 365–380). ­Boston, MA: Kluwer Academic Publishers. Maharaj, I. (1987). Oral immunization of wildlife against rabies by the oral route: Studies on delivery and potentiation of inactivated rabies antigen (Unpublished doctoral dissertation). University of Toronto, Ontario, Canada. Maharaj, I., Froh, K. J., & Campbell, J. B. (1986). Immune responses of mice to inactivated rabies vaccine administered orally: Potentiation by Quillaja saponin. Canadian Journal of Microbiology, 32(5), 414–420. https://doi.org/10.1139/m86-078 Martins, G. L. (1991). The ability of human adenovirus type 5 to replicate in MDBK, MDCK, HeLa and L cells (Master’s thesis, McMaster University). Retrieved from http://hdl.handle.net/11375/23136 Pickering, R. J., Smith, S. D., Strugnell, R. A., Wesseling, S. L., & Webster, D. E. (2006). Crude saponins improve the immune response to an oral plant-made measles vaccine. Vaccine, 24(2), 144–150. https://doi.org/10.1016/j.vaccine.2005.07.097 Prevec, L., Schneider, M., Rosenthal, K. L., Belbeck, L. W., Derbyshire, J. B., & Graham, F. L. (1989). Use of human adenovirus-based vectors for antigen expression in animals. Journal of General Virology, 70(2), 429–434. https://doi.org/10.1099/0022-1317-70-2-429 Prevec, L., Campbell, J. B., Christie, B. S., Belbeck, L., & Graham, F. L. (1990). A recombinant human adenovirus vaccine against rabies. Journal of Infectious Diseases, 161(1), 27–30. https://doi.org/10.1093/infdis/161.1.27 Rupprecht, C. E., Dietzschold, B., Campbell, J. B., Charlton, K. M., & Koprowski, H. (1992). Consideration of inactivated rabies vaccines as oral immunogens of wild carnivores. Journal of Wildlife Diseases, 28(4), 629–635. https://doi.org/10.7589/0090-3558-28.4.629 Schneider, M., Graham, F. L., & Prevec, L. (1989). Expression of the glycoprotein of vesicular stomatitis virus by infectious adenovirus vectors. Journal of General Virology, 70(2), 417–427. https://doi.org/10.1099/0022-1317-70-2-417 Wandler, A. I. (1988). Control of wildlife rabies: Europe. In J. B. Campbell & K. M. Charlton (Eds.), Rabies (pp. 365–380). Boston, MA: Kluwer Academic Publishers. Yarosh, O. K. (1994). Recombinant human adenovirus type 5 vaccine vectors expressing rhabdoviral glycoproteins (Doctoral dissertation, McMaster University). Retrieved from http://hdl.handle.net/11375/7887 Yarosh, O. K., Wandeler, A. I., Graham, F. L., Campbell, J. B., & Prevec, L. (1996). Human adenovirus type 5 vectors expressing rabies glycoprotein. Vaccine, 14(13), 1257–1264. https://doi.org/10.1016/S0264-410X(96)00012-6 Zalan, E., Wilson, C., & Pukitis, D. (1979). A microtest for the quantitation of rabies virus neutralizing antibodies. Journal of Biological Standardization, 7(3), 213–220. https://doi.org/10.1016/S0092-1157(79)80024-4

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17b Oral Vaccine Development in Canada BAIT DEVELOPMENT

Kenneth Lawson1 and Charles MacInnes2 1

Veterinary Research Section, Connaught Laboratories, and Wildlife Research Section, Ontario Ministry of Natural Resources (Deceased), Canada Supervisor, Research Section, Wildlife Branch, Division of Fisheries and Wildlife; Head of Rabies Unit, Ontario Ministry of Natural Resources and Forestry (Retired), Canada

2

Introduction Rabies spread by terrestrial wildlife was more prevalent in southern Ontario from the 1930s on than in any region of comparable size in North America. In 1968, a committee including members from the Ontario Ministries of Health, Agriculture and Food, and Natural Resources, and from Agriculture Canada, invited Connaught Laboratories to discuss means to reduce that problem. The committee explored the possibility of vaccinating foxes, skunks and raccoons to reduce human contact with rabies. The World Health Organization (WHO) also advocated that approach. Connaught had developed oral vaccines for poultry and swine (Lawson et  al., 1966), and there was cautious optimism that comparable means might be developed to reduce rabies in wildlife. The Ministry of Health funded a five-year project at Connaught to develop a vaccine that would immunize foxes against rabies and show that such a product was safe if humans and domestic or wild animals contacted it. In addition, the committee explored economical means to deliver such a vaccine to the three species most responsible for the spread of rabies in southern Ontario.

Vaccines, 1968 to 1973 Connaught was producing ERA, an attenuated live-virus rabies vaccine for pets and livestock, and that was therefore chosen to be the oral vaccine for foxes. Safety of the vaccine virus was established when foxes withstood inoculation of virus 10,000 times more potent than the commercial

vaccine without showing any signs of rabies. Experiments showed that vaccination by the oral route was possible, when vaccine virus administered by stomach tube protected six of six foxes against a lethal challenge. It required 100,000 times more virus by stomach tube than by the usual intramuscular injection. Successful vaccination occurred in the mouth when foxes were immunized by offering them a bait that consisted of freeze-dried rabies vaccine coated with attractant. The results of three challenge trials showed that 81% of animals consuming the bait were protected when only 21% of non-vaccinated (control) foxes survived. Many foxes (44%) fed a high titre freeze-dried vaccine bait were protected for two years against a lethal challenge.

Inactivated Rabies Virus, 1980 to 1984 In 1980 Ontario Ministry of Natural Resources (OMNR) funded Connaught for further research into the oral vaccination of wildlife against rabies. They formed the Rabies Advisory Committee (RAC) with members from various scientific disciplines to direct the research. RAC was initially reluctant to distribute a live virus rabies vaccine over populated countryside, so Connaught was directed to explore oral vaccination using inactivated virus. That work took place over four years, 1980–1984. Five inactivated vaccines were examined in detail. They were potency tested in guinea pigs, and there were no differences, so all were judged suitable for intramuscular use in foxes. These antigens were tested by the oral route: the inactivated vaccines, as well as positive and negative controls, were introduced into the duodenum of foxes by catheter. Vaccine delivered

The Development of Vaccines and Delivery Systems

to the intestines of foxes previously immunized by injection induced a response, but it was clear that inactivated vaccine would not perform well enough in the wild. Because of these poor immune responses, RAC chose to work with live virus vaccine.

were positive for rabies antibody. The sponge bait was sufficiently promising to deliver vaccine to foxes that Canadian and United States patents were secured for the invention. However, methods and machinery to mass produce the huge quantities required to cover southern Ontario posed many problems. Hence, research was directed towards producing a better vaccine container, the blister pack.

Vaccines, 1985 to 2006

The Blister Pack Bait

Plastic Envelope Coated with Sardine Oil

Use of the blister pack required a bait matrix that would stick to the plastic even when dropped from an aircraft. ­After testing 53 mixtures, a formula of animal fat and paraffin was selected. The fat was palatable to captive foxes, skunks, and raccoons, while the wax made the bait firm enough to bounce on impact during air drops and to be non-sticky so that baits could be mass-produced and ­packaged. Seven fragrances were evaluated on foxes, and a chicken stew essence proved best for attracting foxes. The vaccine was injected through the aluminum cover of a 20 × 20 × 10 millimetre plastic container, which was then sealed. The attractant, warm enough to be melted but not so hot as to damage the vaccine, was poured into 35 × 35 × 20 millimetre wells in a plastic tray. The plastic blisters were then hand-pushed into the middle of the fat formula. In 1987, 21,000 such baits were hand produced for field trial. Acceptance was 56% by foxes, 21% by skunks, and 29% by raccoons, values comparable to results from the sponge baits. Mass production of enough baits for actual control of rabies in the wild clearly required automation. Inoform Ltd. of Pickering was hired to design machinery for that purpose. Its final product consisted of two separate machines. The first made and filled the blister packs, working in a laminar flow chamber for human safety. There was concern that persons inhaling droplets of the live virus vaccine might be at risk. The machine thermo-formed into metal moulds sterilized 7.5 millilitre PVC plastic film from a large roll, injected a precise dose of vaccine into each, then sealed the blister packs with sterilized lidding (made of paper, plastic, and aluminum foil), and loaded the finished blisters into trays for transfer to the other machine (see Figure 17c.1, top, in Chapter 17c). The second machine placed an informative ­label into the bottom of a metal mould, poured the melted fat/wax/ attractant mixture on top, and then immersed the blister pack into the wax (see Figure 17c.1, bottom, in Chapter 17c). The ­labels bore a printed message (see Chapter 17c) to ­enhance the safety of any human who might pick up a bait.

The first live-virus bait was made by freeze-drying rabies vaccine, sealing a dose in a plastic envelope and coating that with sardine oil. That was attractive to laboratory foxes, but it would be costly to mass-produce and deliver by hand. Over subsequent years, several designs of a container for live vaccine were tested. The necessary production sequence was to make the container, fill it with a dose of vaccine, seal it, and then coat it with an attractant for foxes and skunks.

Sponge Bait The first test using ERA used a 40 millimetre cube of polyurethane sponge, coated several times with a mixture of tallow, paraffin, attractant, and tetracycline (Plate 6). Components other than the vaccine were sterilized by irradiation. Commercial ERA (14 millilitres, titre 105.3–106.1 MICLD50 per millilitre), or a placebo, was injected into the sponge. The hole was sealed with melted coating mixture. In 1984, 13,000 handmade placebo sponge baits, hand spread on a 10 kilometre square of farm and woodland resulted in 53% of foxes, 38% of skunks, and 29% of raccoons having tetracycline in their teeth, indicating they had eaten a bait. That experiment was duplicated in 1985 to test the efficacy of 14 millilitres of liquid ERA. The baits (13,500) were spread by hand on an area similar to the previous trial. Tetracycline markers indicated that 64% of foxes, 33% of skunks, and 43% of raccoons ate baits. Antibody results were poor, so that a higher vaccine titre was needed to protect wild foxes from rabies. During 1985–1986 the ERA ­virus was adapted to a BHK21/C13 cell line, which produced titres of 107.8–108.0 MICLD50 per millilitre, which was 2 log10 higher than commercial ERA. The stronger vaccine was tested for safety in foxes, raccoons, skunks, cattle, dogs, and cats. In 1986, 15,326 sponge baits containing the stronger virus (ERABHK/C13) were spread for field trial. Acceptance of the bait by foxes was 55% and by skunks 25%. Among foxes whose teeth had tetracycline markings, 53%

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baits dropped at a density of 100/km2 (Rosatte & Lawson, 2001) so that became the bait of choice for raccoons. From 1994 to 1997 the SV formula was field tested alongside the chicken-cod bait for fox acceptance, and from 1998 on SV was the attractant for the fox program, with overall acceptance of 72% (Bachmann et al., 2005).

The moulds containing the blister packs progressed through cooling chambers to solidify the bait wax, then the baits were ejected as 35 × 35 × 15–17 millimetre cubes, weighing 17–19 grams each. These were placed into specially designed cartons and quick frozen to be stored at −30°C. In 1988, 46,213 baits were produced for in-house studies of vaccine stability and their effectiveness for ­immunizing foxes. Some baits were subjected to extreme conditions, such as in full sun for 21 days. The mean ambient temperature for that period was 7.2°C while that of the bait was 9.5°C. During that time, the vaccine lost 0.6 log10 of potency but was still able to produce antibody in 75% of foxes that had consumed a single bait. The 1989 field trial in eastern Ontario employed 400,000 baits. Almost 52% of fox teeth had tetracycline marks, and half of those foxes had rabies antibody. The next year, 787,000 baits were air-dropped over 26,500 km2 of eastern Ontario. Fox acceptance was 65%, and 61% of those had antibody. The viability of vaccine in the baits was evaluated in the wild from 1989 to 1996. The virus was relatively stable, losing only 0.5 log10 of its titre in the first 28 days. More than half (63%) of foxes fed baits (titre 106.2 TCID50/mL) that had been exposed to sun and shade for 21 days developed RVNA (antibody) (Lawson and B ­ ­ achmann, 2001). Foxes vaccinated using ERA in the Ontario bait were challenged after 83 months, and 10/11 (91%) ­resisted the challenge, which killed all six non-vaccinated foxes (Lawson et  al. 1997). That showed that the Ontario ­ ­vaccine-bait had good stability in the field and protected foxes against rabies for at least seven years. In 1991 the two bait machines were capable of producing one million vaccine baits annually. Production was moved from ­Connaught to Langford Laboratories Ltd., and later transferred to Artemis Technologies Inc. (see Chapter 17c). Although the 1991 bait was accepted by, on average, 70% (52%–82%) of foxes over the following 16 years (Bachmann et al., 2005), acceptance by skunks and raccoons was only 35% and 25%, respectively (Bachmann et al., 1990). From 1992 to 1998 OMNR searched for a bait mixture that attracted more raccoons, especially in urban habitats. Many mixtures (43) were tested in Toronto and suburbs. The raccoons outright rejected 19, including the chicken-cod fox bait, and tests of the other attractants for compatibility with the production machines resulted in 18 of 24 being discarded. In 1993 six attractants in the basic fat/wax fox bait were tested for a­ cceptance by captive and wild raccoons. The best two were a sugar-vanilla (SV) and a cheese (CH) bait (Rosatte et  al., 1998), and the SV bait proved easier to mass-produce. In 1994, 58% of raccoons took SV

Ontario Slim Bait Raccoons frequently consumed the bait coating but left the blister pack undamaged. Addition of a flocking substance to the blister pack improved bait adhesion and reduced both the size and the weight of the bait (35 × 35 × 10 mm and 14 grams). This product was named the Ontario Slim (OS) (see Chapter 17c). It was cleaner to handle in the ­aircraft and, because of its smaller size and weight, more baits could be carried per flight. In 1996 an aerial drop to compare the OS and SV baits showed that 58% of raccoons took the OS but only 39% ate the older SV bait (Rosatte et al., 1998). We tested nine plastics of different gauge and type to find one that raccoons would easily puncture. A more fragile blister pack should deliver more fluid vaccine to the raccoon when chewed. The final choice was polystyrene (Rosatte & Lawson, 2001). In 2000 the OS bait replaced the older fox bait because it was also eaten by 68% of foxes, as well as being more effective in raccoons (­Bachmann et al., 2005).

The Ultralite Bait From 1999 to 2004, a concerted effort was made to vaccinate more skunks. The SV attractant was less accepted by skunks than by raccoons. Addition of International F ­ lavors & Fragrances sugar sweetener to the SV formula improved uptake by skunks. On-site and video observations of skunks eating the raccoon bait showed that it was too large and had too much fat-wax matrix. The best skunk bait that was most compatible with major changes to the bait machinery and blister pack materials was one 40 × 20 × 10 millimetres and weighing 4 grams. This ultralite (UL) bait was ­attractive to foxes and raccoons, as well as to skunks (Rosatte et al., 2009). The UL bait with ERA vaccine became the bait of choice for elimination of rabies from all three species. Since the ERA vaccine used for fox vaccination was not as effective in stimulating suitable antibody levels in skunks and raccoons, a recombinant vaccine was adopted for all three. The development and use of that vaccine is described in Chapters 17a and 17c.

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References Bachmann, P., Bramwell, R.N., Fraser, S. J., Gilmore, D. A., Johnston, D. H., Lawson, K. F., ... Voigt, D. R. (1990). Wild carnivore ­acceptance of baits for delivery of liquid rabies vaccine. Journal of Wildlife Diseases, 26(4), 486–501. https://doi.org/10.7589/0090 -3558-26.4.486 Bachmann, P., Bennett, K., Brown, L., Donovan, D., et al. (2005). The path to controlling and eliminating arctic rabies virus variant in Ontario, Canada. In The XV1 International Conference, Rabies in the Americas. Ottawa, ON: CFIA. Lawson, K. F., & Bachmann, P. (2001). Stability of attenuated live virus rabies vaccine in baits targeted to wild foxes under operational conditions. Canadian Veterinary Journal, 42(5), 368–374. Retrieved from https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1476515 /pdf/canvetj00005-0044.pdf Lawson, K. F., Pepevnik, F., Walker, V. C. R., & Crawley, J. F. (1966). Vaccination of swine with erysipelas vaccine (live cultured-modified) by the oral route. Canadian Veterinary Journal, 7(1), 13–17. Lawson, K. F., Chiu, H., Crosgrey, S. J., Matson, M., Casey, G. A., & Campbell, J. B. (1997). Duration of immunity in foxes vaccinated orally with ERA vaccine in a bait. Canadian Journal of Veterinary Research, 61, 39–42. Retrieved from https://www.ncbi.nlm.nih.gov /pmc/articles/PMC1189367/ Rosatte, R. C., & Lawson, K. F. (2001). Acceptance of baits for delivery of oral rabies vaccine to raccoons. Journal of Wildlife Diseases, 37(4), 730–379. https://doi.org/10.7589/0090-3558-37.4.730 Rosatte, R. C., Lawson, K. F., & MacInnes, C. D. (1998). Development of baits to deliver oral rabies vaccine to raccoons in Ontario. Journal of Wildlife Diseases, 34(3), 647–652. https://doi.org/10.7589/0090-3558-34.3.647 Rosatte, R. C., Donovan, D., Davies, J. C., Allan, M., Bachmann, P., Stevenson, B., ... Lawson, K. (2009). Aerial distribution of ONRAB¯ baits as a tactic to control rabies in raccoons and striped skunks in Ontario, Canada. Journal of Wildlife Diseases, 45(2), 363–374. https://doi.org/10.7589/0090-3558-45.2.363

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17c Oral Vaccine Development in Canada BAIT PRODUCTION

Artemis Technologies Inc. Guelph, Ontario, Canada

Introduction Chapters 17a and 17b described the science and development of the baits and the vaccines used in Ontario’s development of the Oravax vaccination rabies control program. This chapter provides further details of this development as the province moved towards mass production of baits and the ultimate adoption of the ONRAB bait – a bait that has proven its effectiveness in the field for the immunization of foxes, skunks, and raccoons and has been a major contribution to the success of Oravax rabies control programs in Ontario, Quebec, and New Brunswick. The chapter also highlights the contributions of Artemis Technologies Inc., a Canadian company based in Guelph, towards the mass production of baits and the successful development of the ONRAB bait.

Bait Production and Design As Chapter 17b relates, in 1968 the Ontario Inter-Ministerial Committee on Rabies invited Connaught Laboratories to discuss the problem of rabies in Ontario. The resulting discussions led to a five-year contract with Connaught Laboratories Limited (funded though the Ontario Ministry of Health) to identify a vaccine that could be safely used to immunize foxes against rabies and to find a method of administering that vaccine to foxes. This work led to a long association of Connaught Laboratories with the development of rabies control programs in Ontario. As the

organization of Connaught changed, key personnel associated with Connaught went on to work with other companies to develop vaccines and delivery systems. The details of the testing and selection of candidate vaccines are dealt with in Chapters 15a and 18. Initially, ERA was selected as the most appropriate vaccine for the oral vaccination of foxes. It was incorporated into several different baits that were produced by the various companies contracted to work with the Ontario Ministry of Natural Resources (OMNR). Over time, the practical concerns of attracting target animals, ensuring that they ingested most of the vaccine in the baits and increasing the payload on a baiting flight (see Chapter 19) meant that the composition and size of baits changed. Table 17c.1 lists those changes and the companies involved with vaccine development, bait design, and production. The remainder of this chapter describes the contributions of the companies listed in Table 17c.1 and notes the people who were crucial to those contributions.

Connaught Laboratories and Bait Production Chapter 17b detailed Connaught’s contributions to vaccine development and bait design. Connaught was also involved in bait production. Initially, the baits required for field trials were produced by hand. The team at Connaught was able to produce 21,000 blister packs over five months for field trials in 1987. This labour-intensive method highlighted the need for automation in the bait-making process. In 1988 a prototype bait machinery was designed by Derek Mancini in cooperation with Ken Lawson (Connaught)

The Development of Vaccines and Delivery Systems

Table 17c.1  The evolution of the Ontario bait in terms of composition and size. Year

Composition

Bait Name (Produced by)

Weight of Bait

1976–1977

Plastic bag with 50 g ground beef

>50 g

1985

Wax covered sponge wrapped in ground beef

1985–1986

Wax covered sponge cube fish oil and artificial chicken stew flavour Wax covered rectangular PVC blister pack fish oil & artificial chicken stew flavour Wax covered rectangular PVC blister pack icing sugar/marshmallow flavour

– (Connaught) – (Connaught) Sponge bait (Connaught) Ontario bait (Connaught/Langford/Artemis) Ontario bait Ontario Slim bait (Artemis) Ultralite bait (Artemis)

1987–1998 1999–2007

2006–present

Wax covered elongated PVC blister pack icing sugar/marshmallow/sweet flavour

>30 g 8–12 g 16–18 g 16–18 g 12–13 g 4g

and was rushed into service to meet the production schedule for the first bait drop in 1989. The machinery comprised two pieces of equipment: the unit dose machine, which formed the blister packs to contain the vaccine, and a bait machine to embed the blister pack in the bait matrix (Figure 17c.1). This equipment produced approximately 390,000 blister pack baits (Plate 7). Mancini’s company also produced the machinery used in the aircraft for aerial bait distribution (see Chapter 19). By 1990 Connaught Laboratories opted to withdraw from the production of rabies baits. A new partner for the project was found in Langford Laboratories, and a dedicated production suite was included as part of its Guelph facility expansion. The production of ERA vaccine and baits was transferred from Connaught to Langford in 1991.

Langford Laboratories/Langford Cyanamid Bait production in 1991 was an intensive operation with 10to 12-hour days and output fluctuating between 10,000 and 18,000 baits per day. That year, Langford produced 46 batches averaging 16,000 per batch (736,000 total). Blister packs were filled with vaccine on one day and embedded in bait matrix the following day. The initial runs highlighted some unanticipated production issues. The bait production machinery was prone to jamming and there are stories about Ken Lawson remedying problems with a well-placed hammer blow. Although Mancini attempted modifications, the situation became unworkable, partly because Lawson was based in Toronto and the production equipment was in Guelph. A large part of the problem was that the prototype equipment had been pressed into service without any testing under typical production conditions. In 1992 Jefdin Enterprises assumed responsibility for maintenance of the equipment as part of a contract with Langford for overall plant maintenance.

Figure 17c.1: Bottom, “Norman” machine to produce baits; top, machine to imbed blister pack in the bait matrix. Source: OMNR.

Process improvement was limited to minor adjustments to the machinery to allow production to continue. In 1994 Langford Cyanamid was acquired by A ­ merican Home Products and became Ayerst Veterinary L ­ aboratories.

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All vaccine production, except for rabies baits production, was transferred to Fort Dodge Animal Health, Iowa. Bait production continued at the Guelph facility until the end of the Langford contract with OMNR in 1997.

Experienced staff retained from Langford C ­ yanamid compressed a year’s worth of production (1.17 million baits) into three months to have product ready to ship in September for the OMNR’s autumn baiting campaign. Artemis Technologies continues to be the sole supplier of baits for the OMNR Rabies Control Program and partners with the OMNR on vaccine and bait research and development. In 1991 the Ontario bait weighed about 18 grams. By 1999 improvements to the blister pack and labelling had reduced the weight of the new Ontario Slim to 13 grams (Plate 8). Since the top surface of the Slim was not coated, the lidding of the blister pack became the label. The bait machine that Artemis staff fondly referred to as “Norman” was redesigned to keep the blister packs face down during coating and, therefore, keep the bait matrix from covering the label (Figure 17c.3). Ontario Slim baits were

Artemis Technologies Inc. Artemis Technologies was established in August 1997 by Andrew Beresford, who had been Viral Vaccines ­Production Manager at Langford Cyanamid, and Alex Beath, the owner of Jefdin Enterprises. Both men believed that they could successfully continue the production of rabies baits as a new small business. In 1997 OMNR posted a Request for Quote and Artemis Technologies placed a bid. The contract was awarded to them in September 1997. Beresford’s last day on the job at Ayerst was 25 September – 15 years after he had joined Langford. The name Artemis Technologies was chosen in honour of the Greek goddess Artemis, the daughter of Zeus and the twin sister of Apollo, who was the protector of wild animals and wilderness. Acquisition of premises for Artemis was the first priority. Leasing a building was not an option as the requirements of a vaccine production facility demanded too many changes to a building to satisfy a lease holder. The possibility of new construction was explored, but then a contact suggested an existing building that met the space requirements and was available immediately. Purchase and possession of 51 Watson Road South on the eastern edge of Guelph took place in October 1997 (Figure 17c.2). Its most recent use had been as a metal stamping company, and extensive clean-up was required before it could be reincarnated as a vaccine production facility. The design and installation of production suites and quality control laboratories, and subsequent inspection and licensing by the Canadian Food Inspection Agency was completed by May 1998. Beresford and Beath acted as their own contractors and did a considerable amount of the work themselves.

Figure 17c.3: View of the redesigned “Norman,” to keep the bait matrix from covering the label of the Ontario Slim baits.

Figure 17c.2: Artemis Technologies Inc., 51 Watson Road South, Guelph, Ontario (2015).

Source: OMNR.

Source: OMNR.

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The Development of Vaccines and Delivery Systems

distributed until 2007. Interior space limitations in the bait distribution aircraft (Chapter 19) and flight weight restrictions effectively limited flying time carrying the Ontario baits (packed 1240 per box) to less than three hours. The O ­ ntario Slims were packed 1728 per box and the corresponding reduction in weight allowed four-hour flights – about the limit of ­operator endurance in the back of the aircraft. Another significant change has been in the attractant incorporated into the bait matrix. The Ontario baits used a chicken stew/fish oil attractant whose smell affected production staff and air crews alike. An icing sugar/marshmallow bait was tested north of Toronto in 1996 (170,000) and 1997 (350,000) (see Chapter 17b). These new attractants appealed to the target animals and were much more acceptable to both production staff and aircraft crews. Marshmallow/icing sugar replaced the chicken stew/fish oil as attractant in 1998. In 2006 OMNR conducted the first field trial of the ultralite bait composed of vaccine in a PVC blister coated with an attractant (Plate 9). The ultralite bait also incorporated the use of the new ONRAB vaccine. The impetus for this bait was twofold: (1) to make the bait more effective at delivering the vaccine to skunks who could more easily manipulate it in their small mouths and (2) to reduce weight. The introduction of the ultralite required a new method of coating the blisters. The original coating machine (­“Norman”) was no longer suitable and rather than try to adapt it to the new process, Artemis designed and built an enrober (Plate 4) – a machine typically used in the confectionery industry to coat (enrobe) an item with a coating medium such as chocolate. The enrober has a current capacity of approximately 65,000 baits per run. A ­ rtemis ­Technologies has also produced baits for use in N ­ ewfoundland and Labrador, New B ­ runswick, and Quebec.

The Vaccines Over time the baiting program has used three different vaccines as target species changed from foxes to raccoons to skunks.

ERA Extensive research at Connaught Laboratories had determined that live attenuated ERA vaccine was effective for immunization of foxes by the oral route. ERA was used by Connaught initially in the sponge bait and Ontario bait, and subsequently by Langford Laboratories and Artemis Technologies in the Ontario bait and Ontario Slim bait. ERA was distributed in Ontario from 1989 to 2008.

V-RG In 1999 the first cases of the mid-Atlantic strain of raccoon rabies occurred in Ontario. In addition to point infection control and trap-vaccinate-release as a response, OMNR implemented the use of rabies vaccine, live vaccinia ­vector (RM RABORAL V-RG, Merial) as part of its control program. Bulk V-RG vaccine manufactured by Merial was filled into ­Ontario baits and Ontario Slim baits at Artemis ­Technologies. V-RG was distributed in Ontario between 1999 and 2003.

ONRAB In Ontario the primary terrestrial vectors of rabies have been red foxes and striped skunks carrying the arctic fox strain, and raccoons carrying the mid-Atlantic raccoon strain. The development of the ONRAB vaccine (using an adenovirus vector AdRG1.3) and the ultralite bait has been a major step forward in achieving the holy grail of rabies control: an effective vaccine against both strains in a bait that is attractive to all species. The development of the adenovirus construct AdRG1.3 was done at McMaster University by Drs Ludvik Prevec and Oksana Yarosh (see Chapter 17b). S­ ubsequent establishment and testing of the cell line and ­virus master seed was done by Microbix Biosystems Inc. ­under contract by OMNR. In 1999 the project was transferred to Artemis Technologies. Beginning in 2001 and in collaboration with Canadian Food Inspection Agency (CFIA) and the Rabies Centre of Expertise (RCofE) in Ottawa, the production of virus standards and development of an infectivity assay was completed, along

Evolution of the Ontario Rabies Bait As shown in Table 17c.1, the shape of the bait and the composition of the attractants have evolved over the years in response to requests from OMNR for improved acceptance in target species and ease of handling on board the bait distribution aircraft, as well as part of the ongoing development by Artemis Technologies to streamline the production process. Changes to the shape of the blister pack and bait have necessitated changes in the Mancini prototype bait machinery and, ultimately, its replacement.

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Bait Production

with real-time virus stability trials. Plate 5 and Figure 17c.4 show the equipment used for the production of ONRAB vaccine at Artemis. In 2004 a dose response trial in captive skunks was conducted by the Rabies Centre of Expertise to determine the effective dose of AdRG1.3 in skunks. A vaccination challenge trial in skunks was completed in 2005 but was unfortunately invalid as an insufficient number of control animals succumbed to challenge. A second vaccination challenge trial in skunks was completed in 2006 with 100% protection of animals presented with the ONRAB bait and 86% of control animals succumbing to challenge. During 2005–2006, and concurrent with the vaccination challenge trials, target and ­non-target ­animal overdose safety tests were conducted at CFIA/ RCofE with no ­reported adverse events and minimal amounts of ­residual ­virus detected. These positive ­results produced the decision to pursue field testing of the vaccine and bait. In 2006 the Biotechnology Research Institute (BRI) at the National Research Council of Canada (NRC) in Montreal was approached to provide expertise in the process of scaling up AdRG1.3 virus production from pilot scale to production scale batches. The cell ­culture optimization work by Dr Amine Kamen, Dr Chun Fang Shen, and the team at NRC-BRI resulted in the ­production of 17,000 litres of bulk virus (2006–2011) and demonstrated that the virus could

be produced on a commercial scale in a c­ ost-effective manner. Bulk ­virus produced at NRC-BRI for use in field trial baits was shipped to Artemis Technologies to be quality control tested and then blended into ONRAB ­vaccine and filled into ultralite baits.

Field Trials of ONRAB Ontario Field Trial, 2006 In 2006 a field trial was undertaken to determine if aerially distributed ultralite baits containing AdRG1.3 successfully elicited an antibody response to the vaccine in wild ­populations of skunks and raccoons. Baits containing a blister pack with 1.8 millilitre volume of AdRG1.3 with a titre not less than 109.5 CCID50/mL were aerially distributed in portions of Dufferin and Grey counties in southwestern ­Ontario. Baits were distributed at two different densities: 150 baits/km2 and 300 baits/km2. A total of 195,885 baits were distributed in the four experimental plots. Bait acceptance was determined by the presence of tetracycline in tooth sections (see Chapter 24c). Rabies antibody in serum was determined by the cELISA test at the CFIA Ottawa Laboratory Fallowfield (OLF). A total of 841 raccoons (Procyon lotor), and 541 striped skunks (Mephitis mephitis) were live-trapped, and samples

Figure 17c.4: Artemis ­owners Andrew Beresford (left) and ­Alexander Beath (right) ­prepare for regulatory inspection in 2012. Source: Dr D. Gregory

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The Development of Vaccines and Delivery Systems

were collected in the study area 18–29 September 2006. Bait acceptance averaged 32% for skunks (using canine teeth), and 72% for raccoons (using second premolar teeth) in areas baited at 150 and 300 baits/km2. For skunks, rabies antibody in serum, based on cELISA inhibition of 16% or greater, averaged 31% (169/541) in all baited areas. For raccoons, rabies antibody in serum, based on cELISA inhibition of 16% or greater, averaged 74% (620/841) in all baited areas. No adverse reactions, morbidity, or mortality were observed.

presence of tetracycline in tooth sections averaged 78.7% for raccoons in areas baited at 75 and 400 baits/km2.

Ontario Field Trial, 2008 In 2008 a field trial study was undertaken using aerially distributed ultralite baits containing AdRG1.3. The baits containing a blister pack with 1.8 ml of AdRG1.3 with a t­itre not less than 109.5 CCID50/mL were aerially ­distributed. A  total of 516,375 baits were distributed over an area of 2574 km2 in portions of Dufferin, Grey, and Wellington counties in southwestern Ontario. Five to seven weeks after bait distribution, 205 striped skunks (Mephitis mephitis) were live-trapped, and blood samples were collected from 163 individuals and second pre-molar teeth from 156 individuals during September and October. Bait acceptance was determined by the presence of tetracycline in tooth sections. Rabies antibody in serum was determined by the cELISA test at CFIA, OLF. The antibody results for skunks using a cELISA titre of ≥16% as a positive antibody response indicates there were 95/163 animals positive (59.5%). No adverse reactions, morbidity, or mortality attributable to the vaccine was observed.

Ontario Field Trial, 2007 In 2007 a field trial was undertaken using aerially distributed ultralite baits containing AdRG1.3. A total of 357,265 baits were distributed in the six experimental plots at two different densities – 75 baits/km2 and 400 baits/km2. The baits containing a blister pack with 1.8 millilitres of AdRG1.3 with a titre not less than 109.5 CCID50/mL were aerially distributed in portions of Dufferin, Grey, and ­Wellington counties in southwestern Ontario. Five to seven weeks after bait distribution, 1424 raccoons (Procyon lotor), 612 striped skunks (Mephitis mephitis), and two red foxes (Vulpes vulpes) were live-trapped and samples collected 17–28 September 2007. Bait acceptance was ­determined by the presence of tetracycline in tooth sections. Bait acceptance as determined by presence of tetracycline in tooth sections averaged 38.3% (106/277) for skunks in areas baited at 75 baits/km2 and 49.6% (124/250) for skunks in areas baited at 400 baits/km2. Mean bait acceptance was 43.6% for skunks in areas baited at 75 and 400 baits/km2. Rabies antibody in serum was determined by the cELISA test at CFIA, OLF. The antibody results for skunks using a cELISA titre of ≥16% as a positive antibody response indicates 140/290 animals were positive (48.3%) at 75 baits/km2 and 131/268 animals positive (48.9%) at 400 baits/km2. No adverse reactions, morbidity, or mortality attributable to the vaccine were observed. The antibody results for raccoons using a cELISA titre of ≥16% as a positive antibody response indicates 297/363 animals were positive (81.8%) at 75 baits/ km2 and 287/332 animals positive (86.4%) at 400 baits/km2. No adverse reactions, morbidity, or mortality attributable to the vaccine was observed. Bait acceptance as determined by the presence of tetracycline in tooth sections averaged 66.9% (236/353) for raccoons in areas baited at 75 baits/ km2 and 85.6% (268/313) for raccoons in areas baited at 400 baits/km2. Mean bait acceptance as determined by the

Quebec Field Trial, 2007 In August 2007 a total of 120,000 rabies vaccine, live ­adenovirus vector (AdRG1.3) vaccine baits were distributed at a density of approximately 150 baits/km2 over an area of ­approximately 1016 km2. The baits were distributed with two Twin Otters airplanes from the OMNR. Flight lines were spaced by 750 metres. A post-bait distribution study was conducted in ­September and October 2007. Bait acceptance as ­determined by the presence of tetracycline in tooth sections was 28.2% (44/156). The marking of second pre-molar teeth in skunks is known to be inconsistent and because of the small tooth size difficult to section and read. Blood samples were collected from a total of 697 r­ accoons and 119 striped skunks, and rabies antibody in s­ erum was determined by the cELISA test at CFIA, OLF. The antibody results for skunks using a cELISA titre of ≥16% as a positive antibody response indicates there were 41/117 animals positive (35.0%). No adverse reactions, morbidity, or mortality attributable to the vaccine were observed. The ­antibody results for raccoons using a cELISA titre of ≥16% as a positive antibody response indicates 595/634 animals were positive (93.8%). No adverse reactions, morbidity, or mortality attributable to the vaccine were observed.

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ONRAB baits. In 2014 there were no reported rabies cases in terrestrial animals in Ontario and, in 2016, only one rabid fox was reported in Quebec (see Chapters 10 and 11). During 2007–2008 the ONRAB trials in southeastern ­Quebec halted the invasion of the raccoon rabies strain from Vermont (see Chapter 11). Similiarly, in 2015 ONRAB baits were used in the control programs that contained and stopped the invasion of the raccoon virus strain from Maine into southern New Brunswick. In ­December 2015 ten raccoons infected with the raccoon virus strain were discovered around Hamilton, ­Ontario, scattered across an area 26 kilometres south and 17 kilometres west and southwest of the first case in Stoney Creek. Extensive control operations using ONRAB baits were immediately undertaken within and beyond the infected area. The epizootic peaked in 2016 (171 raccoon cases overall) and spread some 45 kilometres from the initial reported case. By 2017, however, control efforts began to take effect. By the end of 2017, incidence in raccoons had dropped by 50% and spread was contained in an area only 11 kilometres beyond the 2016 limits (see Chapter 10). As Chapter 10 discusses, additional factors complicated control efforts: spillover into skunks, an overlapping epizootic of canine distemper in raccoons, high raccoon densities, and a wide variety of alternative food sources that probably impacted bait pickup. Despite these concerns, the containment held in 2018, and cases continued to decline. Control measures appeared to be working and ONRAB was again proving its effectiveness. Artemis continued to move ahead with new production initiatives in 2019. It now has its own bioreactor in operation and has received its Canadian licence to manufacture ONRAB at its facility on Watson Road in Guelph, Ontario. This same licence allows it to have contract manufacturing done at the N ­ ational Research Council facility in Montreal, Quebec, Canada. The collaboration between government agencies and private industry reported in this chapter has resulted in an effective Canadian vaccine, which, hopefully, will lead to the eventual eradication of terrestrial rabies in southern Ontario, Quebec, and New Brunswick and will also become a powerful tool in the fight against rabies in other North American jurisdictions.

Quebec Field Trial, 2008 In May and June 2008 a total of 60,210 baits were distributed by helicopter and by hand over an area of 560 km2, yielding an average of 108 baits/km2. In August 2008 a total of 702,000 AdRG1.3 vaccine baits were distributed over an area of 7210 km2 at an approximate density of 150 baits/km2. Flight lines were spaced by 750 metres for both the airplanes and the helicopter. A post-bait distribution study was conducted in S­ eptember and October 2008. Blood samples were collected from a total of 484 raccoons and 54 striped skunks, and rabies antibody in serum was determined by the cELISA test at CFIA, OLF. The antibody results for skunks using a cELISA titre of ≥16% as a positive antibody response indicates 24/54 animals were positive (44.4%). No adverse ­reactions, morbidity, or mortality attributable to the vaccine were observed. The antibody results for raccoons using a cELISA titre of ≥16% as a positive antibody response indicates 325/484 animals were positive (67.2%). No adverse reactions, morbidity, or mortality attributable to the vaccine were observed.

Quebec Field Trial, 2009 In April and May 2009 a total of 70,090 baits were distributed by helicopter and by hand over an area of 2568 km2, which works out to 27 baits/km2. In August 2009 a total of 946 000 AdRG1.3 vaccine baits were distributed over an area of 11,485 km2 at an approximate density of 150 baits/km2. Flight lines were spaced by 750 metres. A post-bait distribution study was conducted in September and October 2009. Blood samples were collected from a total of 431 raccoons and 82 striped skunks, and rabies antibody in serum was determined by the cELISA test at CFIA, OLF. The antibody results for skunks using a cELISA titre of ≥16% as a positive antibody response indicates 15/82 animals were positive (18.3%). No adverse reactions, morbidity or mortality attributable to the vaccine were observed. The antibody results for raccoons using a cELISA titre of ≥16% as a positive antibody response indicates 270/484 animals were positive (55.8%). No adverse reactions, morbidity, or mortality attributable to the vaccine were observed.

A Final Note

Conclusions

Artemis was issued a Canadian licence for ONRAB for use in skunk control programs in May 2013 and is now nearing licensing for use in skunk control programs in the United States. An efficacy trial for ONRAB is ongoing at the United

Subsequent to the 2006 field trials, the incidence of terrestrial rabies in Ontario and Quebec continued to drop with the ongoing operation of government rabies control programs using

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On 11 August 2017, a new multiple-year licence contract was signed between Artemis and the newly named ­Ontario Ministry of Natural Resources and Forestry. This new agreement will allow Artemis to move ONRAB into international markets such as the United States and beyond and at the same time promise continuity of supply of vaccine and baits for the Ontario rabies control program.

States Department of Agriculture/National Wildlife Research Center facility in Fort Collins, Colorado, to acquire a raccoon licence in the United States. In December 2013, ­Andrew Beresford had sold his shares of Artemis Technologies to Alex Beath, and Beath now has total control of the company. With Andrew Beresford’s departure, Artemis has hired very capable science staff to produce the ONRAB product.

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18 Testing Rabies Vaccines at Ottawa Laboratory Fallowfield (formerly the Animal Diseases Research Institute) M. Kimberly Knowles,1 Susan Nadin-Davis,2 Christine Fehlner-Gardiner,1 and G. Allen Casey3 1

Centre of Expertise for Rabies, Ottawa Laboratory Fallowfield, Canadian Food Inspection Agency, Ottawa, Ontario, Canada Animal Health Research, Ottawa Laboratory Fallowfield, Canadian Food Inspection Agency (Retired), Ottawa, Ontario, Canada 3 Canadian Food Inspection Agency (Retired), Ottawa, Ontario, Canada

2

Introduction Since the 1950s the Rabies Laboratory of the Pathology Section of the Animal Diseases Research Institute (ADRI) of the federal Department of Agriculture, currently known as the Centre of Expertise for Rabies, Animal Health Laboratory, Ottawa Laboratory Fallowfield (OLF) of the Canadian Food Inspection Agency has been involved in various projects to develop rabies vaccines. Such studies have focused primarily on oral rabies vaccination (ORV) of wildlife using different vaccine types (live attenuated, recombinant) and involved preliminary evaluations of rabies vaccine immunogenicity, vaccine efficacy trials involving virulent rabies virus challenge, and safety trials in a wide variety of wildlife, domestic, and laboratory animal species. These trials, conducted as both formal and informal collaborative ­research agreements, involved many different organizations and applied a broad base of scientific expertise and experience to this research. Included in the agreements were the Ontario Ministry of Natural R ­ esources (OMNR); several Canadian universities (McMaster ­ University, Queen’s ­University, University of Toronto, ­University of Saskatchewan, and University of Ottawa); private companies (Artemis Technologies Inc., Microbix, and Merial); and other scientific research institutions (Connaught Laboratories and Wistar Institute). A chronological listing of all the collaborations is not attempted here as there were often many overlapping projects and timelines, and some of this information is also described in the chapters in Part 4 of this book. The summary presented describes the principal

events and studies that OLF personnel have contributed to provincial and tertitorial vaccination programs over several decades regarding terrestrial wildlife rabies.

Historical Context As outlined in Chapter 4, the main role of the federal ­government laboratory has been to diagnose rabies virus infection in animals. Acts concerning measures to control the spread of rabies predate Confederation, such as one from 1845 for containing dogs for 40 days after a biting incident (Dukes & McAninch, 1992). In Canada before 1945, the rabies epizootics that occurred were in dogs and these were easily eradicated, by muzzling and tying up (Tabel et al., 1974). In 1947 a disease outbreak in dogs and wildlife species suspected to be rabies in the Northwest T ­ erritories was reported (Plummer, 1947). This rabies outbreak had spread extensively to the south of the country by 1954, prompting Plummer, a former director of ADRI, to suggest that the elimination of terrestrial wildlife r­ abies in Canada would be more difficult than in countries where the main vector was the dog. He made the following v­ isionary statement: “One might be inclined to wish that a vaccine which would be active by the oral route might be devised” (Plummer, 1954, p. 773). Research projects concerning rabies and rabies vaccines have been ongoing at OLF for more than 60 years. As early as 1958, Albert Corner investigated whether the commonly used dog rabies vaccines of the day, low egg passage (LEP)

The Development of Vaccines and Delivery Systems

and high egg passage (HEP) types of the Flury vaccine that contained live attenuated rabies virus, had the ability to cause rabies in cattle (Corner et al., 1958). One part of this project, completed in 1964, involved determining the potency and efficacy of rabies virus vaccines in both cattle and dogs. Collaboration between the OMNRF (formerly the Ontario Department of Lands and Forests and now the Ontario Ministry of Natural Resources and Forestry) and the Department of Agriculture on aspects of rabies research has a long history. Starting in 1963, Michel Beauregard began studying the age and sex ratios of rabid wild carnivores in Ontario (Johnston & Beauregard, 1969; Casey & ­Webster, 1975). The knowledge of the most affected part of a population is obviously important to the development of rabies control strategies. Determination of the prevalence of rabies in terrestrial wildlife species was a necessary part of defining the problem and evaluating the success of the vaccination campaigns. Efforts to control rabies in wildlife initially focused on population reduction, and in a collaborative study with OMNRF 5000 baits were distributed containing diethylstilbestrol (a contraceptive) and tetracycline (a biomarker to monitor bait ingestion). Work on the project ceased after two years with only 22 foxes submitted and showing no detection of tetracycline in bone and teeth sections, the departure of Michel Beauregard, and the change of focus by Ontario to the vaccination of wildlife. However, these early studies established the close relationship between these two organizations and set in motion long-standing activities crucial to the provincial control program; for example, beginning in 1967 and continuing until the present, provincial wildlife staff collected samples for detection of rabies by OLF staff. Two figures within the rabies group at OLF played prominent roles in the rabies control program in Ontario: Ken Charlton and Alexander Wandeler. In the 1970s Kenneth Charlton, leader of the rabies group at the time, undertook several studies to examine rabies pathogenesis in skunks. One experiment involved force-feeding striped skunks with rabies virus infected brain suspension to see if the virus could infect by the oral route (Charlton & ­Casey, 1979a). Although the purpose of the study was to investigate oral exposure as a route for natural rabies virus transmission, it was noted that such basic studies would have implications in selection of the route that rabies vaccines would be given in the field. In a research project submission in 1975, Charlton recognized that skunks were important with respect to rabies transmission and the practicality of oral rabies vaccines for skunks has not

been determined. In recognition of Charlton’s ­scientific expertise, he was appointed a member of the first Ontario Rabies Advisory Committee (RAC) when it was formed to oversee the wildlife rabies control program in Ontario in 1979 (see Chapter 10). Ken Charlton served on the RAC for six years. He agreed to contribute to a program, funded by Ontario Provincial Lottery funds, to develop an oral rabies vaccine for wildlife. At that time it was clear that the only feasible cost-effective method for wildlife rabies control over most affected areas of the province would require oral vaccination. In 1989 OLF gained substantial expertise in this subject when Alexander Wandeler immigrated to Canada from Switzerland, where he had been instrumental in eliminating fox rabies in that country using oral vaccination. Alex Wandeler soon assumed responsibility for the OMNRF collaborative research project; and, upon Charlton’s retirement in 1993, he became leader of the rabies group at OLF until his own retirement in fall 2010.

Logistical Issues Testing Methods In vaccine research programs, the rabies unit, supported by the animal care staff at OLF, has provided a variety of services over the years. Rabies diagnostic services, using the gold standard fluorescent antibody test (FAT) (Beauregard et al., 1965b), provided support for enhanced surveillance activities in Ontario, Quebec, New Brunswick, and Newfoundland and Labrador throughout the years. In addition, methods to detect immune responses to vaccination and protocols for the preparation and administration of challenge virus were ­developed. Since 1970 the development of serological tests for the detection of specific rabies virus antibodies has been pursued actively at OLF. A research progress report dated 1969 stated that the development of an assay was hampered by irregular virus growth characteristics in tissue culture (Beauregard et  al., 1965b). At the same time, Henry Tabel attempted to develop a passive haem-agglutination test (Tabel et al., 1970) but the research was suspended when a similar method was published in the WHO Bulletin. For studies on animals used in experiments, sera were sent initially to James Campbell at the University of Toronto for determination of neutralizing rabies virus titres by the fluorescence inhibition microtest (FIMT) (Zalan et al., 1979) using Evelyn-Rokitnicki-Abelseth (ERA) rabies strain as the challenge virus. James Campbell’s laboratory

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for rabies immunoglobulin used in post-exposure prophylaxis (Müller et al., 2009). A virus neutralization assay similar to the RSNA was also developed for the detection of antibodies to canine distemper virus. This assay was used to examine the seroprevalence of canine distemper in a field study of response of raccoons to the rabies vaccine ImRab (Sobey et al., 2010).

also developed an indirect enzyme-linked immunosorbent assay (ELISA) that exhibited good correlation with the FIMT (Barton & Campbell, 1988) for use with wildlife serum. In 1988 the Ontario RAC approached Dr Charlton regarding the possible move of serological testing in support of the wildlife rabies control program to OLF, a move that was eventually completed in 1993. DEVELOPMENT OF THE RABIES SERUM NEUTRALIZATION ASSAY

DEVELOPMENT OF ELISA METHODS

While a robust test, the RSNA requires highly skilled personnel for its performance, is time-consuming in both the test set-up and the time to obtain the final result, requires working with live virus, and is sensitive to cytotoxic effects of test serum. To overcome these limitations, particularly in light of the large number of samples originating from the Ontario ORV campaigns and animal vaccine experiments, Lindsay Elmgren and Alexander Wandeler developed a competitive ELISA (c-ELISA) in 1993 for detection of rabies virus antibodies in wildlife serum. The c-ELISA is based on immunoassay techniques and software originally developed by Klaus Nielsen and collaborators for diagnosis of brucellosis (Nielsen et al., 1996), and it was validated against the RSNA, using 0.5 IU/mL as the positive threshold value. This semi-quantitative antibody-binding assay employs a peroxidase-labelled neutralizing anti-glycoprotein monoclonal antibody (MAb); inhibition of binding of this MAb to microtiter plates coated with a semi-purified preparation of the ERA rabies virus by the test serum provides a measure of the level of specific antibody therein. The test is completed in approximately five hours and a single technician can process 200 samples easily in a day. The c-ELISA method was initially presented at the fourth international meeting of Rabies in the Americas (Elmgren et al., 1993) and was published three years later (Elmgren & Wandeler, 1996). This test was developed and validated principally using fox sera, as fox rabies was a major concern in Ontario and was the target of ORV programs using ERA. A modification of the c-ELISA, the blocking ELISA, was also developed in an attempt to overcome some of the non-specific effects observed when samples of very poor quality (e.g. carcass chest cavity fluids) were tested with the c-ELISA. However, subsequent testing found that the sensitivity and specificity of the blocking ELISA was unsatisfactory, and it was used in recent years for evaluation of ORV campaigns. With the advent of an Ontario raccoon rabies outbreak in 1999, and the subsequent ORV campaigns targeting this variant, the field samples and experimental animal samples received for serological testing were predominantly

The rabies serum neutralization assay (RSNA) is a standard virus neutralization test in which dilutions of the serum under test are incubated with a defined quantity of infectious virus before being added to a permissible cell line. Although somewhat similar to the FIMT method used by Dr Campbell, the RSNA employs CVS-11 instead of ERA as the challenge virus and mouse neuroblastoma (MNA) cells (Campbell & Barton, 1988). Following an incubation period of several days in which the inoculum can infect and multiply in the MNA cells, the cells are fixed with ­acetone and virus is detected by staining with a fluorescently labelled polyclonal goat anti-rabies ribonucleoprotein conjugate. The neutralizing titre of the serum can then be calculated using the Spearman-Kärber method, by scoring the number of virus positive wells (Lorenz & Bogel, 1973). Results are presented in international units (IU) per millilitre by comparison with the titre of a standard of defined ­neutralizing activity (e.g., WHO 2nd International Standard). The method has been published (Knowles et al., 2009) and is similar to the fluorescent antibody virus neutralization (FAVN) test used internationally for animal ­serology for pets travelling to rabies-free countries(Cliquet et  al., 1998). Since 1993 the RSNA has been used extensively to examine humoral immune response to parenteral and oral vaccination in both experimental animals and field studies, and to provide a reference standard against which other serological test methodologies are compared. Problems of cell toxicity had been encountered when field samples, particularly blood obtained from the chest cavity of carcasses, were tested by RSNA. To determine at what point these samples cause problems, the toxicity caused by fresh sera and chest cavity fluids was compared after various times of storage. Modifications to the RSNA to counter the effects of these samples included seeding the cells at a higher density and including antibiotics at twice the normal concentration. This test has been used to evaluate the neutralizing ability of monoclonal antibodies for several different genotypes of rabies virus as part of the development of a replacement

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from raccoons and skunks. As serological data was limited for these two species, both RSNA and c-ELISA tests were performed on most of the samples. The test correlation was not as high as was previously observed with fox sera. These observations led to the introduction of a number of modifications to the c-ELISA (Fehlner-Gardiner et  al., 2006). These included additional steps during antigen preparation and plate coating to decrease batch-to-batch variation, development of more stringent test acceptance criteria, production of species-specific control sera of defined neutralizing titre, and establishment of new positive threshold values for raccoon, skunk, and fox sera. While the optimal positive threshold value for fox sera remained the same as established by Elmgren and Wandeler, those for raccoon and skunk were higher. As well, the associated sensitivity and specificity of the c-ELISA (versus RSNA) was lower with raccoon and skunk sera than with fox. Validation data, generated at OLF (Fehlner-Gardiner, 2015) and inter-laboratory comparisons with the New York State Department of Health Rabies Laboratory (Fehlner-Gardiner et al., 2012), demonstrated that the c-ELISA is a valuable tool for determination of sero-prevalence in animal populations. This is particularly true when use of virus neutralization assays is impracticable due to sample load, time constraints, and inherent problems of toxicity. The c-ELISA developed at OLF has been utilized in the evaluation of oral vaccines (ERA, V-RG, and ONRAB) field performance in Ontario (Rosatte et al., 2008, 2009, 2011), in Quebec (Seguin et al., 2009; Mainguy et al., 2009), and in New Brunswick (Fehlner-Gardiner et  al., 2012). It was also used in studies of the kinetics of immune response to ImRab, RABORAL V-RG, and ONRAB vaccines in captive raccoon, skunk, and fox studies (Brown et al., 2011), and in field application of ImRab (Sobey et al., 2010). In addition to assays for the detection of rabies virus ­antibodies, methods for detection of antibodies against proteins associated with various vector viruses were developed at OLF. In preparation for the release of V-RG, ­determining the prevalence of antibodies to orthopox viruses in the sera of target species was necessary; for the US collaborators, and in anticipation of the incursion of raccoon rabies into Canada, the raccoon was an important target. Accordingly, competitive and blocking ELISAs were developed and validated in comparison with plaque reduction assays for measurement of anti-orthopox antibodies in raccoon serum (Wilson et al., 2000). Similarly, in preparation for field release of ONRAB, the prevalence of human adenovirus and canine adenovirus antibodies in target species was determined in sera

collected from field samples by Laura Maxwell, a University of Ottawa master’s degree student. Maxwell developed ELISA techniques and compared them with the gold standard of plaque assay determination of serum neutralizing antibodies (Maxwell, 2000). MOLECULAR GENETIC METHODS

To address the need to detect viruses, especially recombinant rabies vaccines that were subject to safety trials and vaccine stability studies, assays based on the polymerase chain reaction (PCR) technique to detect viral nucleic acids (described in more detail in Chapter 23) were employed. PCR-based assays, which use synthetic oligonucleotides (primers) targeting specific DNA sequences and a thermostable DNA polymerase to amplify short segments of DNA, are highly sensitive and specific; customized tests to detect particular viral genomes can readily be developed by appropriate primer design. To improve the specificity and sensitivity of such assays, the PCR product can be further characterized by southern blot analysis (PCR-SB), in which the product is transferred to a membrane and hybridized to a probe targeting internal amplicon sequence. Alternatively, real-time PCR, in which fluorescent probes are used directly for product detection (see Chapter 23), can be employed. Such molecular assays, developed to support studies on adenovirus rabies recombinant vaccines, allowed specific detection of vaccine virus in many tissue types and on a much larger number of samples than had been possible using traditional cell culture methods of viral propagation and detection.

Animal Handling Any vaccine research program requires handling and maintenance of test animals of appropriate species. Since the focus of animal research programs at OLF (and the former ADRI location in Hull) involved use of agricultural species (cows, pigs, sheep, and chickens) along with traditional laboratory species (mice, guinea pigs, and rabbits) staff expertise in the handling of these species was well established. However, with the wildlife rabies virus vaccine program, the targeted three species were the striped skunks (Mephitis mephitis), red foxes (Vulpes vulpes), and later raccoons (Procyon lotor). Staff became well versed in the handling of skunks in the 1970s and 1980s because of the use of this species in studies of the basic biology of rabies, but expertise in handling of other species had to be developed. Moreover, a different menagerie of animals was required to support safety trials of the various oral wildlife rabies

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vaccines. The list of diverse species included coyotes (Canis latrans), grey squirrels (Sciurus carolinensis); meadow voles (Microtus pennsylvanicus), deer mice (Peromyscus leucopus), groundhogs (Marmota monax), ring-billed gulls (Larus delawarensis), red-tailed hawks (Buteo jamaicensis), great horned owls (Bubo virginianus), cotton rats (Sigmodon hispidus), rabbits (Oryctologus cuniculus), starlings (Sturnus vulgaris), white-tailed deer (Odocoileus virginianus), horses (Equus ferus), dogs (Canis familiaris), cats (Felis domesticus), and SCID (severe combined immune deficiency) mice and nude mice (Mus musculus). Many OLF staff had been involved in animal handling over the years but one person in particular, Allen Casey, was instrumental in implementing special techniques for handling many of the species not routinely used at OLF. In the early days, as part of a study entitled “Epidemiological Studies on Rabies” to determine if there was a carrier state existing in Ontario skunks (Beauregard et  al., 1965a), striped skunks were trapped in the local area by staff, with several incidents of staff being sprayed. Later, animals for experiments were purchased, either from commercial sources or through trapping under the auspices of the OMNRF. There were also challenges in housing wildlife because of biocontainment level requirements. In 1977 the Medical Research Council of Canada published guidelines requiring increased biological containment for facilities working with rabies virus and genetically modified organisms. Since OLF was of recent construction, just opened in 1974, and had the specialized facilities required for work with rabies virus in animals, it became the main centre used for such studies. In 1986 the Ontario RAC considered expanding research at OLF, and a feasibility study of Building 210 at OLF was conducted to see if minor modifications would allow for the construction of internal animal holding rooms within a large open space of the building. The building was unsuitable for this purpose however, as major renovations of the containment envelope and ventilation system would have been prohibitively expensive.

these skunks, either by FAT or by mouse inoculation, thus demonstrating that these skunks could not transmit the virus to other individuals. When the 10th passage of virus was inoculated intramuscularly (IM) into three skunks, none developed rabies. Shortly after its creation, Ontario RAC solicited formal proposals for rabies vaccine development from universities and commercial companies. In 1981 Dr Tabel, a former employee of the Pathology Section of ADRI who had moved to the Western College of Veterinary Medicine located at the University of Saskatchewan, received funding to participate in vaccine development by investigating the use of oral rabies vaccines in wildlife species. The inaugural trials employed attenuated live rabies vaccines, such as ERA, that had been used for pet vaccination. As part of this research in 1985–1986, skunks were given ERA/BHK-21 but since the facilities available at the University of Saskatchewan were not acceptable for work involving rabies virus challenge, the animals were shipped to OLF for this essential part of the trial. Seven of the eight skunks given ERA vaccine IM seroconverted, but the only skunk that succumbed to rabies challenge had rabies virus neutralizing antibody (five of seven controls were diagnosed with rabies). Over this same period, Kenneth Lawson and his ­colleagues at Connaught Laboratories were focusing on the prevention of rabies virus infections in foxes (Black & Lawson, 1973). Similar interests drew the two groups ­ headed by Drs Charlton and Lawson together, thereby initiating a 30-year collaboration between them. Agriculture Canada supported Lawson’s studies by providing a location (OLF) for challenge of the foxes and confirmation of the diagnosis of rabies in the experiment animals. These studies required the production of fox variant rabies virus preparations, which were titrated in foxes, for eventual use as the challenge virus in foxes and striped skunks. It was found that ERA, when applied in a bait at a titre of 106.3, was capable of immunizing up to 100% of foxes, and protection from disease lasted up to four years (Lawson et al., 1989). In a later study in which red foxes were vaccinated with ERA in a bait and challenged after 83 months, 10 of 11 foxes that had seroconverted following vaccination survived challenge with rabies virus. Although 6 of 11 had no detectable antibody at the time of challenge, 5 of these 6 survived the challenge and had an anamnestic response, as indicated by elevated titres of antibody when measured at day 77 post-challenge (Lawson et al., 1997). Research on rabies in animals moved from Connaught Laboratories and the University of Saskatchewan to OLF, with the trials conducted in support of OMNRF’s need to

Development of the ERA Vaccine Preliminary testing of the ERA vaccine began in the 1970s. To demonstrate the safety of the vaccine, it was passaged 10 times intra-cerebrally in skunks. The passage needed to be repeated on occasion, as the skunks did not always develop rabies. Virus was detected in the skunk brain by mouse inoculation, with the greatest titre being 106.4 MILD50/ mL, but no virus was detected in the salivary glands from

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achieve permission to use ERA in the field for control of fox rabies starting in 1989 (Rosatte, 1990). However, it became clear that ERA was not a suitable vaccine for control of rabies in skunks because of poor immunological response and susceptibility to vaccine-induced rabies by this species. Groups of eight skunks each were given ERA IM, directly into the intestine, or intra-nasally with rabies occurring in one of the eight skunks inoculated IM or intestinally and in all eight skunks inoculated intranasally, although none in this group had infectious virus in their submandibular salivary glands. These results indicated that ERA virus has a significant residual pathogenicity in skunks. Although all the remaining seven skunks that were given ERA IM survived challenge with rabies virus, overall the results were disappointing since none of eight receiving a bait survived, and only two of seven that received the vaccine intestinally survived (Tolson et al., 1988a). Collaboration between staff at OLF and Robert Stewart of Queen’s University in Kingston began in 1985. Robert Stewart’s research interest at the time was to improve the ERA vaccine by isolation of mutants of the virus that exhibited less reversion to virulence. Early in the 1980s, directed mutagenesis using chemical compounds was thought to produce stable attenuated vaccines. In light of this, Stewart’s laboratory produced 45 small plaque mutants of ERA after exposure to the mutagenic agents 8-azaguanine or 5-fluorouracil. Based on preliminary testing of these isolates for pathogenicity in mice, two viruses were selected for further vaccine studies in skunks: AZA I and AZA II (Tolson et  al., 1990). In the same period, collaboration began with Charles Rupprecht of the Wistar Institute in Philadelphia. Researchers there had produced apathogenic strains of rabies virus that had escaped neutralization by monoclonal antibodies specific to the G protein: CVS 3766 (single site) and 3713 (multiple site), and ERA 3629 (single site). These three strains were tested for vaccine efficacy, together with AZA 1 and AZA 2, in skunks (Rupprecht et al., 1990). Skunks given either of the two AZA mutants orally exhibited only limited protection from a lethal challenge with street rabies virus; only two of seven given AZA 1 and one of eight given AZA 2 survived. AZA 2 produced a high rate of seroconversion (eight of eight) by the intestinal route and all challenged skunks in this group survived (seven of seven). None of the skunks given the other mutants orally seroconverted. The mutant CVS 3766, while apathogenic when given intracerebrally to adult mice, was consistently pathogenic by the intranasal route in skunks. These results demonstrated that skunks are highly resistant to oral immunization by live rabies virus vaccines and that

pathogenicity (by intracerebral route) of the mutant CVS 3766 is markedly different in mice and skunks (Tolson et al., 1990). The most promising of these attenuated ­rabies virus vaccines (SAD-B19, ERA/BHK-21, and AZA 2) were compared for efficacy and safety in the striped skunk by the oral and intranasal routes. The SAD-B19 and ERA/ BHK-21 vaccines were given orally while all three vaccines were given intranasally. Oral administration of SAD-B19 and ERA/BHK-21 vaccines induced neither seroconversion nor significant protection against rabies challenge. Vaccine induced rabies was observed in one skunk which consumed a SAD-B19 vaccine-laden bait, two of six skunks (AZA 2), three of six (ERA/BHK-21), and six of six (SAD-B19) skunks that received vaccine by intranasal instillation (Rupprecht et al., 1990). The collaboration with Stewart ended with the findings that apathogenic mutants were not as satisfactory as V-RG with respect to safety and immunogenicity.

Recombinant Vaccines V-RG In response to the problems with immunogenicity and ­vaccine-induced disease in skunks, efforts focused on development of recombinant vaccines produced through genetic engineering of viral vaccine vectors. Collaboration with the Wistar Institute expanded to include a private company, Transgene, later replaced by Merial, to further investigate the potential value of the vaccinia rabies G gene recombinant V-RG. Approximately 25 experiments were conducted at OLF from 1985 until 2005. V-RG showed promise in foxes: neutralizing antibodies against rabies virus were detected two weeks post vaccination in eight of eight foxes in the bait-fed group, and after challenge with street rabies virus all the foxes were protected (Tolson et al., 1988b; see Chapter 17a). When V-RG was tested in striped skunks, neutralizing antibodies to rabies virus were present in six of seven skunks at 28 days post exposure. When challenged with rabies virus, five of seven survived (Tolson et al., 1987). As part of the safety evaluation of this oral vaccine in target and non-target wildlife, V-RG was given by direct instillation into the oral cavity (DIOC) to a wide range of species: meadow voles, deer mice, groundhogs, grey squirrels, white-tailed deer, ring-billed gulls, red-tailed hawks, and great horned owls. Coyotes received the V-RG in two vaccine-laden baits. Several animals showed high levels of rabies neutralizing antibodies with the absence of any

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Testing Rabies Vaccines at Ottawa Laboratory Fallowfield

lesions suggestive of vaccinia infection indicating that it was a potentially safe oral wildlife vaccine candidate (Artois et al., 1990). A post-doctoral fellow, Neil Tolson, conducted much of this work under Charlton’s guidance. After his departure from OLF, Marc Artois replaced Tolson, his eight-month visit to OLF funded by a biotechnology exchange program between the governments of France and Canada. When V-RG was initially used in raccoons it showed promise by the DIOC route, but when administered in a bait it had poor performance (Brown et al., 2011). This inconsistency in ­results was thought to be due to changes in manufacturing, so further experiments used different lots of V-RG. ­National Institutes of Health potency tests indicated similar relative potency values for the Lots 5F17 and #3740. The inclusion of glycerol in an attempt to increase the duration of the vaccine in the oral cavity did not improve the results. Experimentation with V-RG at OLF was suspended in 1990 when it was found that the human adenovirus type 5 rabies vaccine, AdRG1, had more consistent results when delivered in baits.

virus recovered from feces and oral fluids was examined for possible mutations. Two mutant viruses were detected: one with an insertion of a 72-base-pair sequence in the SV40 promoter region, and another with a 54-base-pair deletion from within the rabies glycoprotein gene (Lutze-Wallace et al., 1995a). This information was considered during the design of some later adenovirus constructs (AdRG1.3) in which the SV40 promoter was omitted. The site of entry of the AdRG1 construct in skunks was further explored, and several studies were conducted to demonstrate the vaccine’s safety. In one study, the tissue distribution of AdRG1 virus was compared to that of human adenovirus type 5 in mice (Knowles, 1992). Other vaccine safety studies were conducted in non-target wildlife species (groundhogs, squirrels, and starlings given the vaccine by DIOC). Further species were not examined as the research with this vaccine was discontinued with the development of alternative adenovirus constructs. To improve the expression levels of the rabies glycoprotein gene by the Ad5 vector, Oksana Yarosh, a PhD candidate at Ludvik Prevec’s lab at the time, constructed two new replication competent vaccines: AdRG1.3 (ONRAB) and AdRG4. These new vaccine constructs both elicited high levels of serum anti-rabies antibodies by parenteral or oral routes in rodent, canine, and skunk model systems (Yarosh et  al., 1996). Microbix, a private company, purchased the AdRG1.3 and AdRG4 constructs and associated intellectual property from McMaster University. Although most previous studies used small research-scale productions of these constructs, the guidelines stipulated that ­pre-production serials be used for safety and efficacy testing in support of licensing applications. However, difficulties in the commercial-scale production of the vaccine became apparent. As interest in direct involvement by Microbix faltered, Artemis Technologies Inc. (see Chapter 17c) began producing vaccine suitable for inclusion in baits and acquired the rights to the adenovirus AdRG1.3 product, the construct selected for further development. Several trials were conducted to determine if AdRG1.3 was efficacious in skunks and raccoons, followed by a formal efficacy trial to provide the data to support approval of field use of the vaccine (Knowles et al., 2012). The potential problem of interference of pre-existing antibodies in the vector in the generation of an immunological response to the rabies virus glycoprotein was a concern; experimentally, this effect had been investigated in raccoons and skunks. An initial study in 1991 suggested that antibodies to Ad5 generated after DIOC and IM inoculation to either the wild type (Ad5) or the parent (Ad5dlE3)

Adenovirus Recombinants The next group of approximately 50 experiments conducted at OLF focused on the potential use of human adenovirus type 5 (Ad5) rabies virus constructs as vaccines for use in skunks and raccoons in particular. As described in Chapter 17a, Ludvik Prevec and his colleagues at ­McMaster University, Hamilton, developed a recombinant human adenovirus 5 containing the rabies glycoprotein gene (AdRG1). This construct was tested for potential use as a vaccine in striped skunks and red foxes at OLF. Groups of skunks received the vaccine in baits, by DIOC, or IM, whereas foxes were given the vaccine by DIOC only. ­Challenge with street rabies virus was performed using ­selected groups of vaccinated skunks and foxes. There were high rates of seroconversion (generally with high antibody titres) in both foxes and skunks, with survival of all challenged vaccinated animals (Charlton et al., 1992). The Biologics Evaluation Laboratory of OLF used the AdRG1 as a model to investigate the genetic stability of this new generation of vaccines constructed using molecular genetics. After serial passage in a cell line, the AdRG1 genome was assessed using restriction endonuclease analysis, and PCR was applied to examine the integrity of the expression cassette for the rabies glycoprotein and flanking viral vector sequences (Lutze-Wallace et  al., 1992; ­Lutze-Wallace et al., 1995b). In a subsequent study, vaccine

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virus negatively influenced the creation of rabies virus antibodies after DIOC exposure to AdRG1. Two of eight skunks seroconverted, compared to six of eight for the control group. In a later study the presence of ­pre-existing antibodies generated after CAV or Ad5 IM inoculation did not interfere with the response when AdRG1.3 was given by DIOC; similar levels of rabies antibodies were developed compared to the placebo group (Knowles et al., 2012). This difference in results may be due to either the difference ­between AdRG1 and AdRG1.3 in eliciting a rabies virus antibody response or the Ad viruses being given orally in the first experiment. The final group of experiments was conducted to demonstrate the safety of ONRAB when given by DIOC to representatives of three wildlife vector species of concern in Ontario (red fox, raccoon, and striped skunk) and to a variety of non-target wildlife species, as well as ­domestic and laboratory species. These later studies benefited from the application of PCR-based tests to detect the vaccine construct specifically. Subsequent to AdRG1.3 vaccine exposure, detection of vaccine virus in the lung, spleen, ­intestine, liver, kidney, and brain of each animal (n = 1280) was attempted using an O ­ NRAB-specific PCR-SB assay. Just 18 tissues (1.4%) tested positive by the PCR-SB test. A quantitative real-time PCR analysis was used to test the excretion of the vaccine in feces and in the oral cavity; only 0.8% of oral swabs and 6.8% of fecal specimens were found to be positive. The low rates of recovery of vaccine virus from tissues, feces and the oral cavity suggested that ONRAB would be very unlikely to have any negative impact on wildlife species (Knowles et  al., 2009a). Investigation into the genetic stability of ONRAB during in vivo and in vitro passaging was the subject of a thesis by Danielle Roberts, a graduate student from the University of Ottawa. ­Nucleotide sequencing of the expression cassette of multiple viral clones recovered after 20 serial passages in cell culture and 5 serial passages in cotton rats, a species susceptible to ­human adenovirus infection, indicated no changes in comparison to the original virus. A competition experiment, which involved the in vitro passaging of a mixture of O ­ NRAB and Ad5, demonstrated that the two viruses do not exhibit noticeably different biological fitness levels in this environment (Knowles et al., 2009b). Ludvik Prevec also produced new human adenovirus type 5 constructs: AdGFox, AdNFox, and AdNskunk using cloned rabies virus genes provided by Susan Nadin-Davis. These constructs have undergone only preliminary evaluation in mice, and experiments in skunks, although planned, were never completed.

Field Stability of Vaccines Since baits are placed in the field and may be exposed for several days before being consumed, there was concern that the rabies vaccine contained within the bait might lose its infectious titre and hence efficacy with time. ­Consequently, information on the stability of vaccines in the field is important and experiments to examine these factors have been ongoing for many years at OLF. These studies involved placing baits from vaccine lots in cages in a simulated field environment for predetermined lengths of time, then collecting and freezing the baits until the viral titre was determined (Lawson & Bachmann, 2001). Even though these cages were not rodent proof, the only observed pest incursion was by slugs. This was a time consuming and resource-intensive function but helped with the identification of problems with vaccine bait. Over the years, stability testing was performed on baits containing all the vaccines in use in Canada: ERA, V-RG, and ONRAB. ERA and ­ONRAB vaccines were determined to be reasonably stable in the field (Bachmann et al., 2005).

Field Cases of Vaccine-Induced Rabies Given the decision to employ the live attenuated ERA vaccine in the field for fox rabies control, despite its ­ ­residual pathogenicity in skunks, active monitoring for ERA-induced cases of rabies acquired in the field has been ongoing for many years. Viral typing methods, as described in Chapter 23, have been used to screen all rabies-positive cases in wildlife and domestic animals in Ontario for the presence of this viral strain. Between 1989 and 2004, over 13 million ERA-containing baits were distributed across the province, but just nine cases of ERA-induced rabies were identified over the 16 years (Fehlner-Gardiner et al. 2008). These nine cases included four red foxes, two raccoons, two skunks, and one bovine calf. This demonstrated the very limited negative impact of this vaccine compared to the large benefits gained from its use to control fox rabies.

Summary The research described in this chapter played an important role in gaining authorization for provincial governments and later, territorial governments, to use one or more of these vaccines (ERA, V-RG, and ONRAB) in their programs. The steep decline in the number of terrestrial wildlife

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cases of rabies in Canada since 1994 (Canadian Food Inspection Agency, 2011) is attributed to the success of the vaccination programs conducted in eastern Canada against both fox and raccoon rabies. While the use of ERA in Ontario throughout the 1990s and 2000s resulted in a major decline in case numbers, it did not completely eradicate the arctic fox variant of rabies from the targeted area. There had been past debate as to the need for a vaccine that specifically targeted skunks for the Ontario program given that the arctic fox variant was the only rabies virus type associated with terrestrial hosts in Ontario (see Chapter 23). It has been predicted that elimination of rabies in the primary reservoir host, the red fox, could result in the elimination of rabies from other terrestrial species. Over time, it became evident that this was not in fact the case; the arctic fox variant persisted in southwestern Ontario with an increasing proportion of cases in skunks, leading to speculation that this species was acting as a secondary reservoir

(Nadin-Davis et  al., 2006). The primary objective in the development of the adenovirus recombinant vaccines was to counter incursions of the raccoon variant. However, the fortuitous high efficacy of ONRAB in controlling rabies in skunks led to its first field distribution in southwestern Ontario in summer 2006 (McAllister, 2006), an effort to eliminate the focus of arctic fox rabies in that area. Since then, until the invasion of raccoon rabies near Hamilton, Ontario, in 2015 (see Chapter 10), skunk cases declined in southern Ontario. Because of this success, various jurisdictions in the United States are doing field trials using ONRAB in their wildlife rabies control programs (United States Department of Agriculture-Animal & Plant Health Inspection Service, 2017; see Chapters 17c and 38). With the successful application of both the ERA and the ONRAB vaccines in the field, although collaborative agreements between OLF and OMNRF are still in effect, this era of rabies vaccine research at OLF has come to a close.

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A., & Casey, G.A. (1974). History and epizootiology of rabies in Canada. Canadian Veterinary Journal, 15, 271–281. Retrieved from https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1696688/ Tabel, H., Bouillant, A., Casey, A., & Webster, A. (1970). Development of a serological test for the detection of antibodies to rabies virus (Animal Pathology Project 700). Ottawa, ON: Department of Agriculture. Tolson, N. D., Charlton, K. M., Stewart, R. B., Campbell, J. B., & Wiktor T. J. (1987). Immune response in skunks to a vaccinia virus recombinant expressing the rabies virus glycoprotein. Canadian Journal of Veterinary Research, 51, 363–366. Tolson, N. D., Charlton, K. M., Lawson, K. F., Campbell, J. B., & Stewart, R. B. (1988a). Studies of ERA/BHK-21 rabies vaccine in skunks and mice. Canadian Journal of Veterinary Research, 52, 58–62. Tolson, N. D., Charlton, K. M., Casey, G. A., Knowles, M. K., Rupprecht, C. E., Lawson, K. F., Campbell, J. B. (1988b). 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19 The Development of Aerial Baiting Peter Bachmann,1 Lucy J. Brown,2 and Neil R. Ayers3 1

Ontario Ministry of Natural Resources and Forestry, Wildlife Research and Monitoring Section (Retired), Peterborough, Ontario, Canada 2 Ontario Ministry of Natural Resources and Forestry, Wildlife Research and Monitoring Section, Peterborough, Ontario, Canada 3 Ontario Ministry of Natural Resources and Forestry, Aviation Services (Retired), Sudbury, Ontario, Canada

Introduction When “Arctic dog disease” in northern Canada was first diagnosed as rabies in the 1940s (Plummer, 1947), aircraft transported specimens from the Arctic to the C ­ anada ­Department of Agriculture diagnostic laboratories in Hull, Ottawa, Lethbridge, and Sackville. Rabies-suspect animals included sled dogs, foxes (Vulpes sp.), and wolves (Canis ­lupus). Inuit and Cree hunters brought specimens from remote camps to trading posts such as Arviat, Churchill, ­Winisk, Fort Albany, Nain, and Fogo. Bush planes provided the essential link to the south. Effective air transport provided fast response for individual cases, but it biased the accuracy of mapping cases in the north, because source locations were always trading posts that had air service. Eventually aircraft became more than just a means of transportation. The Government of Ontario sought to control rabies by the innovative approach of delivering baits containing oral rabies vaccine to wild rabies vectors using aircraft. These rabies control measures were adopted successfully in other parts of Canada and the United States. This chapter ­describes the development of Ontario’s aerial baiting system.

enzootic in Ontario. Given the extent of the problem, the Rabies Research Unit of the Ontario Ministry of Natural Resources (OMNR, now the Ontario Ministry of Natural Resources and Forestry (OMNRF)) developed a system to distribute oral rabies vaccine in edible baits from the air to wild foxes and skunks to control the disease (see Chapter 10). Aerial baiting required solving many interrelated problems. Effective bait distribution relies, more or less, on t­ arget wild animals being attracted to and coming to the baits within their home range, and chewing or ingesting them to absorb the oral vaccine contained in the baits. ­Variations in aerodynamics of airdropped baits limit the control of bait trajectories once they leave the aircraft and where they land. Baits that fall in areas with sparse animal activity, in ­micro-climates that debilitate vaccine potency, or in areas with overabundant non-targets that could diminish returns for target species are essentially wasted. Effective aerial baiting requires (1) knowledge of the habits and movements of the target species; (2) bait design that considers uptake by animals, robustness, size, and bait handling; (3) bait; and (4) dispensing machinery and suitable aircraft.

Wildlife Rabies Control with Airplanes: A Challenge

Bait Delivery from Aircraft: Developing a System

Arctic variant rabies from the north spread into red foxes (Vulpes vulpes) and striped skunks (Mephitis mephitis) in about 100,000 km2 of southern Ontario (Tabel et al., 1974; see Chapter 2). Rabies in those two species drove a major

Trials from 1972 to 1987 evaluated bait delivery options. Bait acceptance by target species used tetracycline to test the efficacy of bait types and delivery systems (see Chapter 24b). Tetracycline was mixed into the bait matrix for distribution.

The Development of Vaccines and Delivery Systems

When a bait was chewed, tetracycline was deposited into teeth. Microscopic examination of a thin section of the involved tooth under ultraviolet light revealed fluorescent lines which confirmed tetracycline and indicated that the animal had eaten a bait. Bait acceptance defines the proportion of animals surveyed that had tetracycline deposits and, therefore,

must have eaten bait(s). Early trial baits contained only a biomarker (Table 19.1). An oral rabies vaccine, ERA, was first included in 1985 (Bachmann et al., 1990). After 1998 OMNR employed other vaccines (see Chapters 10, 17,  18) such as vaccinia-rabies glycoprotein (V-RG) and ­adenovirus-rabies glycoprotein (AdRG, trade name ONRAB).

Table 19.1  Regional allocation of all baits (no vaccine, ERA, V-RG, and ONRAB) deployed by OMNR using Cessnas with private agencies (1975 to 1987) and with Ontario Provincial Air Service aircraft (1989 to present). Test baits with no vaccine contained only a biomarker (1975 to 1993). With the exception of 92,070 baits distributed in New Brunswick in 2008, all ONRAB baits in eastern Canada were deployed in Quebec. ERA Year 1975 1976 1977 1978 1979 1980 1981 1982 1983 1984 1985 1986 1987 1988 1989 1990 1991 1992 1993 1994 1995

No Vaccine Ontario

Ontario

V-RG Quebec

Ontario

Quebec

ONRAB

United States

States

Ontario

Eastern Canada

Sum

3,600 48,330 9,720

3,600 48,330 9,720

52,903

52,903

9,973 21,251 37,329 22,547

10,732 14,972 13,650

9,973 10,732 14,972 34,901

285,010 706,759 674,126 687, 001 699,385 1,458,000 1,629,092

285,010 744,088 674,126 687,001 721,932 1,458,000 2,766,471

148,000

989,379

1996

1,280,289

2,908,760

1997

1,230,840

67,075

2,967,712

1998

965,796

118,404

3,750,832

1999

927,396

128,592

2000

2001

81,700

82,800

4,772,390

820,816

779,644

90,720

3,895,208

826,262

674,225

140,220

4,582,807

312

NY TX NY TX NY TX VT NY TX VT OH NY TX VT OH NY TX VT OH NY TX VT OH PA WV

4,189,049 4,265,627

4,835,032

5,992,878

5,586,388

6,223,514

The Development of Aerial Baiting

ERA Year

No Vaccine Ontario

Ontario

V-RG Quebec

Ontario

Quebec

United States

2002

716,961

600,264

5,326,133

2003

584,172

605,472

5,320,603

2004

482,138

474,542

4,249,245

2005

471,312

276,048

4,004,580

2006

478,098

209,009

2007

2008 2009 2010 2011 2012 2013 2014  Sum

205,653

119,160

3,473,438

391,627

330,000

2,445,052

65,016 173,516

221,050

15,592,966

462,071

3,700,904

983,950

Source: compiled from OMNR data.

313

48,686,139

ONRAB States NY VT OH PA WV NH TN VA NY VT OH PA WV NH TN VA ME NY VT OH PA WV NH TN ME AL FL GA NY VT OH PA WV NH ME AL FL NY VT OH PA WV NH ME OH PA WV

Ontario

Eastern Canada

Sum 6,643,358

6,510,247

5,205,925

4,751,940

195,885

4,475,590

454,974

118,530

3,740,183

972,754 986,177 758,599 343,317 403,664 247,200 74,312

794,745 946,400 810,804 618,097 520,982 400,902 383,760

2,053,565 2,106,093 1,569,403 961,414 924,646 648,102 458,072

4,436,882

4,594,220

78,662,785

The Development of Vaccines and Delivery Systems

effective aerial baiting system for vaccination of foxes and skunks using (1) various aircraft types; (2) baiting systems, material, and personnel; and (3) evaluation of efficacy to find the best combination. Parameters such as bait dispersion and correct time for baiting were developed by studying target species activity patterns through r­ adio-telemetry (Voigt & Lotimer, 1981; see Chapter 26a). Test baits included the meatball, sponge, and blister-pack, the forerunner of the Ontario bait (Bachmann et al., 1990; see Chapter 17). The first airplane employed was a small single-pistonengine high-wing monoplane, the Cessna 172 (Plate 10), chartered from a private company. OMNR relied on the r­ ural road grid to map and navigate for baiting (Figure 19.1 and 19.2). The Cessna 172 has two seats in the cockpit and one rear bench seat. A navigator sat beside the pilot and a baiter sat on the rear bench surrounded by up to 2000 baits in 40 to 42 bags, about 60 kilograms (Figure 19.3). Originally, baits were packaged, 48 baits per lot. Flights occurred in early autumn (one in late winter) and was flown only when there was adequate visibility and wind was less than 25 ­kilometres per hour. The navigator directed the flight path of the airplane, deviating from the plotted lines only if landscape features varied from the map or to target potential fox habitat. With the exception of excessive head or tail winds, or avoiding obstacles, such as towers, the pilot generally maintained the airplane at 100 metres AGL and an air speed of 130 kilometres per hour. The navigator told the baiter when to start and stop dropping baits based on the navigator’s assessment of habitat suitable for foxes while avoiding

Experimental Areas and Bait Stations The original field baiting experiments were initiated in southwestern Ontario. A high concentration of local fox trappers in that region supplied abundant survey specimens and assisted in baiting trials (see Chapter 35). After initial ground-baiting experiments (1972 to 1974), OMNR launched trials in Huron and Grey Counties in 1975, to compare the effectiveness of ground versus aerial baiting. About 3600 meatball baits, in plastic bags, were tossed from the open window of a Cessna 150 airplane flying 100 metres above ground level (AGL) on what were termed bait stations (known fox den sites), at 60 baits per station. In addition, 8150 meatball baits were distributed by ground teams on similar sites. Bait acceptance in foxes appeared comparable for ground (43%) and aerial distribution (40%).

Perfecting the Aerial Baiting System From 1976 to 1987, OMNR distributed baits on 15 experimental plots ranging from 300 to 760 km2, to develop an

Figure 19.2: Flight-lines along the wooded areas between concession road grids. The road grid is an artefact of ­Ontario’s eighteenth- and nineteenth-century rural survey patterns (­Harris & Warkentin, 1974, pp. 123–126).

Figure 19.1: Rudimentary flight-line planning on a 1:50,000 topographic map: the rural road grid. Source: OMNR.

Source: OMNR.

314

The Development of Aerial Baiting

dropping baits on settled areas and in schoolyards, large bodies of water, roads, golf courses, and in-use pastures. The baiter informed the navigator when each lot unit had been ­deployed, which the navigator marked on the map. If that point did not approximate the planned demarcation, the navigator asked the baiter to increase or lower the drop rate to achieve the planned bait density.

The baiter opened each bag and tried to pitch handfuls of three or four baits at a time, while maintaining a rhythm to match the speed of the airplane. Originally, the baits were dispensed from the airplane’s rear window partly open. This was a busy and demanding task and many baiters were airsick. Flight-line planning and flight protocols remained similar throughout, modified slightly after 1980 by adding large wooded areas and standing corn as baitable areas. Bait drops were improved by installing a tray above the rear bench linked to a polyvinyl chloride chute angled out of the baggage hatch to the rear of the airplane, protruding below the fuselage (Plate 10 and Figure 19.4). OMNR installed a ­battery-powered metronome (Figure 19.4), which produced an audible beat, guiding the baiter to maintain an accurate drop rate. Given the target bait density, the rate was standardized to one bait per second (60 beats/minute) at an air speed of 130 kilometres per hour. The standard rate was varied from 50 to 70 beats/minute to adjust for changes in ground speed caused by variable wind conditions since estimating the ground speed while airborne was difficult and inaccurate. Communication between the navigator and the baiter was improved by wiring an audible horn and a red flashing signal light into the metronome to tell the baiter to stop or start. Flight-lines in experimental areas were generally 25 to 30 kilometres long and one flight, typically 1.5 to 2 hours, covered only a portion of the entire area. At the end of a flight, the aircraft returned to the airport to reload and then continued

Figure 19.3: Early packaging and dispensing of baits for dispersal from Cessna aircraft. The plan was to dispense the baits in demarcated segments along flight-lines, one lot per segment, to attain a predetermined bait density (baits per km2). Source: OMNRF.

Figure 19.4: Making baiting easier with a tray (above the rear seat of the Cessna ­aircraft) linked to an exit funnel (•), ­connected to a 1.3-metre (15-centimetre diameter) ­polyvinyl chloride chute and a metronome (•) that governed the bait dropping rhythm with an audible beat. Source: OMNRF.

315

The Development of Vaccines and Delivery Systems

baiting at the point where it left off on the previous flight. It took seven to eight hours (three to four flights per aircraft) to complete each area and, depending on the bait density, to distribute up to 24,000 baits. Because of habitat variations and flight-line deviations, inaccurate ground speed estimates, and differences in road spacing, target bait densities were not always achieved. In those early trials, fox bait acceptance ranged from 37% to 74% (Bachmann et al., 1990). Furthermore, the bait acceptance did not appear to improve significantly at densities greater than 20 baits per km2 (MacInnes, 1988). The planned number of baits per km2 was the f­ oundation for calculating bait inventories. Bait density combined with flight-line spacing was the crux of flight-line planning. Planned bait dispersion and aircraft ground speed determined the drop rate (baits/second).

innovations, including baits designed for mass production, automated bait dispensing, and improved flight planning and navigation.

Larger Aircraft: The Twin Otter The ideal aircraft required a good payload, cabin space, long flight range, low-speed manoeuvrability, and safe low-altitude capabilities. Fortunately, the OMNR Provincial Air Service (OPAS) had a fleet of aircraft intended primarily for fighting forest fires. OPAS was founded in 1924 to find fires in large northern forests and transport crews to fight them (West, 1974, pp. 30–33). Pilots, flight crew, and maintenance staff were full-time OMNR staff, so the planes were available for a variety of roles, including aerial photography, fish stocking, wildlife surveys, and many research applications. Given that range of functions, OMNR pilots were skilled in many types of flying. Ground service crews travelled with the aircraft, but major repairs required return to a permanent base. A critical feature for the rabies program was that pilots and crews were full-time OMNR staff, and the planes had permanent bases with experienced maintenance staff and more equipment. Thus, the rabies program paid internal OMNR rates per flight hour, which were substantially less than commercial charter rates. The aircraft of choice was the de Havilland DHC-6 ­Series 300 Twin Otter, which had short take-off and landing c­ apability (Plate 11). Adapted for forest firefighting, but also used in passenger and material transport, surveys, and aerial photography, its useful load (fuel, crew, and payload) is about 2300 kilograms. Given its extensive use in aerial photography and equipment transfers, a 4­4-centimetre circular hatch allowed modification for dropping baits through the fuselage at the rear of the cabin. Test flights in 1988 verified very low-altitude capabilities (75 to 80 ­metres AGL); the optimal estimates for baiting were 150 to 250 ­metres AGL. The range and endurance of the Twin Otter is approximately 1430 kilometres and 5 hours. Two other single-engine airplanes were considered for the job: the single-engine DHC-2 Turbo Beaver, the Twin Otter’s smaller cousin; and the Cessna 208 Caravan. The deciding factor was safety – if one of the Twin Otter’s turbine engines failed, the other engine would keep the aircraft airborne.

Assessing Early Results In the 1988 trials, baits were distributed by ground teams, but only 35% of foxes ate them. The Cessna airdrops reached significantly more foxes, thus convincing the OMNR team that aerial distribution was more efficient and effective. Cessnas, costing $130 per hour (1980 rate), had a limited load capacity (2000–2500 baits) and their range was inadequate for larger areas. The rabies enzootic area in southern Ontario was almost 100,000 km2,, and any field campaign was expected to cover from 30,000 to 60,000 km2 annually, depending on the regional prevalence of rabies. A flight began with ferry time to get from the airport to the start of baiting, and ended after getting back to the airport after baits had all been dropped. The actual time on bait lines was divided into on-time, when baits were being dropped, and off-time, when the navigator switched the machine off over unsuitable habitat. Minimizing ferry time cut costs. In the small-scale experiments, the Cessna could cover only 550 km2 per day, and had to return to base frequently for more baits; ferry time was up to 30% of the overall flying time (MacInnes et al., 1992). The limited range of the Cessna required up to five different operational bases to bait large areas. Four Cessnas needed 15 to 20 days to cover 30,000 km2, not including delays caused by bad weather.

Wildlife Rabies Control in Southern Ontario

Automated Bait Production and Distribution

The success of the initial trials led OMNR to implement a rabies control experiment in 1989 in southeastern Ontario, on an area of about 30,000 km2 (MacInnes et al., 2001). That plan required a more efficient aircraft plus complementary

OMNR expected to drop up to a million baits a year, so mass production and handling methods were essential for successful operations. The meatball bait used from 1975

316

The Development of Aerial Baiting

to 1986 was clearly not suited for a large-scale program. The need was for a compact, light, and robust bait using readily available ingredients with a simple shape that was suitable for mechanization of production and distribution. The Ontario bait (OB), the first production bait, was a fat- (oleo) and wax-based bait matrix that was attractive to foxes and skunks and well-suited for mass production (see Chapter 17b). The machine that made the baits loaded them into custom designed cardboard trays, which were then loaded into rugged cardboard cartons, sized so they would fit neatly onto a commercial wooden pallet that could be handled by a forklift tractor. Carton and pallet sizes were designed to fit snugly into freezer-equipped tractor-trailer transports. From the production machine,

the pallets of boxed baits were moved to a large commercial freezer room for storage at −20°C to maintain vaccine potency (Lawson & Bachmann, 2001). From there they were loaded into freezer trailers and hauled to the airfield. The OB measured 3.5 × 3.5 × 2 centimetres. Each tray held six rows of 24 baits stored on edge, and there were eight trays, thus 1152 baits in a carton. The trays were transferred to plastic tubs at the airfield, to make them easier to load and handle in the aircraft. The tubs were stored at −20°C in the freezer trailer until they were loaded onto the aircraft (Lawson & Bachmann, 2001). The full tubs were braced by a cargo net directly behind the cockpit (location B in Figure 19.5). One full tub weighed about 26 kilograms. When the OB was modified to the smaller Ontario slim bait (OS) there were

Figure 19.5: Baiters loading the bait conveyor belt. Location A is the cockpit; B is the stored baits; C1 is the bait-loading platform; C2 shows baits on the conveyor belt; C3 is the cover over the rotating drum with fingers to pick up the baits and direct them down the chute. The distance from A to C3 is five metres. Source: OMNRF.

317

The Development of Vaccines and Delivery Systems

1728 per carton, and with the much reduced ultralite bait (UL), in bagged lots there were 3240 or 3600 per carton.

Automated Bait Dispensing The speed of the Twin Otter meant that a baiter could not throw baits at a steady rate for long periods. Ontario considered two proposals for an automated bait ejection system: (1) a giant roll of two layers of plastic with regularly spaced baits between the layers – when the layers were pulled apart the baits would pop out and fall down the hatch, and (2) a conveyor belt on which baits were loaded and then picked off by protruding metallic fingers at the end of the belt then dropped down the hatch. Both systems proposed a variable speed control to link baiting rate to aircraft ground speed, thus controlling bait density. The simpler conveyor belt system designed by Inoform/Demand Maintenance Ltd was chosen. It included an electronic control panel designed by Redford Robotics to monitor the bait machine and record the number of baits dropped (Figure 19.6). The bait machine was bolted in the centre of the cabin. It consisted of a loading platform, the conveyor belt, and a rotating drum, with a series of staggered fingers, directly above the hatch through the floor (Figure 19.5 and 19.6). The rotating drum was driven by an electric stepper motor with DC power (28 V) supplied directly from the airplane. During operational flights, the baiters, each straddling the side of the conveyor, removed a bait tray from a tub, placed it on the loading platform and pushed the baits by hand onto the conveyor belt rows, which matched the rows of the tray (Figure 19.5). The conveyor belt advanced the baits towards the rotating drum, where each finger plucked and flicked a bait (Figure 19.6) down the hatch through a chute (Figure 19.7). In the earlier years, wax fragments of oleowax baits would build up on the drum and fingers, causing obstructions and snags. The accumulated wax was removed in flight by the baiters with scrapers and more thoroughly while the airplane was on the ground between flights with electric heat-guns and solvent. The chute could be closed manually to prevent baits from falling out accidentally. With the advent of the UL in 2006, the partitioning tracks and drum were removed; baits were simply scattered evenly on the conveyor belt and allowed to tumble down the hatch.

Figure 19.6: Rotating drum with a protruding finger picking up a bait from the conveyor and flicking it down the chute. The rear control panel is on the right. Source: OMNRF.

rate, switch the conveyor belt on and off, record the on- and off-times, and tally the number of baits dropped. A second panel (Figure 19.6), on the machine itself, displayed the baiting machine status (on/off) and had an override off switch in case of a machine problem. COUNTING BAITS

The number of baits required for a flight was based on the baiting area (km2), bait density (baits per km2), and an estimate of off-time, which was proportional to the area of excluded habitat. Typically two additional tubs were loaded per flight. The tally of baits dropped during a flight was based on (1) the difference between baits loaded and baits remaining on board, and (2) the record from the bait machine control panel. Typically, the two results differed only by 2% to 3%.

Bait Machine Control Panel A control panel in the cockpit (Figure 19.8) (MacInnes et  al., 1992) allowed the navigator to vary the bait drop

318

The Development of Aerial Baiting

Figure 19.7: The dispensing chute in a Twin Otter. Source: OMNRF.

Flight Navigation In 1989, the OPAS Twin Otters were equipped with LORAN-C navigation receivers. The LORAN module ­ ­received radio signals from ground transmitter stations and used those signals to triangulate the aircraft’s position (latitude and longitude coordinates). A series of coordinates could be loaded into a module’s memory to assign waypoints representing flight-line start and end positions. The airplane would simply fly planned flight-lines from waypoint to waypoint (Plate 12) using the LORAN beacon (Leptich et al., 1994). The modules in the aircraft were portable and interchangeable; one unit could be loaded for an upcoming flight while the other was airborne. Unfortunately, the memory of a module was limited and data entry was slow – numbers representing the latitude and longitude coordinates of individual waypoints were entered sequentially with a rotating knob. LORAN also calculated and displayed the aircraft ground speed. With this number and given the desired bait dispersion, the navigator could adjust the baiting rate via the control panel (Figure 19.8: control A) using a chart, known as the Bachmann table (Table 19.2), which shows the interrelationships of the baiting rate with ground speed and desired bait dispersion.

Figure 19.8: The bait machine control panel in the cockpit showing various timers/tallies (B, E, D, F); the bait rate control (A); and the bait on/off switch (C). Source: OMNRF.

were assembled into mosaics to make flight-line plots more manageable. Adjoining the maps, each 80 centimetres × 65 centimetres, required a large floor space (Figure 19.9), and minor variations in contiguous map sheets made precise alignment arduous and in some cases unachievable. Differences in the survey patterns of adjacent townships, and hence road alignments, impaired

FLIGHT PLANNING AND WAYPOINTS

Initially, flight-lines were plotted on National Topographic Series (NTS) paper maps (1:50,000) to establish the waypoints for LORAN input. In 1989, the plans for southeastern Ontario covered approximately 20,000 km2, or 150 townships, requiring more than 80 maps. Since flight-lines could span several maps, individual maps

319

The Development of Vaccines and Delivery Systems

Table 19.2  A Bachmann table. Using the ground speed from LORAN-C (or GPS) and knowing the planned bait dispersion, the navigator looked up the appropriate baiting rate (baits per second) and used the control panel (Figure 19.8) to set the baiting rate (e.g., at 250 kilometres per hour and a bait dispersion of 40 baits per flight kilometre, the bait rate was set at 2.8 baits per second). Eventually the BAITTRAK system automated the entire procedure. Aircraft Ground Speed Knots Miles per Hour Km per Hour

105 121 194

110 127 204

120 138 222

125 144 232

130 150 241

Baits per Flight-Km (Bait Dispersion) 12 14 16 18 20 22 24 26 28 30 32 34 36 38 40 42 44 46 48 50 52 54 56 58 60 62 64 66 68 70 72 74 76 78 80

135 155 250

140 161 259

145 167 269

150 173 278

155 178 287

160 184 296

165 190 306

0.9 1.0 1.2 1.3 1.5 1.6 1.8 1.9 2.1 2.2 2.4 2.5 2.7 2.8 3.0 3.1 3.3 3.4 3.6 3.7 3.9 4.0 4.2 4.3 4.5 4.6 4.8 4.9 5.1 5.2 5.4 5.5 5.7 5.8 6.0

0.9 1.1 1.2 1.4 1.5 1.7 1.9 2.0 2.2 2.3 2.5 2.6 2.8 2.9 3.1 3.2 3.4 3.5 3.7 3.9 4.0 4.2 4.3 4.5 4.6 4.8 4.9 5.1 5.2 5.4 5.6 5.7 5.9 6.0 6.2

1.0 1.1 1.3 1.4 1.6 1.8 1.9 2.1 2.2 2.4 2.6 2.7 2.9 3.0 3.2 3.3 3.5 3.7 3.8 4.0 4.1 4.3 4.5 4.6 4.8 4.9 5.1 5.3 5.4 5.6 5.7 5.9 6.1 6.2 6.4

1.0 1.2 1.3 1.5 1.6 1.8 2.0 2.1 2.3 2.5 2.6 2.8 3.0 3.1 3.3 3.5 3.6 3.8 4.0 4.1 4.3 4.4 4.6 4.8 4.9 5.1 5.3 5.4 5.6 5.8 5.9 6.1 6.3 6.4 6.6

1.0 1.2 1.4 1.5 1.7 1.9 2.0 2.2 2.4 2.5 2.7 2.9 3.1 3.2 3.4 3.6 3.7 3.9 4.1 4.2 4.4 4.6 4.8 4.9 5.1 5.3 5.4 5.6 5.8 5.9 6.1 6.3 6.5 6.6 6.8

Baits per Second (Baiting Rate) 0.6 0.8 0.9 1.0 1.1 1.2 1.3 1.4 1.5 1.6 1.7 1.8 1.9 2.1 2.2 2.3 2.4 2.5 2.6 2.7 2.8 2.9 3.0 3.1 3.2 3.3 3.5 3.6 3.7 3.8 3.9 4.0 4.1 4.2 4.3

0.7 0.8 0.9 1.0 1.1 1.2 1.4 1.5 1.6 1.7 1.8 1.9 2.0 2.2 2.3 2.4 2.5 2.6 2.7 2.8 2.9 3.1 3.2 3.3 3.4 3.5 3.6 3.7 3.8 4.0 4.1 4.2 4.3 4.4 4.5

0.7 0.9 1.0 1.1 1.2 1.4 1.5 1.6 1.7 1.9 2.0 2.1 2.2 2.3 2.5 2.6 2.7 2.8 3.0 3.1 3.2 3.3 3.5 3.6 3.7 3.8 4.0 4.1 4.2 4.3 4.4 4.6 4.7 4.8 4.9

0.8 0.9 1.0 1.2 1.3 1.4 1.5 1.7 1.8 1.9 2.1 2.2 2.3 2.4 2.6 2.7 2.8 3.0 3.1 3.2 3.3 3.5 3.6 3.7 3.9 4.0 4.1 4.2 4.4 4.5 4.6 4.8 4.9 5.0 5.1

0.8 0.9 1.1 1.2 1.3 1.5 1.6 1.7 1.9 2.0 2.1 2.3 2.4 2.5 2.7 2.8 2.9 3.1 3.2 3.3 3.5 3.6 3.7 3.9 4.0 4.1 4.3 4.4 4.5 4.7 4.8 4.9 5.1 5.2 5.4

0.8 1.0 1.1 1.3 1.4 1.5 1.7 1.8 1.9 2.1 2.2 2.4 2.5 2.6 2.8 2.9 3.1 3.2 3.3 3.5 3.6 3.8 3.9 4.0 4.2 4.3 4.4 4.6 4.7 4.9 5.0 5.1 5.3 5.4 5.6

0.9 1.0 1.2 1.3 1.4 1.6 1.7 1.9 2.0 2.2 2.3 2.4 2.6 2.7 2.9 3.0 3.2 3.3 3.5 3.6 3.7 3.9 4.0 4.2 4.3 4.5 4.6 4.8 4.9 5.0 5.2 5.3 5.5 5.6 5.8

Source: compiled from OMNR data.

woodlot uniformity, the feature used for planning in smaller experimental plots in southwestern Ontario. Initially, parallel flight-lines were plotted allowing 1.0 kilometres flight-line spacing in forested areas; this was increased to 1.3 kilometres to approximate one flightline per concession over the fabric of the fragmented farmland townships. The result was over 800 waypoints. Flight-lines were plotted such that the first waypoint started and last waypoint ended as near as possible to the operations airport base to minimize ferry time (Plate 12).

Waypoint values where checked before entry but occasional errors occurred, especially in loading the modules. One flight-line had the next stop in Nanortalik, Greenland, and another had a flight going over New York state! Also, LORAN triangulation errors could be as high as ±200 metres, thereby increasing uncertainty about flight-line accuracy. The Geographic Positioning System (GPS) replaced LORAN after 1993 and reduced positioning errors to less than ±50 metres (an estimate also confirmed by Leptich et al., 1994). The GPS units had a serial interface so waypoints

320

The Development of Aerial Baiting

Figure 19.9: Flight planning in the old style required extensive floor space to encompass large baiting areas with 1:50,000 topographic maps. Source: OMNRF.

deviations to bait acceptance. Tinline (personal communication, ­September 1994) also found very little difference in off-time estimates when flight-lines were projected parallel, perpendicular, or diagonal to road grids. That meant that flight-lines could be plotted indiscriminately, regardless of the grid, thereby simplifying flight-line planning and flights. In 1989 and 1990 extra baits were dropped on baitable habitats to compensate for areas that were not baited (i.e., excluded areas). After 1990 an off-time factor, proportional to excluded areas, was applied to arrive at a net area (= inclusive areas only) for calculating bait numbers. At first, off-time was estimated at 20% (farmland) and 25% (woodland) and subsequently adjusted using data from previous years’ baiting campaigns. Those estimates were further modified after 1998, when the addition of raccoons (Procyon lotor) and skunks as target species necessitated changes to bait density, flight-line spacing, and bait type (see Chapter 10). With the introduction of the BAITTRAK, discussed later in this chapter, system changes could be simply reprogrammed.

were uploaded directly to the receiver units from a computer database.

Refinements In the Aircraft Most of the seats were removed from the aircraft cabin to make room for the bait machine, retaining only seats needed for the bait crew, so they could be seated during take-off and landing. Before the bait machine was installed, the cabin floor was covered with a plastic sheet to facilitate easy to clean up before the plane went back to its regular service. A custom cargo rack was built to firmly secure the tubs of baits. OMNR OPAS adapted the aircraft communication system so that the bait crew could communicate using headphones sets that connected them to the pilot, the navigator, and each other.

Bait Density and Flight-Line Spacing

Aircraft

Until 1993 small-scale experiments continued, some without vaccine, to fine tune baiting protocols and found little or no difference in fox bait acceptance at 2.0 kilometres flight-line spacing and the standard bait density of 20 baits per km2 (MacInnes et al., 2001). In 1992 flight-line spacing was 1.8 kilometres and this was increased to 2.0 kilometres in 1994 and maintained after without any major

HELICOPTERS

The greater manoeuvrability of helicopters and their ability to hover proved advantageous for precision baiting in confined rural and semi-urban or urban tracts. In 2002 OMNR used a Bell 206 L1 Long Ranger II to drop baits to target

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The Development of Vaccines and Delivery Systems

foxes in urban Sudbury (the Long Ranger was 10.1 metres long, had a wingspan of 11.3 metres, a cruising speed of 195 kilometres per hour, and a useful payload of 875 kilograms). The Long Ranger was also used in 2006 and 2007 along river ravines in Greater Toronto and in 2008 and 2009 in Niagara Region, Guelph, and Cambridge. After 2009 OMNR tackled outbreaks of rabid skunks in southwestern Ontario on focused eight-kilometre by eight-kilometre plots and continue to bait semi-urban areas of the Niagara Region with a Eurocopter EC 130 B4. This helicopter was similar in size to the Long Ranger (10.6 metres long, wingspan 10.6 metres) but was faster (210 kilometres per hour) and had a larger payload (1050 kilograms). Baits were thrown from helicopters manually through an open window or door. Since 2002 about 314,000 baits have been distributed with helicopters.

coordinates from flight-lines drawn on paper maps using AutoCAD software. Eventually, this culminated with a flightline planning package (FLTPlan) developed by the Queen’s GIS Lab using digital maps to produce flight-line information to be displayed on a screen in the cockpit (­ Hauschildt et al., 2001). In effect, flights were planned on digital maps on the computer then uploaded and retraced in the air by the aircraft. Imbedded in this software were protocols for crew assignment, flight management, and monitoring. Flight plans were created with FLTPlan, an application based on AutoCAD Map 2000 and Microsoft ACCESS database software. FLTPlan creates a project that is linked to an AutoCAD drawing. Each project contains airport, ­aircraft, crew, and flight information. Flight-lines within a flight, or entire flights within a project, may have different bait densities and off-time estimates, but they must have the same flight-line spacing. As each flight-line is chosen, the operator assigns a bait density and an estimate of offtime. FLTPlan keeps a running account of flying time as the operator adds flight-lines to a specific flight. Flying time is determined by (1) the maximum gross take-off weight of the aircraft (the weight of the empty aircraft plus fuel, crew and payload) and (2) the time duration that staff can work comfortably in the cabin of the aircraft without fatigue or sickness. Although flights of up to five hours were possible, crew fatigue/sickness limited flights to two to four hours. All information entered in FLTPlan was stored in a number of different tables in ACCESS, which is data management software. The main database was copied to the aircraft’s onboard GPS before take-off. The waypoints (­latitude and longitude) for each flight-line were used by the GPS to navigate the flight. Flight planning involves identifying a suitable airport, selecting a group of flight-lines, and assigning the correct bait density and off-time estimate to each line. However, several factors affect these choices. Flight-lines were almost always parallel to one another, but ferry times and flight time through air space of major airports had to be minimized. Where possible, flight-lines were perpendicular to water bodies and ran parallel to international borders, river valleys and mountain sides, for safety. Special permission and planning were often required when flying near or over restricted zones, such as army bases, nuclear plants or penitentiaries; and over national and provincial parks; national historic sites; and Indigenous lands. Federal Aviation Administration (FAA) charts, recently available in digital format from AeroNav Services, were added as a layer in AutoCAD. Those maps provided pilots with detailed information on airports, radio frequencies,

PIPER PA31–350 NAVAJO CHIEFTAIN

The Piper Navajo Chieftain, a low-wing piston-engine twin airplane, also has a floor hatch similar to the Twin Otter. The Chieftain (length: 9.9 metres, wingspan: 12.4 metres, cruising speed: 360 kilometres per hour, and useful payload: 1275 ­kilograms) is smaller and less expensive than the Twin Otter. With the development of smaller and lighter baits, this aircraft was more economical to operate. To fit over the floor hatch in the Chieftain, the baiting machine conveyor was adapted to rotate forwards (Bachmann & Silver, 2004). The Chieftain was used in 2004 and 2005 in New York State, Vermont, and New Hampshire to target raccoons, accumulating 82 hours and distributing about 795,000 coated-sachet baits (CS). ­Unfortunately, the OPAS Navajo Chieftain was sold in 2006. DHC-2T MK III TURBO BEAVER

In 1994 the OPAS Turbo Beaver was used to distribute about 6000 baits along river ravines south of Bradford, Ontario, and bait a limited sector south of Ithaca, New York. The Turbo Beaver cabin proved too cramped for a bait machine, and there were concerns for the safety of singleengine aircraft at the low altitudes used for baiting.

Digital Flight Planning The process of reading waypoint coordinates from maps and entering them by hand was slow and prone to error. In 1993 GPS receivers replaced LORAN-C. GPS receivers could upload waypoint information via a serial port. In 1994 the Geographic Information Systems (GIS) Lab at Queen’s University, in collaboration with the OMNR Rabies Research Unit, developed a process for digitizing waypoint

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The Development of Aerial Baiting

hazards (e.g., towers), restricted zones, water bodies, and local topography. Pilots received a printout of each flight with the most up-to-date FAA chart. The navigator received a checklist of tasks to be completed before each flight and a printout of all flight-lines to be flown during the assigned flight. The navigator recorded the number of baits dropped along each line against a predetermined table of estimates. The number of baits dropped was calculated at the end of the flight, as discussed.

BAITTRAK In 2002 the OMNR Rabies Research Unit worked with OES Inc and the Queen’s University GIS Lab to develop the BAITTRAK system to control bait dropping and provide navigation assistance for the pilot. The system consisted of a GPS unit independent of the aircraft’s GPS and a computer to manage flight information, data input, and storage and the baiting rate. Additional components of BAITTRAK included an on/off switch in the cockpit (Figure 19.10) and a cockpit display showing ground speed, bearing, and distance to waypoints (Figure 19.11). It also had a display showing the airplanes path and a display for the navigator showing bait rate and numbers. It served as a communications hub for the cockpit crew and baiters, and its computer stored waypoints, baiting rate, and bait numbers (Figure 19.12). The bait controller, at the rear of the baiting machine, controlled the bait conveyor and was the communications hub for the computer and cockpit displays.

Figure 19.10: The on/off switch pendant for the navigator. Compare this simple arrangement to the original navigator control panel in Figure 19.8. The S/F switch is a manual mode for decreasing or increasing the speed of the rotating drum and thereby decreasing or increasing bait densities. Source: OMNRF.

Figure 19.11: The BAITTRAK cockpit display. When the aircraft is flying on a flight-line, the small black triangle is centred at the top of the display. Source: OMNRF.

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The Development of Vaccines and Delivery Systems

Figure 19.12: The BAITTRAK computer display panel at the rear of the aircraft is linked to the bait machine via the bait controller. The coordinates of the waypoints of one flight are displayed here. Source: OMNRF.

concern to maximize fox and skunk encounters with the baits and minimize wasted baits and human contact with them. The test baits used in the experiments (see the next two sections of the text) were the same as those being used operationally, only with an inert liquid (two millilitres) to simulate the oral vaccine. Bait scatter experiments were launched to address the fate of baits dropped from aircraft by assessing (1) the ­extent of deviation, or drift, from the original point where the baits were released to the target, (2) bait spread or ­scatter, and (3) possible controls. In those experiments, baits were dropped by 20s or 30s (sometimes up to 100s), from Twin Otter aircraft, and teams recovered as many baits as possible, recording precisely where each landed on the ground to map a scatter profile.

Data created with FLTPlan and stored in ACCESS were copied to compact flashcards or, more recently, USB drives, and then read into the BAITTRAK computer. With all flights in memory, the navigator could access any flight or select additional flight-lines should an assigned flight be diverted by bad weather. The BAITTRAK computer automatically adjusted the baiting rate to the speed of the aircraft, allowing the navigator to concentrate on dropping baits only on suitable sites. An override switch allowed the navigator to change bait densities manually in rabies hot spots or under-baited areas (Figure 19.10). When the flights were completed, the actual flight data were compared to pre-planned flight-lines (Figure 19.13). That information detailed the drop location of individual bait lots as required by Canadian federal authorities and provided evidence of the exact locations of dropped baits in case of litigation. Finally, these provided a good record of baited and excluded areas for future off-time projections. Differences between planned and actual bait deployment could affect the level of bait uptake by target species and thus might require remedial action.

BAIT SCATTER EXPERIMENT AT MACFARLANE LAKE, 1988

In initial experiments near Sudbury, OB (20 grams) were dropped on a frozen lake that was slightly snow covered in mid-winter from 90, 150, 245, or 305 metres AGL, with a 25 kilometres per hour west wind. Finding the dark green baits on the white surface of the lake was easy but intermittent snowfall concealed many. In tail winds, the baits landed directly on or within 150 metres forwards of the target, but in head winds they landed 300–500 metres behind the target. In cross-winds impact was 0–75 metres forward of the target, 25–150 metres leeward, and, as expected, bait

Scatter of Airdropped Baits The scatter of baits falling from a moving aircraft was influenced by the shape and weight of the bait, speed and altitude of the aircraft, wind speed and direction, and turbulence (Skews, 1991). The cost of baits was an ongoing

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The Development of Aerial Baiting

Figure 19.13: BAITTRAK data output provides a record of the actual flight-lines (Flights 7, 8, 9), as flown, superimposed on planned flight-lines, as originally drawn (straight lines). Source: OMNRF.

The drift of CS was 64% greater than OS and UL. The scatter area of the lighter CS was only 80% that of the other two baits, but because many had drifted outside the search zone, that estimate was minimal (Table 19.3). In a 33  ­kilometres per hour crosswind, CS landed up to 235 ­metres from the target. Scatter and drift of OS and UL were similar in most wind conditions (Table 19.3). In reality, the path of baits cannot be controlled after they leave the aircraft, given the influences of wind and prop wash. Navigators did their best to drop baits on suitable areas. Flights were generally maintained at 150 metres AGL, especially while dropping lighter baits such as CS and UL.

scatter increased by 33% at 305 AGL. Propeller turbulence increased the effect of the wind. A tail wind more or less neutralized the prop wash, so baits landed directly on or slightly forwards of the target. BAIT SCATTER EXPERIMENTS AT EARLTON, 1999, AND BROCKVILLE, 2005

At Earlton airport, scatter patterns of the OS (13 grams), fish-meal polymer (FP, 23.6 grams), and CS (2.2 grams) baits were examined (Brown, 2001). The baits were dropped over a target marker from 150 metres, at 250 to 270 kilometres per hour ground speed, in still air or in various winds. A handful of red chalk dust was released with each group of baits to mark the drop target. Wind direction was variable (Figure 19.14). Overall, the scatter of the very light CS was 22% greater than the bulkier FP and OS (Table 19.3, Figure 19.14). The difference in scatter and drift of FP and OS was negligible. Those experiments confirmed that the wind and prop wash can significantly affect the scatter of baits. On a recently harvested cornfield near Brockville, the scatter of UL (4 grams), OS, and CS baits were examined. UL, a much smaller modification of OS, was intended for skunks but could also be eaten by foxes and raccoons. The baits were dropped in variable winds. Scatter was greater for baits dropped from 245 metres than from 150 metres (Table 19.3).

Bait Survival It was essential that the bait and vaccine container remain intact when dropped from an aircraft so that a target animal could be immunized if it ate the bait. Plastic bags that were used with meatball and sponge baits provided an airfoil that slowed the fall and helped keep those baits intact on impact. The fat-wax baits depended solely on the bait matrix and durability of the vaccine container to survive. To ensure that airdropped baits could withstand a ground impact, some throw and drop survival experiments were conducted from 1987 to 2004 to assess bait matrix damage and liquid loss, or leakage, from the vaccine container.

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The Development of Vaccines and Delivery Systems

Figure 19.14: Bait scatter profiles (Earlton). In the bait scatter experiments test baits were dropped on a target point (•) and then as many baits as possible were recovered to map a scatter profile, an area delineated by the outermost recovered baits. Experimental essentials included a test plot (about 500 metres × 500 metres) and labelled baits to identify variables (altitude, wind direction). As a visual cue for ground observers to register the target, a very visible pigmented (red) chalk was released with each bait ejection. The figure shows scatter profiles of FP (--), OS (-----), and CS (·····) baits relative to the target (•) deployed from 150 metres AGL in various wind directions (b, c, d) and low or no wind (a). Source: OMNRF.

coated blister-pack (CB, 4 grams), and veggie slim (VS, 13 grams), which had vegetable oil instead of oleo in the attractant matrix, and UL. Baits were dropped from 150 m, frozen or unfrozen, onto grass or pavement. VS suffered the most damage, with 9% to 35% with matrix damage and 8% to 35% with leakage (Table 19.4). AS and CB suffered only 3% or 4% matrix damage or liquid loss, and there was variation related to surface type and whether baits were frozen or not. UL, with one exception, had only minor damage and no leakage at all. UL was first used operationally in 2006. As expected, baits falling on the hard surface sustained the most damage and leakage. Fortunately, the targeted habitats in rural areas during operational baiting were mostly relatively soft and pliable surfaces, such as loose soil, grass or fallen foliage. Frozen baits generally appeared to be more robust – a real benefit; most of the baits transferred from freezer transport storage are still frozen while being dispersed on individual flights.

BAIT SURVIVAL EXPERIMENTS AT MAPLE RESEARCH STATION

Handmade OBs were thrown against a cement wall. That caused minor fractures or dents to the fat-wax matrix but no leakage from the vaccine container. Next, baits were dropped from a 50 metres water tower onto lawn and gravel surfaces. OB prototypes sustained minor surface damage but, again, no leakage. In the first aerial test in 1988, OBs were dropped from a helicopter flying 150 to 305 metres above the ground onto grass, pavement, or gravel. As expected, baits dropped on a hard surface sustained more damage (64%) than on a soft surface (7%), as did baits dropped from 305 metres (25%) than lower levels (19%). There was no leakage in any of those tests. BAIT SURVIVAL EXPERIMENT AT TRENT UNIVERSITY, PETERBOROUGH

In 2004 the helicopter drop was repeated with three diminutive variations of OB: Artemis sachet (AS, 4 grams),

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Table 19.3  Results of bait scatter experiments, 1999 and 2005. Bait Scatter Drift (m) Year

Wind Condition

AGL (m)

Bait type

1999

No/low

150

Cross (40° fore)

150

Head (60° port)

150

Tail (60° star-b)

150

No/low

150

FP OS CS FP OS CS FP OS CS FP OS CS UL OS CS UL OS CS UL OS CS UL OS CS UL OS CS UL OS CS

2005

245

Cross (3° aft)

150

245

Head (3° port)

150

Tail (3° star-b)

150

2

n

Area (000 m )

92 96 89 85 52 91 22 20 81 76 41 97 74 100 86 102 96 94 68 54 28 91 80 25 75 84 83 84 95 70

7.81 8.26 11.94 8.84 7.07 6.90 2.10 3.43 6.43 7.83 7.90 8.78 2.83 5.03 5.02 5.21 8.89 7.39 9.89 7.06 4.35 13.94 12.04 2.22 5.22 5.71 7.87 4.83 8.58 2.62

Mean

Min

Max

Site

35 38 101 37 53 145 55 64 211 50 56 134 33 40 47 91 61 173 124 98 176 182 138 235 56 47 128 88 88 122

2 4 44 3 10 96 31 33 165 6 15 96 3 9 12 20 6 56 83 46 132 135 91 184 4 6 31 19 34 65

68 119 185 89 133 201 78 92 261 95 123 178 73 94 111 191 119 225 194 133 223 254 200 256 95 86 224 274 254 263

fore aft aft fore aft port/aft port port port/aft port port port fore fore aft aft aft aft starboard starboard starboard starboard starboard starboard aft aft aft fore fore fore

Source: compiled from OMNR data.

Table 19.4  Results of bait survival experiment at Trent University, 2004. Artemis Sachet

Coated Blister-Pack

Drop surface

Bait condition

Matrix Damage %

Liquid Leakage %

Matrix Damage %

Soft

Frozen

1.0 n = 182 3.6 n = 193 7.2 n = 221 4.0 n = 202 4.0 n = 798

0.5

0 n = 153 0.7 n = 145 0.9 n = 231 12.4 n = 193 3.7 n = 722

Unfrozen Hard

Frozen Unfrozen

Sum

0 5.4 3.0 2.4

Liquid Leakage % 0 0 0.9 12.4 3.6

Source: compiled from OMNR data.

327

Ultralite

Veggie Slim

Matrix Damage %

Liquid Leakage %

Matrix Damage %

0 n = 170 1.4 n = 72 0 n = 201 0 n = 141 0.2 n = 584

0

0 n = 249 1.3 n = 226 8.3 n = 145 34.6 n = 159 9.0 n = 779

0 0 0 0

Liquid Leakage % 0 0.9 2.1 34.6 7.7

The Development of Vaccines and Delivery Systems

The air and ground crews were permanent staff, predominantly from OMNR or, on occasion, Queen’s University. Most of the baiting crews were short-term hires. Regardless of their origin, the teams comprised remarkable and dedicated individuals.

Aerial Baiting Logistics, Routines, and Adversities Many steps were necessary for a successful baiting campaign. Baits were ordered six months in advance. OPAS aircraft were reserved: number and dates depended both on the extent of rabies that season and the timing of other priority needs for the planes, especially for fighting forest fires. Temporary staff were hired and trained depending on the number of baits to be spread. Accommodations and meals were arranged in advance. OMNR Rabies Unit personnel organized transport for all staff and materials, both from home to the operations bases and locally around the latter. They ensured that there were comfortable ground facilities at each airport to enable staff to relax and eat between flights. They also kept operations areas cleaned and rented dumpsters for disposal of discarded bait trays, and so on. OPAS brought their own staff to maintain the planes. The optimal base for operations was a small, low-traffic airport located near the centre of the baiting area. On site, Jet-A fuel for the Twin Otters was essential, although in a few cases a large fuel truck was rented for the operations. There had to be adequate space for staff and their gear and baits. Since the baits had to be kept frozen, they were often kept in the freezer trailer that brought them from the manufacturer. Smaller airports were ideal, having little competing traffic, simplified take-off and landing control, and quick turn-around times for refuelling and loading baits. Proximity to emergency response capabilities, retail outlets, and accommodations was important. A radius of less than 240 kilometres from the base to the boundaries of a baiting area allowed coverage of up to 45,000 km2 from a single site. Three of the more memorable venues were Irvine Lake (1990–1995), a landing strip in the middle of the forest near Mazinaw Lake; Brockville Municipal Airport (2000–2005), and Stratford Municipal Airport (1994–2013). Other sites include Collingwood in 2006 and 2007; Cornwall in 1989 and 1994; Hanover in 2011; Kingston in 1989 and 2010 to 2013; Orillia-Barrie-Oro in 1993 and 2008; Smith’s Falls in 2002; Toronto Island in 2005; Buttonville in 2006; and St Catharines in 2009 to 2014, as well as the many airfields in the United States, as far south as Pleasanton, Texas.

OPAS AIR CREW

Two OPAS pilots and one aircraft maintenance engineers (AME) were assigned to each Twin Otter. Pilots had ultimate control of the aircraft and were responsible for briefing all staff on all aspects of air safety operations. AME were responsible for maintaining, servicing, and fuelling the aircraft. BAITING CREW

One navigator and two or three baiters formed a b ­ aiting crew, and two such crews were assigned to each aircraft. The navigator sat beside the pilot, and they shared a ­computer-produced flight-line map on GPS. The navigator watched the habitat on the ground and switched the bait machine on and off as needed. The navigator recorded the numbers of baits dropped on each flight leg. On the ground, the navigator collected the map and data record for the next flight and made sure that the correct number of bait tubs was loaded. The navigator also entered the current flight map into the GPS system. Baiters loaded the bait tubs onto the airplane. In flight, they loaded baits onto the conveyor, kept the baiting machine running, and kept the cabin clean by loading empty trays into tubs. They ensured that tubs were held in place by cargo nets, in case of turbulence shaking the cabin. At the end of a flight, baiters tallied unused baits and cleaned the cabin and baiting machine before the next flight. The navigator recorded their count of unused baits on the flight sheet. GROUND CREW

The OMNR Rabies Unit coordinator managed all ground activities to make sure the operation ran smoothly. The radio operator kept in touch with the pilot when the plane was in the air, at least every 30 minutes, and kept a record of the requests and reports. The radio operator also prepared the flight manifests. Another technician kept physical track of the baits and tubs in both the freezer truck and the planes, and ensured that each flight had the correct number. Two technicians cleaned, maintained, and repaired the aircraft bait machines as appropriate. The onsite flight planner prepared and modified flight plans. After 2006 that role was done off-site using FLTPlan and BAITTRAK software and emailed to the airport.

Staff The wildlife rabies control aerial baiting team included the OPAS air crew, baiting crew, and ground crew managers.

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The Development of Aerial Baiting

average turbulence after two or three flights. Briefer flight times also helped.

Daily Routine Before any flying, briefings were held to inform and train staff in bait handling and loading procedures, bait machine operations, aircraft safety, and daily routines. Weather permitting, take-off was at first light depending on the time of year. Baits were loaded on the airplane and flight data uploaded into the BAITTRAK computer, and crews boarded their assigned airplanes. At the same time, a system check was performed on the aircraft and the engines were warmed up (which took about 10 minutes). Flights were routinely 2 to 2.5 hours but had been as long as 3 to 4 hours. On landing, assigned personnel removed garbage, cleaned or repaired the bait machine, refuelled the aircraft, loaded bait tubs, and programmed flight data (Plate 13). Provided that there were no unanticipated interruptions, the process took about 10 to 15 minutes. At the end of the day (6 to 8 pm), bait machines were thoroughly cleaned; any unused baits were returned to the freezer. Under optimal conditions, one Twin Otter could manage four to five flights per day covering 3200 to 4400 km2 and distribute 80,000 to 120,000 baits. Each flight was flown at 250 to 270 kilometres per hour and 150 metres AGL. Pilots attempted to follow flight-lines as much as possible, although it was challenging on windy days.

Baiting beyond Southeastern Ontario By 1994 baiting operations covered all rabies-prone areas of southern Ontario (see Chapter 10). Small parts of northern Ontario were occasionally infected by foxes dispersing from the south or from James Bay (Nadin-Davis et  al., 2006). All these events occurred where the boreal forest had been cleared for agriculture, creating fox habitat. In 1995 vaccination projects began in Quebec, New York State, and Texas. By the end of 2014 almost 80 million baits had been dropped, many of those in 13 US states, targeting raccoons, coyotes (Canis latrans), and grey foxes (Urocyon cinereoargenteus). Raccoons in New Brunswick were also targeted (Table 19.1). On a historical note: on 11 September 2001, two Ontario Twin Otters were dropping baits to contain raccoon rabies in West Virginia and Ohio when the 9/11 terrorist attacks hit New York City, Washington, and a site in Pennsylvania. All airplanes in US airspace were ordered to land immediately. One of the Twin Otters was baiting and had to land at the nearest airfield, in Charleston, West Virginia, some distance from the operations base in Youngstown, Ohio. The pilot had to request special permission to fly back to the home base. The request was granted a day and a half later. As far as is known, that Ontario Twin Otter was the only civilian aircraft to fly that day in the United States.

Weather Adverse weather hindered any aerial baiting operation. Flight altitudes of 150 metres to 200 metres required a ceiling of at least 350 metres for safety. Early morning starts during late summer were often delayed by fog. Flights operated normally in light rain but were grounded by heavy rain or thunderstorms. On a few occasions, planes had to land at a remote airport and even stay overnight. A few flights were aborted in mid-flight by bad weather. In such cases the navigator’s notes or later, the BAITTRAK system, enabled the plane to resume baiting at the exact location of the stoppage as the weather improved. Winds greater than 50 kilometres per hour caused such turbulence for low-level flying that aircraft were kept on the ground.

Reflections OMNR’s mandate to control and eliminate wildlife rabies over extensive areas has finally been realized. The full protocol to drop vaccine baits to control rabies took years to develop. OMNR has been fortunate in its association with very capable and dependable individuals and partners, including OMNR Rabies Research Unit (­ David Johnston, Dennis Voigt, Ian Watt, Charles MacInnes, Bruce Pond, Doug Gilmore, Sarah Fraser, Mike Pedde, Laurie Calder, Beverly Stevenson, Andrew Silver, Kim Bennett, Mark ­ Gibson, Kathryn MacDonald, and countless field technicians), Western Air Services (Bill Cruikshank), C ­ onnaught Laboratories (Ken Lawson), Inoform/Demand Maintenance (Derek Mancini, Paul Johannsen), Redford ­Robotics (Peter Smith), OPAS (all the pilots, aircraft maintenance engineers, and support staff), Queen’s University GIS Lab (Rowland Tinline, David Ball, Carolyn Fielding, Peggy Hauschildt), OES

Motion Sickness Motion sickness was a constant problem. The baiting crew had little opportunity to see the horizon out the cabin windows and were on their feet when the bait machine was running. The smell of the baits sickened some people. ­Anti-nausea pills helped, although most people adapted to

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Technologies (Michael Reeve, Mark Donkers), and Artemis Technologies (Andrew Beresford, Alex Beath). Those partnerships were remarkably effective in harnessing the facets of the aerial baiting program into a cohesive system

from bait production to baits on the ground. With time and experience, the precision of the baiting campaigns came to resemble military operations. Obstacles along the way were quickly removed.

Acknowledgments The authors appreciate the input of David Johnston, Johnston Biotech (formerly of Rabies Research Unit) for adding crucial information to this chapter and providing photographs. Kim Bennett, Mark Gibson, Chris Davies, Dennis Donovan, Beverly Stevenson, and Andrew Silver of Ministry of Natural Resources and Forestry, Wildlife Research and Monitoring Section, reviewed the manuscript and suggested vital revisions. Charlie MacInnes and Mark Gibson from OMNR provided the photographs reproduced in this chapter. Mike Coyne, of Aviation Services, updated terminology and specifications. The authors also thank the Air Service (formerly OPAS) staff for delivering safe and efficient operation during the aerial baiting programs.

References Bachmann, P., Bramwell, R. N., Fraser, S. J., Gilmore, D. A., Johnston, D. H., Lawson, K., ... Voigt, D. R. (1990). Wild carnivore acceptance of baits for delivery of liquid rabies vaccine. Journal of Wildlife Diseases, 26(4), 486–501. https://doi.org/10.7589/0090-3558-26.4.486 Bachmann, P., & Silver, A. (2004). The Piper Navajo and aerial rabies baiting. The Electric Firebird, October, 8–9. Brown, L. (2001). Dispersion of three different baits used to vaccinate coyotes, foxes, and raccoons against rabies. In Proceedings (speaker abstracts) of Rabies in the Americas: XII International Meeting on Advances in Rabies Research and Control in North America (pp. 56–57). Ottawa, ON: CFIA. Harris, R. C., & Warkentin, J. (1974). Canada before Confederation: A study in historical geography. New York, NY: Oxford University Press. 338 pp. Hauschildt, P., Tinline, R., & Ball, D. (2001). Outfoxing rabies. GPS World, 14, 34–41. Lawson, K. F., & Bachmann, P. (2001). Stability of attenuated live virus rabies vaccine in baits targeted to wild foxes under operational conditions. Canadian Veterinary Journal, 42, 368–374. Retrieved from https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1476515/ Leptich, D. J., Beck, D. G., & Beaver, D. E. (1994). Aircraft-based Loran-C and GPS accuracy for wildlife research on inland study sites. Wildlife Society Bulletin, 22, 561–565. Retrieved from https://www.jstor.org/stable/3783080 MacInnes, C. D. (1988). Control of wildlife rabies: The Americas. In J. B. Campbell & K. M. Charlton (Eds.), Rabies (pp. 381–405). ­Boston, MA: Kluwer Academic Publishers. MacInnes, C. D., Johnston, D. H., Bachmann, P., Pond, B. A., Fielding, C. A., Nunan, C. P., ... Tinline, R. (1992). Design considerations for large-scale aerial distribution of rabies vaccine-baits in Ontario. In K. Bögel, F.-X. Meslin, & M. Kaplan (Eds.), Wildlife rabies ­control (pp. 160–167). Kent, England: Wells Medical. MacInnes, C. D., Smith, S. M., Tinline, R. R., Ayers, N. R., Bachmann, P., Ball, D. G. A., ... Voigt, D. R. (2001). Elimination of rabies from red foxes in Eastern Ontario. Journal of Wildlife Diseases, 37(1), 119–132. https://doi.org/10.7589/0090-3558-37.1.119 Nadin-Davies, S, A., Muldoon, F., & Wandeler, A. I. (2006). Persistence of genetic variants of the arctic fox strain of rabies virus in southern Ontario. The Canadian Journal of Veterinary Research, 70, 11–19. Retrieved from https://www.ncbi.nlm.nih.gov /pubmed/16548327 Plummer, P. J. G. (1947). Preliminary note on arctic dog disease and its relationship to rabies. Canadian Journal of Comparative ­Medicine, 11, 154–160. Retrieved from https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1661247/pdf/vetsci00283-0004.pdf Skews, B. W. (1991). Autorotation of many-sided bodies in an airstream. Nature, 352(6335), 512–513. https://doi.org/10.1038/352512a0 Tabel, H., Corner, A. H., Webster, W. A., & Casey C. A. (1974). History and epizootiology of rabies in Canada. Canadian Veterinary Journal, 15, 271–281. Retrieved from https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1696688/­ Voigt, D. R., & Lotimer, J. S. (1981). Radio tracking terrestrial furbearers: System design, procedures, and data collection. In J. A. ­Chapman & D. Pursely (Eds.), Proceedings of Worldwide Furbearer Conference (pp. 1151–1188). Frostburg, MA: Worldwide Furbearer Conference. West, B. (1974). The Firebirds. Toronto, ON: Ministry of Natural Resources.

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Plate 1: (above and overleaf) The names and administrative boundaries of Canada over time, 1713–2001. For comparison, all but the Dobbs map use the same Lambert Conformal projection of Canada. Source: Used by permission from the Historical Atlas of Canada.

Plate 2: Uapikun Learns About Rabies (English and Innu-aimun). Source: Whitney, 2012.

Plate 3: Dufferin Division of Connaught Medical Research Laboratories, 1961. The red arrow points to Building 16 where the rabies vaccine for wildlife was developed in the 1980s. The yellow arrow points to Building 60 that was used for veterinary biologics and opened in 1960. Source: Sanofi Pasteur Canada (Connaught Campus) Archives.

Plate 4: The blister pack enrobing machine designed and built at Artemis by Alex Beath and Bob Whiteley with the help of some local contractors. The machine has been used for coating ultra-lite baits and is capable of placing many different bait flavours on the blister packs. Source: OMNRF.

Plate 5: The ONRAB vaccine production unit in 2012. Artemis Technologies Inc. Guelph, Ontario.

Plate 7: Blister pack bait in olefin wax matrix. In this instance a colourant had been added to the bait matrix to make them less visible to predators such as crows. Source: OMNRF.

Plate 6: A coated sponge and a raw sponge are at the centre of the picture. The baits on the left and right are in plastic bags – an experiment to slow the rate of fall for air-dropped baits to minimize cracks in the coating and protect the vaccine from contamination by bacteria. The bag on the right contains a hamburger meatball as an extra attractant. Source: OMNRF.

Plate 8: The Ontario Slim was lighter (it weighed 13 grams) than previous baits. Source: OMNRF.

Plate 9: The ultralite bait was four grams in a coated sachet. Source: OMNRF.

Plate 10: A Cessna 172. Meatball bait can be seen dropping from the chute under the aircraft. This Cessna is 8.3 metres long, has a wingspan of 11 metres, cruises at 210 kilometres per hour, and has a useful load (crew, fuel, baits) of 340 kilograms.

Plate 11: A DHC-6 Twin Otter with non-retractable landing gear. A trail of baits can be seen leaving the chute under the aircraft. The Twin Otter is 15.8 metres long, has a wingspan of 19.8 metres, cruises at 280 kilometres per hour, and handles a useful load (crew, fuel, baits) of 2300 kilograms.

Plate 12: Planned flight-lines for flights originating from the Stratford Municipal Airport. Each shaded area is a flight. The coordinates of the numbered points at the end of each flight-line are stored as waypoints. The hockey-stick configuration for most flights was chosen to ensure that baiting took place from take-off to landing thereby minimizing non-productive ferry time. The flight-lines were prepared by FLTPlan software developed by the GIS Lab at Queen’s University.

Plate 13: Loading bait tubs on a Twin Otter. (a) The picture on the left is Charles MacInnes director of the OMNR Rabies Research Unit during the period in which aerial baiting and vaccine production were developed. (b) The picture on the right is Peter Bachmann, one of the authors of this book.

Plate 14: Animal Diseases Research Institute, Nepean. Circa 1990. Source: Courtesy: the Canadian Food Inspection Agency.

Plate 15: Animal Diseases Research Institute, Lethbridge, Alberta. 2005. Source: Courtesy: the Canadian Food Inspection Agency, Lethbridge.

Plate 16: Microphotograph (100×) of tooth dentin of a juvenile fox showing tetracycline fluorescence under excitation light filtered near ultraviolet light (top), and blended with polarized light showing those tetracycline lines projected on daily incremental lines of growth (bottom). Source: Ontario Ministry of Natural Resources and Forestry.

Plate 17: Microphotograph (100×) blending fluorescence (green lines) and polarized light in tooth cementum of an adult fox showing tetracycline lines with respect to annual growth zones. Source: Ontario Ministry of Natural Resources and Forestry.

Plate 18: Microphotograph (400×) of a brain tissue impression with chromogen-induced magenta inclusions, also meeting other positive criteria (intensity and distribution) = P-dRIT, RABV antigen-positive (striped skunk) with dRIT. Source: Ontario Ministry of Natural Resources and Forestry.

Plate 19: Microphotograph (400×) of a brain tissue impression with visible inclusions, but not meeting the other positive criteria ­(colour intensity and distribution), indicative of an indeterminate result = I-dRIT. Source: Ontario Ministry of Natural Resources and Forestry.

Plate 20: The spread of raccoon rabies in the eastern United States after the relocation of rabid raccoons from Florida. Source: Ontario Ministry of Natural Resources and Forestry. Reproduced with permission from C. MacInnes.

Plate 21: Arctic foxes (Vulpes lagopus) in the tundra during the summer (left) and the winter (right). Source: (left): photo by D. Berteaux; (right): photo by G. Savory.

Plate 22: Arctic fox (Vulpes lagopus) and red fox (Vulpes vulpes) in oilfields. Photos by G. Savory.

Plate 23: A roosting silver-haired bat (Lasionycteris noctivagans). Source: M. Brock Fenton.

Plate 24: A big brown bat (Eptesicus fuscus) flying with an open mouth. The open mouth is not indicative of a threat. The bat emits high frequency echolocation calls through its open mouth and changes the shape of its mouth to control its sonar beam. Source: M. Brock Fenton.

Plate 25: Top panels: Brochures produced by Canadian Food Inspection Agency (left to right): 2007, 2002, 2011. Bottom panels: ­Agriculture Canada Health of Animals Branch (left to right): 1968 and 1986. Source: CFIA. Used with permission.

Plate 26: Number of submissions for Ontario, 1985 to 2012, for rabies testing, compared with selected provinces. Source: created from CFIA data.

Plate 27: Graph of number of PEP treatments (red line) to number of rabies-positives (blue line) from 1958 to 2012. The ratio of PEPs/ positives is shown in black. Source: created from CFIA, PHO, and OMNRF data.

Plate 28: Migrations of the Paleo-Eskimos and the Neo-Eskimos (Thule) from Siberia to the Arctic. Adapted from Raghavan et al., 2014.

Plate 29: ORV zones for coyote, grey fox, raccoon, and skunk in 2013 and enhanced surveillance zones (shown in red) in 2012. Source: Wildlife Services.

PART 5

Data Collection and Diagnostic Methods

Overview The chapters in Part 5 deal with development of methods and organizational structures that have evolved to provide for collection of specimens, testing, diagnosis, and reporting of rabies in Canada. That evolution has produced a successful system for providing the information required to guide management and control efforts at the federal and provincial or territorial levels. The first three chapters (20, 21, and 22) describe the system as it developed under the control of the federal government. Chapter 20 relates the history of the diagnostic laboratories and describes the standard tests for rabies for submitted specimens. The system was meant for passive surveillance. Usually, specimens were submitted for testing only when human contact with rabid animals was suspected, so knowledge about the presence of rabies came after the fact. Chapter 21 describes the evolution this passive surveillance system, discusses results from the system, and evaluates its effectiveness as a surveillance tool. Chapter 22 discusses another dimension of the system: rabies specimens are dangerous goods. This chapter describes the methods, costs, and concerns of transporting those specimens from across Canada to the diagnostics labs maintained by the federal government. The system has not been static and several major technical advances, discussed in Chapters 23 and 24, have increased the information obtained from rabies testing, lowered costs, and instigated changes in the nature of surveillance. Since the 1990s viral typing of rabies, described in Chapter 23, has impacted the understanding the epizootiology of rabies in Canada and has played an important part in the ongoing development of rabies control methods. Chapter 24 discusses four other examples of technical advances. Chapter 24a describes how Quebec has developed an enhanced surveillance system that is designed to proactively look for rabies cases rather than waiting to respond to cases reported from passive surveillance. Chapter 24b discusses the concept of biomarkers and their use in testing the impact of oral vaccine baits in Ontario. Chapter 24c describes the direct rapid immunohistochemical test (dRIT) and the testing in Ontario that led to its use in low-cost and rapid testing of field specimens. It made possible the enhanced surveillance program that is now a major part

Data Collection and Diagnostic Methods

of the province’s response to the most recent outbreak of the raccoon strain of rabies in southern Ontario. Chapter 24d describes recent developments in nucleotide sequencing and discusses how those developments will provide more opportunities to assess the evolution and spread of the rabies virus and the effectiveness of wildlife control programs.

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20 Laboratory Development and Standard Basic Diagnostic Methods for Rabies in Canada Allan Webster1 and David J. Gregory2 1

Agriculture Canada (Retired), Ottawa, Ontario, Canada Canadian Food Inspection Agency (Retired), Ottawa, Ontario, Canada

2

Introduction The early history of rabies diagnostic laboratories and rabies testing methods used in Canada are inseparably linked to the early work of Pasteur; several notable pioneers in rabies diagnosis, treatment, and prevention; and the development of institutions in a young and growing country. This history is discussed in the first part of the chapter. The remainder of the chapter is divided into two further sections. The first describes the basic diagnostic methods used in Canada and their evolution, linked with the formation of the federal rabies research unit at the Animal Diseases Research Unit (ADRI) in Nepean. The second deals with the formation of the Centre of Expertise for Rabies at the Animal Diseases Research Institute (ADRI), Nepean, which has led to advances in genetic tools for rabies diagnosis and in turn has provided a powerful new set of tools for rabies research. This more advanced testing is covered in Chapters 23 and 24. Louis Pasteur (1822–1895, Dole, France) first treated Joseph Meister in 1885 with a fixed rabies vaccine, the success of which brought him immediate fame. During a meeting of the Academy of Science in France, he proposed the founding of Pasteur Institutes worldwide. This led to an international campaign to build the Pasteur Institute, which was founded in 1887 and inaugurated in Paris on 14 November 1888. One of its first patients was the British medical pathologist Dr John George Adami, who had been exposed to rabies while in England in 1888 (“Obituary,” 1926). The American bacteriologist Anna Wessels Williams

(1863–1954) obtained samples of rabies-infected nervous tissue from the Pasteur Institute in 1896 and worked towards making the large-scale production of rabies vaccine in the United States possible (US National Library of Medicine, 2014). These events led to the availability of human rabies vaccine in North America, increased the recognition that laboratories were essential for rabies diagnosis in Canada, and trained the personnel needed to conduct these tests. Charles H. Higgins (1942), a graduate of Massachusetts State College at Amherst had, on the advice of Dr James B. Paige, a graduate of McGill University, enrolled in a course of veterinary science at the Faculty of Comparative Medicine and Veterinary Science, Montreal, in 1894. Dr Adami had been appointed professor of pathology at McGill University by that time. Following graduation in 1896, Dr Higgins worked in Jamaica, New York, and Massachusetts, before being appointed as assistant pathologist at the Department of Agriculture in Montreal by Dr Adami (Higgins, 1942).

The Evolution of Rabies Diagnostic Laboratories in Canada Pathology was first taught at the Montreal Veterinary College, founded in 1866 by Duncan McEachran, a graduate of Edinburgh Veterinary College (see Chapter 4). He formed a close association with the medical faculty and students of McGill University, allowing his students to attend

Data Collection and Diagnostic Methods

Figure 20.1: Montreal Veterinary College, Montreal. Circa, 1895. View-2796. Courtesy: McCord Museum.

classes in the same basic subjects as the medical students. Eventually, the Montreal Veterinary College became affiliated with McGill University as the Faculty of Comparative Medicine and Veterinary Science. In addition to his duties as principal and professor at the Montreal Veterinary College, McEachran was appointed chief inspector of livestock by the Dominion Government in 1876, serving in this capacity until 1902. By contrast, the United States Bureau of Animal Industry was not founded until 1891. Also, the Ontario Veterinary College (founded in 1962) did not include pathology in its curriculum during the 1860s, 1870s, and 1880s (Saunders, 1987). The forerunner of the Animal Pathology Division was established at the Montreal Veterinary College in 1866

(Figure 20.1; Saunders, 1987), in a cooperative effort between McGill University and the Dominion Government. Under the guidance of Dean Duncan McEachran (Figure 20.2), a small laboratory was built in 1898 (Karstad, 1985). It was designated as McGill’s Outremont Station, Quebec, and it was to be devoted to the study and prevention of animal disease, such as bovine tuberculosis, in Canada. Dr Higgins, the first veterinary pathologist appointed by the Department, was given the responsibility of organizing the work at this station in 1899. In July 1902 the Dominion Service was reorganized into the Health of Animals Branch, and under the direction of J. G. Rutherford, its new head, its activities moved from Outremont to temporary quarters at 138 Queen Street, Ottawa. The Health of Animals

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patients and carry out its own rabies diagnosis,” he continued (“Rabies Epidemic,” 1908, p. 5). His main concerns were the distance and time people needed to travel to New York to receive the Pasteur treatment; the cost of treatment, including the travel cost and accommodation for 21 days for treatment; and given the uncertainty of the diagnosis in Canada at that time, the number of specimens being sent from Ontario to New York for diagnosis. During an outbreak of rabies in Canada in 1909, Higgins carried out microscopic examination of the brains of suspect animals, as well as rabbit inoculation, for rabies diagnosis. With the completion of the Biological Laboratory on the Central Experimental Farm (Figure 20.3) in 1903 in Ottawa, rabies diagnosis in Canada became a reality.

Animal Diseases Research Institute, Hull In 1917 a farm was purchased in Hull, Quebec, for research purposes. During 1922 the Biological Laboratory moved to a house on Cliff Street in Ottawa (Figure 20.4) before a new laboratory was built on the Research Farm in Hull in 1927, now 100 Gamelin Blvd, Hull (Dukes & McAninch, 1992) and the site of the National Archives. In 1928 the Biological Laboratory moved to Building 9, built on the grounds of the former research facility of ADRI in Hull, Quebec (Figure 20.5). One of the chapter authors (Webster) recalls that adjacent to Building 9 in the early 1960s was a smaller two-storey building, a rabbit warren of small offices and labs for both poultry and pathology sections, all on the same floor. A separate wing contained the rather large post-mortem room. Joining the two wings was the incinerator – a large hole in the floor with a sliding metal lid that could be pulled aside and could accommodate at least one full-grown horse or cow carcass at a time. The building was hot in the summer. There was no air-conditioning in those times, and no screens on the windows. Windows had to be left open in the summer to get some air through and let in the flies and smoke from the incinerator. During the winters, the windows were closed but leaked cold air. Heating was not efficient. And at sporadic times, members of the RCMP showed up to burn truckloads of marijuana and other such drugs resulting in the ever-present smoke from burning carcasses being laced with the drug of the day. Webster also recalls that the rabies lab consisted of two rooms. In the first, specimens submitted for rabies diagnosis were received, unpacked, numbered, and prepared for brain examination. One end of a table was covered with newspaper on which the brain of each specimen

Figure 20.2: Dr Duncan McNab McEachran, Montreal, QC, 1895. Courtesy: McCord Museum- II – 109119.

Branch was then composed of the Contagious Diseases Division and the Pathological Division. Dr Higgins was appointed chief of the Pathological Division. Because of the nature of the work, it was felt advisable to move its activities to separate quarters, and in 1902 Dr Higgins became head of the new Biological Laboratory built on the Central Experimental Farm in Ottawa. He held this post of laboratory head until his retirement in 1917. Coincidentally, during the early years of the laboratory at the Central Experimental Farm, canine rabies became a problem in Canada, often as a result of dogs imported from the United States for hunting purposes: “There is an epidemic of rabies among the dogs of Canada and the United States,” stated Dr B. L. Riordan in the Toronto Daily Star on 12 October 1908 (“Rabies Epidemic,” 1908, p. 5). Dr Riordan was undergoing treatment at the Pasteur Institute in New York, having received a bite from a rabid dog in Ontario. “Ontario needs to be able to treat its own

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Figure 20.3: The Biological Laboratory, the Central Experimental Farm, Ottawa. Circa 1912.

Photograph by William James Topley, Library and Archives Canada/PA-10303.

was removed and prepared for microscopic examination or for animal inoculation. Instruments were washed and sterilized, newspapers were replaced, and garbage was removed (to the incinerator). Then the paperwork continued, experimental mice were inoculated for each specimen as required, and the table was made ready for the next shipment – or for lunch and the regular game of cribbage, whichever came first. This small room also had workbench space for paperwork, the personal space of a biologist, and the personal space of Albert Bourgon, the technician who had been at this job for some time, trained everyone, and basically ran the diagnostic function. The second small room in the rabies lab was home to the unit head, Dr Michel Beauregard who had a regular desk. It had a workbench along one wall with three microscopes for examining slides of stained brain tissue. A 1.3-metre microscope space also served as the personal space of the second biologist. It also was the only route (over papers, books, microscope, and biologist) to the window, outside of which was the only fire escape ladder for the section. In the early 1960s on a slow day, 20 to 30 specimens could be received, prepared, and examined; mice inoculated if required; and initial results telephoned or mailed. For those heavier days of 100 or more specimens, the results might not have been mailed the same day, but positive rabies cases with human involvement were reported by phone. Safety issues were not predominant, but laboratory clothing was

Figure 20.4: Biological Laboratory, Cliff Street, Ottawa Headquarters of Pathological Division, 1922 to 1928. Courtesy: the Canadian Food Inspection Agency.

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Figure 20.5: Animal Diseases Research Institute 100 Gamelin Blvd., Hull, Quebec. 1928 to 1974. The building in Hull was designated is a recognized federal heritage building 22 May 1985.

Courtesy: the Canadian Food Inspection Agency.

worn by all, and the person removing brain material from the head wore rubber gloves and, later, a face shield. Dr Mike Beauregard left the unit to return to teach at the veterinary school at Ste Hyacinthe, Quebec, and there was a succession of unit heads over the next few years until Dr Ken Charlton arrived in 1974. This small group of four – one technician, two biologists, and Dr Charlton – remained as the core of the rabies unit. It was a great honour for the technician and two biologists to receive Merit Awards from the Government of Canada in 1991. As the work load became more demanding over time, additional staff were hired. This allowed more time to research newer techniques in diagnosis and enhance research programs. Specimens for rabies diagnosis were received from Health of Animals field veterinarians who did all the investigational work for the program (see Chapter 31). Each specimen had been numerically tagged by the veterinarian, packed in paint pails, and shipped to the laboratory with supporting documentation. Depending on travel distance, dry ice may have been enclosed as well (especially those from western Canada). When received at the laboratory, specimens were removed from the shipping containers and prepared for brain removal. Each specimen was given a unique lab number indicating the year and a sequential number starting 1 January of that year. This laboratory number remained with the specimen throughout its testing and was reported on the submitted forms. Results were typed on copies of the form and returned to the field veterinarian, who then notified the individual concerned. If a person had

contact with an animal found to be rabies-positive, the results were phoned directly to the veterinarian the same day. While the unit was still in Hull, specimens were sometimes received directly from members of the public. This was not encouraged as the results had to be reported back through the local field veterinarian. But what could be said to the person who carried a live fox into the lab with blood dripping off his arm where the fox had bitten him? And the fox was indeed rabid. The gentleman received treatment and survived his experience. This reporting system had been established early in the history of the unit and basically remains. Some modifications have occurred: newer forms require less manual typing, more information is gathered for epidemiological studies, and computers in quicker compilation and dissemination of information.

Animal Diseases Research Institute, Nepean The ADRI laboratory remained at 100 Gamelin Street, Hull, until it moved to a new building in Nepean, Ottawa, opened on 27 November 1974 by the Honourable E. F. Whelan, minister of agriculture for Canada. This newly constructed laboratory and surrounding facilities was a great improvement to that of ADRI in Hull. Modern construction techniques provided better environmental conditions in the interior: hepa filters, directed air flow, tighter containment in some areas, more spacious labs – with one exception. There was no insulation around 337

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Figure 20.6: The Rabies Laboratory, Animal Diseases Research Institute, Lethbridge, Alberta. Circa 1952.

Courtesy: the Canadian Food Inspection Agency, Lethbridge.

the windows, resulting in overworked air conditioners in the summer and snow in the inside during the winter. Following some discussion between the architect and the builder, this was fixed and the rabies unit enjoyed greater space, greater security, and overall a better atmosphere for work. More stringent safety measures were required: face shields, chain-link gloves for use when opening heads, surgical gloves and disposable gowns when handling potentially infectious material, and a laminar flow bio-hood for tissue culture work were some of the measures adopted. A separate, restricted access post-mortem room for preparing specimens was added. About this time Dr Ken Charlton took over as head of the Rabies Unit. His expertise and enthusiasm led the unit into new areas of study, in addition to the routine diagnostic functions of the laboratory. Dr Charlton was involved in studies on the pathogenesis of rabies virus in wildlife, the development of a vaccine for the baiting of foxes and skunks, and the development of a recombinant vaccine for skunks. These areas are examined more closely in other chapters of this book. In the 1990s, when rabies became categorized as a bio-containment level 3 organism in Canada, it necessitated the construction of a new level 3 wing at ADRI Nepean. All work on pathogenic rabies viruses, including diagnosis, had to be conducted within this facility. This further improved safety and containment of work performed on this pathogen. In 1997 when the Canadian Food Inspection Agency (CFIA) was created by bringing together a number of facilities and groups involved with food safety and the health of

animals and plants used for food production, ADRI Nepean became a part of CFIA. A few years later, to better reflect the institute’s involvement in many aspects of the CFIA’s mandate, the institute was renamed the Ottawa Laboratory Fallowfield (OLF) (Plate 14) as it is referred to today.

Animal Diseases Research Institute, Lethbridge To help with the overload of rabies specimens being sent for diagnosis, two other laboratories were opened to conduct rabies tests in Canada, one in Lethbridge, Alberta, and the other in Sackville, New Brunswick. The laboratory at Lethbridge began as a small house (Figure 20.6) built on the quarantine station on 730 hectares to investigate the equine disease dourine. Additions to the laboratory included a residence in 1950, which housed the bacteriology section, and in response to the rabies outbreak in 1952 in northern Alberta, housed the rabies laboratory. A peak year for fox populations in the Northwest Territories occurred in 1952, with a resulting movement of foxes south and east. Between 8 June 1952 and 30 May 1953, some 96 animals were diagnosed with rabies. The estimated number of actual cases in livestock based on clinical symptoms was 260 to 360. The laboratory was overloaded, and so if an area had three positives, no further submissions were taken unless there was human contact. Further, the distance from Fort Vermilion to Lethbridge was about 1600 kilometres. After countless additions during the 1980s, the Lethbridge laboratory is now one of two remaining federal facilities conducting rabies diagnosis in Canada (Plate 15). 338

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Figure 20.7: Canada, Division of Animal Pathology Branch Laboratory Maritime Area, Sackville, NB. Circa 1949. Courtesy: Dr R. G. Stevenson, Head of the Laboratory.

rabies. Negri bodies, as they came to be called, are found frequently in the pyramidal cells of Ammon’s horn, and the Purkinje cells of the cerebellum (Novak, 2010). In 1905 Anna Wessels Williams (US National Library of Medicine, 2014) published her own method of preparing and staining tissue which became the standard test for rabies and made it possible to get test results within half an hour. Rabies diagnosis, before 1903, was based on clinical signs, histopathologic signs, and animal inoculation. With William’s publication, the determination of Negri bodies became standard practice and remained so until after 1960. It is not known when Dr Higgins started looking for Negri bodies, but later stated that he had “spent considerable time in detecting these bodies but subsequently had his findings checked with animal inoculation” (Report of the Veterinary Director General, 1912, p. 79). Because the time for a diagnosis was considerable using animal inoculation, this practice could endanger the patient, so his advice to the patient was to visit the Pasteur Institute for treatment immediately. The standard testing procedure for rabies virus in suspect animals at ADRI, Hull, in the early 1960s, was the staining of microscope slides with impression smears of brain tissue to find the diagnostic lesions, the Negri bodies (Mallory, 1938; Tierkel, 1966). As Dr Higgins noted, microscopic examination demanded considerable training, and it was often a long and tedious task to render a diagnosis. When animal to human contact had occurred (i.e., bites, handling, possibility of contact with infectious saliva) and

Health of Animals Laboratory, Sackville The laboratory at Sackville, New Brunswick, was established in 1949 in the Baxter House, on Mount Allison Campus by Dr Julius F. Frank, Animal Pathology Division, Health of Animals Branch, Canada Department of Agriculture. This was a student residence that was converted into a temporary laboratory (Figure 20.7). The volume of diagnostic work outgrew this facility, so a new laboratory was constructed starting in 1956 on land leased by the university on campus. This new laboratory (Figure 20.8) was opened on 6 January 1969 by J. G. Taggart, the deputy minister of agriculture, and the Honourable Milton Gregg, minister of labour. With a gradual decline in rabies in Canada through the 1990s, Sackville was closed in 1995. The laboratory building was renamed the Bennett Building after its benefactor.

Standard Basic Methods for Rabies Diagnosis and Typing Methods in Canada Negri Body Test In 1903 Dr Adelchi Negri (1876–1912), an Italian pathologist and microbiologist, reported on what he thought to be the etiologic agent of rabies: round or oval inclusions within the cytoplasm of nerve cells of animals affected by 339

Data Collection and Diagnostic Methods

Figure 20.8: Animal Pathology Division, Marine Area Branch Canada Department of Agriculture Sackville, New Brunswick. 1969. Courtesy: Mount Allison University Archives.

seen earlier in the course of the disease when brain tissue was tested with FAT. Quite often, these particles could be seen before the formation of the typical Negri body required for a positive diagnosis by older staining techniques. FAT provided a quicker and more reliable laboratory diagnosis, which resulted in a more timely medical intervention for the patient.

the examination of the slides did not reveal the presence of Negri bodies, the suspect brain tissue was inoculated directly into the brains of five experimental mice, which were held under observation for 30 days or until mice died and were proven to be infected (mouse inoculation test, MIT). A small sample of brain tissue from all submitted specimens was frozen and retained for future studies. Three major improvements to this protocol were made over the years. In all cases changes were made to improve the reliability and sensitivity of the test in a laboratory, which handled a large number of specimen submissions with a small number (three to four) of personnel. For example, in 1975, some 6000 specimens were received and tested. Between June 1986 and December 1990, a total of 52,600 specimens suspected of having rabies were examined by a staff of five. Techniques that were economical in both resources and time while retaining specificity and reliability were required.

Mouse Inoculation Test The second improvement to diagnosis was the MIT, used where the initial FAT was negative but human involvement had occurred. Rabies virus could be demonstrated by FAT in the brain of experimental mice before the development of clinical signs. Accordingly, sufficient mice were injected with the test brain material, and starting on day 4 post-inoculation and continuing to the end of the 30-day observation period (or until virus was found), two mice were sacrificed and examined for virus (FAT). This resulted in a more timely and reliable diagnosis test (Webster et al., 1976).

Fluorescent Antibody Test

Rabies Tissue Culture Infection Test

In 1965 after exhaustive comparisons between the staining of brain tissue with William’s modification of Van Gieson’s stain and the use of fluorescein-labelled antibodies, the laboratory switched to the fluorescent antibody test (FAT) as the first of the two-pronged diagnostic procedure (Beauregard et  al., 1965). Rabies virus particles could be

The third major improvement was the development in 1987 of the rabies tissue culture infection test (RTCIT) (Webster, 1987). It was known that certain cell cultures could support the growth of rabies virus. Baby hamster kidney (BHK-21)

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cells were well known to support the growth of fixed viruses, but field virus was often more difficult to propagate. Working visits to various laboratories – New York State Public Health; Centers for Disease Control and Prevention, Atlanta, Georgia; Queen’s University, Kingston; the Wistar Institute, Philadelphia; and the Pasteur Institute, Paris – all contributed to this test being developed at ADRI, Nepean. The cell line that was adopted was the murine neuroblastoma (NA-C1300) cell line obtained from Dr T Wiktor of the Wistar Institute because rabies virus from wildlife and domestic animals in Canada could be grown more easily and faster in this particular line. Following human contact, a submission that was rabies FAT negative had been followed by the second confirmatory, which had used some 30,000 mice per year and required 30 days for completion. FAT was replaced by the RTCIT, which gave more precise results in four days and saved considerable expense in animal and human resources. The NA cell cultures were also more sensitive to infection with low doses of rabies virus than were the experimental mice. It was a great honour for ADRI, Nepean, to be asked to write the chapter on the RTCIT for the World Health Organization’s fourth edition of Laboratory Techniques in Rabies (Webster & Casey, 1996). The use of RTCIT ended at OLF on 1 July 2011 (C. Fehlner-Gardiner, personal communication, 2012). RTCIT had been routinely performed as a confirmatory test on rabies diagnostic submissions with a history of human exposure that negative on FAT. But the accuracy of FAT had greatly improved with the introduction of new, superior reagents and the acquisition higher quality microscopes during the 1990s. A review of data gathered between 1995 and October 2010 of 66,099 RTCITs carried out following FAT with negative results justified this decision.

foxes in eastern Canada. This strain is found in the majority of domestic animal rabies in Ontario. A closely related virus strain was found in the southeastern Georgian Bay area of Ontario. Skunk rabies, which has been endemic in Alberta, Saskatchewan, and Manitoba, is a second major antigenic group and is believed to have originated from the northcentral United States. Domestic animals with rabies in that area were usually infected by this skunk strain. Last, a heterogeneous group of viruses was found to be associated with bats in various parts of the country, and the MAb profiles appear to be bat-species specific. Bat rabies virus appears to be more significant in transmission of rabies to humans and animals in Canada in recent years (Copeland et al., 1985; Webster et al., 1985; Webster et al., 1987; McLean et al., 1985). Growth of virus isolates in cell cultures and their subsequent testing with MAbs is a powerful tool in the recognition of sources of infection for epidemiological studies (see Chapter 29). Dr Alexander Wandeler joined the rabies group at ADRI Nepean in 1989 and led the unit for many years until his retirement in 2010. In that time extensive work was undertaken on the utility of MAbs for viral typing. The laboratory amassed a large collection (approximately 500) of these antibodies, many of which were generated on site and used to examine the antigenic characteristics of many field isolates from both Canada and abroad. This collection of MAbs remains a valuable resource, which has been accessed by many groups around the world (see Chapters 23 and 24 for genetic testing methods).

Immunohistochemistry Rabies diagnosis using the gold standard FAT is best performed on smears, impressions, and frozen sections prepared from fresh tissue and is widely accepted as the best method to visualize small particles of rabies viral antigen in rabies-infected tissues. One type of specimen that can be problematic for diagnosis is formalin-fixed paraffin-embedded (FFPE) tissue, which is formalin fixed before suspicion of rabies in a differential disease diagnosis. As a result FFPE tissues are sometimes submitted for testing. One of the earlier methods of handling these samples involved the use of pepsin enzyme digestion and staining with peroxidase-anti-peroxidase stain. This allowed for good preservation of the morphological details of the cells and demonstration of viral antigen (Bourgon & Charlton, 1987). Other methods developed used the basic methods of enzyme digestion and colorimetric substrates. One such variant,

Monoclonal Antibody Test During a trip to the Wistar Institute, the rabies unit was provided with a panel of monoclonal antibodies (MAbs) prepared by Dr Wiktor. With this panel, the unit was able to describe various distinct rabies virus isolates in Canada (Charlton et al., 1986; Webster et al., 1986). Jean Smith of CDC Atlanta also gave the unit a number of monoclonal antibodies. For many years all rabies field virus isolates had been thought to be one strain. However, staining cell cultures infected by various rabies virus isolates from Canada with fluorescein-tagged MAbs showed that this was not the case. In Canada, one (Canadian Arctic) strain came down from the Arctic into various areas, and has since the 1960s been regarded as the dominant strain found in skunks and

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called the avidin-biotin-complex (ABC) method, used to examine the presence of viral antigen in fixed tissue, was developed in support of pathogenesis studies (Balachandran & Charlton, 1994). In this method, an anti-rabies antibody (originally rabbit) is applied to dewaxed, proteinase K–treated tissue sections, followed by a multistep detection process using biotinylated goat anti-rabbit and a streptavidin-biotin complex, with a final colorimetric detection employing the horseradish peroxidase enzyme component of the complex. This method is still in use at the Nepean laboratory for diagnosis of FFPE submissions. In addition, monoclonal antibodies may be used to detect rabies virus variants. Active surveillance on suspect rabid animal species with no human contact is carried out in the eastern provinces and territories by Canadian Wildlife Health Cooperatives (CWHC) using the dRIT test, discussed further in Chapter 24c. With the exception of British Columbia, all CWHC networks are attached to universities. At present, for enhanced surveillance programs for rabies in the western provinces and territories (Manitoba, Saskatchewan, Alberta, Northwest Territories, and Yukon), Prairie Diagnostic Services at the University of Saskatoon offers an immunohistochemical test (IHC), as does the Animal Health Centre in Abbotsford, British Columbia, mainly for bats. Confirmation on rabies-positives using the IHC test is carried out at CFIA’s Lethbridge laboratory using the direct fluorescent antibody (dFA) test if the sample is fresh or

the fixed sample is sent to OLF, Nepean. No legislative requirement is set for test confirmation by a CFIA laboratory, but the finding is reported to CFIA depending on human or animal contact with the rabid specimen. Alberta has a testing contract with the CFIA Lethbridge laboratory for a skunk rabies surveillance program.

Summary Basic differences in cell culture infection rates (Webster et al., 1988; Webster et al., 1989a; Webster et al., 1989b) and in virus pathogenicity of various virus strains in animals (Charlton et al., 1988) have also been studied. Comparisons of the two main virus strains, from skunks in eastern and western Canada, showed differing infection rates in NA cells and BHK cells, as well as differing viral titres in cell culture supernatant fluids. These studies and the establishment of persistent infections in cell culture have helped to understand some of the mechanisms of rabies virus infections in wildlife species. Rabies diagnosis at ADRI, Lethbridge, and the Sackville laboratory was initially performed by demonstration of Negri bodies and animal inoculation (Niilo, 1989). By 1965 FAT was accepted for use in all Canadian laboratories, and by 1970 this had become the standard for rabies testing in the three Canadian laboratories.

References Balachandran, A., & Charlton, K. M. (1994). Experimental infection of non-nervous tissue in skunks (Mephitis mephitis) and foxes (Vulpes vulpes). Veterinary Pathology, 36(1), 51–54. https://doi.org/10.1177/030098589403100112 Beauregard, M., Boulanger, P., & Webster, W. A. (1965). The use of fluorescent antibody staining in the diagnosis of rabies. Canadian Journal of Comparative Medicine, 29, 141–147. Retrieved from https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1494414/ Bourgon, A. R., & Charlton, K. M. (1987). The demonstration of rabies antigen in parrifin-embedded tissues using the peroxidase-anti peroxidase method: A comparative study. Canadian Journal of Veterinary Research, 51, 117–120. Retrieved from https://www.ncbi .nlm.nih.gov/pmc/articles/PMC1255284/pdf/cjvetres00057-0119.pdf Charlton, K. M., Webster, W. A., Casey, G. A., Rhodes, A. J., MacInnes, C. D., & Lawson, K. (1986). Recent advances in rabies diagnosis and research. The Canadian Veterinary Journal, 27(2), 85–89. Retrieved from https://www.ncbi.nlm.nih.gov/pmc/articles /PMC1680190/pdf/canvetj00590-0053.pdf Charlton, K. M., Webster, W. A., Casey, G, A., & Rupprecht. C. E. (1988). Skunk rabies. Review of Infectious Diseases, 10(Suppl. 4), S626–S628. https://doi.org/10.1007/978-1-4613-1755-5_5 Copeland, L., Gregory, D., & Webster, W.A. (1985). Rabid beaver incident – British Columbia. Canada Diseases Weekly Report, 11(51), 214–215. Retrieved from http://publications.gc.ca/collections/collection_2016/aspc-phac/H12-21-1-11-51.pdf Dukes, T., & McAninch, N. (1992). Health of Animals Branch, Agriculture Canada: A look at the past. The Canadian Veterinary Journal, 33(1), 58–64. Retrieved from https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1481176/pdf/canvetj00050-0060.pdf

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Laboratory Development and Standard Basic Diagnostic Methods Higgins, C. H. (1942). Reminiscences of events: Before and after formation of the Health of Animals Branch. Canadian Journal of Comparative Medicine, 6(6), 159–162. Retrieved from https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1584179/pdf/vetsci00115-0007 .pdf Karstad, L. (1985). Historical background of the research program of the Animal Pathology Division. In Research management ­review by the Animal Pathology Division with overview, historical background and questionnaire (pp. 1–14). Ottawa, ON: Agriculture Canada. Mallory, F. B. (1938). Pathological techniques. Philadelphia, PA: W.B. Saunders. McLean, A. E., Noble, M. A., Black, W. A., Kettyls, G. D., Johnstone, T., Webster, A., ... Gregory, D. (1985). A human case of rabies – British Columbia. Canada Diseases Weekly Report, 11(51), 213–214. Retrieved from http://publications.gc.ca/collections/collection _2016/aspc-phac/H12-21-1-11-51.pdf Novak, M. J. 2010. Negri’s bodies. Retrieved from http://www.whonamedit.com Obituary: John George Adami, C.B.E., M.D., F.R.S., F.R.C.P., F.R.C.S., Hon. D.Sc., LL.D. (1926). British Medical Journal, 2(3427), 507–510. Rabies epidemic, says Dr Riordan. (1908, October 12). Toronto Daily Star, p. 3. Report of the veterinary director general for the year ending March 31, 1912. (1912). Ottawa, ON: Department of Agriculture. Retrieved from The Internet Archive website: https://archive.org/details/1913v47i9p15b_0928 Saunders, L. Z. (1987). From Osler to Olafson. The evolution of veterinary pathology in North America. Canadian Journal of Veterinary Research, 51(1), 1–26. Retrieved from https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1255268/pdf/cjvetres00057-0003.pdf Tierkel, E. S. (1966). Rapid microscopic examination for Negi bodies and preparation of specimens for biological test. In Laboratory Techniques in Rabies (2nd ed., pp. 26–41). Geneva, Switzerland: World Health Organization. US National Library of Medicine. (2014). Changing the face of medicine: Dr Anna Wessels Williams. Retrieved from https:// cfmedicine.nlm.nih.gov/physicians/biography_331.html Webster, W. A. (1987). A tissue culture infection test in routine rabies diagnosis. Canadian Veterinary Journal of Research, 51(3), 367–369. Retrieved from https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1255339/pdf/cjvetres00059-0085.pdf Webster, W. A., & Casey, G. A. (1988). Diagnosis of rabies infection. In J. B. Campbell, & K. M. Charlton (Eds.), Developments in Veterinary Virology Series: Vol. 7, Rabies (pp. 201–202). Boston, MA: Springer. https://doi.org/10.1007/978-1-4613-1755-5_9 Webster, W.A., & Charlton, K. M. (1989). The apparent infection of NA-C1300 cell cultures by nucleocapsid material of the Canadian Arctic strain of rabies virus. Canadian Journal of Microbiology, 35(8), 811–813. https://doi.org/10.1139/m89-135 Webster, W. A., & Casey, G. A. (1996). Virus isolation in neuroblastoma cell culture. In F.-X. Meslin, M. M. Kaplin, & H. Koprowski (Eds.), Laboratory techniques in rabies. (4th ed. pp. 96–103). Geneva, Switzerland: World Health Organization. Webster, W. A., Casey, G. A., & Charlton, K. M. (1976). The mouse inoculation test in rabies diagnosis: Early diagnosis in mice during the incubation period. Canadian Journal Comparative Medicine, 40(30), 322–325. Retrieved from https://www.ncbi.nlm.nih.gov /pmc/articles/PMC1277774/pdf/compmed00039-0106.pdf Webster, W. A., Casey, G. A., & Charlton, K. M. (1985). Human rabies acquired outside of Canada. Canada. Diseases Weekly Report, 11(4), 13–14. Retrieved from http://publications.gc.ca/collections/collection_2016/aspc-phac/H12-21-1-11-4.pdf Webster, W. A., Casey, G. A., Charlton, K. M., & Wiktor, T. J. (1985). Antigenic variants of rabies virus in isolates from eastern, central and northern Canada. Canadian Journal of Comparative Medicine, 49(2), 186–188. Retrieved from https://www.ncbi.nlm.nih.gov /pmc/articles/PMC1236146/pdf/compmed00002-0064.pdf Webster, W. A., Casey, G. A., & Charlton, K. M. (1986). Major antigenic groups of rabies virus in Canada determined by anti-nucleocapsid monoclonal antibodies. Journal of Comparative Immunology, Microbiology and Infectious Diseases, 9(1), 59–69. https://doi .org/10.1016/0147-9571(86)90076-7 Webster, W. A., Casey, G. A., Charlton, K. M., Sayson, R. C., McLaughlin, B., & Noble, M. A. (1987). A case of human rabies in western Canada. Canadian Journal of Public Health, 78(6), 412–413. Retrieved from https://www.ncbi.nlm.nih.gov/pubmed/3325161 Webster, W. A., Charlton, K. M., & Casey, G. A. (1988). Growth characteristics in cell culture and pathogenicity in mice of two terrestrial rabies strains indigenous to Canada. Canadian Journal of Microbiology, 34(1), 19–23. https://doi.org/10.1139/m88-004 Webster, W. A., Charlton, K. M., & Casey, G. A. (1989a). Persistent infections of a field strain of rabies virus in murine neuroblastoma (NA-C1300) cell cultures. Canadian Journal of Veterinary Research, 53(4), 445–448. Retrieved from https://www.ncbi.nlm.nih.gov /pmc/articles/PMC1255574/pdf/cjvetres00052-0077.pdf Webster, W. A., Casey, G. A., & Charlton, K. M. (1989b). Bat-induced rabies in terrestrial mammals in Nova Scotia and Newfoundland. Canadian Veterinary Journal, 30(8), 679. Retrieved from https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1681141 /pdf/canvetj00561-0069a.pdf

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21 Passive Surveillance Frances Muldoon,1 David J. Gregory,2 and Rowland R. Tinline3 1

Animal Diseases Research Institute (Retired), Ottawa, Ontario, Canada Canadian Food Inspection Agency (Retired), Ottawa, Ontario, Canada 3 Professor Emeritus, Geography, Queen’s University, Kingston, Ontario, Canada 2

Introduction It is only by collecting data and using them that you can get sense. – Osler (1914, p. 432)

Surveillance methods can be divided into two general categories: active or passive. Passive surveillance, known as “cold pursuit” in medical terms (Piriyawat et  al., 2002, p. 1062), involves collecting data and testing of specimens from animals suspected of having a disease because of the suspicious symptoms they exhibit and their having interaction with humans or other animals, which could pass the disease agent to a new host. Passive surveillance is usually based on conditions that make the disease under surveillance reportable to the animal or human health authorities. Active surveillance, also known as “hot pursuit” in medical terms (Piriyawat et al., 2002, p. 1062), depends on researchers or agencies taking samples directly and randomly from a group or population to determine the extent of a disease (see Chapter 24a for examples). Since those samples are taken for a specific purpose, they tend to be planned and limited to brief or sequential periods, and they place intensive demands on resources. Typically, the samples tend to be on live asymptomatic animals and may be associated with methods of tracking specific animals with ear tags or radio collars (see Chapters 26a and 26b for examples). In some cases, however, samples are taken from whatever animals are available, and these samples may include road kills, trapped carcasses, or animals euthanized for other tests (see Chapter 24a for examples). Active surveillance

has been used to (1) validate passive reports or to enhance the completeness or timeliness of those reports, (2) look for disease spread into new areas, (3) monitor control programs, such as in rabies control to assess bait uptake and seroconversion after vaccination, and (4) monitor population levels (­Piriyawat et al., 2002; see Chapters 24b and 24c on biomarkers and dRIT). Active surveillance or hybrids of active and passive surveillance will be discussed in more detail in Chapters 24a and 24d, as will new serological methods of testing. Passive surveillance was one of the many tasks given to the Canada Department of Agriculture in 1867 (see Chapter 4) and was conducted when it had the time. By 1926 the collection and publication of data was compulsory for all provinces and territories. This, coupled with improvements in diagnostic capability, was the beginning of passive surveillance for rabies, a system that has ­underpinned much of the analysis and decision making described throughout this book. This chapter discusses the evolution of the system and assesses its usefulness and the quality of the reported data. As William Osler (Figure 21.1) noted, collecting data allows us to make sense of a situation.

Data Collection before 1925 Regardless of the disease, timely, accurate, and consistent disease reporting is important to everyone involved in the prevention and control of the reported disease and, more importantly, to the general public. For the federal veterinarians of the Canadian Food Inspection Agency (CFIA),

Passive Surveillance

Toronto, on 24 July 1897 printed a report from the Board of Health Department on rabies covering the previous seven years in Ontario (“Rats, Sewers and Rabies,” 1987). The summary outlined the animals involved, the number of outbreaks, the number of people bitten and treated, and any human deaths. After 1900 the newspaper continued to be the main reporting means but by 1902, the first annual reports of the veterinary director general (VDG) for the Department of Agriculture were published. While it was more detailed in account, it was by fiscal format (year ending 31 March) and depended on others sending their reports to the VDG, resulting in delays for publication. While rabies cases were diagnosed either by Negri body staining or animal inoculation, the actual numbers of rabid cases was not often reported. In 1905 the establishment of the first regulations relating to rabies (as a named disease under the Animal Contagious Disease Act of 1903), required that all cases of rabies be reported, investigated, and when the diagnosis was positive, quarantined. By 1920 the number of premises under quarantine was recorded, and soon after that the numbers of animals quarantined were also recorded (Report of the Veterinary Director General, 1926). On 22 April 1919, an Order in Council before P ­ arliament for the establishment of a Dominion ­ Department of Health made provision for the collection and publication of ­information relating to public health. Regular submission of ­vital statistic returns by almost all provinces and territories started in 1920, with the first comprehensive annual report in 1923. By January 1926 Quebec had also joined the system. This enabled the Department of Agriculture to collect, collate, and disseminate data on all diagnosed positive rabies cases on a regular basis (see Chapter 2).

Figure 21.1: William Osler (1849–1919). Canadian physician, “the founder of modern medicine”: Veterinary pathologist, ­physician, educator, bibliographer, historian, author, and ­practical joker. II-62556.3 Photograph of Dr William Osler, Montreal, QC, 1881. © McCord Museum

the national herd health picture is important for Canada to maintain its credibility and standing with the Office International des Epizooties (OIE) and with the veterinary services of its trading partners. Making this information available depends on an effective disease-reporting system and information collation and dissemination (Hare, 1997). This information is made available through the efforts of animal owners; veterinary practitioners, both private and governmental; public and private diagnostic laboratories; wildlife agencies; and many other sources. This section will deal with early efforts to collect, collate, and disseminate data on rabies in Canada. Before 1900 rabies reports were usually made by word of mouth or in the newspaper. For example, The Evening Star,

Data Collection since 1925 Starting in 1925 the Department of Agriculture began recording rabies-positive cases annually, providing the data to anyone when requested. These reports indicated the number of positive rabies cases either by province or territory or by county, as in Ontario, and by species for the fiscal year, running from April to March. Other avenues for the dissemination of disease information on control and prevention of rabies will be discussed in Chapter 33 on communication strategies. In the 1980s the annual report by the Department changed from a fiscal year to a calendar year, providing an easier way to handle data

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statistically and to compare reports from other departments and countries. This was the first in a series of changes that improved the usefulness of the data for surveillance and research.

Universal Transverse Mercator Code (UTMC) The LSCS required a redesign of the rabies specimen reporting form AGR 1605. This provided the impetus for consideration of alternatives to improve location codes. One option was to use the postal code (Tinline & Gregory, 1988) as a means of locating rabies cases for epidemiological purposes. Unfortunately, postal codes in rural areas cover large areas, giving a poorer resolution than the nearest town system. The chosen solution was a geocode map grid system that was easy to use, provided a constant resolution and depended on Canada’s well maintained National Topographic Series (NTS) maps that covered most of Canada at the 1:50,000 scale. In central and eastern Canada and British Columbia, the grid was based on the Universal Transverse Mercator Code (UTMC) using the NTS map. The UTMC was a system standard with many provincial and federal agencies interested in mapping data. Reporting resolution was 100 metres (Tinline & Gregory, 1988). In the prairie provinces of Manitoba, Saskatchewan, and Alberta, the Legal Land System (LLS) was adopted for use which allowed resolution to the quarter section (65 hectares). Thus, the geographic coordinates of each case could be obtained and the data mapped for reporting and analysis (Tinline & Gregory, 1988). Recently, the submission form was adjusted to accept the addition of latitude/longitude – values obtained using a handheld Geographic Positioning System (GPS) receiver accurate to approximately five metres on the ground, or websites such as Google Earth, which allows the user to position the cursor over a chosen location on an aerial photo/map and retrieve the latitude/longitude. The result is faster and more accurate reporting, assuming the location measured in the field was the location at which the specimen was taken and the observer used the GPS or website properly. Following the takeover of field submissions by the provinces and territories in 2014, the submission form was changed again to require the submitter to provide the animal location in latitude/longitude coordinates in decimal degree format (a mandatory field). This requirement improved reporting to CFIA’s area offices, provincial and territorial medical and wildlife agencies, and international agencies such as the United States Department of Agriculture (USDA) and OIE.

Nearest Town Code In 1977 Agriculture Canada’s Health of Animals Division initiated the nearest town code for the rabies specimen submission reports to increase the spatial resolution of rabies reporting (Tinline & Gregory, 1988). Using a code book and a combination of numbers and letters to indicate the province or territory, county, township, and nearest town, federal veterinarians were required to enter the code for the town nearest the rabies case on the rabies specimen submission form. While the nearest town code was an important step towards improving rabies reporting, it had three drawbacks. First, in densely populated areas, towns are close together, and in rural areas, towns are farther apart; therefore, the resolution of the code varied with population density. Second, the code book was derived from a wide series of map bases and was difficult to update, especially as changes in administrative boundaries and associated place names were commonplace. Third, the system recorded the address of the p ­ erson affected, which was not always the location where the rabid animal was found. Field veterinarians became frustrated with the differences between the maps they were using and the codebook. Given the lack of interest in this system, compounded by its high error rate, a more userfriendly system was sought.

Laboratory Sample Control System In 1985 a new Laboratory Sample Control System (LSCS) was put in place at Animal Diseases Research Institute (ADRI), Ottawa. The system was digital and was meant to (1) track and improve the flow of information internally, (2) speed up reporting to health units and district veterinary offices (DVOs), (3) and provide more complete information on each submission. The change also provided an opportunity to improve location coding. Further, from a research point of view, the system allowed researchers to access submission records and not just summaries of rabies-positives. As well, access to detailed data information for each submission, whether positive or negative for rabies, allowed summary data to be reported as required rather than being restricted to specific time periods – a major concern in the analysis of rabies data.

Submissions While positive rabies cases have been tabulated since 1926, collection of the number of specimens submitted or negatives was not tabulated until 1985. Although the

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submissions data were available in paper form, given the large number of submissions relative to positive cases, tabulating this information retrospectively was extremely time-consuming. The availability of submissions data added a new dimension to the analysis of rabies in Canada, particularly in terms of appreciating how the mandate of the diagnostic laboratories has affected collection and diagnosis, and understanding how the public and public health officials have used the system. Compare, for example, Table 21.1 (submissions) and Table 21.2 (positives) for 1985–2017 by province and territory in Canada. During this period 280,326 submissions were made, of which 29,195 (10.4%) proved positive

for rabies. Of these submissions, 38.4% were domestic pets (dogs and cats) but these were only 7.7% of positives. This is not unexpected since the priority of the diagnostic system is human health and that means investigating contacts with animals who, directly or indirectly, could be exposed to the rabies virus. In comparison submissions of foxes and skunks, the two major rabies vectors in Canada, were 18% of tested specimens but 68.8% of all reported positives. In effect, rabid wild animals were self-reporting since the typical circumstances initiating submission (an animal found dead on a property; one acting aggressively near humans, pets, or livestock; one fighting with domestic animals) were potential indicators that the animal was rabid and should

Table 21.1  Submissions in Canada, including survey samples, 1985 to 2017. Prov/Terr BC AB SK MB ON QC NB NS PE NL YK NT NU Total % Total

Total

Fox

Other

8,744 18,705 20,042 14,754 157,878 51,859 3,766 1,413 361 1,397 43 593 771

Dog/Cat 2,141 6,621 8,176 7,160 50,670 30,515 1,057 381 134 318 27 244 309

5,262 3,952 2,378 309 22,505 5,835 466 530 115 120 3 12 0

Bat

Raccoon 197 219 520 645 23,185 4,253 1,359 211 19 0 0 0 0

Skunk 140 4,920 4,835 3,143 12,073 1,127 195 20 10 0 0 1 0

22 199 593 423 17,445 3,683 209 85 29 837 4 203 406

701 1,289 1,019 763 16,248 3,272 212 62 20 62 2 22 22

Livestock 164 823 1,866 2,062 14,614 2,782 244 100 33 19 4 0 0

Wildlife 117 682 655 249 1,138 392 24 24 1 41 3 111 34

280,326

107,753 38.4

41,487 14.8

30,608 10.9

26,464 9.4

24,138 8.6

23,694 8.5

22,711 8.1

3,471 1.2

% Total 3.1 6.7 7.1 5.3 56.3 18.5 1.3 0.5 0.1 0.5 0.0 0.2 0.3 100

Note: Wild = wolves and coyotes; Other = all other animals. Source: compiled from CFIA data. Table 21.2  Positive rabies cases in Canada, 1985 to 2017. Prov/Terr

Total

Fox

BC AB SK MB ON QC NB NS PE NL YK NT NU Total % Total

374 279 2,768 2,123 19,653 3,234 120 14 5 132 0 144 349 29,195

0 1 1 34 8,822 1,795 0 3 3 110 0 111 269 11,149 38.2

Skunk 4 116 2,273 1,685 4,587 260 15 0 0 0 0 0 0 8,940 30.6

Live 0 5 159 242 2,818 353 1 2 0 3 0 0 0 3,583 12.3

Dog/Cat 4 14 112 110 1,476 419 1 2 1 9 0 26 64 2,238 7.7

Note: Wild = wolves and coyotes; Other = all other animals. Source: compiled from CFIA data.

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Bat 364 142 212 30 1,127 197 22 7 1 1 0 0 0 2,103 7.2

Raccoon 0 5 6 561 145 81 0 0 0 0 0 0 798 2.7

Wild 0 0 0 4 204 53 0 0 0 9 0 5 16 291 1.0

Other 2 1 6 12 58 12 0 0 0 0 2 0 93 0.3

% Total 1.3 1.0 9.5 7.3 67.3 11.1 0.4 0.0 0.0 0.5 0.0 0.5 1.2 100.0

Data Collection and Diagnostic Methods

be submitted. As noted in the discussion of rabies incidence in several provinces (Alberta, Ontario, and Quebec; see Chapters 7, 10, and 11, respectively), this passive surveillance system, focusing on human contact with potential rabid animals, has proven effective in identifying the presence of rabies in a given area. The level of submissions from provinces and territories also reflects the history of incidence in a province or ­territory. Figure 21.2 shows the ratio of negatives submitted relative to each positive case reported from each province and two territories from 1985 to 2017. Provinces and territories with long-term, continuous experience with rabies over that period (Saskatchewan, Manitoba, Ontario, Quebec, ­ ­ Newfoundland and Labrador, and the north: Northwest Territories and Nunavut) show fewer negatives for every positive than provinces with sporadic incidence (­British Columbia, Alberta, New Brunswick, Nova Scotia, and Prince Edward Island). In provinces with sporadic ­incidence, the threat of rabies remains and submissions continue at a high level to have the earliest possible warning about rabies in that jurisdiction. This same phenomena was noticed by Pond and Tinline in a study of rabies reporting in the 1960s to the 1980s by the DVOs responsible for assessing risk and, therefore, authorizing the submission of specimens. DVOs were interviewed in districts with continuous and relatively high incidence (category A), and districts with sporadic and low incidence (category B). Veterinarians from category A districts were less likely to submit specimens than veterinarians from category B districts. While DVOs from both types of region were equally vigilant about submitting

specimens where humans were at risk, DVOs in category B districts were more likely to submit specimens where humans were not at risk in hope that a positive diagnosis would be an early warning of rabies in their area. As a consequence category B districts had relatively more negative than positive submissions. Recent events in Ontario reflect how the reporting system has reacted to (1) a successful control program, (2) enhanced surveillance in anticipation of the spread of the raccoon strain of virus from New York, and (3) a change in reporting protocol for bats. In Ontario rabies-positives declined rapidly in the early 1990s as the ORAVAX wildlife control program, which began in 1989, took effect (see Chapter 10). As expected, submissions dropped (Figure 21.3) but the province remained on high alert. Between 1995 and 2015, even though rabies incidence in Ontario was low, the ratio of negatives to positives was an order of magnitude higher than before 1995 (approximately 4 negatives for each positive before 1995 and compared to 43 negatives for every positive between 2005 and 2017). The spike in submissions in 1997 and the consequent rise in the negative-positive ratio in Figure 21.3 occurred because the Ontario Ministry of Natural Resources and Forestry (OMNRF) submitted many more specimens from southeastern Ontario hoping to discover the first cases of the impending invasion of the raccoon strain of virus from neighbouring New York. The rise in the negative-positive ratio in the early 2000s and its subsequent decline reflects a rapid rise in submissions in bats and then an equally rapid decline. As Chapter 10 discusses, the rise appeared to be a reaction to the death of a boy in Montreal from a bat bite

Figure 21.2: The number of negative submissions for each rabies-positive diagnosed in Canada’s provinces and territories between 1985 and 2017. Yukon is not shown as there were no rabies-positives during that period. The order of the provinces in the figure is west to east followed by the territories in the north. Source: created from CFIA data.

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Figure 21.3: Submissions in ­Ontario from 1985 to 2017 showing negatives, positives, and the ratio of negatives to positives (N/P). The second order polynomial trend line fitted to the negatives to positives ratio (N/P) was statistically significant (p = .05). Source: compiled from CFIA data.

in 2000. Subsequent research published in 2009 showed that the risk from bats when there is no physical contact is very low. Consequently, recommendations for submitting bat specimens were revised in Quebec, Ontario, and other provinces and submissions subsequently declined.

available for analysis, and the inclusion of submissions in the digital data set. Although the changes have been for the better, they have also highlighted several limitations in the data which will be discussed in the section “Concerns with Canada’s Rabies Data.”

The Pluses of Canada’s Rabies Dataset

Assessment of Canada’s Passive Surveillance Data

In general, Canada has one of the best datasets in the world because, at appropriate levels of aggregation, it has consistently reported key details (species, date, location) of rabies incidence across an entire country over an extended time. Although the dataset’s primary purpose was to document human interactions with potentially rabid animals, the discussion of rabies in the various provinces and territories (see Overview, Part 3) demonstrates that the data were reasonable in providing adequate detail for surveillance, research, and the management of control programs for companion animals,

As the quotation from William Osler notes at the beginning of the chapter, collection of data allows for an interpretation of a situation. Data has to be accurately reported to make sense from it. As Louis Nel (2013) states, the absence of reliable and sustained data compromises the priority given to the control of rabies. The CFIA data has been collected since 1926 and has seen several changes in the location code of the submissions, the reporting period, the level of detail

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livestock, and wildlife. Further, as previously mentioned, the data system has provided appropriate early warning of the initial presence of the rabies virus in wildlife and, in this regard, seems to do as good a job or a better one than more intensive and expensive active surveillance methods. The reasons for this overall quality are simple. Canada has had one federal agency (under several names: Department of Agriculture, Agriculture Canada, and now CFIA) to look after collection and diagnoses since 1925. Reporting was compulsory across Canada. This meant that collection was directed through DVOs and was guided by clear standards (see Chapter 31). Further, the samples were diagnosed using standard methods in a small number of federal laboratories (three laboratories). Finally, the federal agency responsible for rabies has maintained good relationships with its provincial and territorial counterparts in health in assessing the risk of human exposure and deciding about post-exposure prophylaxis. Unfortunately, as the concluding chapter in this book notes (Chapter 39), the federal agency has recently divested itself of responsibility for the collection of specimens, leaving that duty to various provincial and territorial agencies. The impact on data quality has yet to be determined.

those ledgers and transcribe them into an Excel spreadsheet. The resulting spreadsheet listed each rabies-positive diagnosis by year, by month, or by quarter; by species; by province or territory; and by the county or its equivalent in which the specimen was found. The result encompassed the years 1926–1984. Starting in 1985, all submission records were digital and included positives, negatives, and additional data as noted below. DATES

Data before 1985 had two major problems in reporting dates. First, data obtained from the ledgers from 1926 to 1974 was based on the fiscal year (April to March of the next year). Fortunately, until 1957, each individual record listed the quarter or month the specimen was received so dates could be adjusted to the calendar year as required. Unfortunately, month or quarter was not recorded from 1957 to 1973, so data had only a calendar year designation. Hence the data used in this book for this period was stored by the dominant year (e.g., data for April 1959 to March 1960 was stored as 1959). There was an exception for western Canada. For most of this period Canada had two diagnostic labs: one in Hull, Quebec, and one in Lethbridge, Alberta. The Lethbridge lab served western Canada (Manitoba to British Columbia) and the north (Yukon and the rest of the Arctic – which was then all the Northwest Territories). Fortunately, the Lethbridge laboratory had retrospectively assembled its data into digital records from 1953 onwards and those records included a full data field (day/month/year). Hence, for the west and the north there is no confusion arising from fiscal or calendar year entries. The next problem concerns the date used to represent the rabies case. All tabulated records (ledger or otherwise) before 1985 recorded only the date the specimen was received at the lab. From 1985 on two dates were available: the date the specimen was collected and the date the specimen was received at the laboratory. Analysis of the differences between samples of the two dates showed a mean lag of two to three days. This lag increased when a weekend separated the collection date and the received date. Further, there is no way of knowing how the collection date related to the onset of rabies in a positive specimen. Given an estimated incubation period of a week in most small mammals, delays in communication between field staff and those involved with potentially rabid animals, and the lag between collection and reception, analyses in this book used the month as the minimum level of aggregation. As well, because of the fiscal and calendar year concerns mentioned above, analyses over the entire span of the data

Concerns with Canada’s Rabies Data For detailed analysis, however, the dataset has been problematic especially in recording the location of rabies incidents in space and time. As a result, data reporting has had to be aggregated to be reliable and consistent. Generally, the resulting level of aggregation has been adequate for reporting trends but less than adequate for detailed assessment of spread and potential interactions between various species involved. Some of the data problems have been structural, relating to choices made about data collection, storage, and structure, and others have related to human error and the lack of adequate feedback between data users and data collectors. The following sections demonstrate some of those concerns. DATA COLLECTION

As mentioned, before 1985 data was stored on paper and typically available in summary fiscal or annual reports. Most of the original paper submission forms dating back to 1950s still exist, but given the gaps and the tremendous effort required to transcribe that information into digital form, it has not been done. For reporting purposes clerks, at the time, consolidated information on submissions that tested positive into annual ledgers. As part of CFIA’s contribution to this book, a student was hired to work through

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(1926 to present) were forced to use the year as the minimum level of aggregation.

search-place-names/search), provincial or territorial directories of municipalities, or the Google search engine, an especially helpful tool when spelling errors compounded the lookup process. These problems were further complicated by boundary changes or name changes in the county structure over time and a tendency for location reporting to use old familiar names rather than the most recent ones. As well, the county structure does not cover the entire provine in Ontario and Quebec. Some cities and their suburbs, northern areas, and Indigenous reserves are excluded from the county structure. For example, in Quebec in 2012 there were 86 regional county municipalities and then 47 non-Indigenous municipalities (mainly urban) and 47 Indigenous communities not covered by this structure. Further, the entire northern half of the province, the Nord-du-Québec administrative region, was not part of the regional county system. As well, Quebec went through a major set of administrative boundary changes in 2002, but the subsequent locations listed in in the dataset often reflect the previous structure. The overall solution for the location unit in the d ­ ataset in this book was to use Statistics Canada census division names and the associated maps available from that agency to define county units. For the most part, census divisions boundaries are derived from provincial and territorial units and their names typically reflect county structures (Table 21.3). Although the decision to standardize on census divisions entailed a great deal of data cleaning to reassign locations, it meant the county unit in the data is inclusive of all municipalities and covers the entire area. Note that the Northwest Territories and Newfoundland and Labrador do not correspond to census divisions. Incidence was low in those areas and, therefore, appropriate place names became the standard in the dataset for those areas and for mapping and analysis. In sum, location data used in this book were aggregated where possible to the level of Canada’s census divisions. This decision reflects the nature of the available data and the ongoing changes in administrative boundaries in ­Canada. The recent decision by CFIA to require latitude/ longitude coordinates for the location where a specimen was collected should allow future analyses to aggregate the data to whatever boundaries are useful for an analysis.

LOCATION

Despite the changes in location coding already discussed, these codes were often missing or inaccurately reported in the available datasets. Indeed, over time, the only consistent location entry has been the county, the district, or the regional county municipality in which the specimen was collected. Hence those units have become the de facto minimum level of aggregation in the dataset. The county unit was used in the Maritimes and Ontario, the district unit was used in the western provinces and the territories, and the regional county municipality unit was used in Quebec. Although these units are roughly comparable in administrative function across Canada, their size and shape vary between and within provinces and territories reflecting local variations in physiography, the design of original settlement surveys, and ongoing amalgamations as authorities attempt to adjust boundaries to reflect changing human population distributions. The various maps of incidence in the provincial and territorial chapters reflect this diversity. Typically, those maps show that larger units are associated with sparse populations, and while maps using those units show trends, the details of incidence are hidden. Indeed, in the territories, rabies data are typically reported by settlement name as the districts are too large to be meaningful in terms of mapping and understanding rabies incidence. There are further complications in the reported location data since 1985. That data records two location fields: owner-city (the location of the specimen’s owner) and county (a generic term for county, district, or regional municipality). For the most part entries in the dataset make sense: the owner-city lies within the county. In other cases the owner-city lies outside the county. This makes sense when pets are involved and the county where the rabies incident occurred was a vacation region. It also makes sense where livestock was involved given that some farmers have wide spread holdings that transcend county boundaries. In the case of wildlife, however, the argument is not as clear. Given situations in the data when the province listed for the data is questionable or the listed county is a place name rather than a county name or the owner-city is a county name, it appears likely that the columns were transposed on data entry. Where possible, the data have been adjusted so that place names in the county field were converted to county names using the transposed data in the owner-city field or, when this was not possible, using Natural Resources Canada’s place names file (http://www4.rncan.gc.ca/

SPECIES

Until the introduction of the Laboratory Control Sample System in 1985, species were reported generically in the dataset (i.e., bat, bovine, cat, dog, fox, stripped skunk, etc.). From a research perspective, this made it impossible to

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For analyses that include data before 1985, the generic ­coding system must be used. Hence, the datasets used in this book have both a generic species coding field and a ­species-specific field when that data was available.

Table 21.3  Correspondence between provincial and territorial county names and other administrative units with Statistics Canada’s census divisions. Province/Territory

Nature of Census Divisions

Alberta Manitoba Saskatchewan British Columbia

Groups of municipalities such as cities, municipal districts, and rural municipalities

New Brunswick Nova Scotia Prince Edward Island Newfoundland and Labrador Northwest Territories Nunavut Ontario Quebec Yukon

SAMPLES AND CLINICALS

The provincial and territorial chapters (see Part 3) indicate that, in addition to specimens collected via passive surveillance, samples were often added to the dataset as a result of active surveillance and specific research projects. This has occurred in the north (see Chapter 14b), Alberta (see Chapter 7), Ontario (see Chapter 10), Quebec (see Chapter 11), and Newfoundland and Labrador (see Chapter 13). For the most part those samples have been identified and flagged in the datasets so that, as required, analyses can be performed on passive surveillance data. However, a very small number of specimens obtained from active surveillance are probably listed within the passive surveillance data. Another potential source of error in the data was the early practice of recording rabies-positives from clinical observation rather than laboratory testing. This was done to facilitate compensation payments in livestock. Although most of these data has been flagged and eliminated from the passive surveillance datasets, a small possibility still exists that rabies-positive data before 1985 includes clinical diagnoses in livestock.

Correspond with regional districts or municipalities Correspond with counties

Census divisions are delineated separately from provincial administrative boundaries Do not correspond to the administrative regions Correspond with the administrative regions Upper-tier municipalities (counties, districts, regional municipalities, single-tier cities) Mostly correspond to regional county municipalities or equivalent territories Treated as a single census division

Source: compiled from Standard Geographical Classification (SGC) 2016, Statistics Canada.

examine questions such as the role of arctic and red foxes in rabies transmission, and the correlations between species of bats and rabies. From 1985 onwards, however, CFIA required that a detailed species code be entered from a list of 230 possibilities for each specimen received at the laboratory. Hence, it became possible to differentiate three fox species (arctic fox, AFX; red fox, RFX; swift fox, SFX) and some 23 bat species (little brown bat, LBB; big brown bat, BBB; silver-haired bat, SHB, etc.; see Chapter 27). There are, however, two further concerns with these data. First, a small number of specimens are still submitted with the generic designation (fox, bat) for species. In Ontario, for example, 169 specimens of a total of 20,280 bat submissions ( 1000) in foxes in a rabies-free area of France.

Rabies Exposure in Humans and Domestic Animals by Red Foxes Costs associated with rabies include post-exposure treatment or PET (vaccine, immunoglobulin) for humans, domestic animal vaccination and quarantine, and livestock compensation (see Chapter 34). Southern Ontario supports a major cattle industry (both beef and dairy) among other livestock (goats, horses, sheep, and swine), a fairly substantial rural population, and urban conglomerates, all maintaining large numbers of dogs and cats. Those factors heightened exposure potential for humans and domestic animals. From 1977 to 1980, 3366 PET were administered in Ontario: 280 PET (153 incidents) or 8% were due to rabid red foxes, compared with 40% dog, 21% cat, 12% cattle, and 19% for 23 other domestic animals and wildlife (Honig, 1985). Of the fox exposures, 8% were bites, 3% were scratches, 81% were handling or other contact (saliva), and 8% were other or unknown; 28% of dogs and 62% of cats registered bites and scratches, and 96% cattle exposures were due to handling. The Ontario Ministry of Health Annual Report (1985) registered 4508 PET in 1983 and 1984 in Ontario with the following sources: 30% dog, 24% cat, 12% cattle, 12% fox, and 22% other domestics and wildlife. Undoubtedly, proximity to humans elevated domestic-mediated PET in contrast to species incidence. However, the indirect sources of the majority of PET were most likely red foxes and striped skunks, with domestic animals as intermediaries. PET species quantification is slightly inflated in domestic animals since they are more likely the cause of multiple

Prevalence of Rabies Virus Antibody in Red Foxes The presence of RABV antibodies (RABV-AB) is generally credited to an immune response from a previously failed infection or non-lethal exposure (possibly a low dose of RABV, unsupported variant), but it could indicate an individual that survived the disease (Blancou et  al., 1991; Wandeler, 2004). Wandeler et  al. (1974b) indicated that foxes rarely survive a full blown infection, and experimental foxes that have survived had only low or no antibody levels (Blancou et al., 1983). However, Blancou et al. (1991) suggested that it can never be ascertained whether a fox demonstrating antibodies will eventually die of rabies because rabid foxes have been shown to develop antibodies prior to showing clinical signs. In durable enzootics, some

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Red Fox (Vulpes vulpes) and Rabies

exposures, requiring more PET per incident. Based on Honig (1985), an average PET per animal was: 2.8 dog, 2.0 cat, 1.9 cattle, 1.8 fox, and 2.7 horse. Varughese (1985) delineated 1229 incidents (or animals) of human exposure in Canada in 1984 as 28% dog, 25% cat, 12% fox, 8% cattle, and 27% other, requiring PET per incident (animal) of 7.6 dog, 3.7 cat, 1.7 fox, 2.6 cattle, and 2.5 other. PET sources in the United States in 1981, where rabid skunks, raccoons, and bats predominated, somewhat mirrored Ontario (rabies incident are in parentheses): 32% dog (2%), 23% cat (4%), 10% bat (11%), 8% raccoon (10%), 8% cattle (5%), 6% skunk (63%), 1% fox (3%), and 10% other wild and domestic (2%) (Helmick, 1986). There have been no documented cases of red foxes causing a human rabies death in Ontario. In fact, there are no records of human deaths from arctic variant rabies from red foxes. There was a report of a man that died from hydrophobia in 1914 in Alaska (Ferenbaugh, 1916), but the source was never ascertained, and Johnson (1971) described a human rabies death caused by a wolf bite in Alaska in 1942. Kuzmin (1999) noted a human rabies case in Siberia from a wolf, and Lassen (1962) reported a human case in Greenland from a dog. Vyazhevich (1959) described a red fox-mediated human case in central USSR, but the RABV variant was unclear. Mørk and Prestrud (2004), citing various authors, summarized four human rabies deaths in Siberia and the northern part of European Russia, one from an arctic fox, but the others did not report sources. Bolstered by a concentrated human population, and confronted with a different RABV variant (i.e., cosmopolitan), fox-source human rabies deaths in the former USSR ranged from 36% to 47% (n = 258 to 337) from 1966 to 1975 (Botvinkin & Kosenko, 2004), and 38% (n = 32) in central Europe from 1969 to 1977 (Steck & Wandeler, 1980). In the United States, from 1951 to 1970, 5% (n = 110) of human rabies deaths were caused by foxes (Winkler, 1972). Since the first incursion of arctic variant rabies in 1958, there were two documented human rabies cases in Ontario, possibly implicating red foxes but indirectly. The first case was in 1959 in Port Perry caused by a skunk (McLean et al., 1960) and the second, in 1967 near Ottawa (see Chapters 3b and 10), was due to a cat (one other human case in 2012 was non-indigenous). While the frequency of wild-domestic animal contacts has not always been quantified, when such case reports were available (1977–1980), those interactions were 41% fox-dog, 21% skunk-dog, 12% dog-dog, and 4% cat-cat (Honig, 1985). Evidence from radio-tracking in Ontario indicated infrequent incursions by red foxes into or near

pastures and farmyards – potentially encountering livestock or dogs and cats. Also, incidence of rabies in foxes and domestic animals from passive surveys were fairly synchronous throughout, implying a causal fox-domestic animal relationship (Figure 26a.3). Individual case reports (from Canada Department of Agriculture) during 1974 detailed some examples of (diagnosed rabid) red fox-domestic animal/human contact scenarios: (1) owner’s two dogs killed a fox, (2) a fox was found dead beside a chained dog, (3) a fox fought with a dog, (4) a fox fought with a dog in a pen, (5) a fox was shot by a farm owner in the barnyard, (6) a fox attacked an owner’s dog, and (7) a fox was found dead in a horse stall.

The Red Fox and Wildlife Rabies Control Initially, rabies control in wildlife enzootic areas, such as SORE, consisted of isolating and protecting the public from the source of infection (wild animals) by monitoring incidence, immunizing domestic animals, relying on PET (Nunan et al., 2002), and providing public education. That process is costly and interminable. Rabies control by culling, or depopulation, to reduce vector density and interrupt contact is labour-intensive and only marginally successful. Methods of depopulation, some of which are controversial and not appropriate in all situations and environments, include hunting (and bounties), poison baits, gassing fox dens, trapping, and reproductive inhibitors (Debbie, 1991). Under initial enzootic conditions, intensive culling has proven successful but was found to have no lasting impact, especially with the resilient red fox (Linhart, 1960; Parks, 1968; Wandeler et  al., 1974a; Bögel et al., 1981). Macdonald (1980) proposed that culling strategies do not work because removing a fox (or foxes) from a territory just leaves an empty space or vacuum, which is readily re-inhabited by another fox. Bounties applied in the mid- to late 1950s in Ontario (Department of Lands and Forests District internal reports of fox bounties), did nothing to lower red fox populations nor prevent the introduction of rabies into southern Ontario. One option that was considered in Ontario was the use of strychnine to poison foxes and control the spread of rabies. That proposal was shelved, mostly because of the concerns and perils of dispersing toxic material near people, pets, and livestock. A chemical reproductive inhibitor, diethylstilbestrol, was distributed in baits in Carleton County of eastern SORE in 1967 to impede reproduction in foxes (D. Johnston, personal communication, 1979). Debbie (1991) noted that

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Ecology and Epizootiology of Wildlife Rabies

diethylstilbestrol was effective only over a very short period during a vixen’s reproductive cycle – and therefore ineffective in the long run. Voigt and Tinline (1982) found that intensive levels of fox trapping and hunting did decrease the severity of rabies outbreaks, but not their frequency. Vaccinating wild animals against rabies to interrupt RABV transmission was a third option for rabies control. Initially costly and not without its problems, wildlife vaccination was expected to provide a lasting solution by replacing susceptible animals with immune animals (i.e., herd immunity) and permanently precluding RABV transmission (Johnston et al., 1988). Lawson et al. (1997) had shown in laboratory trials that post-oral vaccination immunity in foxes may last up to seven years. Vaccine delivery methods include parenteral, that is, direct intra-muscular injection, or oral (optionally, enteric), that is, absorption in mucous membrane during ingestion. Parenteral vaccination of wildlife is extremely effective but labour-intensive and limited to urban or confined rural areas as indicative of Ontario’s trap-vaccinate-release programs (Rosatte et  al., 1992). Ontario opted for oral rabies vaccination (ORV) to distribute vaccine-laden baits to control and eliminate rabies in red foxes over the extensive areas of SORE (see Chapter 10). ORV for foxes was reviewed globally (World Health Organization, 1973, p. 38), initially tested in laboratory and small field trials (Baer et al., 1971; Black & Lawson, 1973), and then applied in extensive programs in Europe and North America (Steck et  al., 1982; Schneider et  al., 1983; MacInnes et al., 2001; Bachmann et al., 2005). In Ontario integrated research concentrated on vaccine-bait development, including efficacy and safety, vector biology and epizootiology, and baiting strategies. Laboratory trials with baits and a modified live vaccine (ERA) were very effective (Black & Lawson, 1980; Lawson et al., 1997) and safe (Lawson et al., 1987; see Chapters 17and 18) in red foxes. Knowledge of red fox biology and epizootiology was acquired almost exclusively from radio-tracking (movement, interaction), fox population analyses (age structure, reproduction, and density), and rabies incidence data (Voigt & Tinline, 1980; MacInnes et  al., 1988). The Ontario Fox computer model was developed in partnership with Queen’s University to simulate conditions, such as rabies spread and response scenarios, to initialize control strategies (Voigt et al., 1985; see Chapter 10). A variety of baits and tactics (spatial, temporal, dispersal), mostly using aircraft for distribution, were tested in a series of experiments from 1972 to 1991 to formulate a comprehensive baiting system (Bachmann et al., 1990; Chapters 10 and 19). In a seven-year (1989–1995) ORV control experiment with

ERA and Ontario baits (see Chapters 10, 17b, and 17c), Ontario fox rabies was eliminated in red foxes from a 30,000 km2 region of eastern SORE (MacInnes et al., 2001). Rabies in skunks in that region also disappeared even though ERA was not effective in immunizing skunks by the oral route. The success of the control experiment prompted serial shifts of ORV campaigns throughout SORE (and in some years, adjacent Quebec) starting in 1993, always targeting red foxes with vaccine-baits, and covering anywhere from 25,000 to 65,000 km2 annually. In 1992–1993, 1997, and 2000–2002, vaccine-baits were distributed in select areas of northern Ontario (Bachmann et  al., 2005) in response to the localized rabies outbreaks near Kirkland Lake, Cochrane, Kapuskasking, and Sudbury. Also, oral vaccine (ERA) in baits was distributed in green areas and river ravines of the Greater Toronto Area from 1989 to 1999 to immunize urban red foxes (Rosatte et al., 2007). From 1989 to 2004, bait uptake in red foxes, determined by tetracycline-biomarker assay (Johnston et  al., 1987; see Chapter 24b), averaged 71% annually (52% to 82%, n = 6848) and post-baiting rabies virus antibody in red foxes, via sero-diagnosis (Campbell & Barton, 1988; Elmgren & ­Wandeler, 1996) was 40% (6% to 61%, n = 6848) (Bachmann et al., 2005). The prevalence of RABV in active surveys of red foxes dwindled during 1989 to 1994: 1.9% (n = 795), 2.7% (n = 2083), 1.1% (n = 3185), 0 (n = 605), 0.2% (n = 975), and 0.5% (n = 824); from 1995 to 2004, there were no RABVpositive foxes (n = 4961) (Bachmann et al., 2005). Mean annual rabies cases in red foxes based on passive surveys fell by 97% from 1995 to 2004 to 19 cases compared with 659 cases from 1957 to 1990 (CFIA, 1957 to 2005). From 2010 to 2016 there were no reported rabid foxes in Ontario. Unlike in eastern and central SORE, rabies in skunks in the western portion of SORE did not disappear after the extirpation of rabies in foxes following ORV. Sporadic cases of rabid skunks still persist in that region. Subsequent ORV campaigns, particularly targeting skunks with ONRAB vaccine (Rosatte et al., 2011), which does immunize skunks orally, but also aiming to maintain an immunized red fox population, are ongoing. In 2017 a single rabid red fox appeared in Waterloo region of western SORE after being free of rabid foxes for seven years.

Research Questions and Considerations A great deal of literature has been published on the red fox, its biology, and relationship with rabies throughout its range. Any additional information related to this subject

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Red Fox (Vulpes vulpes) and Rabies

might include (1) the impacts of ORV on fox populations in Ontario; (2) the possibility of reintroduction of rabies in southern Ontario; (3) the red fox-striped skunk rabies connection; (4) the distribution and migration of red foxes in view of climate change and other factors, such as predators; (5) the co-evolution of the fox-RABV; and (6) the alterations to RABV variants. What are the ecological impacts of bioengineering the elimination of rabies in foxes (and skunks) using ORV, or does it matter or is it even cost-effective to find out? What might the perils be if we don’t find out? Essentially, ORV was applied to minimize the threat of rabies to humans, to protect public health, and to lower its costs, not for any ecological need to protect foxes. Will fox densities, reproduction, and social behaviour change and cause other problems? Or will other mortality factors (i.e., mange, other diseases), population-reducing factors (e.g., coyotes), or lowering fecundity compensate for rabies mortalities? How might increasing coyote populations and changes in land-use patterns (Ray, 2000) contribute to changes in red fox abundance and behaviour? Despite a slight increase in average fox pelt prices, the red fox harvest in Ontario decreased by 52% from 1998 to 2007 compared with the previous decade (Wildlife Section Report, 2010). Similarly, average annual fox specimen returns in post-ORV surveys in southwestern Ontario (2002–2007) had decreased by 76% compared to 1994–1999. Although estimating population trends from harvest data is not always reliable, could those results indicate an actual decline in red fox numbers, primarily in southern Ontario? Anecdotal information from local hunters and trappers from various regions of southern Ontario corroborated those data – there appear to be fewer red foxes! However, red foxes are becoming more visible and abundant in northern Ontario, north of Lake Superior (K. Abraham, personal communication, May 2015), which would indicate a shift to alternative habitats by this very adaptable species, possibly spurred on by such factors as warming climate or loss of habit buttressed by changes in land-use patterns that are highlighted by urban sprawl in many rural areas of southern Ontario. Also, in some areas of rural southern Ontario, red foxes appear to be centring their activity closer to human habitations, a factor possibly caused by territorial constriction caused by crowding through increasing coyote numbers (B. Stevenson, personal communication, May 2015) and coyote-avoidance behaviour by foxes (Voigt & Earle, 1983). What are the chances of the reintroduction of RABV, possibly an altered variant, into fox populations in southern Ontario? After a number of years without ORV and

perennial recruitment of new individuals, the immune status of wild red foxes will be negligible. Can the existing ORV measures in Ontario respond to a new wave of rabid red foxes? On the other hand, if, indeed, red fox populations are in decline, and fox densities are undermined expansively, the perils of fox-mediated rabies in southern Ontario might become a thing of the past. Lynch (2000) and Hannah (2011) described the ever increasing abundance and northern expansion of red foxes, associated with warming temperatures, and their encroachment on arctic fox territories. Displacement and elimination of arctic foxes by the more aggressive red fox has been documented (Bailey, 1992; Linnell et  al., 1999; Post et  al., 2009; see Chapter 26b). Will the expansion of red foxes and potential displacement of arctic foxes alter the dynamic of the arctic rabies enzootic (Kim et al., 2013 and Chapter 26b)? Will that inter-species contact impact any fox-human interactions in the north? What are the potential risks of modifications of the arctic RABV (or any other variant), such as increased virulence, co-evolving with extended red fox populations in polar regions in the resurgence and migration of rabies, similar to the 1950s scenario, or introduction to subsidiary hosts?

Conclusions Rabies in red foxes has been a global concern since the late 1940s. The ubiquitous, resilient, and highly susceptible red fox was an ideal rabies vector, and owing to its adaptability, a public health threat. In Canada rabies in red foxes originated in the north and migrated south, concentrated, and became enzootic in southern Ontario. The complex interaction of host (fox), environment and RABV defined the epizootiological construct of the disease. Fox activity and dynamics, such as reproduction, social interactions and movement, all contributed to the characteristics and perpetuation of the disease. Rabies control by ORV, which was originally formulated solely for red foxes, was instrumental in eliminating the disease in other wildlife in Ontario and elsewhere. While questions about the long-term effects of bioengineered rabies control on fox populations remain unanswered, vigilance must be maintained to prevent any re-incursion of the disease. Climate-mediated expansion of red foxes north, encroaching on arctic fox territories, and the potential evolution of the RABV associated with that red fox expansion could alter dynamics of rabies in polar regions.

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Acknowledgments The information on red foxes of Ontario presented in this chapter was garnered and analysed by many field and laboratory workers from 1973 to 2005. These include Ian Watt, Frank Matejka, Barry Earle, Jim Broadfoot, Wayne Lintack, Douglas Gilmore, Sarah Fraser, Richard Bramwell, Michael Pedde, Laurie Calder, Kathy MacDonald, Joanne Wesson, Beverly Stevenson, Andrew Silver, Kim Bennett, Lucy Brown, Terry Medd, Mark Gibson, Kathryn MacDonald, and numerous seasonal and part-time staff. Thanks to Rowland Tinline, formerly of Queen’s University, and David Gregory, formerly of the Canadian Food Inspection Agency, who reviewed the initial draft of this chapter and provided constructive ideas and revisions. Also, many thanks to Kim Bennett, Mark Gibson, and Beverly Stevenson, of the Wildlife Research and Monitoring Section of the Ontario Ministry of Natural Resources and Forestry, for refining pertinent editorial and factual content for the final manuscript. Special thanks go to David Johnston and Dennis Voigt, both consummate red fox biologists, who imparted their knowledge and experiences very effectively during my field and laboratory work with them.

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26b Fox Rabies ECOLOGY OF RABIES IN THE ARCTIC FOX (VULPES LAGOPUS)

Audrey Simon,1 Denise Belanger,2 Dominique Berteaux,3 Karsten Hueffer,4 Erin E. Rees,5 and Patrick A. Leighton1 1 Université de Montréal, Faculté de médecine vétérinaire, Saint-Hyacinthe, Québec, Canada Université de Montréal, Faculté de médecine vétérinaire (Retired), Saint-Hyacinthe, Québec, Canada 3 Université du Québec à Rimouski, Rimouski, Québec, Canada 4 University of Alaska Fairbanks, Fairbanks, Alaska, United States 5 Senior Biostatistician Epidemiologist, National Microbiology Laboratory, Public Health Agency of Canada, Saint-Hyacinthe, Quebec, Canada 2

Introduction Rabies occurs across the Arctic and is regarded as enzootic in northern Canada (north of 60°N), coastal northern and western Alaska, Greenland, and the former Soviet Union from its western border to the Far East with discontinuous affected areas (Tabel et al., 1974; ­Secord et al., 1980; Baer, 1991; Kuzmin et al., 2004; Mork & Prestrud, 2004; Mansfield et al., 2006; Nadin-Davis et al., 2008; Kim et al., 2014). The main reservoir host of rabies in the Arctic is the arctic fox (Vulpes lagopus), also known as the polar fox or the white fox (Plate 21). The presence of rabies virus and its establishment in the fox populations from North America had been demonstrated at the end of the 1940s (Plummer, 1947; Williams, 1949). Arctic rabies is caused by a unique variant of the rabies virus referred to as the arctic rabies virus variant, which circulates within the Arctic and subarctic regions with sporadic incursions towards more southern regions, occasionally leading to establishment of enzootic rabies in these areas (Rosatte, 1988). However, arctic-like rabies virus variants, distinct from the arctic lineages but related phylogenetically, are more widely distributed, occurring throughout the northern hemisphere as far as southern and eastern Asia and the Middle East, where they circulate in dogs and wild canids such as red foxes (Vulpes vulpes) and raccoon dogs (Nyctereutes procyonoides) (Mansfield et  al., 2006; ­Nadin-Davis et  al., 2007; Kuzmin et  al., 2008). In the Canadian Arctic, rabies cases in domestic animals and wildlife are reported every year, and the rate of post-

exposure prophylaxis (PEP) treatment per inhabitants is higher than in the more southern regions of Canada (Aenishaenslin et al., 2014; Rosatte, 1988; Canadian Food Inspection Agency [CFIA], 2013). This chapter outlines some relevant characteristics of arctic fox ecology as it relates to rabies ecology in the Arctic and then discuss what is known about the epidemiology of rabies in this species, the main gaps in our understanding, particularly with regard to the maintenance of the Arctic rabies virus variant in low-density populations of arctic foxes, and finally, the potential impacts of climate change and northern development on rabies in the Canadian Arctic.

Arctic Fox Ecology Distribution and Habitat The arctic fox has a circumpolar distribution and is found throughout the Arctic (north of the Boreal forest), as well as in alpine areas, ranging from northern Greenland at 88°N to the southern tip of Hudson Bay, Canada, 53°N. This small predator lives mainly in Arctic and alpine tundra, coastal areas, and islands (Fuglei & Ims, 2008). The arctic fox is also known to use other habitats, such as sea ice, to forage during periods of food scarcity (Tarroux et  al., 2010). In North America, the arctic fox is found throughout the Arctic tundra, including the islands of the Canadian Arctic Archipelago, as well as some of the Aleutian Islands in Alaska where foxes have been introduced (Audet et al., 2002).

Ecology and Epizootiology of Wildlife Rabies

suggested by rabies outbreaks with high mortality that often occur as fox populations reach a high density (Elton, 1931; Chapman, 1978; Ritter, 1981; Prestrud et al., 1992). Current knowledge is insufficient to conclude that rabies is, in fact, an important regulator of arctic fox populations. However, rabies is likely one of several mortality factors involved in the decline of arctic fox populations following a population crash in their primary prey (Follmann et al., 1988). Reduced food supply causes increased foraging movements, which, when associated with a population of high density, may facilitate rabies virus transmission because of increased contacts during movement and aggressive encounters while competing for scarce food sources such as scavenged carcasses (see “Spread and Persistence of Rabies in the North” below).

Foraging Ecology Arctic foxes are opportunistic predators and scavengers, feeding mostly on small rodents and birds but eating almost anything that is available in the tundra (berries, insects, fish, seabirds and their eggs, lemmings, seals, carrion, and food waste from dump sites) (Audet et al., 2002). Diet composition varies greatly among habitats. Arctic foxes inhabiting coastal areas take advantage of marine food resources such as seabirds, fish, seal pups, and scavenged carcasses of marine mammals whose availability is relatively stable among seasons and from year to year (Angerbjörn et  al., 2004). In contrast, foxes in inland habitats tend to have a less diversified diet with a strong dependence on cyclical lemming populations (Lemmus spp. and Dicrostonyx spp.) (Elmhagen et al., 2000). Thus, the abundance and stability of food resources differ considerably between the inland and coastal habitats, resulting in resource-driven population fluctuations that are very strong in inland foxes but less pronounced in coastal foxes (Angerbjörn et al., 2004). However, inland and coastal foxes represent extreme cases along a continuum of life-history strategies observed in arctic foxes, with many individuals occupying intermediate habitats and exploiting both lemmings and coastal food sources depending on their seasonal and annual availability (Gagnon & Berteaux, 2009; Tarroux et al., 2012).

Social Organization The arctic fox is a solitary forager in which the social group consists of the breeding pair and their young, and occasionally an additional nonbreeding female (Cameron et al., 2011). Its range of territoriality is associated with the density of occupied dens and may be higher among coastal foxes (Norén et  al., 2012). Arctic foxes typically mate in March or April and gestation lasts around 52 days (Audet et al., 2002). Females give birth in underground dens, which are generally large, and the same den is used year after year (Tannerfeldt et  al., 2003). Both the female and the male are active in parental care but hunt and rest alone (Garrott et al., 1984). The cubs emerge from the den when they are three to four weeks old and are weaned at six to seven weeks (Audet et al., 2002). They are independent at 12 to 14 weeks and begin to disperse in the fall, reaching sexual maturity at the age of 9 to 10 months (Audet et al., 2002). In rare cases, young from a litter of the previous year remain with the parents and help rear a new litter of siblings (Norén et al., 2012).

Reproduction and Mortality Patterns of reproduction and mortality are strongly related to food abundance. On one extreme of the inland-coastal gradient, inland foxes show great variation in reproductive output over the lemming cycle: during periods of food scarcity, a female arctic fox may not reproduce at all, whereas during periods of food abundance (e.g., during a lemming peak), the same fox may produce up to 18 cubs, corresponding to the largest litter size in the order Carnivora (Tannerfeldt & Angerbjörn, 1998). Thus, inland fox densities may vary more than tenfold between the peak and the trough of the lemming population cycle (Mork & Prestrud, 2004). In contrast, coastal foxes, with their more-stable food supply, consistently produce approximately five cubs every year (Tannerfeldt & Angerbjörn, 1998). Major known causes of mortality in arctic foxes include starvation, trapping, predation by avian predators (eagles, hawks, jaegers, and snowy owls) and mammalian predators (dogs, polar bears, red foxes, wolves and wolverines), and diseases (Audet et al., 2002). Rabies has the potential to serve as a regulating factor for arctic fox populations, as

Movement Movement behaviour in arctic foxes varies considerably between seasons and in relation to food abundance (Wrigley & Hatch, 1976; Norén et al., 2011). Daily foraging movements generally occur within a relatively well-defined home range that varies in area from 4 to 60 km2 according to spatial and temporal patterns of prey abundance (Audet et al., 2002; Eide et al., 2004). The overlap of home ranges also varies considerably according to food resources, increasing in areas where prey resources are clumped, highly

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abundant and predictable (coastal areas) (Eide et al., 2004). Seasonal movements occur in late autumn, early winter, and spring (Wrigley & Hatch, 1976; Audet et  al., 2002). Dispersal by juveniles mainly occurs in late summer and early fall, but when the local food sources are abundant, juveniles may remain in their natal home range throughout the winter (Chesemore, 1968; Eberhardt et al., 1983). Winter movements of arctic foxes are not well understood as they are difficult to study. In winter, most arctic foxes remain near their summer range, but some foxes become more mobile, foraging alone or congregating in large numbers at food sources and venturing onto the sea ice to forage (Chesemore, 1968; Smith, 1976; Andriashek et  al., 1985). The conditions that cause foxes to make excursions onto the sea ice are not well understood, but such excursions seem to occur during years when terrestrial food sources are scarce, suggesting that sea ice is an important additional foraging habitat (Pamperin et al., 2008; Tarroux et al., 2010). In addition to daily movement within their home range, arctic foxes are known to engage in sporadic

long-distance forays during which individuals may travel outside of their usual home range. During winter forays, individuals may travel remarkable distances, with collared individuals shown to move more than 1000 kilometres out onto the sea ice, often scavenging on seal carcasses remaining from human hunters and polar bear predation (Pamperin et  al., 2008; Tarroux et  al., 2010). These sporadic movements, reported primarily in Alaska and Canada, may therefore promote the genetic homogeneity observed among arctic fox populations connected by sea ice (Audet et  al., 2002; Dalén et  al., 2005; Carmichael, 2006; Geffen et al., 2007; Tarroux et al., 2010). Finally, large-scale winter migrations (or massive dispersal), involving large numbers of foxes travelling rapidly in a sustained direction, are occasionally observed following a decline in the numbers of lemmings and have been documented in Canada and Russia (Chesemore, 1968; Wrigley & Hatch, 1976). As well as having pronounced differences in their reproductive strategies and life-history traits, coastal and inland foxes display differences in their movement patterns, with

Figure 26b.1: Arctic and red fox ranges in North America. Source: Canadian Geographic.

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long-distance movements and nomadic behaviour being far more common among inland foxes (Dalén et al., 2005; Norén et al., 2011).

income (Gagnon & Berteaux, 2009). Because of its great capacity for reproduction when conditions are favourable, the conservation status of the species is good, except for the Fennoscandian population (or Baltic Shield). Over-hunted more than a century ago, the population of Fennoscandian arctic foxes remains low despite their protected status in the region, mainly because of the low abundance of rodent prey combined with competition with sympatric red foxes ­(Angerbjörn et al., 2013).

Interactions with Red Foxes, Humans, and Domestic Animals Over the last century and potentially linked with increased food resources because of climate warming in the north and increased human development in the south, the red fox has expanded its range above the treeline, where it now competes with the arctic fox for dens and food (Ovsyanikov & Menyushina, 1987; Hersteinsson & Macdonald, 1992; Tannerfeldt et  al., 2002; Gagnon & Berteaux, 2009; Gallant et al., 2012). Figure 26b.1 shows the general areas where these interactions have been reported. Sharing similar fundamental food niches, red foxes can exclude arctic foxes from the most productive den sites where alternative prey are more available during periods of low rodent density, as well as monopolizing carrion resources in the winter and even killing and eating its smaller competitor (Frafjord et  al., 1989; Elmhagen et  al., 2002; Pamperin et  al., 2006; Killengreen et al., 2011; Rodnikova et al., 2011). Such interactions certainly increase the contact rate between the two species, favouring the transmission of the rabies virus and other infectious agents (see below). Arctic foxes are relatively unafraid of people, and foxes are regularly sighted in human settlements. This peri-domestic activity increases opportunities for physical contact between foxes, humans, and domestic animals, especially dogs, which can chase and kill foxes (Ginsberg et  al., 1990). Foxes are attracted to settlements by the availability of anthropogenic food sources, which may increase survival of foxes when lemmings and other prey are rare (Killengreen et al., 2011), and may also enter villages in winter seeking shelter, finding refuge under pile dwellings. Arctic foxes are commonly seen feeding at dumpsters in human settlements associated with oilfields in the Arctic (see Plate 22), especially during the winter when food is in short supply (Garrott et al., 1983; Pamperin et al., 2006). Furthermore, oilfields appear to have a strong effect on the winter movements of arctic foxes, which forage close to oilfields in northern Alaska, thus increasing the potential for contacts between humans, domestic animals, and foxes (Eberhardt et al., 1983; Pamperin, 2008). Beyond such peri-domestic contacts, the primary interaction between foxes and people is in the context of fur trapping. Indigenous peoples have always used the exceptional fur of the arctic fox and with the advent of the fur industry, foxes quickly became an important source of

Epidemiology of Fox Rabies in the Arctic Host Species and Potential Reservoirs The arctic fox is the primary reservoir of the rabies virus in the Arctic. In addition to the arctic fox, rabies from the arctic variant has been documented in numerous wildlife species throughout the arctic and subarctic regions: red fox, wolf (Canis lupus), ringed seal (Pusa hispida), polar bear (Ursus maritimus), reindeer (Rangifer tarandus), raccoon dog, and skunk (Mephitis mephitis) (Rausch, 1958; Odegaard & Krogsrud, 1981; Ritter, 1981; Loewen et  al., 1990; Taylor et al., 1991; Mork & Prestrud, 2004; MacDonald et al., 2011). In domestic animals, rabies caused by the arctic variant is frequently reported in dogs (Canis familiaris) and is occasionally detected in sheep (Ovis aries) in the south (Sikes, 1968; Leisner, 2002; Mansfield et al., 2006; Nadin-Davis et  al., 2008). Rabies in marine mammals is considered rare, with only a few cases reported in seals (Odegaard & Krogsrud, 1981; Mork & Prestrud, 2004). Interestingly, in the north there is no evidence for the arctic fox variant being maintained in areas where arctic foxes are absent, despite occasional outbreaks in red foxes in such areas (Rausch, 1958). However, it is clear that the variant can occasionally spread southwards. In Ontario, following sporadic invasions of the arctic fox rabies virus variant from northern to southern regions, red foxes have efficiently transmitted and maintained the virus in the absence of arctic foxes, acting as another potential reservoir for this rabies virus (Rosatte, 1988; see Chapter 10). Skunks may also play an important role as a reservoir in some areas, such as southern Ontario (MacInnes et  al., 2001; Nadin-Davis et al., 2006; Rosatte et al., 2007). Spillover of rabies virus from the arctic fox to other species is most likely to occur during epizootic periods when the virus circulates at a high level in the fox population (Gordon et  al., 2004). In particular, the virus may spread within the carnivore community and at a higher

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frequency among species sharing the same ecological niche. Wolves, which can live in close proximity to arctic foxes (­Hendrickson et al., 2005), are more likely to become infected during epizootic events in populations of arctic foxes (Chapman, 1978; Weiler et al., 1995). As mentioned previously, arctic and red foxes compete for a similar niche, likely leading to frequent aggressive interactions, including territorial fighting and predation (Pamperin et  al., 2006), that may increase the chances of transmission of the rabies virus between the two species. Furthermore, the genetic similarity of rabies virus isolates from arctic and red foxes suggests that the rabies virus is easily transmitted between these species and widely dispersed over their combined large ranges (Nadin-Davis et al., 2012). The complex reservoir system maintaining rabies in wildlife creates additional challenges for appropriately directing pathogen control ­efforts (Rosatte et al., 2007; Singer & Smith, 2012).

in the Arctic include the small human population, protective garments worn in the cold climate, and general awareness of the clinical signs of the disease in animals (rabid animals are readily recognized and killed by inhabitants of northern communities) (see Chapter 14d). However, underreporting because of lack of rabies diagnostic facilities cannot be excluded (Secord et al., 1980; Mork & Prestrud, 2004). Lower human virulence of the Arctic strain relative to other rabies strains has also been suggested, based on rabies serum neutralizing antibody in unvaccinated Canadian Inuit and Alaskan trappers (Orr et al., 1988; Follmann et al., 1994; Kuzmin et al., 2008), but this hypothesis needs further testing (see Chapter 14b). Human exposure to the rabies virus occurs most often through bites from rabid animals (wildlife and domestic) but could potentially occur when hunters and trappers handle infected carcasses (Follmann et  al., 1994). In Alaska and Russia, several attacks of rabid wolves against humans have been reported (Rausch, 1958; Secord, et  al., 1980; Kuzmin, 1999). Their bites are often multiple, deep, and located in the head; rabid wolves may therefore pose a particularly high risk for human exposure to rabies (Mork & Prestrud, 2004). However, the most common exposure for people is through contact with domestic dogs, which may become infected following attacks by rabid foxes and wolves or consumption of carcasses of rabid animals (Rausch, 1972; Tabel et al., 1974). Human and domestic animal exposures to the Arctic rabies virus variant are not limited to the enzootic Arctic areas. For instance, exposure of people and dogs from Svalbard is likely due to repeated introduction of virus following migration of arctic foxes over sea ice (MacDonald et al., 2011; Mork et al., 2011; Orpetveit et al., 2011). A major ongoing concern is the potential exposure of humans and domestic animals in highly populated southern regions to the Arctic rabies virus. Indeed, there are several examples of southward spread of rabies from the Arctic, particularly in Canada, where multiple incursions have been documented over the past century, creating major challenges for human and animal health (Tabel et  al., 1974; Nadin-Davis et  al., 2006; Nadin-Davis et al., 2008; Mork et al., 2011). As mentioned earlier, the incursion of the arctic rabies virus variant in southern Ontario from the Arctic during the 1950s was followed by its establishment in red fox populations (Rosatte, 1988; see Chapter 10). The rabies virus periodically has invaded other provinces and territories, but without sustained circulation (MacInnes et al., 2001; Mansfield et al., 2006; Nadin-Davis et al., 2008). The wide distribution of red foxes and their spatial overlap with a­ rctic foxes create an ongoing threat of incursion of the arctic rabies strain

Prevalence of Rabies in the North Relatively few studies measuring rabies prevalence in arctic fox populations have been published, and these rely on estimates from trapped foxes (see Chapters 14b and c). From the paucity of available data it appears that the prevalence of rabies varies between different local fox populations and is considerably higher during an epizootic (9%–75%) than in years when no epizootic was observed (0.3%–3%) (Prestrud, et al. 1992; Ballard et al. 2001; Mork et al. 2011). The majority of epidemiological data come from passive surveillance systems, which ignore the vast areas of the Arctic with no or only extremely limited human populations available to detect and submit specimens, especially areas far from the coast. Furthermore, in such systems testing is generally limited to animals with suspected rabies that have potentially exposed humans or domestic animals. Thus, the cases diagnosed through these systems very likely represent a greater underestimation of the frequency of rabies cases in wildlife, with an elevated prevalence of rabies compared to the wild population, but peaks in the number of reported cases continue to provide a valuable signal of the occurrence of rabies epizootics.

Exposure of Humans and Domestic Animals Very few human rabies deaths have ever been reported in the Arctic (see Chapter 37). They include a case in Greenland in 1960 secondary to a dog bite, and six cases in the Russian Arctic, including one caused by a bite from an arctic fox and another from a wolf (Mork & Prestrud, 2004). Possible explanations for this low number of human cases

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into more temperate regions, followed by the long-term local maintenance of the strain and potential adaptation to other host species, such as skunks. Therefore a better understanding of the ability of the red fox to serve as a longterm reservoir host for this strain is crucial in estimating and managing this threat to public health (Nadin-Davis et al., 2012).

the Arctic rabies variant that suggest the disease spread by the migration of arctic foxes across the sea ice from Russia to Svalbard, and from North America to Greenland (Mansfield et al., 2006; Mork et al., 2011). The potential for seasonal variation of contact rates within arctic fox populations is largely unknown, and information derived from the literature is mainly speculative. At the onset of the mating season (March), the contact rates likely increase as foxes move extensively and actively defend their territories against intruders (Audet et al., 2002; Mork & Prestrud, 2004; Tarroux et  al., 2010). After cubs are born (May–June), breeding foxes travel less and remain close to their dens but continue to actively defend their territories. In the spring and summer, young foxes remain near their dens. During fall dispersal of the young of the year (August– November) contact rates are expected to increase (Rausch, 1972; Mork & Prestrud, 2004; Kim et al., 2014). Similarly, during winter (December–February), when arctic foxes increase their home range to forage, contact rates between individuals could also increase (Frafjord & Prestrud, 1992). In particular, during scavenging when foxes congregate at food sources, increasing contact rates and aggressive interactions may facilitate disease transmission (Rausch, 1958; Follmann et al., 1988). A plausible pattern of seasonal variation in rabies transmission is as follows: because of the high population density of susceptible foxes in the fall, the virus spreads rapidly during this period (especially following a decline in lemming populations); the number of infected individuals continues to increase throughout the winter because of contact during foraging until the onset of mating in late winter; at that time the increased prevalence and high contact rate leads to a peak in viral transmission followed by disease (Rausch, 1972; Mork & Prestrud, 2004). Seasonal variation in the number of reported rabies cases is broadly consistent with the above mechanisms modulating contact rates. Most rabid foxes are reported in November through March, coincident with the increased movement during fall dispersal and winter foraging when food is scarce, with the majority of cases reported in late winter and early spring (Aenishaenslin et al., 2014; Kantorovich, 1964; Ritter, 1981; Leisner, 2002; Kim et al., 2014). However, given that trapping activities occur during winter, an alternative explanation could be that suspect animals are more easily seen, captured, and sent for analysis by trappers in winter, leading to a detection bias for rabid animals during this period. Thus, until more detailed knowledge about seasonal changes in contact rates and rabies transmission among arctic foxes is obtained, hypotheses regarding the seasonal variation in rabies transmission remain highly speculative.

Contact Rates and Transmission of Arctic Rabies Virus Since rabies virus transmission generally requires physical contact between individuals, spatial and temporal variations in contact rates have a strong influence on the probability of rabies occurrence and spread (White et al., 1995). Although such contacts are required for transmission, latent and infectious periods can vary in duration and not all contacts with an infected individual result in a transmission event. Contact rates within an arctic fox population may depend on population density, home range size and overlap, and movements, all of which are influenced by the fluctuating availability of food resources in the Arctic. The contact rate between arctic foxes and other susceptible species, especially red foxes and wolves, is also mainly related to population densities, overlap between home ranges, and habitat use of each species (Hendrickson et al., 2005; Holmala & Kauhala, 2006; Kauhala & Holmala, 2006). Previous research points towards a connection between high population densities of arctic foxes and rabies epizootics (Elton, 1931; Chapman, 1978; Ritter, 1981; Prestrud et al., 1992), but this hypothesis has never been tested empirically, and epizootics have also been reported when fox population densities are low (Rausch, 1958). A possible relationship between lack of food, greater fox dispersal movements, and the start of epizootics was suggested based on observations in Russia (Audet et al., 2002). In inland foxes, because of their extreme population fluctuations linked to the lemming cycle and their tendency to disperse during periods of food scarcity, the spatio-temporal dynamics of rabies infection may well be influenced by resource-driven pulses of dispersal in high-density populations of starving foxes. Indeed, rabies dynamics seem to track population fluctuations in Alaska, with cyclic occurrence of rabies epizootics every three to four years (Ritter, 1981; Kim et al., 2014). For coastal foxes, the episodic nature of epizootics could be the result of occasional introduction of rabies by migrant inland foxes, as suggested by epidemiological data from Greenland and Svalbard (Mansfield et al., 2006; Mork et al., 2011; Norén et al., 2011; Raundrup et al., 2015). The role of migrants in sparking rabies outbreaks is also supported by genetic studies of

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the population density is much lower than that required in red foxes to maintain rabies, reaching only 0.3 fox per km2 ­(Angerbjörn et al., 1999; Legagneux et al., 2012). Several hypotheses have been proposed to explain the maintenance of the rabies virus under the conditions of exceptionally low host density found in the Arctic. Long incubation periods (as long as six months) could delay the onset of symptoms, slowing epidemic spread and allowing infected foxes to spread the virus over considerable distances and among regional fox populations (Rausch, 1958; Mork & Prestrud, 2004), which could play an important role in rabies persistence when host densities are low. In the red fox the rabies virus (European variant) may be excreted in saliva as early as one month before development of clinical signs (Aubert, 1992), but no comparable information exists for arctic foxes. Scavenging of infected fox carcasses is another potential mechanism for rabies virus to persist (Tabel et  al., 1974; Ballard et al., 2001; Gildehaus, 2010). Scavenging of arctic fox carcasses by other foxes is quite common (see the section on rabies resurgence in Chapter 14d), and cold temperature may help preserve the virus, which is present in organ tissues of naturally and experimentally infected arctic foxes (Secord et al., 1980; Gildehaus, 2010). In addition, aggregation around scavenged carcasses during periods of food scarcity may favour contact between foxes that would not otherwise occur in a very low-density population, increasing virus persistence by creating focal points for rabies transmission. Human settlements likely play a similar role by providing artificial and concentrated sources of food. Finally, the presence of other carnivore species such as the red fox could explain the enzootic situation of the rabies virus in some Arctic regions. The pooled density of red and arctic foxes may be high enough to allow rabies epizootics, as is the case for raccoon dogs and red foxes in northern Europe (Holmala & Kauhala, 2006), and the presence of red foxes and other carnivores may help ensure a baseline density of susceptible hosts that allows rabies transmission to continue even when arctic fox populations crash.

Host-Virus Interactions and Pathogenicity Current knowledge about the pathogenicity of Arctic rabies virus comes from a few experimental infection studies (Mork & Prestrud, 2004; Gildehaus, 2010). These revealed high variation in the incubation period (eight days to six months) and a short symptomatic period with rabid foxes dying within two days of the onset of symptoms. Rabies antibodies have been found in arctic foxes in Alaska without detection of the virus, suggesting that some foxes survive the infection or can carry the virus for a long time (Ballard et al., 2001). Furthermore, some experimentally infected foxes failed to develop clinical disease, suggesting a relatively long incubation period or a high innate resistance to infection by the Arctic rabies virus variant (Follmann et al., 2004; Follmann et al., 2011). However, at the time when these studies were terminated, it was not possible to determine whether the animals had already passed through the latent period to become infectious but not yet symptomatic. Secord et al. (1980) found the presence of rabies virus in the brain of apparently healthy trapped foxes, suggesting they were likely in the incubation period or prodromal stage of disease. Symptomatic rabid arctic foxes lose their shyness, may follow dog teams, and are more likely to enter human settlements (Mork & Prestrud, 2004), behaviours that facilitate virus transfer to domestic dogs (Leisner, 2002). However, it is not clear whether tameness towards humans is connected to rabies, as healthy arctic foxes are known to be fearless towards humans in Fennoscandia (Holmala & Kauhala, 2006). Rabid arctic foxes can also display ferocious behaviour: they may snap and bite or run in circles (Ballard et al., 2001; Mork & Prestrud, 2004; Orpetveit et al., 2011). Both furious and dumb rabies have been described in the arctic fox (Mork & Prestrud, 2004). The role of variability in rabies-induced behaviour in driving transmission dynamics is currently unknown.

Spread and Persistence of Rabies in the North In theory rabies infection is more likely to be transmitted at higher susceptible host densities, but it is currently unclear what role densities of foxes play in the persistence of rabies in the Arctic. In Europe, models suggested that a threshold density of 1.0 red fox per km2 was necessary to allow an epizootic to occur (Anderson et al., 1981), yet arctic fox rabies spread through the population of red foxes in southern Canada, where fox densities were less than 1.0 per km2 (MacInnes et al., 2001). Even at the highest reproductive rates of arctic foxes, which occur exclusively in the peak phase of the lemming cycle in inland populations,

Potential Impacts of Climate Change and Northern Development on Arctic Rabies Ecology The Arctic has experienced a significant warming trend over the past 30 years at about twice the rate of lower latitudes, and its land, freshwater, and marine ecosystems are already changing in response to increased temperatures (Intergovernmental Panel on Climate Change [IPCC], 2007; Blunden

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et al., 2011). In addition to climate warming, Arctic ecosystems face increasing perturbations from a variety of anthropogenic activities in the north, such as increased shipping activity, resource development, and increased human populations (Mallory et  al., 2006; Ferguson et  al., 2012). Such changes have important repercussions on spatial and temporal characteristics of host habitat use, population densities, home ranges, predator-prey relationships, and competition among sympatric species. All these factors are expected to modify the transmission dynamics of zoonotic agents such as rabies virus (Kim et al., 2014). Although the impact of climate warming on the current ecology and epidemiology of rabies in the Arctic has yet to be documented (Hueffer et al., 2011), this section summarizes several predicted effects of climate warming on arctic fox ecology caused by fading rodent cycles, shrinking Arctic habitats (e.g., sea ice for winter foraging), and red fox expansion (Geffen et al., 2007; Fuglei & Ims, 2008; Ferguson et al., 2012; Schmidt et al., 2012).

decades, the ice connection between the islands of the Arctic Ocean and the continent will no longer exist, and these islands could become the last refuge for arctic wildlife and native flora, protecting them from invasive species from the south (Fuglei & Ims, 2008). Kim et al. (2014) reported a positive correlation between sea ice extent and number of rabies cases. This correlation could be due to sea ice facilitating the long range movement of arctic foxes and thereby increasing disease spread (Kim et al., 2014). Thus, sea ice loss and the increased isolation of some arctic fox populations would presumably lead to decreased opportunity for rabies transmission between populations. In this context climate warming is likely to have a greater effect on the dynamics of rabies in arctic fox populations than in red fox populations whose ecology is less tied to sea ice. Given that both seals and polar bears are vulnerable to sea ice loss, marine food becomes less available for arctic foxes as sea ice cover decreases (Kim et al., 2014). Especially when inland food sources are scarce, this lack of availability in marine resources may decrease the survival of arctic fox populations relying on it (Roth, 2003; Kim et al., 2014). However, the example of maintaining a large population of arctic foxes in Iceland, a completely ice-free island, seems to show that the absence of ice is not an insurmountable barrier to the maintenance of this species (Fuglei & Ims, 2008). However, as arctic foxes adjust to the decreasing availability of sea ice, the resulting changes in population distribution and abundance, as well as large foraging movements to counter food scarcity, are likely to substantially alter the spatio-temporal dynamics of rabies in the Arctic.

Climate Warming and Lemming Populations Lemming populations appear to be highly sensitive to climate warming, with cycles dependent on the stability and duration of cold winter temperatures (Fuglei & Ims, 2008). In fact, lemmings are highly dependent on snow cover for shelter, protection against cold temperatures, and access to food resources. Milder winters and earlier spring snowmelt weaken the snowpack in the north, drowning lemmings and exposing them to predators earlier in the year. In the short term, these deaths, resulting in an increase in carcasses, should benefit the arctic foxes. However, in the medium term, the decline in lemming populations in North America will likely reduce overall reproductive rates and population size of arctic foxes. This was observed for arctic foxes on the Scandinavia peninsula (Kausrud et al., 2008; Schmidt et al., 2012), where the absence of peaks in lemming abundance between 1985 and 2000 was associated with a steep decline in populations of arctic foxes (Fuglei & Ims, 2008). In the long term, provided arctic foxes can adapt to other ecological changes associated with climate warming, a warmer climate should increase plant biomass and therefore lead in theory to an increase in the abundance and variety of rodent prey available for foxes (Fuglei & Ims, 2008).

Northern Development and Red Fox Range Expansion Globally, the range of the red fox (Chapter 26a) has shifted northward over the course of the last century, with increasing overlap in distribution with the arctic fox (Ovsyanikov & Menyushina, 1987; Hersteinsson & Macdonald, 1992; Tannerfeldt et  al., 2002; Gagnon & Berteaux, 2009; Gallant et al., 2012). This range shift has been attributed to global warming, but this link is questioned by some authors and has not been clearly demonstrated (Hersteinsson & Macdonald, 1992; Gallant et al., 2012). Another explanation, in addition to possible effects of climate change, may be increased human presence in the north (Gallant et al., 2012). By creating artificial feeding grounds for foxes, human settlements may impact local arctic and red fox densities, contact rates among foxes, and contact between foxes and domestic dogs or humans. Several studies suggest that an increase in food supply in developed areas, such as oilfields,

Climate Warming and Decreased Sea Ice Extent For several years, there has been a significant decrease in sea ice in the Arctic (about 3% decrease per decade for 30 years) (IPCC, 2007). If this trend continues, within a few

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may have stabilized or increased arctic fox densities, leading to concerns about increased contact rates with human and domestic animals (reviewed in Ballard et al., 2001). Intensive northern development, favouring the concentration of humans and domestic animals in villages, could then particularly increase the risk of human exposure to rabies. In particular, anthropogenic food subsidies may be monopolized by red foxes at the expense of arctic foxes, thereby favouring the northward expansion of red foxes in the regions with considerable human activities (Gallant et  al., 2012). The ecology of rabies could be substantially altered by the invading red fox population, potentially resulting in increasing human exposure to rabies, or, on the contrary, resulting in a massively reduced rate of rabies in southern portions of the Arctic as red foxes extirpate arctic foxes from their expanding range but do not, themselves, provide a competent reservoir population for rabies maintenance. These potential links again emphasize the need to have a better understanding of the ability of the red fox to serve as a long-term reservoir host for the Arctic rabies virus variant.

rabies transmission events (e.g., the movement behaviour of arctic foxes, aggregation around carcasses, interactions with red foxes, and the northward range expansion of red foxes); (2) characteristics of the Arctic rabies variant that influence transmission and persistence (e.g., the role of variant-induced behaviour, length of infectious and asymptomatic states, and resistance to infection); and (3) the impact of climate warming and northern development on rabies dynamics. In addition to investigating these gaps, future work in this area could include developing tools for understanding and predicting the dynamics of rabies in a changing Arctic ecosystem and new management options for rabies in northern regions. Predicting shifts in outbreak frequency under climate change and the intensity and geographic extent of rabies virus exposure risk for dogs and humans during outbreaks would be valuable for public health, and could be informed by a modelling approach (see Chapters 10 and 11). Although arctic rabies in red foxes has been successfully controlled by wildlife vaccination within limited areas in the south, management presents distinct challenges in Arctic regions, given the potential size of control areas coupled with a sparse and mobile population of arctic foxes, limitations in surveillance, and possible inefficiency of oral vaccines under Arctic conditions (MacInnes et al., 2001; Mork & Prestrud, 2004; Holmala & Kauhala, 2006; Mansfield et al., 2006; Rosatte, 2011). Lyophilized oral vaccines have been shown to produce adequate immunity of arctic foxes in captivity and provide a promising alternative to liquid oral vaccines under frozen conditions, but the efficacy of these vaccines has yet to be demonstrated in the field (Follmann et al., 2004).

Discussion: Important Gaps and Research Needs Rabies ecology in the Arctic is not well understood. Current knowledge has important gaps about the epidemiology of rabies in the Arctic and the main information needed to gain a better understanding of the consequences of current environmental changes for rabies dynamics in northern ecosystems. These gaps include (1) aspects of host ecology that influence the frequency and spatial distribution of

Acknowledgments This chapter was written as part of an ongoing study on the ecology of rabies in northern Quebec. The authors want to thank the Government of Quebec for funding.

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Ecology of Rabies in the Arctic Fox (Vulpes lagopus) Rausch, R. L. (1972). Observations on some natural-focal zoonoses in Alaska. Archives of Environmental Health, 25(4), 246–252. https:// doi.org/10.1080/00039896.1972.10666170 Ritter, D. (1981). Rabies. In R. A. Dieterich (Ed.), Alaskan Wildlife Diseases (pp. 6–12). Fairbanks, AK: University of Alaska. Rodnikova, A., Ims, R. A., Sokolov, A., Skogstad, G., Sokolov, V., Shtro, V., & Fuglei, E. (2011). Red fox takeover of arctic fox breeding den: an observation from Yamal Peninsula, Russia. Polar Biology, 34(10), 1609–1614. https://doi.org/10.1007/s00300-011-0987-0 Rosatte, R. (2011). Evolution of wildlife rabies control tactics. Advances in Virus Research, 79, 397–419. https://doi.org/10.1016 /B978-0-12-387040-7.00019-6 Rosatte, R. C. (1988). Rabies in Canada – History, epidemiology and control. The Canadian Veterinary Journal, 29(4), 362–365. Rosatte, R. C., Power, M. J., Donovan, D., Davies, J. C., Bachmann, P., & Muldoon, F.C. (2007). Elimination of arctic variant rabies in red foxes, metropolitan Toronto. Emerging Infectious Diseases, 13(1), 25–27. Roth, J. D. (2003). Variability in marine resources affects arctic fox population dynamics. Journal of Animal Ecology, 72(4), 668–676. https://doi.org/10.1046/j.1365-2656.2003.00739.x Schmidt, N. M., Ims, R. A., Hoye, T. T., Gilg, O., Hansen, L., Hansen, J., ... Sittler, B. (2012). Response of an arctic predator guild to ­collapsing lemming cycles. Proceedings of the Royal Society Biological Sciences Series B, 279(1746), 4417–4422. Secord, D. C., Bradley, J. A., Eaton, R. D., & Mitchell, D. (1980). Prevalence of rabies virus in foxes trapped in the Canadian Arctic. The Canadian Veterinary Journal, 21(11), 297–300. Retrieved from https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1789818/ Sikes, R. K. (1968). Arctic rabies. Archives of Environmental Health, 17(4), 622–626. https://doi.org/10.1080/00039896.1968.10665292 Singer, A., & Smith, G. C. (2012). Emergency rabies control in a community of two high-density hosts. BMC Veterinary Research, 8, 79. https://doi.org/10.1186/1746-6148-8-79 Smith, T. G. (1976). Predation of ringed seal pups (Phoca hispida) by the arctic fox (Alopex lagopus). Canadian Journal of Zoology, 54(10), 1610–1616. https://doi.org/10.1139/z76-188 Tabel, H., Corner, A. H., Webster, W. A., & Casey, C. A. (1974). History and epizootiology of rabies in Canada. The Canadian Veterinary Journal, 15(10), 271–281.Retrieved from https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1696688/ Tannerfeldt, M., & Angerbjörn, A. (1998). Fluctuating resources and the evolution of litter size in the arctic fox. Oikos, 83(3), 545–559. https://doi.org/10.2307/3546681 Tannerfeldt, M., Elmhagen, B., & Angerbjörn, A. (2002). Exclusion by interference competition? The relationship between red and ­arctic foxes. Oecologia (Berlin), 132(2), 213–220. https://doi.org/10.1007/s00442-002-0967-8 Tannerfeldt, M., Moehrenschlager, A., & Angerbjörn, A. (2003). Den ecology of swift, kit and arctic foxes: A review. In M. Sovada & L. Carbyn (Eds.), The swift fox: Ecology and conservation of swift foxes in a changing world (pp. 167–181). Regina, SK: University of Regina Press. Tarroux, A., Berteaux, D., & Bety, J. (2010). Northern nomads: Ability for extensive movements in adult arctic foxes. Polar Biology, 33(8), 1021–1026. https://doi.org/10.1007/s00300-010-0780-5 Tarroux, A., Bety, J., Gauthier, G., & Berteaux, D. (2012). The marine side of a terrestrial carnivore: Intra-population variation in use of allochthonous resources by arctic foxes. PLoS One, 7(8). https://doi.org/10.1371/journal.pone.0042427 Taylor, M., Elkin, B., Maier, N., & Bradley, M. (1991). Observation of a polar bear with rabies. Journal of Wildlife Diseases, 27(2), 337–339. https://doi.org/10.7589/0090-3558-27.2.337 Weiler, G. J., Garner, G. W., & Ritter, D. G. (1995). Occurrence of rabies in a wolf population in northeastern Alaska. Journal of Wildlife Diseases, 31(1), 79–82. https://doi.org/10.7589/0090-3558-31.1.79 White, P. C. L., Harris, S., & Smith, G. C. (1995). Fox contact behaviour and rabies spread: A model for the estimation of contact probabilities between urban foxes at different population densities and its implications for rabies control in Britain. Journal of Applied Ecology, 32(4), 693–706. https://doi.org/10.2307/2404809 Williams, R. B. (1949). Rabies in Alaska. Canadian Journal of Comparative Medicine and Veterinary Science, 13(6), 136–143. Retrieved from https://www.ncbi.nlm.nih.gov/pmc/issues/137408/ Wrigley, R. E., & Hatch, D. R. M. (1976). Arctic fox migrations in Manitoba Canada. Arctic, 29(3), 147–158. https://doi.org/10.14430 /arctic2798

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27 Bat Rabies in Canada M. Brock Fenton,1 Alan C. Jackson,2 and Paul A. Faure3 1

Department of Biology, University of Western Ontario, London, Canada Department of Internal Medicine (Neurology), University of Manitoba, Winnipeg, Canada 3 Department of Psychology, Neuroscience, & Behaviour, McMaster University, Hamilton, Ontario, Canada 2

Introduction Anything that promotes a positive image of bats is a good thing. – Brock Fenton

Rabies is one of the oldest and most feared diseases. Fortunately, it is also one of the rarest human diseases in Canada (see Chapter 3b). Reports of human fatalities in Canada caused by rabies virus infection date back to at least the early nineteenth century and include the governor-in-chief of British North America, the fourth Duke of Richmond, who died of rabies in 1819 (Tabel et al., 1974; Jackson, 1994; see Chapter 3a). Since 1924 the Public Health Agency of Canada has recorded 26 human fatalities caused by rabies, with cases in Quebec (12), Ontario (7), Saskatchewan (2), Alberta (2), Nova Scotia (1), and British Columbia (2) (Varughese, 1987; Johnstone et  al., 2008; Jackson, 2011b; Chapter 3b). Worldwide, the majority of human deaths from rabies are caused by canine rabies virus variants, which cause 59,000 deaths annually (Hampson et al., 2015). In Canada and the United States, most recent human fatalities from rabies have resulted largely through contact with wildlife – mainly bats. Since 1970 seven of the last nine (78%) human cases of rabies in Canada originated from bats, including all the indigenously acquired cases (Table 27.1; see also Chapter 3b and Chapter 29). In Canada and the United States from 1950 to 2009, 60 indigenously acquired human fatalities were caused by bat rabies virus variants. One-third of these cases involved no history of exposure to bats, and 28%

had no direct contact with bats (De Serres et  al., 2008; Jackson, 2011a). All mammals are susceptible to rabies virus infection, and bats are no exception (Rupprecht et al., 2002). Bat rabies is known throughout Canada in all areas where bats occur, except in the northern territories, where bat submissions to the Canadian Food Inspection Agency (CFIA) have not yet tested positive for rabies (see Chapters 2, 14a, 14b, 14c, 14d). In Canada, population densities and diversity of both bats and humans are highest within 300 kilometres of the US border. This influences our perception of rabies in bats. Although the proportion of bats naturally infected with rabies virus has probably changed little over time, public awareness and fear of bat rabies has increased, leading to increased numbers of suspect animals submitted for laboratory testing (Constantine, 1967; Baer & Adams, 1970; Bradley, 1979; Rosatte, 1987). In reality, the incidence of rabies in bats in Canada is very low (e.g., Klug et al., 2011). Rabies in bats has a long history, and it seems likely that rabies virus has been present in North American bats long before it was first isolated from a lactating female Florida yellow bat (Lasiurus (Dasypterus) floridanus) in 1953 (Venters et al., 1954). The first confirmed case of bat rabies in Canada was from a big brown bat (Eptesicus fuscus) near Vancouver, British Columbia in 1957 (Avery & Tailyour, 1960). The possibility that migratory bats might transfer rabies into Canada from the United States had been suggested a few years earlier (“Possibility of Bats,” 1954). Ontario was the next province to report bat rabies in 1961 (Beauregard & Stewart, 1964), followed by Manitoba in 1965, Quebec in 1968, Saskatchewan in 1970 and Alberta in 1971 (Dorward et  al., 1977). Since

Bat Rabies in Canada

Table 27.1  Fatal human cases of rabies in Canada, 1970 to 2019, showing the year of fatality, age and sex of the patient, the province where the death occurred, the disease transmitting organism (vector), and the strain of rabies virus (variant) isolated from each patient, if known. Patient Year

Age/Sex

Province

Vector/Virus Variant

References

1970

15/male

Saskatchewan

bat/?

Dempster et al., 1972

1977

63/male

Nova Scotia

bat/?

King et al., 1978

1984 1985

43/male 22/male

Quebec Alberta

dog (Dominican Republic)/? bat/?

2000

9/male

Quebec

bat/variant associated with silver-haired bat

2003

52/male

British Columbia

bat/variant associated with Myotis bat

2007

73/male

Alberta

bat/variant associated with silver-haired bat

2012

41/male

Ontario

2019

21/male

British Columbia

dog (Dominican Republic)/Haitian canine rabies virus variant bat/variant associated with silver-haired bat

Picard, 1984; Webster et al., 1985 Dolman & Charlton, 1987; Webster et al., 1987 Despond et al., 2002; Elmgren et al., 2002; Turgeon et al., 2000 Parker et al., 2003; Walker et al., 2016 Johnstone et al., 2008; McDermid et al., 2008 Dyer et al., 2013; Wilcox et al., 2014 Brown, July 16, 2019; K. Knowles, personal communication, October 2019

Source: Adapted from Jackson (2011b) in Canadian Journal of Neurological Sciences, 38, 689–695. With permission. Table 27.2  Reported rabies incidence in bats by province, 1957 to 2017. Provinces in this table are ordered west to east across Canada. Period 1957–1959 1960–1969 1970–1979 1980–1989 1990–1999 2000–2009 2010–2017  Totals   % Total

Total

BC

AB

SK

MB

0 82 403 566 499 859 446

3 22 73 92 98 139 75

0 0 137 68 52 27 32

0 0 34 52 60 43 71

0 3 2 2 12 11 6

2855  

502 17.6

316 11.1

260 9.1

36 1.3

ON

QC

NB

NS

PE

NL

0 56 150 339 246 526 185

0 1 7 10 25 103 64

0 0 0 1 5 6 11

0 0 0 2 1 2 2

0 0 0 0 0 1 0

0 0 0 0 0 1 0

1502 52.6

210 7.4

23 0.8

7 0.2

1 0.0

1 0.0

Source: compiled from CFIA data.

then, those provinces have accounted for 99% of all positive rabies cases in bats in Canada. The Atlantic provinces account for the remaining 1% of cases. By the end of 2017 no cases have been reported in Canada’s northern territories (Table 27.2). Between 1970 and 1999 the incidence of rabies in bats averaged just less than 50 cases per year. Until 1970 bats accounted for less than 1% of confirmed cases of rabies. Until the mid-1990s this value grew slowly to average about 2.6% of all cases. Since then, the relative contribution of bats to rabies incidence has averaged around 30% of all cases annually (Figure 27.1). This shift

is primarily due to the dramatic drop in incidence of rabies in terrestrial wildlife in Ontario (see Chapter 10). This change reflects the introduction of wildlife rabies control programs beginning in 1989. Nevertheless, these statistics suggest that bats play an important role in the epidemiology of rabies in Canada, at least in areas below the tree-line where humans more frequently encounter bats. This chapter discusses bat rabies in Canada from three perspectives: first, in relation to our knowledge of the biology and ecology of bats; second, in the context of the biology of the rabies virus; and third, in the context of

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Ecology and Epizootiology of Wildlife Rabies

Figure 27.1: Incidence in bats by year by annual total and by percentage of all rabies cases. Source: created from CFIA data.

Vespertilionidae and Nyctinimops macrotis – Molossidae) have each been reported once (Van Zyll de Jong, 1985). Resident bats in Canada range in adult body mass from 4 grams to 35 grams, all are Vespertilionids, and all eat arthropods, mainly insects. These bats differ in their social structure and roosting habits (Table 27.3). The little brown bat and the big brown bat are the most common species in Canada. They are highly gregarious mammals that frequently roost in human-made structures, forming maternity colonies numbering in hundreds or thousands of individuals, and this undoubtedly increases the likelihood that they will encounter and interact with humans (Childs et al., 1994). Interestingly, although big brown bats are typically the most numerous species to be submitted (Table 27.4) for rabies testing by members of the public, the little brown bat, hoary bat (Lasiurus cinereus), and silver-haired bats (Lasionycteris noctivagans) are also frequently reported as rabies-positive from laboratory submissions in Canada (e.g., Dorward, 1977; Pybus, 1985; Schowalter, 1980; Prins & Loewen, 1991; and Table 27.4).

the impact of rabies virus on the behaviour of bats. Because bats have been implicated as natural reservoirs for a variety of zoonotic viruses, there has been considerable renewed interest in understanding the biology and ecology of bats and the mechanisms of pathogen maintenance in bat hosts (Calisher et al., 2006; Wong et al., 2007; George et al., 2011). Bats are among the smallest of mammals regularly afflicted with rabies. This is a mixed blessing when considering the fatal nature of the disease and the risk it poses to humans. The positive side is that their small size and secretive habits means that bats rarely come in contact with and bite people. The negative side is that it is easy to overlook a bat bite (Jackson & Fenton, 2001) and this can put a victim in jeopardy (Figure 27.2). It is imperative for people to avoid being bitten by bats and to take appropriate preventive measures after recognized exposures to bats. Biologists and others that regularly come into contact with and handle bats should have a rabies pre-exposure immunization series, have their antibody titres tested regularly, and obtain booster doses of vaccine as needed.

Hibernation

Bats in Canada

Canadian bats are heterothermic, sometimes allowing their body temperatures to track the ambient temperature, other times remaining homeothermic (warm-blooded) (Audet &

Nineteen species of bats regularly occur in Canada (Table 27.3) and two others (Nycticeius humeralis –

468

Bat Rabies in Canada

useful in determining their level of stress and vulnerability to rabies. Relatively little experimental work has been done on the influence of hibernation on the pathogenesis and maintenance of rabies virus in bats. The suprascapular brown adipose tissue of bats has a high metabolic capacity and is a key source of lipid energy for thermogenesis during arousal from hibernation (George & Eapen, 1959; Hayward & Ball, 1966). Rabies virus has been isolated from the brown fat of naturally infected bats (Bell & Moore, 1960; Sulkin et al., 1960a), and early studies suggested that brown fat might serve as a reservoir for the virus during hibernation (Sulkin et al., 1957, 1959; Sulkin, 1962). Hibernation is associated with very low levels of rabies virus replication, which results in suspension of the progression of the infection until body temperatures reach more normal (homeothermic) levels (Sadler & Enright, 1959; Sulkin et al., 1960b). In addition, reduced viral spread would be expected because of inhibitory effects of hypothermia on fast axonal transport (Bisby & Jones, 1978) and trans-synaptic spread.

Reproduction

Figure 27.2: (A) Small puncture wound (arrowhead) involving the right ring finger of a bat biologist caused by a defensive bite from a canine tooth of a silver-haired bat (Lasionycteris noctivagans) (scale bar = 10 mm). (B) Skull of a silver-haired bat (length = 17.1 mm) resting on a distal phalanx, which demonstrates the small size of the bat and its teeth. See Plate 23 for a photo of a silver-haired bat.

Canadian bats give birth to young once a year, usually in June or July. The litter size usually is one or two, although eastern red bats (Lasiurus borealis) may have three or even four pups in a litter (Table 27.3). Mating usually occurs in late summer or in autumn and females store sperm in the uterus over the winter. Females ovulate in spring when they leave hibernation, and fertilization and pregnancy ensue. The gestation periods are typically about 60 days, although this may vary with prevailing temperature conditions. Pregnant and lactating females of most Canadian species gather in nursery colonies, typically sites with high diurnal temperatures ensuring rapid growth of the young (before and after birth) and high milk production. Two foliage roosting species, eastern red bats and hoary bats, do not form nursery colonies and lead a more solitary existence. In these bats, the largest group will be a female and her dependent young or a mating pair. Mating appears to occur in the fall, but for most species there are no data. In spite of its wide distribution and the fact that the big brown bat often lives in houses or other buildings, we know very little about their mating system and behaviour. Vonhof et al. (2006) demonstrated with genetic data that two different males sired just over half of the twins born to female big brown bats, indicating that females frequently mate with more than one male. In little brown bats mating occurs in the fall and involves both

Source: Jackson and Fenton in Lancet 357:1714, 2001; Copyright Elsevier. With permission.

Fenton, 1988; Barclay et al., 2001; Willis & Brigham, 2003). Coping with winter and the seasonal absence of food is an extension of this thermoregulatory strategy resulting in a combination of migration and hibernation. Although bats that hibernate are generally considered to be inactive during winter, Lausen & Barclay (2006) used acoustic monitoring to demonstrate considerable bat activity throughout the winter at prairie sites in Alberta. These findings provide clear evidence that even in winter bats may be active and that some species (perhaps several) hibernate in cracks and crevices, not just in more extensive underground settings such as caves and mines. It remains to be determined how important winter hibernacula such as cracks and crevices are to bats in Canada. Brigham (1987) showed that big brown bats caught in buildings in winter were virtually without fat. Assessment of the body condition of bats (Pearce et al., 2008) could be

469

Ecology and Epizootiology of Wildlife Rabies

Table 27.3  Provincial distribution of bats showing social behaviour, roost use, and litter size.

Common Name

Scientific Name

Distribution by Province

Social Structure

Big brown bat

Eptesicus fuscus

BC, AB, SK, MB, ON, QC, NB

colonial

California myotis Tricoloured bat (previously Eastern pipistrelle) Eastern small-footed bat Evening bat Fringed myotis Big-eared free-tailed bat

Myotis californicus

BC

colonial

hollows and 1–2 crevices** hollows and crevices 1

Perimyotis subflavus

ON, QC, NB, NS

colonial

foliage*

2

colonial colonial colonial colonial

hollows and crevices* hollows hollows and crevices* hollows and crevices

1 2 1 1

solitary

foliage

2

colonial

hollows and crevices 1 hollows and 1 crevices** hollows and crevices 1 hollows and crevices* 1

Pallid bat Eastern red bat Western red bat Silver-haired bat Spotted bat Townsend’s big-eared bat Western long-eared bat Western small-footed bat

ON, QC ON (1 record, post-storm) BC BC (1 record, post-storm) BC, AB, SK, MB, ON, QC, NB, NS, Lasiurus cinereus PE, NL Myotis keenii BC BC, AB, SK, MB, ON, NS, PEI, NL, Myotis lucifugus YT, NT Myotis volans BC, AB BC, AB, SK, MB, ON, QC, NB, NS, Myotis septentrionalis PE, NL, YT, NT Antrozous pallidus BC Lasiurus borealis ON, QC, NB, NU, BC, AB, SK, MB Lasiurus blossevilli No records Lasionycteris noctivagans BC, AB, SK, MB, ON, QC, NB, NS Euderma maculatum BC Corynorhinus townsendii BC Myotis evotis BC, AB, SK Myotis ciliolabrum BC, AB

Yuma bat

Myotis yumanensis

colonial

Hoary bat Keen’s bat Little brown myotis Long-legged myotis Northern long-eared bat

Myotis leibii Nycticeius humeralis Myotis thysanodes Nyctinimops macrotis

BC

colonial colonial colonial colonial solitary solitary colonial solitary (?) colonial colonial colonial

Roost Type

hollows* foliage foliage hollows and crevices crevices hollows** hollows and crevices* hollows and crevices hollows and crevices**

Litter Size

2 2–4 2–4 1–3 1 1 1 1 1

*occasionally roosts in buildings; **commonly roosts in buildings Sources: Brock Fenton, Paul Faure, Robert Barclay, Mark Brigham, Craig Willis, Hugh Broders.

males and females mating with multiple partners (Barclay et al., 1979; Thomas et al., 1979; Waiping & Fenton, 1988).

et al., 2009, 2011) may allow us to better document the importance of food resources to the condition of bats. Lack of evidence of competition between bats (interspecific, intraspecific) has implications for bat-bat contact and the potential transmission of rabies. Bell (1980) documented how bat-bat interactions away from roosts could have influenced exposure to rabies. Within roost contacts between individuals are usually, but not necessarily, intraspecific. The relative lack of data about the behaviour of solitary species (which tend to be cryptic), combined with few details about migration, make it difficult to put information about rabies and bats in a broader context. Because solitary, tree-roosting bats typically roost away from human dwellings or places where they are easily observed, this could bias the number of bats submitted for testing and, consequently, estimates on the prevalence of rabies because only sick bats that are obviously behaving abnormally are likely to be encountered by humans (Klug et al., 2011).

Roosts Several species of bats often form nursery (summer) colonies in buildings (Table 27.3), increasing the likelihood of exposure to humans. Big brown bats are the only Canadian species that regularly overwinter in buildings, which influences their interactions with humans. Roosts occupied by pregnant and lactating females provide a thermal regime that promotes growth and, depending upon structure, varying degrees of protection from prevailing weather. A combination of protection from weather and dependence upon a dependable food resource (insects emerging from water) appeared to account for successful reproduction even during an inclement summer (Syme et al., 2001). Details about the specific insect prey consumed (Clare

470

Bat Rabies in Canada

exceed 100 individuals, and in some cases 1000. But our database about the movements of individually marked little brown bats is much less extensive than the one for big brown bats. We may not have enough information to accept or dismiss the notion of a fission-fusion society in other colonial bats. At this time it appears that L. borealis and L. cinereus are not colonial. We do not know the situation for Euderma maculatum, but other bats in Canada appear to at least form maternity colonies. Recent work with proximity tags reveals how interactions between female bats and their young influences roost use (Ripperger et  al., 2019). Such levels of interaction suggest more complex social structure than previously demonstrated.

Table 27.4  Submissions and rabies-positive (P) bats, 1985 to 2017 Common Name Big brown bat Little brown bat (myotis) Unspecified Silver-haired bat Yuma bat California myotis Northern long-eared bat Long-eared bat Keen’s bat hoary bat Eastern red bat Long-legged myotis Western small-footed bat Fruit bat Leaf-nosed bat Fruit bat Vampire bat Tricoloured bat (previously Eastern pipistrelle) Townsend’s big-eared bat Fringed myotis Fruit bat Pallid bat Western red bat Spotted bat  Totals

Total

N

P

U

26,472

24,747

9,209 1,438 1,388 596 586 537 435 298 272 151 81 56 46 22 17 9 8

9,064 1,367 1,241 571 558 530 396 287 210 136 78 52 46 22 17 9 5

110 51 137 22 22 7 36 10 59 13 3 4 0 0 0 0 3

35 20 10 3 6 0 3 1 3 2 0 0 0 0 0 0 0

1.2 3.5 9.9 3.7 3.8 1.3 8.3 3.4 21.7 8.6 3.7 7.1 0.0 0.0 0.0 0.0 37.5

8 6 5 5 2 1

7 3 5 5 2 0

1 3 0 0 0 1

0 0 0 0 0 0

12.5 50.0 0.0 0.0 0.0 100.0

2101 189

5.0

1,619 106

41,648 39,358

%P 6.1

Movements and Migrations We remain relatively ignorant about the migrations of bats – whether they travel alone or in groups – and if they use distinct flyways. Outside the relatively few band recoveries of little brown bats between summer and winter grounds (Davis & Hitchcock, 1965; Hitchcock, 1965; Fenton, 1969, 1970; Humphrey & Cope, 1976) and repeated observations on marked individuals at the same sites in summer, we lack information about the details of where bats that summer in Canada spend the winter. Isotopic analysis indicates north to south migrations of hoary bats (Cryan, 2003) and tricoloured bats (Fraser et al., 2012). The details of migratory behaviour of bats have remained relatively unchanged since 1970. McGuire et  al. (2011), however, showed that some silver-haired bats flew directly south across Lake Erie during fall migration, while others followed the north shore of Lake Erie and crossed into the United States in the Niagara area. Band recoveries indicate that big brown bats are relatively sedentary, travelling perhaps less than 75 kilometres between summer and winter areas. Five distinct strains of rabies virus have been reported from big brown bats (Nadin-Davis et al., 2010) and three according to Streicker et  al. (2010). Less sedentary species of bats in the United States tend to have fewer distinct strains of rabies (Streicker et al., 2010).

(N = negative, P = positive, U = undetermined). Source: compiled from CFIA data.

Social Structure There is increasing evidence that bats like the big brown bat form fission-fusion societies in which individuals roost with an extended group of roost mates. On any given day, the individuals comprising a colony in a day roost may differ from the composition of the day before or the group composition that will occur a week later. Individuals have a repertoire of roosts and roost mates. The benefits to individuals roosting in a group may be partly thermoregulatory (Willis & Brigham, 2007) and, in some cases, access to information about foraging sites and areas (Wilkinson, 1992). Fission-fusion societies may be composed of smaller unit colonies. Fission-fusion societies may explain more about bat-bat transmission of rabies than roost philopatry in big brown bats (Nadin-Davis et al., 2010). Little brown bats may form more stable social units, at least during the time when females are pregnant and then lactating. Nursery roosts of these bats in buildings often

Recent Advances in Our Knowledge of Bat Biology Advances in our knowledge of bats in Canada have occurred over the past 10 to 20 years. First, although it had been common to refer to silver-haired bats as a solitary

471

Ecology and Epizootiology of Wildlife Rabies

Impact of Rabies Virus Infection on Bat Behaviour

species living in trees (e.g., Barbour & Davis, 1969), it is now clear that females of this species form nursery colonies, typically in hollows in trees (Nagorsen & Brigham, 1993). Because silver-haired bats are migratory and are forced to locate new, temporary roosts frequently during their spring and fall migrations (e.g., Barclay et al., 1988), this may result in a higher probability of bats contacting humans and explain why the silver-haired bat virus variant is more often associated with human rabies fatalities. Second, while we had thought that tricoloured bats formed nursery colonies in hollows, we now know that they roost in groups in foliage (Veilleux et al., 2003) or in old man’s beard lichen (H. Broders, personal communication, 2003). These changes could have important implications for the epidemiology of rabies in bats in Canada. Knowing that the silver-haired bat is colonial and that tricoloured bats roost in foliage can influence our view of either species with respect to exposure to rabies.

Evolution by natural selection will favour rabies virus variants that cause robust changes in host behaviour which facilitate transmission of the virus from an infected host (eventually fatal) to an uninfected host. Thus, the rabies virus has adapted for virus-mediated changes in host behaviour. Bats are not vicious creatures. For example, a bat flying with its mouth open is emitting echolocation calls (Plate 24). In flying bats, unlike many other mammals, an open mouth display is not aggressive or hostile. Normally, bats remain hidden by day perhaps to avoid predators. Bats that have been disturbed may feel threatened and attempt to bite in self-defence. This is normal behaviour and is not symptomatic of rabies. There are, however, credible reports of unprovoked attacks by rabid bats on humans, their pets or other animals, and on inanimate objects. In this case, bats that attack are cause for concern and should be considered suspect for rabies (Venters et al., 1954; Kough, 1954; Brass, 1994). Attempting to handle injured, sick, grounded, or moribund bats frequently leads to bat bites of humans and their pets (Avery & Tailyour, 1960; Constantine, 1967; Brass, 1994). After any bite exposure the biting bat should be submitted to a qualified laboratory for testing. Injured, sick, grounded, moribund, or obviously behaving abnormally bats pose a much greater likelihood of having rabies than bats actively sampled (surveyed) from the environment (Constantine, 1967; Schowalter, 1980; Prins & Yates, 1986; Pybus, 1985; Prins & Loewen, 1991; Klug et al., 2011), and so these animals also pose the greatest risk to the humans who handle them. Therefore, extreme caution is warranted whenever bats are being captured for rabies testing (e.g., wear thick leather gloves, use a broom or folded towel to transfer the bat into a secure container). Many bat species are highly social and form colonies ranging from tens to hundreds to thousands (or even millions) of individuals (Kunz, 1982). Social grooming and biting of conspecifics are very common in bats (Brass, 1994; Wilkinson, 1986). Social grooming may increase the probability of intraspecific virus transmission because saliva from one individual is transferred to another. Males often bite females at the nape of the neck while mating, and social dominance hierarchies are established and regularly enforced by biting. Bats frequently bite each other on the ears, forearm, wings, and hind feet – superficial areas that are richly innervated and well vascularized (Shankar et al., 2004; Chadha et al., 2011). Biting the foot is an effective means of displacing individuals from favoured or

Medical Epidemiology of Bat Rabies Viruses in Canada About 10 years ago, Nadin-Davis et al. (2001) molecularly characterized bat rabies viruses from bat species indigenous to Canada (see Chapter 23). Bat rabies viruses in the Americas have four principal phylogenetic groups (I–IV). Group I is associated with colonial, non-migratory species (Myotis spp. and big brown bats); Group II is associated with solitary, migratory species (Lasiurus spp. and silverhaired bats); Group III also circulates in big brown bats and likely emerged more recently in this host; and Group IV is harboured by insectivorous and hematophagous bats of Latin America. The researchers found remarkable spillover of rabies virus variants into Myotis species from bats of other genera and the greatest level of interspecies spillover (6/19 or 32%) occurred by the silver-haired bat rabies virus variant, whereas variants associated with big brown bats, silver-haired bats, and Lasiurus spp. were usually infected by variants of their specific cluster (Nadin-Davis et  al., 2001). In the five human cases of rabies in Canada caused by rabies virus variants since 2000, three were caused by rabies virus variants associated with silver-haired bats and one with a variant associated with Myotis bats (Table 27.1). More recently, Turmelle et al. (2011) have provided details about the phylogeography of big brown bats, indicating some quite isolated genetic units. Future work should align the phylogeography of this species with that of variants of rabies virus.

472

Bat Rabies in Canada

Paralytic (Dumb) Rabies

important roosting sites. Consequently, ample opportunity exists for the generation of percutaneous puncture wounds and the potential for viral transmission by infected saliva directly injected into superficial tissues or muscles. Because bats are the only mammals capable of powered flight, there is also potential for transmission of rabies virus between colonies separated by relatively long distances. Rabies virus infects the central nervous system, causing neuronal dysfunction and inflammation of the brain (encephalitis) and spinal cord (myelitis) with little associated neuronal degeneration affecting neuronal cell bodies ­(Jackson & Fu, 2013). The onset of rabies in bats is characterized by a short prodromal phase of non-specific signs typically lasting one to three days, eventually progressing to severe neurologic disease before the onset of coma, respiratory failure, and death (Courter, 1954). ­Rabies is behaviourally manifest as two distinct clinical forms – f­ urious (encephalitic) rabies and dumb (paralytic) rabies – ­although the underlying pathogenesis responsible for each form still remains poorly understood (Jackson, 2013). Detailed descriptions of aberrant behaviour and case reports of rabid bats interacting with humans are given in Constantine (1967) and Brass (1994). Bats with furious or dumb rabies may show signs of weight loss or dehydration; nevertheless, reports of clinically ill bats continuing to eat and drink are not uncommon.

Bats expressing dumb rabies typically exhibit moderate to severe paralysis, often in the peripheral extremities initially bitten (e.g., wing or hind leg). Loss of motor coordination and ataxia also occur, including tremor and convulsions. Perhaps there is a greater burden of involvement in the peripheral motor nerves, nerve roots, and spinal cord in paralytic rabies than in encephalitic rabies (Jackson, 2007). Unlike with the furious form, bats with paralytic rabies display lethargy and no hyperesthesia. Bats with dumb rabies may also be abnormally tame (friendly), inquisitive, and placid. These behavioural changes can cause the sick bat to approach conspecifics or other animals (including humans) without fear (and vice versa), thereby placing the rabid bat in closer proximity, which facilitates biting and disease transmission. Paralytic rabies may be more common in highly social colonial species (Constantine et al., 1968; Kuzmin & Rupprecht, 2007). The incubation period for rabies virus in insectivorous bats is highly variable. Longer incubation periods may facilitate higher viral titres in the salivary glands of infected animals and thus disease transmission (Baer & Bales, 1967). Some bats shed virus in their saliva for 12 to 15 days before showing clinical signs of disease (Constantine, 1971). Bats inoculated with fixed rabies virus strains experimentally in the laboratory tend to exhibit shorter incubation times than bats infected with street virus from natural sources, perhaps because of the use of higher than natural viral doses, as well as rapid uptake and direct spread in peripheral nerves. Experimentally inoculated bats can have incubation times as short as 5 to 14 days and as long as 6 months (Baer & Bales, 1967), whereas incubation periods in bats captured from the wild are often longer (e.g., 28 to 209 days – Moore & Raymond, 1970; Shankar et al., 2004). By contrast, both the prodromal (1–3 days) and the clinical phases (1–10 days) of infection are usually quite short (Moore & Raymond, 1970), although Constantine (1967) reported that one Brazilian free-tailed bat (Tadarida brasiliensis) developed signs of rabies 28 days after inoculation and survived with illness for 76 days, and Baer and Bales (1967) reported one T. brasiliensis that readily ate and drank for 87 days after onset of paralysis. Laboratory infection studies have shown that viral replication slows and incubation times increase in cooler temperatures (Sadler & Enright, 1959; Sulkin et al., 1960b), suggesting that the onset of disease can be prolonged in bats undergoing hibernation, resulting in a seasonal variation in the cycle of infectivity that may facilitate the long-term maintenance of rabies virus in some bat populations (George et al., 2011).

Encephalitic (Furious) Rabies Bats expressing furious rabies can appear hyperactive, aggressive, irritable, or restless, and may also fly erratically. Their aberrant behaviour can result in unprovoked attacks on other animals or inanimate objects. This accounts for reports of bats taking flight from day roosts or dropping down from the night sky to bite unsuspecting humans. Furiously rabid animals react to disturbances, are easily agitated, and may show hyperesthesia to sensory stimuli. They may also be active and fly during the day. Bats with furious rabies are prone to excessive biting, including hang-on biting, which would facilitate infectious saliva contact with a wound and disease transmission, and self-mutilation. Grounded bats tend to bite. Furious rabies has been observed in both solitary and colonial bats, although it may be more common in solitary or tree-roosting migratory species (Bell, 1980; Schowalter, 1980; Kuzmin & Rupprecht, 2007). Furious rabies in bats is also more frequently observed in intracranial laboratory inoculations of rabies virus compared to bats infected intramuscularly and intradermally, or in captive, naturally infected bats (Baer & Bales, 1967; Constantine, 1967).

473

Ecology and Epizootiology of Wildlife Rabies

Not all bats exposed to rabies virus necessarily develop disease. We now understand that bats can have a lethal or non-lethal infection with rabies virus. After an exposure bats may not have clinical disease because they develop neutralizing serum anti-rabies virus antibodies that confer protective immunity and result in an abortive infection (Franka et al., 2008). We also know that maternally derived serum neutralizing anti-rabies virus antibodies cross the placenta and presumably confer protective immunity on newborn bat pups (Constantine et al., 1968). For years it was commonly believed that bats were capable of transmitting infectious virus without showing signs of illness or succumbing to the disease themselves – that they served as asymptomatic carriers of rabies. Although this does not appear to be correct, there are some reports of infected bats exhibiting clinical signs of rabies and then returning to normal health (Pawan, 1936; Constantine, 1967). More recent studies using modern methods for detecting rabies virus infection indicate that bats with clinical signs of rabies do not recover from disease, and inoculated bats that remain healthy have survived infection but are not carriers (Moreno & Baer, 1980; Franka et al., 2008). Bats and other mammals can shed infectious virus in their saliva several days before the onset of illness, but after neurological signs are evident the outcome is invariably death, with the animal often suffering horribly in the final hours of its life.

exposure are individuals who have been bitten, scratched, or landed on, or who have had bat saliva or other infectious materials (e.g., brain) contaminate abrasions or cuts in the skin or contact their mucous membranes. And because of their small size, bat bites and scratches may not be obvious (Figure 27.2). Since the mid-1990s PEP has also been administered to persons sleeping unattended in a room with a bat. In these situations, it is not possible to exclude the possibility of an exposure if the bat was unavailable for testing. Over time this recommendation has been expanded to include additional situations of persons unable to report possible bite exposures, such as children or intoxicated or cognitively impaired individuals in the same room as a bat (National Advisory Committee on Immunization [NACI], 2002). It has now become routine for PEP to be administered to (or requested by) any individual in the same (or even an adjacent) room as an untested bat (NACI, 2009). However, researchers have recently re-evaluated the benefits, risks, and costs associated with administering PEP in this setting by calculating the number of medical professionals and material costs required for preventing a single case of rabies for any possible human to bat exposure without evidence of contact (Huot et al., 2008; De Serres et al., 2009). The NACI is now recommending that PEP be given only when there is direct human contact with a bat that is unavailable for testing, or when a possible bat exposure (e.g., bite, scratch, or saliva from a bat in a wound) cannot be excluded (NACI, 2009; Warshawksy & Desai, 2010).

Bat-Human Encounters

Recommendations

There is ongoing discussion about the risk bats pose to humans and what constitutes a rabies virus exposure. The best way to confirm the diagnosis of rabies in an animal is by submitting the head (brain) to a certified laboratory for detection of rabies virus antigen in the brain. Humans directly exposed to bats that are known or suspected to be rabid should receive rabies post-exposure prophylaxis (PEP). This is not necessary if the bat in question does not test positive for rabies. In the case of bats, examples of direct

Whenever possible, the only persons who should handle bats are biologists or other trained wildlife professionals. Humans who receive bat bites should immediately wash and thoroughly flush and clean the wound with soap and water and report the incident to the local medical officer of health or other provincial agency officials as soon as possible so that appropriate preventative measures for rabies can be initiated.

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Journal of Wildlife Diseases, 40(3), 403–413. https://doi.org/10.7589/0090-3558-40.3.403 Streicker, D. G., Turmelle, A. S., Vonhof, M. J., Kuzmin, I. V., McCracken, G. F., & Rupprecht, C. E. (2010). Host phylogeny constrains cross-species emergence and establishment of rabies virus in bats. Science, 329(5992), 676–679. https://doi.org/10.1126 /science.1188836 Sulkin, S. E. (1962). Bat rabies: Experimental demonstration of the “reservoiring mechanism.” American Journal of Public Health, 52(3), 489–498. https://doi.org/10.2105/AJPH.52.3.489 Sulkin, S. E., Krutzsch, P. H., Wallis, C., & Allen, R. (1957). Role of brown fat in pathogenesis of rabies in insectivorous bats (Tadarida b. mexicana). Proceedings of the Society for Experimental Biology and Medicine, 96(2), 461–464. https://doi. org/10.3181/00379727-96-23507 Sulkin, S. E., Krutzsch, P. H., Allen, R., & Wallis, C. (1959). Studies on the pathogenesis of rabies in bats. I. Role of brown adipose tissue. 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Canadian Medical Association Journal, 136(12), 1277–1280. Retrieved from https:// www.ncbi.nlm.nih.gov/pmc/articles/PMC1492215/pdf/cmaj00144-0047.pdf Veilleux, J. P., Whitaker, J. O., & Veilleux, S. L. (2003). Tree-roosting ecology of reproductive eastern pipistrelles, Pipistrellus subflavus, in Indiana. Journal of Mammalogy, 84(3), 1068–1075. https://doi.org/10.1644/BEM-021 Venters, H. D., Hoffert, W. R., Scatterday, J. E., & Hardy, A. V. (1954). Rabies in bats in Florida. American Journal of Public Health, 44(2), 182–185. https://doi.org/10.2105/AJPH.44.2.182 Vonhof, M. J., Barber, D., Fenton, M. B., & Strobeck, C. (2006). A tale of two siblings: Multiple paternity in big brown bats (Epteiscus fuscus) demonstrated using microsatellite markers. Molecular Ecology, 15(1), 241–247. https://doi.org/10.1111/j.1365 -294X.2005.02801.x Wai-Ping, V., & Fenton, M. B. (1988). Non-selective mating in little brown bats (Myotis lucifugus). 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28 Striped Skunks and Rabies: Ecology and Epizootiology Margo J. Pybus Alberta Fish and Wildlife Division and University of Alberta, Edmonton, Alberta, Canada

Introduction Rabies virus is an ancient lifeform that adapted over centuries to facilitate its transmission in various hosts. The virus occurs in antigenically and genetically distinct variants in mammalian species over geographically discrete areas and in principle reservoir species (Smith et  al., 1986; Blanton et  al., 2009; see Chapter 29). Just as all rabies viruses are not alike, all skunks are not alike. Most of the documented rabies cases in skunks occur in striped skunks (Mephitis mephitis), and they are the focus of this chapter. While rabies virus occurs in free-ranging striped skunks throughout their distribution across North America, defined patterns and specific factors indicate a fine-tuned relationship between the virus and the many generations of skunks exposed to it. Time and biotic conditions gave rise to a prairie skunk rabies variant throughout the Great Plains region of Canada and the United States. Similar situations did not arise in eastern portions of the continent, where the principle rabies variant found in skunks is associated with foxes (Vulpes vulpes) (Webster et al., 1986) and more recently, raccoons (Procyon lotor) (Guerra et al., 2003). Further to this, the genetic makeup of skunk rabies variant suggests two separate origins as reflected in its distribution in (1) California and the north central states, as well as the Canadian prairies, and (2) Texas and Kansas (Smith et al., 1986, 1995). The types overlap in Missouri and Arkansas. Given the Canadian focus of our book, this chapter concentrates on relationships between rabies virus and striped skunks in the northern prairie region of North America. It

includes the ecology of (northern) prairie skunks, the factors that laid the foundation for a northern prairie skunk variant of rabies, and a case study in the development of a rabies control program in Alberta that capitalized on the biological framework present in northern prairie landscapes.

Ecology of Striped Skunks in the Northern Prairies Striped skunks are small omnivorous mustelids with a niche speciality for consuming a wide range of seasonally abundant insects, fruits, berries, forbs, and leaves, as well as small mammals, birds, bird eggs, amphibians, carrion, and human garbage. The species occurs across southern Canada from Nova Scotia to British Columbia and throughout the continental United States, except the southwestern deserts. Overall, a long-term pattern persists in undisturbed skunk populations of 10-year cyclical peaks in population numbers across Canada, as reflected in early Hudson Bay trapping data from 1850 to 1914 (Hewitt, 1921). From 1885 onward, the data also suggest recurring, although not consistent, minor peaks and troughs on a three- to five-year cycle. As outlined later, it is likely that the cyclic nature of the population change is in part driven by effects of rabies virus. Rosatte (1987) provides a detailed synthesis of what is known about striped skunk ecology across the species range. This chapter focuses on aspects of that ecology that lay a foundation for enzootic and epizootic rabies outbreaks in northern striped skunk populations.

Striped Skunks and Rabies

are particularly at risk of over-winter mortality, whether at communal or solitary den sites. Skunk populations are aggregated through long periods spent in communal dens. In northern prairie and parkland habitats, they make extensive use of buildings as centres of activity associated with winter and summer den sites (Gunson et al., 1978; Gunson & Bjorge, 1979; Showalter & Gunson, 1982; Rosatte, 1984), making them more available to be detected in passive disease surveillance programs. Females, the largest portion of the population, actively select buildings as winter den sites. The occurrence of shared winter dens increases with increasing latitude across North America (Davis, 1951; Dean, 1965; Verts, 1967; Gunson & Bjorge, 1979) and in northern regions, d ­ en-related activity can begin in October and severely reduced activity can extend from late November to mid-March. Communal winter dens of 5 to 20 skunks occur in northern areas. Den occupants consist of juvenile and adult females, as well as one adult male. Juvenile males spend the winter in solitary dens, often in underground burrows. Communal den occupants generally are not related, and there is considerable mixing of individuals during pre-denning activities as females seek a den site, adult males seek and defend communal sites, and juvenile males investigate communal sites already claimed by an adult male or seek a site where females have congregated and a male is not yet present. It is a period of increased aggression among males in particular, as evidenced by fresh bite wounds on males captured in late fall and carcasses of dead males found at occupied communal sites (Gunson & Bjorge, 1979). Striped skunks are not true hibernators, although body temperatures are reduced during winter periods of inactivity (Mutch & Aleksiuk, 1977). Reduced body temperatures slow viral replication and extend the period of rabies infection (Sulkin et al., 1960; Sulkin, 1962). In the case of prairie skunks, this mechanism facilitates transmission by reducing the risk of extensive mortality of overwintering skunks prior to spring dispersal. Such mortality would reduce the opportunities for subsequent transmission and eliminate local viral populations. However, skunks in winter dens have regular arousal periods (Sunquist, 1974), and such activity apparently provides sufficient opportunities for contact among members of the communal den (Gunson & Bjorge, 1979) to maintain low-level transfer of rabies virus. Occasional forays outside the den on mild winter days (Figure 28.1) also occur (Bjorge, 1977; Andersen, 1981), as determined by ambient temperature and snow depth (Mutch & Aleksiuk, 1977). Therefore, mild winters or

Habitat Use Originally striped skunks used largely prairie or forestfringe habitats; however, the species adapted well to ongoing human-related landscape modifications and now occurs widely in agricultural lands, rural towns and acreages, and major urban centres in all regions across Canada south of the boreal forests (see Chapters 8 and 9). The northern prairie landscape is characterized by flat, open grasslands used for intensive cereal crops or cattle ranching, interspersed and often bisected by uncultivated dryland coulees, shallow intermittent sloughs, and a few large meandering river valleys. Striped skunks are locally abundant in major river valleys and adjacent agricultural areas, often in association with fence lines, rock piles, granaries, irrigation canals, and local ponds and sloughs – wherever there is sufficient food on a seasonal rotation; abundant escape cover to avoid primary predators, such as coyotes (Canis latrans) and great-horned owls (Bubo ­virginianus); and appropriate sites for protected winter dens. Local human infrastructural elements support local concentration and abundance of skunks. While skunks primarily use open grassy habitats, even in urban areas, they avoid extensive open landscapes under agricultural cereal crop rotation. Modern agricultural practices across the arable prairies of western Canada further modify and concentrate the number and distribution of skunks. Thus the combined effects of topography, human infrastructure and land use, and seasonal food availability provide a foundation for clustered skunk populations across broad prairie landscapes and set the stage for isolated foci of enzootic skunk rabies in residual pockets of natural habitats.

Behaviour and Seasonal Activity Patterns As with most species, survival of small and medium-sized mammals in natural systems is a product of selective response to limiting factors. Availability of suitable den sites, particularly during harsh prairie summer or winter conditions, can be a primary limiting factor on the population distribution and structure of striped skunks, and further contributes to clustered occurrence of skunks in local aggregations. Dens generally provide amelioration of thermal and moisture limitations in prairie regions and allow increased energy conservation, which may be particularly important for fitness of reproductive females during periods of food scarcity (Bjorge, 1977; Bjorge et al., 1981). Even some skunks that secure suitable dens lose considerable body weight during prolonged winters, and juveniles

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of rabies virus to new micro-foci within the skunk population. In addition, dispersing juveniles may be at higher risk of exposure to rabies virus since the fall period is the period of highest incidence of rabid skunks in northern areas (Hayles & Dryden, 1970; Gunson et al., 1978).

Breeding Aggression Mating occurs in late February and March. Adult males actively conduct roaming explorations to seek females at winter dens. During this time aggressive interactions between males often lead to significant bites and wounds. Similarly, once male territoriality over a female has been settled, mating activity includes the male biting the nape of the female during copulation. Mated females aggressively fight and repel subsequent males, with additional biting wounds inflicted on both individuals (Parker, 1962; Verts, 1967). Thus the seasonal behaviours and activity patterns of striped skunks facilitate transmission of rabies virus in a manner that provides a threshold of infected individuals sufficient to maintain the virus but not overwhelm the host population. Striped skunks are opportunistic carnivores and therefore provide limited opportunities for establishing a virus that relies on a transmission pattern of transfer in saliva. However, the inherent level of intra-specific aggression among striped skunks provided a foundation on which the virus could adapt and establish local enzootic foci to maintain a viral population. As reported by many authors (Verts, 1967; Houseknecht, 1969; Webster et al., 1974; Parker, 1975; Gunson et al., 1978), a bimodal peak in annual incidence, with maximum occurrence in winter and a secondary rise of cases in late spring (April), is characteristic of rabies ­epizootiology in northern skunk populations; it appears to reflect increased contact rates among skunks before ­winter denning, and spring territorial disputes and subsequent mating behaviour with females, respectively. Extensive aggressive behaviour in striped skunks may be a primary factor affecting transmission dynamics of skunk rabies variant. Striped skunks have significant inherent resistance to the rabies virus, and it takes relatively large viral doses to establish infections in individual skunks (Sikes, 1962). This may ensure that many intra-specific aggressive behaviour events do not transfer sufficient virus to establish a new infection, thus limiting the potential for mortality in the overall population and providing conditions for enzootic maintenance rather than o ­ ver-expression of rabies leading to elimination of the virus over large

Figure 28.1: Winter forays from den site. Source: M. J. Pybus.

increased Chinook events (warm winter winds that significantly reduce accumulated snowpack in prairie regions) may lead to increased skunk activity and contact among communal den members and with other dens. Exchange of individuals among den sites may provide opportunity for increased transfer of rabies virus and establishment of new enzootic micro-foci, thus increasing the distribution of rabies virus available for activation in spring.

Migration/Dispersal Striped skunks are a relatively sedentary species with activities often limited within small home ranges. In northern regions most individuals spend much of their life within 3–5 km2 (Storm, 1972; Bjorge et al., 1981), although home ranges or dispersal movements can be somewhat larger for roaming males in fall and in late winter or spring (Sargeant et al., 1982). Primary location shifts are associated with denning. Adult skunks move two to three kilometres to winter den sites (Gunson & Bjorge, 1979), and some individuals go back to the same summer range in successive years (Bjorge, 1977). Juvenile females are the primary dispersers and although individual outliers can range more widely (Andersen, 1981), most juveniles move in the order of 15 to 20 kilometres (Gunson & Bjorge, 1979; Andersen, 1981; Bjorge et  al., 1981) in apparent search of acceptance into a winter den. Young female siblings disperse to multiple winter dens (Schowalter & Gunson, 1982). Such dispersal maintains genetic diversity within the population, which is particularly important in a species with only one breeding male in each communal den. This may also ensure transfer

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geographic areas. Similarly, over-expression of the virus within a communal den would lead to immediate local extinction of the virus. However, in the late stages of disease progression within an infected skunk, aggressive behaviour is increased. Early settlers in western regions were aware that rabid skunks in the furious stages of infection display particularly persistent and aggressive biting behaviour. Settlers and cowboys in western regions were encouraged to use skunk skirts as a barrier around the bottom of their tents to keep out rabid skunks (Parker, 1975). Persistence in biting by late-stage rabid skunks may ensure transfer of sufficient virus to maintain the viral population in this relatively resistant host species. Specific to management of rabies, the innate resistance may be a natural barrier, which contributes to reduced efficacy of oral vaccines in striped skunks (Charlton et al., 1992) and thus limits this tool as a mechanism for control of skunk rabies variant.

states and into North Dakota in the late 1950s (Tabel et  al., 1974). It reached southern Manitoba in 1959 and expanded westward towards Saskatchewan, reaching the Manitoba-Saskatchewan border by 1963 (Hayles & Dryden, 1970). The wave front continued westward and approached the Alberta-Saskatchewan border in 1969–70 (Tabel et  al., 1974; Gunson et  al., 1978). In the absence of disease control programs, the front of active infection waxes and wanes in these jurisdictions on a three- to fiveyear cycle (Pybus, 1988a). Expansion and contraction of the natural geographic distribution of skunk rabies appears to reflect skunk life history patterns in prairie landscapes in conjunction with the cyclic replacement of previous ­rabies-related mortality. Prairie skunks provide relatively sedentary rabies vectors with small home ranges, limited dispersal, and isolated pockets of local skunk abundance. This leads to relatively small enzootic foci of disease with a slowly expanding outward periphery. The clumped distribution of skunks found dead of rabies (Greenwood et  al., 1997) further reflects viral transmission within winter dens. The presence of winter dens often in proximity to humans provides increased opportunity to find, report, and test dead skunks in winter months; however, results are considered a reflection of the overall effects of rabies virus in skunks using more natural habitats. The well-defined behaviour of skunks in prairie habitats lays a foundation for effective rabies management and control through diligent and consistent population reduction efforts maintained over several years (beyond one three- to five-year cycle) and with the use of effective methods of removal (a combination of traps, poison, and gas) (Pybus, 1988a, 1988b; Hanlon et  al., 1999). Rabies control programs in Alberta shortened the life expectancy of skunks (Schowalter & Gunson, 1982) and limited the extent of juvenile dispersal in areas of population reduction (Rosatte & Gunson, 1984). Local biotic features and innate resistance pose challenges to developing oral vaccination programs but support local intensive population reduction (Rosatte et  al., 1986; Pybus, 1988a, 1988b) or perimeter ­trap-vaccinate-release (Rosatte et al., 1987; Gremillion-Smith & Woolf, 1988) as effective rabies control methods to eliminate local foci by suppressing transmission rates within locally sparse or vaccinated populations, respectively, and providing barriers to further spread. In Alberta provincial and municipal authorities have delivered an ongoing skunk rabies surveillance and control program since 1970 (Pybus, 2010). Despite

Life History Mated females move to individual parturition dens. Gestation extends 62 to 66 days, with an average litter of five to seven kits. Parturition occurs in late May or early June. The kits are weaned in two months and are independent and dispersed by fall. As with most mammals, significant mortality occurs in the first year of life. Subsequent lifespan for the survivors is generally two to four years, with an average of three years (Verts, 1967; Showalter & Gunson, 1982). Mortality factors include human-related activities (vehicle collisions, shooting, gassing), wildlife diseases (rabies, distemper), and predation. High population turnover reduces intra-specific contact rates and lowers the force of infection for maintaining rabies presence but supports low-level enzootic occurrence. The three-year average lifespan is reflected in a general pattern of cyclic occurrence of rabies virus in prairie skunk populations not subjected to population control (Pybus, 1988a).

Overview In Canada skunk rabies currently persists in free-ranging skunks over large rural prairie landscapes in southern Manitoba and Saskatchewan, with occasional cases in southern Alberta. This was not always the case. An epizootic wave of skunk rabies spread through the northern

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contiguous skunk populations and similar habitats among Alberta, Saskatchewan, and Montana, rabies virus has not established an enzootic population in skunks in Alberta (Pybus, 1988b; Canadian Food Inspection Agency, 2010).

Canadian Contributions to Research and Management of Prairie Skunk Rabies Approach Wide open spaces and independent thinking have sustained a distinct western approach to facing many challenges. In Alberta rabies and rabies control in striped skunks fits the established pattern. The outbreak of rabies that swept south out of the Arctic and into Alberta in the early 1950s was seen as invasion by an undesirable agent. The response was swift, harsh, and extensive (Ballantyne & O’Donoghue, 1954; Ballantyne, 1958). A similar philosophy was applied as rabies in striped skunks approached Alberta’s eastern border in 1970 (“we don’t have it and we don’t want it”); however, based on cumulative research and understanding of the disease, the methods were modified to target a specific host in specific habitats (Gunson et  al., 1978). The approach continues as dedicated rabies control targeting striped skunks has been applied within rabies risk areas consistently since 1970 (Pybus, 1988a, 2010).

Figure 28.2: Trapping skunks at winter den site. Source: M. J. Pybus.

Management When it comes to rabies management, it was readily apparent that different vector populations posed different challenges to controlling the effects of rabies infections. The extent of Canadian contributions overall to rabies management are detailed throughout this book. However, specific to prairie skunk rabies, it is apparent that with the right policy, approach, and political will, targeted population control can be effective in the right place at the right time and applied with diligence. In the early years of rabies control in Alberta (see Chapter 7), a massive program of trapping, poisoning, and shooting any carnivore was applied across broad regions of the province to protect people and livestock. It would be inconceivable now to deliver such a major intervention, but it was deemed appropriate in the decade it was delivered. Later programs were much more targeted to remove only striped skunks using the same methods (Figures 28.2, 28.3, 28.4,

Figure 28.3: Setting poisoned eggs at summer den site. Source: M. J. Pybus.

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at the time but is known now as a one health approach to disease management. In 1953 Alberta established the Central Rabies Control Committee. Representatives from wildlife, agriculture, and public health joined forces, knowledge, experiences, and resources to wage a concerted battle against the rabies virus invading the province from the Arctic. The committee remains in place today. It has directed and modified Alberta’s rabies programs over the years to incorporate new knowledge and

and 28.5) and through local radial depopulation (within five kilometres of an infected skunk) using live traps, kill traps, or poisoned eggs in selective sites specific to catching and killing skunks. Dead skunks were also collected, and any skunks with porcupine quills were a good indicator of rabies in the area (Figure 28.6). The other significant contribution to rabies management as directed against skunks in Alberta was the early application of what was a relatively unique relationship

Figure 28.4: Depopulation at a communal winter den. Source: M. J. Pybus.

Figure 28.6: Skunk with porcupine quills. Quills in an animal’s face are often an indicator that the animal was rabid.

Figure 28.5: Depopulation by shooting. Source: M. J. Pybus.

Source: M. J. Pybus.

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understanding, and applies the cumulative value of the information to the mutual benefit of all participants and their associated interests.

virus. Publications cited throughout this chapter are examples of the significance of their contribution to rabies management within and well beyond the prairies.

Knowledge and Understanding

Training

The variant rabies virus in striped skunks has its own specific adaptations and characteristics. As they did with fox and raccoon rabies variants in eastern regions, researchers and managers in prairie regions of western Canada provided an extensive body of knowledge and understanding of the ecological relationships between skunks and rabies

Rabies programs have long been a training ground for young enthusiastic biologists to gain a solid foundation for a career in various aspects of the wildlife profession. “Graduates” from the Alberta rabies programs often went on to make significant contributions in wildlife, habitat, and disease management. A few examples are outlined here.

The Face of Skunk Rabies Management in Alberta Dave Schowalter: early skunk trapper with a special interest in bats. Numerous publications, extensive career in teaching, and significant curatorial contributions to museum collections across Alberta. John Gunson: early rabies program manager, went on to a career in provincial carnivore management. Per Andersen: master’s thesis in skunk biology led to an extensive career in provincial habitat management and conservation. Ron Bjorge: diligence and meticulous planning applied during his master’s thesis on skunk ecology laid the foundation for a successful career as a wildlife biologist, culminating in his position as director of wildlife management at Alberta Fish and Wildlife. Rick Rosatte: started off in the Alberta skunk rabies programs, moved into Ontario’s rabies programs, and pioneered a wide range of field activities associated with successful rabies management in skunks and raccoons. Margo J. Pybus: working career began as the field and program manager of the Alberta skunk rabies program and expanded into a career in provincial, national, and international wildlife disease management.

References Andersen, P. A. (1981). Movements, activity patterns and denning habits of the striped skunk (Mephitis mephitis) in the mixed grass prairie (Unpublished master’s thesis). University of Calgary, Calgary, Alberta, Canada. Ballantyne, E. E. (1958). Rabies control in Alberta wildlife. Veterinary Medicine, 23, 87–91. Ballantyne, E. E., & O’Donoghue, J. G. (1954). Rabies control in Alberta. Journal of the American Veterinary Medical Association, 125, 316–326. Blanton, J. D., Robertson, K., Palmer, D., & Rupprecht, C. E. (2009). Rabies surveillance in the United States during 2008. Journal of the American Veterinary Medical Association, 235(6), 676–689. https://doi.org/10.2460/javma.235.6.676 Bjorge, R. R. (1977). Population dynamics, denning, and movements of striped skunks in central Alberta (Unpublished master’s thesis). University of Alberta, Edmonton, Canada. Bjorge, R. R., Gunson, J. R., & Samuel, W. M. (1981). Population characteristics and movements of striped skunks (Mephitis mephitis) in central Alberta. Canadian Field-Naturalist, 95, 149–155. Canadian Food Inspection Agency. (2010). Positive rabies in ­Canada: January 1 to December 31, 2010. http://www.inspection .gc.ca/english/anima/disemala/rabrag/statse.shtml#a2010 Charlton, K. M., Artois, M., Prevec, L., Campbell, J. B., Wandeler, A., & Armstrong, J. (1992). Oral rabies vaccination of skunks and foxes with a recombinant human adenovirus. Archives of Virology, 123(1–2), 169–179. https://doi.org/10.1007/BF01317147 Davis, W. B. (1951). Texas skunks. Texas Game and Fish, 9, 18–21.

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Striped Skunks and Rabies Dean, F. C. (1965). Winter and spring habits and density of Maine skunks. Journal of Mammalogy, 46(4), 673–675. https://doi.org/10.2307 /1377941 Greenwood, R. J., Newton, W. E., Pearson, G. L., & Schamber, G. J. (1997). Population and movement characteristics of r­ adio-collared striped skunks in North Dakota during an ­epizootic of rabies. Journal of Wildlife Diseases, 33(2), 226–241. https://doi.org/10.7589 /0090-3558-33.2.226 Gremillion-Smith, C., & Woolf, A. (1988). Epizootiology of skunk rabies in North America. Journal of Wildlife Diseases, 24(4), 620–626. https://doi.org/10.7589/0090-3558-24.4.620 Guerra, M. A., Curns, A. T., Rupprecht, C. E., Hanlon, C. A., Krebs, J. W., & Childs, J. E. (2003). Skunk and raccoon rabies in the ­eastern United States: Temporal and spatial analysis. Emerging Infectious Diseases, 9(9), 1143–1150. https://doi.org/10.3201/eid0909 .020608 Gunson, J. R., & Bjorge, R. R. (1979). Winter denning of the striped skunk in Alberta. Canadian Field-Naturalist, 93, 252–258. Gunson, J. R., Dorward, W. J., & Schowalter, D. B. (1978). An evaluation of rabies control in skunks in Alberta. Canadian Veterinary Journal, 19, 214–220. Hanlon, C. A., Childs, J. E., & Nettles, V. F. (1999). Recommendations of a national working group on prevention and control of rabies in the United States. III – Rabies in wildlife. Journal of the American Veterinary Medical Association, 215, 1612–1619. Hayles, L. B., & Dryden, I. M. (1970). Epizootiology of rabies in Saskatchewan. Canadian Veterinary Journal, 11, 131–136. Hewitt, C. G. (1921). The conservation of the wild life of Canada. New York, NY: Charles Scribner’s Sons. Houseknecht, C. R. (1969). Denning habits of the striped skunk and the exposure potential for disease. Bulletin of the Wildlife Disease Association, 5(3), 302–306. https://doi.org/10.7589/0090-3558-5.3.302 Mutch, G. R. P., & Aleksiuk, M. (1977). Ecological aspects of winter dormancy in the striped skunk (Mephitis mephitis). Canadian ­Journal of Zoology, 55(3), 607–615. https://doi.org/10.1139/z77-077 Parker, R. L. (1962). Rabies in skunks in the north-central States. In Proceedings of the 65th annual meeting of the U.S. Livestock Sanitary ­Association (pp. 273–280). Retrieved from https://www.usaha.org/upload/Proceedings/1961_SIXTY_FIFTH_ANNUAL_MEETING.pdf Parker, R. L. (1975). Rabies in skunks. In G. M. Baer (Ed.), The natural history of rabies (vol. 2, pp. 41–51). New York, NY: Academic Press. Pybus, M. J. (1988a). Rabies and rabies control in striped skunks (Mephitis mephitis) in three prairie regions of western North America. Journal of Wildlife Diseases, 24(3), 434–449. https://doi.org/10.7589/0090-3558-24.3.434 Pybus, M. J. (1988b). Rabies control by skunk depopulation in southern Alberta, 1983–1986. Prairie Naturalist, 20, 7–14. Pybus, M. J. (2010). Rabies and rabies management in Alberta. Alberta Sustainable Resource Development. Fish and Wildlife Division. Retrieved from https://open.alberta.ca/publications/0778588856 Rosatte, R. C. (1984). Seasonal occurrence and habitat preference of rabid skunks in southern Alberta. Canadian Veterinary Journal, 25, 142–144. Rosatte, R.C. (1987). Striped, spotted, hooded, and hog-nosed skunk. In M. Novak, J. A. Baker, M. E. Obbard, & B. Malloch (Eds.), Wild furbearer management and conservation in North America (pp. 599–613). Toronto, ON: Ontario Trappers Association and ­Ontario Ministry of Natural Resources. Rosatte, R. C., & Gunson, J. R. (1984). Dispersal and home range of striped skunks (Mephitis mephitis), in an area of population ­reduction in southern Alberta. Canadian Field-Naturalist, 98, 315–319. Rosatte, R. C., Pybus, M. J., & Gunson, J. R. (1986). Population reduction as a factor in the control of skunk rabies in Alberta. Journal of Wildlife Diseases, 22(4), 459–467. https://doi.org/10.7589/0090-3558-22.4.459 Rosatte, R. C., Kelly-Ward, P. M., & MacInnes, C. D. (1987). A Strategy for controlling rabies in urban skunks and raccoons. In ­Integrating man and nature in the metropolitan environment: Proceedings of the National Symposium on Urban Wildlife. Columbia, MD: National Institute for Urban Wildlife. Sargeant, A. B., Greenwood, R. J., Piehl, J. L., & Bicknell, W. B. (1982). Recurrence, mortality, and dispersal of prairie striped skunks, Mephitis mephitis, and implications to rabies epizootiology. Canadian Field-Naturalist, 96, 312–316. Showalter, D. B., & Gunson, J. R. (1982). Parameters of population and seasonal activity of striped skunks, Mephitis mephitis, in Alberta and Saskatchewan. Canadian Field-Naturalist, 96, 409–420. Sikes, R. K. (1962). Pathogenesis of rabies in wildlife. I. Comparative effect of varying doses of rabies inoculated into foxes and skunks. American Journal of Veterinary Research, 23, 1042–1047. Smith, J. S., Reid-Sanden, F. L., Rounillat, L. F., Trimarchi, C., Clark, K., Baer, G., & Winkler, W. G. (1986). Demonstration of antigenic variation among rabies virus isolates by using monoclonal antibodies to nucleocapsid proteins. Journal of Clinical Microbiology, 24, 573–580. Smith, J. S., Orciari, L. A., & Yager, P. A. (1995). Molecular epidemiology of rabies in the United States. Seminars in Virology, 6(6), 387–400. https://doi.org/10.1016/S1044-5773(05)80016-2 Storm, G. L. (1972). Daytime retreat and movement of skunks on farmlands in Illinois. Journal of Wildlife Management, 36(1), 31–45. https://doi.org/10.2307/3799186 Sulkin, S. E. (1962). Bat rabies – Experimental demonstration of the “reservoiring mechanism.” American Journal of Public Health, 52, 489–498.

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29 Recent Advances in the Epizootiology of Wildlife Rabies Susan Nadin-Davis Ottawa Laboratory Fallowfield, Canadian Food Inspection Agency (Retired), Ottawa, Ontario, Canada

The Concept of Rabies Reservoirs As recently as 50 years ago, it was generally believed that the rabies virus was a single homogeneous pathogen. However, as panels of monoclonal antibodies (MAbs) directed to various rabies virus antigens were developed, it became possible to directly compare the antigenic profile of isolates from different species and regions. Such studies showed for the first time that distinct viral variants existed and that these were geographically restricted in their range and associated with particular epizootics. Hence, the concept of a reservoir species, responsible for maintaining a viral variant within a defined geographical area was established. While in many countries of the world, the dog is the principal reservoir for many rabies virus lineages, in Canada rabies is maintained by certain wildlife species. Viral-typing tools, comprising both antigenic and genetic characterization of specimens, as described in Chapter 23, have revealed the existence of several distinct viral variants across Canada and their association with specific reservoir hosts. This chapter summarizes current knowledge of the viral variants presently circulating in Canada and explores their evolutionary relationships with viruses of other countries. This latter activity was facilitated by a global collection of rabies viruses, recovered by Alex Wandeler over several decades and now housed at the Ottawa Laboratory Fallowfield (OLF) site. Through genetic comparisons using these specimens, as well as nucleotide sequence information available from the GenBank public database co-ordinated by the National Center for Biotechnology Information in the

United States, the evolutionary relationships of Canadian rabies viruses to those present around the world is now being revealed.

Viruses of Terrestrial Mammals Studies conducted in the mid-1980s examined the antigenic diversity of the viruses collected from terrestrial species across Canada. Two major viral groups were identified: those associated with terrestrial species from Ontario, Quebec, and the Canadian north where foxes were principally affected, and those associated with terrestrial species from the prairie provinces of Saskatchewan, Manitoba, and Alberta, where skunk rabies was particularly prevalent (Webster et  al., 1985, 1986). The same viral variant was identified within a specific area irrespective of the host species from which the isolate was recovered. This was the first clear demonstration of the evolutionary origins of two distinct epizootics. Fox rabies spread to southern Canada from the north in the 1950s and 1960s and then died off in most regions, with the exception of Ontario where it persisted for several decades (see Chapters 2 and 10) until its prevalence was reduced by provincial control programs. Skunk rabies in the prairie provinces spread into southern Canada from the US midwest (see Chapter 28). These variants are now referred to as the arctic fox (AFX) and Western skunk (WSK) variants, respectively. These early studies, which employed panels of up to 43 anti-nucleoprotein (anti-N) MAbs, identified some antigenic variation within these two main groups. Based on

Ecology and Epizootiology of Wildlife Rabies

distinct binding to one MAb, a subgroup of the arctic variant was identified within a relatively limited region of southeastern Georgian Bay in Ontario; similarly a single MAb differentiated a subgroup of the western skunk variant in Alberta (Webster et al., 1986). Such variation may reflect some of the genetic heterogeneity within these variants that were identified later (see below). As additional MAbs became available, refinement of the panels enabled variant identification using much reduced numbers of MAbs (Nadin-Davis et al., 2001; Fehlner-Gardiner et al., 2008; see Chapter 23). The raccoon viral variant, which was identified as a distinct antigenic viral type (Smith et  al., 1984), spread rapidly across the eastern United States in the 1970s and 1980s (Jenkins & Winkler, 1987) and reached the Canadian border in the late 1990s. Methods to rapidly discriminate this variant from other rabies viruses were developed (see Chapter 23) in anticipation of its eventual incursion into Canada (Wandeler & Salsberg, 1999).

to the OLF over 25 years. These surveillance records for eastern Canada reveal that in the early 1990s, foxes were the most commonly affected species, composing approximately 50% of total reported rabies cases, while the skunk, composing between 15% and 20% of all cases, was by far the most significant secondary host species (see Chapter 10). In light of this observation, a more detailed comparison of the viruses recovered from these two species was sought to explore the possibility that distinct variants might circulate in these species. Since skunks were a reservoir host in western Canada, it was believed that skunks might maintain a viral variant distinct from that maintained in the fox population that was not detectable by MAb-based analysis. Accordingly, a collection of viruses recovered from Ontario and Quebec between 1990 and 1993 from many different host species, including foxes and skunks, was subjected to genetic analysis using the newly developed reverse transcription polymerase chain reaction (RT-PCR) method (Nadin-Davis et  al., 1993). Initially two N gene products, one from a fox and one from a skunk, were generated, cloned into a plasmid vector, and then sequenced. Using the resulting sequence data, maps of restriction endonuclease sites were generated and a

Arctic Fox Rabies Virus THE PICTURE IN ONTARIO IN THE 1990S

The data in Table 29.1 summarize the total case numbers reported for eastern Canada from all submissions

Table 29.1  Annual summary of rabies cases identified from all submissions from eastern Canada to the Ottawa laboratory, 1990 to 2014. Year

Bat

Red fox

Skunk

1990 1991 1992 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012 2013 2014

26 49 28 24 18 22 25 31 31 19 45 67 92 88 63 74 50 78 43 39 36 37 28 43 25

1,149 926 1,1660 944 322 1,336 880 333 17 16 41 42 48 25 8 11 3 3 2 4 0 4 21 0 1

356 389 286 227 145 101 74 40 34 47 63 62 46 22 25 18 24 36 31 10 10 1 1 1 1

Raccoon

Other wildlife

Livestock/pets

Human

Positive

Submit

% Pos

26 25 35 14 6 1 0 0 1 9 46 89 26 16 5 2 5 50 27 0 0 0 0 0 1

355 444 377 31 200 33 55 00 00 22 33 66 55 1 33 22 22 22 1 1 00 44 66 44 33

541 451 463 409 220 90 54 33 12 17 23 26 18 16 21 18 18 14 14 13 0 2 9 3 1

0 0 0 0 0 0 0 0 0 0 1 0 0 1 0 0 0 1 0 0 0 0 1 0 0

2,133 1,884 2,009 1,649 731 353 238 137 95 110 222 292 235 169 125 125 102 184 118 67 46 48 66 51 32

10,114 9,889 10,389 10,186 7,655 6,434 5,965 9,766 6,386 7,725 13,642 12,610 9,495 10,348 9,555 6,048 6,498 6,972 5,835 4,394 3,625 3,326 2,826 2,361 1,100

21.09 19.05 19.34 16.19 9.55 5.49 3.99 1.40 1.49 1.42 1.63 2.32 2.47 1.63 1.31 2.07 1.57 2.64 2.02 1.52 1.27 1.44 2.34 2.16 2.91

Source: compiled from CFIA data.

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Figure 29.1: AFX rabies viral variants in Ontario and western Quebec, 1989 to 1993, using N gene classification. The sample set, which consisted of a small proportion of total rabies-positive submissions, comprised 91 foxes, 40 skunks, 4 dogs, 3 cats, and 8 others. N1 = ▲; N2 = ●; N3 = ✚; N4 = ♦; N5 = ■

Based on the resulting RFLP patterns, the viruses were divided into five major types (N1 to N5) according to their geographical distribution rather than the host species from which they had been recovered (Figure 29.1). It was shown that N1 (▲) viruses were clustered in eastern Ontario and north along the border between Ontario and Quebec; N2 (●) viruses were recovered from southwestern Ontario,

number of differences between the two clones were identified. The presence of these differences, designated as restriction fragment length polymorphisms (RFLPs) as described in Chapter 23, was explored using PCR products generated from a collection of virus samples recovered from diagnostic specimens submitted to OLF from across Ontario.

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north to Gogama and west of the area of the N1 virus in eastern Ontario; N3 (✚) viruses were found in southwestern Ontario; N4 (♦) viruses were concentrated around the southern shore of Georgian Bay; and the two samples of N5 (■) virus were near Timmins and La Reine in the north. Minor sub-variants of some of these types were also evident (Nadin-Davis et al., 1993). This regional variation was further examined using many of these same virus samples to score the RFLP profiles of the G gene that encodes the less conserved viral glycoprotein. As predicted, this analysis suggested a pattern of rabies virus variant type distribution similar to that identified by the N gene study, but it also exposed a greater genetic variation because of the higher level of G gene heterogeneity (Nadin-Davis et al., 1999). Some of the geographic regions harbouring distinct viral types had previously been identified as having distinctive epidemiological cycles of rabies. For example, eastern Ontario, which harboured N1 viruses and reported a high percentage of cases in red foxes, had a pronounced and regular cycle of disease incidence in which peaks of high and low case numbers repeated in a three-year cycle. In comparison many other areas exhibited less pronounced disease periodicity and reported a higher proportion of cases in other species, including skunks and cattle (Tinline & MacInnes, 2004). Moreover, certain geographical landscape features, particularly rivers, lakes, and the Canadian Shield, seemed to form the boundaries between areas harbouring distinct viral types, particularly between N1 and the combination of N2, N3, and N4 viruses in southwestern Ontario. Nadin-Davis et  al. (1999) suggested that geographical ­barriers might restrict host movements, and consequently viral spread, between such areas. A re-analysis of a subset of this collection of Ontario viruses using nucleotide sequencing provided further insights into the evolution of these viruses (Real et  al., 2005). This study suggested that variation by distance was the most significant factor operating on this system. Rabies had spread from the north into southern Ontario in two streams (see Figure 10.8, Chapter 10): one southwards along the Ottawa River Valley and across the river into Ontario (N1) and the other around Georgian Bay (N2) subsequently diverging into N3 and N4 types. The most divergent viruses were those recovered from areas farthest from the original incursion points. Hence there was more diversity in southwestern Ontario than in eastern Ontario.

The studies described above have demonstrated that a single viral variant was responsible for terrestrial rabies across this province but that genetically distinct viral types, having small genetic differences of less than 2% circulated in specific regions. In many cases the nucleotide changes associated with the different viral types were synonymous in nature, that is, they did not result in changes to the encoded amino acid. This would explain the difficulty in developing MAb panels that could discriminate between many of these viral types. However, these variants were sufficiently distinct and stable as to be reproducibly detected by RFLP methods; therefore, these genetic differences had epidemiological utility for tracking movements of specific variants within Ontario. THE 1989 TO 1993 OUTBREAK IN CENTRAL ONTARIO

During the late 1980s and early 1990s, while these studies on genetic variation of the viruses of terrestrial species in Ontario were being initiated, there was an outbreak of rabies in central Ontario and western Quebec in an area roughly bounded by North Bay, Blind River, Timmins, and Rouyn-Noranda (Figure 29.1). Surveillance performed south of the outbreak region in the late 1980s clearly identified the spread of rabies from southern Ontario, up around the eastern shore of Georgian Bay, and into this region, consistent with the involvement of the N2 variant (Figure 29.2). Molecular typing of several samples from the outbreak region did indeed identify exclusively N2 viruses in 1989 and 1990. However, from 1991 onwards, an increasing proportion of N1 viruses were detected (Figure 29.3), and by 1993, the last year of the outbreak (“First Bait Drop,” 1992; MacInnes, 1993) only the N1 virus was identified (Nadin-Davis et  al., 1994) in northern Ontario and western Quebec. Even more notable was the identification of two isolates in 1991 from the more northern portion of the study area (Timmins and La Reine in Figure 29.1) that generated RFLP patterns that were quite distinctive and previously unidentified. These two viruses were subsequently shown to be more typical of the viruses, designated as N5 (Nadin-Davis et al., 1994), that circulate in northern Canada. These observations established that the outbreak had been due to a convergence of no less than three types of the arctic fox variant: N1 from eastern Ontario, N2 from southern Ontario, and N5 from northern Ontario. The value of molecular epidemiological investigation was established by this example because we were able to trace the origins and spread of an outbreak

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Figure 29.2: N2 virus samples shown by year in Ontario and Quebec, 1989 to 2001. Source: author.

through sparsely populated areas where surveillance was limited or even absent. Moreover, the identification of the N5 virus in northern Ontario in subsequent years as far south as North Bay in Ontario and Magpie on the north shore of the St. Lawrence River in Quebec (Figure 29.4) indicated the potential for re-incursion of the arctic variant from northern Canada into southern Ontario. Such an event could undermine the provincial rabies program aimed at control and eradication of the AFX variant in southern Ontario.

PERSISTENCE OF AFX VARIANT TYPES IN SKUNKS IN ONTARIO

The extensive rabies control efforts by provincial officials, which started in eastern Ontario in 1989 and continued across the province throughout the 1990s (see Chapter 10), had by the mid-1990s eliminated terrestrial rabies in eastern Ontario and substantially reduced cases in the rest of southern Ontario. As shown in Table 29.1, rabies cases in the targeted fox population declined throughout the 1990s, as did cases in all other non-flying mammalian species (wild

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Figure 29.3: N1 virus samples shown by year in Ontario and Quebec, 1989 to 2001. Spread was outwards from a core area near Ottawa, and a remnant of that spread remained in the Peterborough area from 1996 to 2001. Source: author.

and domestic). These observations, together with genetic typing data, indicated that these cases in non-reservoir species were due primarily to spillover of the AFX variant. Fox and skunk cases increased slightly in the early 2000s because of outbreaks in northern Quebec, central Ontario and Newfoundland and Labrador (Figure 29.4), but from 2004 onwards red fox case numbers continued to decline. No cases were reported from 2010 until 2016. All cases in this host in that period occurred in northern Canada (Figure 29.4). Cases in striped skunks, however,

continued to occur in southwestern Ontario focused on an area including Grey, Dufferin, Wellington, and Perth counties. Moreover the surveillance data showed a longterm trend in which the proportion of skunk cases relative to fox cases had consistently risen since the mid-1990s, and from 1997 onwards skunk cases consistently outnumbered those in foxes in southern Ontario. These observations strongly suggested that the skunk was playing a maintenance role for AFX variant rabies in this area (Nadin-Davis et al., 2006a).

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Figure 29.4: N5 virus samples shown by year in Ontario and Quebec, 1989 to 2013. Source: author.

Viral typing of samples from 1989 to 2006 demonstrated that by 1995 virus type N4 had disappeared from Ontario and that the remaining cases were associated with virus types N1, N2, and N3. The N1 samples were concentrated in the Peterborough area (Figure 29.3) and were from skunks. This outbreak was a residual from the control program in eastern Ontario that had eliminated rabies in terrestrial animals in the east and north (see Chapter 10). The AFX rabies focus that persisted in skunks in Grey, Dufferin, Wellington, and Perth

counties in southwestern Ontario was caused by the N2 and N3 viruses that had circulated in the region previously (Nadin-Davis et al., 2006a; see Chapter 10). These observations helped spur the development of oral vaccine alternatives to Evelyn-Rokitnicki-Abelseth (ERA) that were more efficacious in skunks (see Chapter 17). Despite these efforts, viral variants that have emerged from the N2 type have continued to circulate at low levels in this area up until the present (Nadin-Davis & FehlnerGardiner, 2019).

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1951, while more recent analysis of whole genome data suggests the progenitor virus circulated around 1935 (Nadin-Davis, unpublished data). Surveillance records suggest that rabies emerged in the Canadian high Arctic in the late 1940s, a timeframe that is in close accord with these estimates. It is thus proposed that the emergence of AFX rabies and its incursion into Canada occurred within a very short time. Detailed molecular analysis of the Arctic/AL viruses, as illustrated by representative samples shown in the tree of Figure 29.6, identified two distinct clades of “Arcticlike” viruses: AL1, which has been found in Korea, Inner Mongolia, Russia, Siberia, and northern India; and AL2, which appears to be widespread in much of India and neighbouring countries including Iran. The true Arctic clade can be divided into four main groups: A1, found only in Ontario (ON AFX), includes types 1 to 4 as described above; A2 recovered from Alaska, Canada, and Siberia, but that, at least on the American continent, appears to be limited to Alaska in recent years; A3, which has been found in Siberia and Alaska but which has also circulated extensively across northern Canada and Greenland as the type 5 viruses described in earlier sections of this chapter; and A4, a group found to date only in Alaska (Kuzmin et al., 2008; Nadin-Davis et al., 2012b). The dataset reported in the study by Nadin-Davis et al. (2012b) has provided evidence for frequent transmission of viruses between red and arctic foxes, a finding of some significance regarding the maintenance and spread of this viral type. Information on the population structure of these two fox species would provide further insight and understanding of these transmission patterns.

THE 2003 NEWFOUNDLAND AND LABRADOR OUTBREAK

The periodic spread of rabies from the Canadian north into other areas of eastern Canada, most notably into northern Quebec and the province of Newfoundland and Labrador, has also been documented. Indeed, one such incursion which occurred in 2002–2003 spread all the way to the island of Newfoundland (see Chapter 13). Sequence analysis of the viruses responsible for this outbreak showed that the variant responsible had been widespread in Quebec from 2000 onwards before the Newfoundland outbreak and still circulated in Labrador in 2004 (Nadin-Davis et al., 2008). In contrast, viruses that had been recovered from Cartwright, a coastal community on the Labrador mainland, just months before the Newfoundland outbreak, were phylogenetically distinct, despite being suspected as the source of the island incursion. On this basis it appeared more likely that foxes ranging from eastern Quebec onto pack ice or ice floes may have been the source of the Newfoundland incursion. AFX VARIANT EVOLUTION: VIEWS FROM THE OTHER SIDE OF THE WORLD

As rabies virus sequences obtained from a larger number of samples from across the Arctic became available, phylogenetic analysis of these data provided information about their evolutionary relationships. As expected, rabies viruses from specimens recovered from Canada, Alaska, Greenland, and parts of Siberia were all closely related (see Chapter 37). More surprisingly, viruses from many countries of central Asia, including Iran, Pakistan, Afghanistan, India, Nepal, Mongolia, and Korea, were also quite closely related to these arctic viruses, and this entire rabies viral lineage has thus been designated as arctic/arctic-like (AL) (Kuzmin et  al., 2004; Mansfield et  al., 2006; ­Nadin-Davis et al., 2003b; Nadin-Davis et al., 2007) as illustrated in Figure 29.5. Using Bayesian methods applied to such sequence data to predict timelines for the evolution of this entire Arctic/AL lineage, a wide range of dates for the emergence of this lineage have been suggested (Kuzmin et  al., 2008), although a recent study estimated that the lineage has emerged within the last 200 years, probably from progenitors within central Asia, followed by spread of the true Arctic viruses into northern climes and transmission into arctic fox populations, which facilitated its circumpolar spread (Nadin-Davis et al., 2012b). Indeed, Nadin-Davis et  al. (2012b) estimated that the Arctic clade based on N gene sequence data of this lineage emerged around

Western Skunk Rabies Virus The antigenic distinctness of the virus circulating in the western prairie provinces from that in Ontario and the Canadian north was established based on comparisons using MAb panels (Webster et  al., 1985, 1986). Genetic studies on the variant that came to be known as the WSK virus targeted two isolates recovered in 1991 which were characterized at several different genetic loci (Nadin-Davis et al., 1997, 2002). These studies established that the WSK variant was more closely related to certain laboratory viruses, including the Pasteur virus (PV), Street-AlabamaDufferin (SAD) strain, and the challenge virus standard (CVS) strain, than to the AFX variant. Furthermore, a genetic comparison of WSK viruses with several viruses of the ­north-central skunk (NCSK) variant from skunks

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Figure 29.5: A phylogenetic tree generated from an alignment of 1350 bases of N gene sequence from 60 rabies viruses sampled worldwide showing the relationship of Canadian variants within this global diversity. The multiple sequence alignment was created in CLUSTALX and exported in PHYLIP format for importation into the MEGA, version 4, software for analysis by the neighbour joining method using 1000 bootstrap data replicates. Significant bootstrap values, provided as percentages at major branch points, are illustrated to the left of the branch. An Australian bat Lyssavirus, a rabies-related viral isolate of the Lyssavirus genus, is used as an outgroup. The solid vertical lines to the right of the tree indicate the seven major lineages of rabies viruses predicted by the tree and described previously (see Bourhy et al. 2008). Left of these lines, the countries or regions within which each clade or lineage circulates, together with its reservoir host, is indicated.

Notes: Letters indicate the country of origin thus: ALL, Germany; AFS, Republic of South Africa; AUS, Australia; BRZ, Brazil; CAN, Canada; CH, Chile; CHI, China; COL, Columbia; CUB, Cuba; EST, Estonia; ETH, Ethiopia; FRA, France; GUI, Guinea; IN, India; INDO, Indonesia; IRN, Iran; ISL, Israel; MAR, Morocco; MEX, Mexico; MOZ, Mozambique; NAM, Namibia; NEP, Nepal; NIG, Nigeria; PAK, Pakistan; PHI, Philippines; POL, Poland; PR, Peru; RUS, Russia; SRL, Sri Lanka; TAN, Tanzania; TD, Trinidad; THA, Thailand; US, United States of America (preceded by two-letter state abbreviation); YAK, Yakutia (region of Siberia); ZIM, Zimbabwe. State abbreviations employed are AL, Alaska; AZ, Arizona; CA, California; FL, Florida; NY, New York; PA, Pennsylvania; TX, Texas; WA, Washington.

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Figure 29.6: A phylogenetic tree generated from an alignment of 500 bases of partial N gene sequence from 90 viral samples of the ­arctic/arctic-like lineage using the Pasteur virus variant as an outgroup.

Notes: Analysis was performed as described in the caption to Figure 29.5. The source of each sample is indicated by its country code as provided in the legend to Figure 29.5. In some cases this code appears within the sample designation and not at the end. Additional codes employed here include GRN (Greenland) and SIB (Siberia). Division of the samples into two arctic-like (AL) clades and the four arctic (A) clades, as described in the text, are indicated. Source: author.

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in the US midwest established their close epidemiological relationship (Davis et  al., 2013). This information supports the hypothesis that the skunk cases observed in the Canadian prairies are the result of cross-border spread of the NCSK epizootic that ranges over several northern states of the United States.

variant) spread rapidly and was reported to have reached the US–Canadian border by the early 1990s. The first incursion of this variant into Canada was reported to have occurred near the town of Prescott, Ontario, in July 1999 (Wandeler & Salzberg, 1999); this was the start of an outbreak that lasted until 2005. There have been four other incursions of raccoon variant rabies into Canada: two in New Brunswick, the first in 2000–2002 (MacInnes, 2000) and the second in 2014; an incursion into Quebec from 2005 to 2009 (see Chapter 11 and Nadin-Davis et al., 2018); and an incursion into Ontario in the Hamilton area in December 2015. The vast majority of rabies cases in raccoons in eastern Canada since 1999 (see Table 29.1) are due to infections with the RRV variant. In each of the first three incursions, the provincial control actions implemented, based on those developed in Ontario (Rosatte et al., 2001), appear to have successfully terminated these outbreaks within five years or less. The outbreak near Hamilton, Ontario, has been contained, and the annual number of cases is dropping but, at the time of writing, the outbreak is ongoing (see Chapter 10). A key element of the effective control strategy was the prompt identification of cases caused by the raccoon variant, which allowed for efficient mobilization of provincial control activities. Since incursion of this variant into Canada had been anticipated for some time, there were concerted efforts to develop typing tools that would rapidly and unequivocally identify this virus variant, as described in Chapter 23. Despite the extensive spread of the raccoon variant rabies virus throughout the eastern seaboard of the United States during the 1980s and 1990s, only limited genetic characterization of this variant had been performed. A study of the diversity of the mid-Atlantic RRV used N and G gene sequences to define several distinct lineages and estimated the year of emergence of this variant at 1973, a value that is in excellent agreement with surveillance records, which first identified this variant in West Virginia in 1977 (Biek et al., 2007). A Canadian study of the genetic diversity of the RRV variant that targeted the variable G-L non-coding region and employed isolates from across the entire geographical range of the virus estimated that the most recent common ancestor (TMRCA) of the mid-Atlantic virus dated to 1976 (95% highest posterior density [HPD], range 1971–1980) while TMRCA of the entire raccoon viral lineage was dated to 1946 (95% HPD, range 1924–1965). These estimates agree well with surveillance records (Szanto et  al., 2011). This study also identified two phylogenetically distinct RRV variants circulating in western and eastern regions

ORIGINS OF THE WSK VARIANT

Inclusion of the WSK variant in phylogenetic studies on rabies viruses recovered from around the globe clearly establish its association with a set of viruses now known as the cosmopolitan lineage (Figure 29.5). This lineage, first identified as the virus variant responsible for disease in dogs from many parts of the world (Smith et al., 1992), is thought to have been widely distributed from western Europe to many other countries during the colonization period (as reviewed by Nadin-Davis & Bingham, 2004). Indeed, this skunk-associated virus is phylogenetically quite closely related to a number of other viruses that circulate in North America, including those associated with skunks in California, foxes in Arizona and Texas, dogs in Mexico, and mongooses in Cuba and Puerto Rico (Nadin-Davis et al., 2006c). These North American viruses most likely arrived in the New World after being carried by domestic animals previously infected in the Old World. The disease could then have been transmitted by inter-specific spillover events to various wildlife species. While many spillover infections are epidemiological dead-ends, occasionally a spillover event results in a new virus-host association in which the disease is able to persist and spread. Evidence for such events is provided by many phylogenetic studies performed on viral collections from around the world (e.g., the emergence of fox rabies from a dog lineage in Brazil; Bernardi et al., 2005).

Raccoon Rabies Variant The raccoon rabies virus (RRV) variant appears to have emerged relatively recently, since surveillance records have only recognized this outbreak in Florida since the late 1940s (McLean, 1971). Later MAb studies conducted in the United States have identified the virus as a distinct type (Smith et al., 1984). This RRV variant appeared to be confined to Florida until the 1970s, when it was identified in West Virginia (Jenkins & Winkler, 1987). This inadvertent translocation of the disease was attributed to movement of infected hunting animals from Florida (Nettles et  al., 1979). Since then, this new outbreak (often termed the ­mid-Atlantic raccoon rabies

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of New York State, reflecting two distinct foci of infection that entered the area in the early 1990s. The western type was responsible for the first Ontario outbreak beginning in 1999 (Nadin-Davis et al., 2006b). Following the determination of the whole genome sequence of an Ontario RRV isolate (Szanto et al., 2008), extensive whole genome sequencing of a large collection of isolates from eastern North America has been achieved (Nadin-Davis et al., 2017b). These data have confirmed that cross-border virus spread was responsible for all Canadian incursions with the exception of the Hamilton outbreak which appears to have resulted from a long distance translocation of an infected animal (Trewby et al., 2017). These studies have also illustrated the impact of topographical features on disease spread (Nadin-Davis et al., 2018), information of value to control programs. Phylogenetically, the RRV variant is most closely related to the south central (SCSK) skunk variant known to circulate across much of the southern states of the United States and which is also quite distinct from the Canadian WSK variant (see Figure 29.2). Both the RRV and SCSK variants cluster closely with all American bat variants, an observation that has elicited the suggestion that both of these terrestrial variants may have emerged after spillover transmission of viruses from bat reservoirs. Alternatively, the raccoon variant may have emerged directly from the SCSK lineage.

associated with particular bat species (Nadin-Davis et al., 2001) as detailed below.

Viruses of Big Brown Bats The bat species most commonly reported as rabid in Canada is the big brown bat (Eptesicus fuscus) which has a range that extends across southern Canada (see Chapter 27). By antigenic typing, seven major viral types (designated BBCAN1–7), with some intra-type variation in binding to specific MAbs, were found to be associated with this species (Nadin-Davis et  al., 2001). Phylogenetic analysis of these same rabies viruses, as well as additional viral isolates, has identified one large group which was readily subdivided into two main subgroups (comprising types BB2 and BB3/4/5 respectively) while a second smaller group of viruses constituted a very distinct type (BB1) (Nadin-Davis et al., 2001, 2010). These genetic types reflect the principal antigenic groupings as illustrated in Figure 29.4. The later study, by Nadin-Davis et  al. (2010), examined a sufficiently large number of big brown bat viruses to determine the distribution of these viral types across the country. Indeed, three of these BB types (BB1, BB3, and BB4) were restricted in their range to western Canada and specifically to British Columbia in all but one case. The BB2 type was found only in eastern Canada (Ontario, Quebec, and Atlantic Canada) while the most recently emerged BB5 type was the most broadly distributed, from Ontario to British Columbia. Using Bayesian methods of analysis on dated samples for prediction of the year of emergence of these viral lineages, it was estimated that the viral progenitor that had given rise to all BB-associated viruses had circulated around 1573 (95% HPD 1338–1763) with emergence of the different types at various times thereafter. The BB5 type was estimated to have emerged in 1936 (95% HPD 1838–1939); however, the BB5a subtype (Figure 29.7), restricted in its range to Ontario, appeared to have emerged very recently, around 1991 (95% HPD 1972–1993), and may have been responsible for the increased rabies cases observed throughout the 1990s and into the early years of the 21st century. All but one of these viral types are known to have occurred in the United States; thus, cross-border incursion from the United States may be the original source of many, if not all, of these viruses. To explore the effect of the big brown bat population structure on the distribution of their associated rabies virus types across Canada, genetic studies on this host species were undertaken (Nadin-Davis et al., 2010). A set

Viruses Associated with Bat Species As described in Chapter 27, insectivorous bats of North America were only recognized as being rabies virus reservoirs in the 1950s. The first detection of rabies in a bat in Canada was reported in British Colombia (Avery & Tailyour, 1960), followed by the publication of several reports a few years later in Ontario (Beauregard & Stewart, 1964). Since then, our knowledge of the role of bat species in maintaining and transmitting the disease has increased substantially. Webster et al. (1986) used a panel of 43 anti-N MAbs to explore the diversity of bat-associated rabies viruses in Canada and identified four main antigenic profiles, designated B1 to B4, which were associated with certain bat species and exhibited some geographic localization. The situation was re-evaluated several years later using an extended collection of MAbs and genetic methods of virus characterization in which selected regions of the genome were sequenced. This later study identified significant virus diversity in which distinct viral variants were found to be

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hosts, hoary (L. cinereus) and red (L. borealis) bats, were identified as distinct variants that had evolved from a common ancestor (Nadin-Davis et  al., 2001, 2002). The viruses associated with silver-haired bats have also been recovered from at least two tri-coloured bats (Perimyotis subflavus), formerly known as eastern pipistrelle bats, in 2000 and 2001 (Figure 29.7). This finding is consistent with reports that this bat species is a reservoir for a variant closely related genetically with that of the silver-haired bat in the United States (Smith, 2002). The viruses associated with Myotis bat species are quite heterogeneous. Studies in which host (see section below on species identification) and viral genes were sequenced in parallel have revealed spatial clustering of certain viral variants (e.g., eastern and western types) and the association of particular variants with certain reservoir hosts (Nadin-Davis et al., 2017a). The limited distribution of several of these viral variants is due to the restricted ranges of some of these host species; thus, Myotis evotis appears to be an important reservoir in western Canada while Myotis lucifugus and Myotis septentrionalis are important in eastern Canada. Recent reductions in the numbers of Myotis bats submitted for rabies diagnosis in eastern Canada may be a result of the introduction and rapid spread in North America of white-nose syndrome, a fungal agent that is causing large-scale die-offs of certain bat populations (Frick et al., 2010). One notable observation from Figure 29.7, originally mentioned by Nadin-Davis et al. (2001), is that the phylogeny of the bat viruses appears to respect aspects of bat behaviour and migratory patterns. Both big brown and Myotis bats are considered to be non-migratory, although they do travel some distance between hibernacula and their summer roosts, such as maternity colonies; these bats can form reasonably large colonies. In contrast silver-haired and Lasiurine bats are solitary and migratory in nature and travel long distances between summer and winter ranges. With the exception of the BB1 type, all viruses associated with the non-migratory bats are genetically heterogeneous but form one large group (group I), which may have originated from a single viral progenitor. The viruses associated with the migratory bats form another distinct group (group II); these viruses are more genetically homogenous than those of group I (see Figure 29.7), though it is unclear if this is just an apparent difference resulting from more limited sampling of rabid migratory bats. The BB1 type clusters distinctly but more closely with group II viruses and may have emerged subsequent to a spillover infection by a progenitor related to group II viruses. Such events, in which new virus-host associations occasionally occur after spillover infections, are now well-

of microsatellite loci was used; these are sequences located throughout non-coding regions of the bat genome that comprise multiple short tandem repeats of variable repetitions. Because of the high level of mutation observed within these repetitive sequences, these loci are useful targets for sensitive investigation of the sub-population structure of a species (see Chapter 29). Microsatellite size screening was conducted on DNA extracted from a collection of big brown bats recovered from across Canada, and the resulting data were examined with a series of software tools designed to probe the species’ population structure. It was evident that two major populations existed: one in the east (Ontario, Quebec, and Atlantic Canada) and one in the west (BC to Saskatchewan), with, sadly, no specimens available from Manitoba in between. A second study that targeted the bat cytochrome oxidase subunit 1 (COX1) gene, a mitochondrial locus that is maternally transmitted and often used for species identification (see below), also identified two groups of bat populations but discriminated those of British Columbia from the bats recovered from the rest of Canada (Nadin-Davis et  al., 2010). When the conclusions of the COX1 and microsatellite studies were combined, it appeared that there were three groups of big brown bats distributed across the country: those in British Columbia, those in the western provinces of Alberta and Saskatchewan, and those in eastern Canada (east of Manitoba). Pronounced philopatry of female big brown bats was proposed as an important mechanism that prevented spread of bat populations from British Columbia to the east. The Rocky Mountain range that runs down the eastern side of the province may be a significant barrier to bat movements between British Columbia and the rest of Canada. These studies on host population structure may help to explain the distribution of many of the viral variants harboured by big brown bats (Nadin-Davis et al., 2010).

Viruses of Other Bat Species In Canada, apart from big brown bats, limited numbers of rabies-positive cases are regularly reported for a number of other bat species, and these bat species are considered important rabies reservoirs. Antigenic analysis has identified distinct viral types (shown in brackets) that are specifically associated with Lasiurus bats (LACAN), silver-haired bats (Lasionycteris noctivagans) (SHCAN) and several bat species of the Myotis genus (MYCAN) (Nadin-Davis et al., 2001), as illustrated in Figure 29.7. By phylogenetic methods, the viruses circulating in the two main Lasiurine

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Figure 29.7: A phylogenetic tree generated from an alignment of 430 bases of partial N gene sequence from 52 viral samples showing the diversity of rabies viruses that have circulated in Canada in recent times. Analysis was performed as described in the legend to Figure 29.5. Significant bootstrap values at major branch points are illustrated to the left of the branch. Vertical lines indicate the major lineages, clades, and groups of viruses predicted by the tree. Genetic groupings are indicated to the right of the dotted lines and antigenic nomenclature to the right of the solid lines. Samples presented in italics represent spillover events listed from top to bottom of the tree: 02N0238RAC, a raccoon from Montreal infected with the BBCAN3 (BB2) variant, 2002; HUBC2003, a human case infected with the MYCAN (MYO-WEST) variant from British Columbia, 2003; several specimens infected with the MYCAN (MYO-EAST) variant including: 98L2117DG, a dog from Alberta, 1998; 04N6533CAT, a cat from PEI, 2004; 93N9722FX, a fox from PEI, 1993; 05N5845FX, a fox from Ontario, 2005; 06N2456BB, a big brown bat from Ontario infected with the LACAN (HRB) variant; the SHCAN (SHB) variant was found in the following specimens: 79L1020LB, a little brown bat from Alberta in 1979; 09N2773RFX, a fox from Peterborough, ON, in 2009; HUPQ2000, a human case from Quebec, 2000; 04L414SK and 04L348SK, skunks from Stanley Park in Vancouver, 2004; HUAB2007, a human case from Alberta, 2007; specimen 06N1625RAC was a raccoon infected with the AFX variant from Ontario, 2006. Source: author.

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documented and appear to be the basis for virus-host switching that leads to new persistent epizootics (see below). Within the worldwide phylogeny of rabies viruses (Figure 29.5) those associated with bats of the Americas comprise a distinctive outlying lineage, often referred to as the American indigenous lineage (Nadin-Davis et al., 2002). Because of the relatively small number of bats indigenous to Canada, compared to those native to the United States and other parts of the Americas, the number of bat-associated rabies virus variants circulating in Canada is relatively limited when compared to the entire American continent, but they are in many respects representative of the variants that circulate in insectivorous bats. The relatively close genetic proximity of two terrestrial rabies virus variants, the raccoon and SCSK variants, to the American bat clade does suggest, as indicated above, a common ancestry of all these viruses.

rabies (Morimoto et  al., 1996). Based on the very small Canadian sample set, the same situation appears to hold true in Canada. The human case in 2012 was diagnosed in a male patient with recent travel history to the Dominican Republic (see Chapter 3b). The viral variant responsible was found by the author to be genetically closely related to other viruses originating from the Dominican Republic and Haiti, thus confirming this as an exogenously acquired case. Humans are by no means the only terrestrial species to which bat variants are transmitted. Since the institution of routine viral typing to all rabies-positive specimens, spillover infections from bats into other terrestrial species have been identified on several occasions. These cases were identified by antigenic typing and often confirmed by genetic analysis, the results of which are illustrated in Figure 29.7 for several notable examples, including the typing of the viruses in two positive foxes (in 1993) and a positive cat (in 2004) from PEI, which has no terrestrial rabies, to the MYO variant; a MYO variant from a dog in Alberta (in 1998); a group of skunks from Stanley Park in the heart of Vancouver (in 2004) that were infected with the SHB variant; and a raccoon from Montreal (in 2002) infected with a BB2 variant. The last observation, which confirmed the absence of the raccoon variant in Quebec, was notable in light of fears of an incursion of the raccoon variant from the United States, an event that was to occur three years later. In 2009 a red fox from eastern Ontario was infected with the SHB type and not the AFX variant, thereby supporting this area’s apparent freedom from the AFX variant since its elimination some years before (MacInnes et al., 2001). Through the use of an in situ hybridization (ISH) method applicable to formalin-fixed tissues as detailed in Chapter 23, other spillover events have been identified; for example, the presence of a MYO variant in a cat from Nova Scotia (in 2003), a SHB (SHCAN) variant in a horse from Nova Scotia (in 1992) and a BB2 (BBCAN2) variant in a horse from New Brunswick (in 1992). The last two identifications were made on archival material that had been stored for many years before the tools for viral typing on this type of specimen became available. This approach also confirmed the role of a MYO variant in the 2003 human case diagnosed posthumously.

The Role of Bats in Human and Animal Disease With the development of antigenic and genetic tools to identify viral variants and our improved knowledge of the identity of host reservoir species responsible for maintaining such variants, it has become possible to infer the host species responsible for exposures in cases of clinical rabies in non-reservoir species. In Canada such events were first documented in the 1980s when viral-typing tools became available (Webster et  al., 1987, 1989), and nowhere is this activity of greater interest than in the rare cases of human rabies reported in recent years. Between 1980 and 2017, five human cases were reported across the country (Table 29.2); these and earlier cases are described more fully in Chapter 3b of this book. Only antigenic methods were applied to the case in 1985 where the role of a ­bat-associated virus was supported and in agreement with the patient’s known contact with a bat weeks prior to disease onset. Genetic methods were key tools applied to the next four cases where availability of rabies-infected material from the patients did not always support antigenic methods of analysis. Figure 29.7 shows the phylogenetic evidence documenting that three of these cases were a result of infection with bat-associated variants, two from the s­ ilver-haired bat variant and one from a Myotis variant. The frequent involvement of the silver-haired bat variant in indigenously acquired human cases in the United States has been previously noted (Messenger et  al., 2002), and there has been some speculation that unique biological properties of this viral variant, including its ability to propagate at temperatures below those normally encountered in the body, may facilitate its growth in extremities of the body and explain its disproportionate role in causing human

Species Identification for Better Epidemiological Information Our knowledge of rabies epizootiology clearly depends on accurate identification of the host species of all rabiespositive specimens. In most cases specimens submitted for rabies diagnosis are readily assigned to host species 503

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Table 29.2  Viral variants responsible for five human rabies deaths in Canada, 1989 to 2017. Case designation Patient details

Rabies virus variant

Anecdotal evidence for bat contact HUPQ2000 HUBC2003 HUAB2007 HUON2012

Reference(s)

Bat (variant unknown) McLean et al., 1985; Webster et al., 1987 SHB Elmgren et al., 2002

12 year old boy, QC, 2000, family contact with bat documented Male, BC, 2003, diagnosed posthumously – no MYO known bat contact 73 year old male, AB, 2007, documented bat bite 6 SHB months before clinical symptoms developed Male, ON, 2012, Known travel to Dominican Republic Cosmopolitan lineage

Nadin-Davis et al., 2003a Johnstone et al., 2008; Nadin-Davis et al., 2009 unpublished data (author)

Source: author.

based on accompanying information or the morphology of the specimen. However, this is not always the case, especially for certain bat species. Their small size, phenotypic plasticity, and sometimes poor condition of the carcass can make species identification based on morphological traits very difficult. A study to explore the extent of species misidentification of bat specimens was undertaken at OLF. For each bat species that is regularly submitted to the CFIA for rabies testing, up to 10 specimens were collected from the rabies diagnostic groups at both Nepean and Lethbridge. DNA recovered from each carcass was used as a template for a process known as genetic barcoding, a tool developed and championed by Dr P. Hebert at the University of Guelph for species assignment (Hebert et  al., 2003). The method entails sequencing of a portion of the COX1 gene located on the mammalian mitochondrial genome. Comparison of sequence data from an unidentified specimen with a database of COX1 sequences generated from a large collection of vouchered species does in most cases allow assignment of the specimen to a species with high accuracy. When this approach was applied to a collection of bats compiled from diagnostic submissions from across Canada, it was found that a few bat species, particularly those of the Myotis genus, were frequently misidentified (Nadin-Davis et  al., 2012a). Such a finding clearly indicated a limitation in the acquisition of accurate information on the role of these bats as rabies reservoirs. More recent studies have employed this approach to clearly identify several Myotis species as rabies reservoirs (Nadin-Davis et al., 2017a), and the use of novel genetic methods, e.g. microarray technology, to enable rapid species identification has been explored (Lung et al., 2013). This would be particularly u ­ seful when the submission of a very limited amount of sample precludes accurate species assignment. Ultimately, such methods could eventually be extended to other species.

Future Issues The relative ease with which RNA viruses can mutate and potentially adapt to new environments means that rabies virus epizootics around the world are never static and are continually changing over time. Possible events that may change the future rabies landscape in Canada are listed below.

Expansion of Outbreaks to New Areas Expansion occurs constantly, with spread of known epizootics into new regions, such as the spread of AFX rabies from the north into southern Canada.

New Virus-Host Associations Although spillover infections to non-reservoir species rarely result in persistence and maintenance of the virus in its new host, such events do occur in exceptional circumstances. A recent example of this phenomenon is the emergence of a new epizootic in skunks in Flagstaff, Arizona, in which multiple spillovers of a big brown bat virus to skunks resulted in the establishment of this viral variant in this new terrestrial host with sustained intra-host transmission for several years (Leslie et al., 2006; Kuzmin et al., 2012). Indeed, such a phenomenon likely explains in retrospect how the cosmopolitan variant, which was probably originally maintained in the dog, became established in many different wildlife species around the world. Accordingly, it is essential to continue to undertake surveillance and monitoring of the rabies virus types responsible for disease. Detection of clusters of rabies cases in wildlife from variants not normally associated with that species, as for example the cases of SHCAN rabies in skunks in Stanley Park, Vancouver, could herald the emergence of a new virus-host association. Prompt attention to such events could prevent rabies outbreaks from becoming

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well established and thereby avoid long-term protracted efforts for eradication. The lack of control strategies for insectivorous bat rabies means that these mammals will remain a potential source of new terrestrial rabies epizootics for the foreseeable future.

of warming trends specifically on rabies reservoir hosts may include, but are not limited to the following: • Changes in arctic/red fox interactions with unknown consequences for the spread of rabies to southern ­Canada (Chapter 37). • Modified ranges of the raccoon and skunk reservoir hosts, thereby altering the distribution of their associated rabies variants. • Increased northern range of insects and thus insectivorous bat species giving rise to the potential for northwards spread of indigenous bat-associated rabies viruses, as well as the introduction of new bat species and their associated viruses.

Incursions of New Variants into Canada The incursion of new variants into Canada is best exemplified by the incursion of raccoon rabies northwards from the United States into Canada. While raccoon rabies persists south of the border, further incursions remain possible. In addition, incursions of other rabies virus variants remain a possibility. In particular the illegal movement of animals between countries could result in the introduction of exotic variants of rabies from anywhere in the world. This can lead to public health problems and has the potential to establish new rabies virus variants in Canadian wildlife. The maintenance of a collection of rabies and rabies-like viruses (all members of the Lyssavirus genus) at OLF has enabled antigenic and genetic characterization of many of the major viral lineages now known to circulate worldwide. This knowledge would enable rapid identification of rabies cases resulting from the introduction of an exotic variant.

Concluding Remarks Continued surveillance and rabies viral-typing activities will ensure that changes in the epizootiology of rabies in Canada are recognized early enough to allow proactive measures to be taken to protect public and animal health. Moreover, as control activities reduce or even eliminate incidence of rabies in terrestrial animals, the contribution of insectivorous bats as rabies reservoirs will proportionately increase, especially in the absence of any rabies control measures suitable for application to these reservoirs. One major factor that might mitigate this problem is whitenose syndrome, which, despite its very recent recognition, has had devastating impacts on populations of certain bat species in many locations in eastern North America (Frick et al., 2010); the impact of this epidemic on bats and their role as rabies reservoirs is yet to be determined.

Potential Effects of Climate Change The relatively large effects of climate change in northern Arctic regions will make Canada particularly susceptible to its consequences by impacting the distribution and ecology of pathogens and their hosts. The consequences

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Archives of Virology, 142(5), 979–992. https://doi.org/10.1007/s007050050133 Nadin-Davis, S. A., Sampath, M. I., Casey, G. A., Tinline, R. R., & Wandler, A. (1999). Phylogeographic patterns exhibited by Ontario rabies virus variants. Epidemiology and Infection, 123(2), 325–336. Nadin-Davis, S. A., Huang, W., Armstrong, J., Casey, G. A., Bahloul, C., Tordo, N., & Wandeler, A. (2001). Antigenic and genetic divergence of rabies viruses from bat species indigenous to Canada. Virus Research, 74(1–2), 139–156. https://doi.org/10.1016 /S0168-1702(00)00259-8 Nadin-Davis, S. A., Abdel-Malik, M., Armstrong, J., & Wandeler, A. I. (2002). Lyssavirus P gene characterisation provides insights into the phylogeny of the genus and identifies structural similarities and diversity within the encoded phosphoprotein. Virology, 298(2), 286–305. https://doi.org/10.1006/viro.2002.1492 Nadin-Davis, S. A., Sheen, M., & Wandeler, A. I. (2003a). Use of discriminatory probes for strain typing of formalin-fixed rabies virus-infected tissues by in situ hybridization. Journal of Clinical Microbiology, 41(9), 4343–4352. https://doi.org/10.1128 /JCM.41.9.4343-4352.2003 Nadin-Davis, S. A., Simani, S., Armstrong, J., Fayaz, A., & Wandeler, A. (2003b). Molecular and antigenic characterization of rabies viruses from Iran identified variants with distinct epidemiological origins. Epidemiology and Infection, 131(1), 777–790. https://doi .org/10.1017/S095026880300863X Nadin-Davis, S. A., Muldoon, F., & Wandeler, A. I. (2006a). Persistence of genetic variants of the arctic fox strain of rabies virus in southern Ontario. Canadian Journal of Veterinary Research, 70, 11–19. Retrieved from https://www.ncbi.nlm.nih.gov/ pubmed/16548327 Nadin-Davis, S. A., Muldoon, F., & Wandeler, A. I. (2006b). A molecular epidemiological analysis of the incursion of the raccoon strain of rabies virus into Canada. Epidemiology and Infection, 134(3), 534–547. https://doi.org/10.1017/S0950268805005108 Nadin-Davis, S. A., Torres, G., de los Angeles Ribas, M., Guzman, M. R., Cruz de la Paz, R., Morales, M., & Wandeler, A. (2006c). A molecular epidemiological study of rabies in Cuba. Epidemiology and Infection, 134(6), 1313–1324. https://doi.org/10.1017 /S0950268806006297 Nadin-Davis, S. A., Turner, G., Paul, J. P. V., Madhusudana, S. N., & Wandeler, A. (2007). Emergence of arctic-like rabies lineage in ­India. Emerging Infectious Diseases, 13(1), 111–116. https://doi.org/10.3201/eid1301.060702 Nadin-Davis, S. A., Muldoon, F., Whitney, H., & Wandeler, A. I. (2008). Origins of the rabies viruses associated with an outbreak in Newfoundland during 2002–2003. Journal of Wildlife Diseases, 44(1), 86–98. https://doi.org/10.7589/0090-3558-44.1.86 Nadin-Davis, S. A., Sheen, M., & Wandeler, A. I. (2009). Development of real-time reverse transcriptase polymerase chain reaction methods for human rabies diagnosis. Journal of Medical Virology, 81(8), 1484–1497. https://doi.org/10.1002/jmv.21547 Nadin-Davis, S. A., Feng, Y., Mousse, D., Wandeler, A. I., & Aris-Brosou, S. (2010). Spatial and temporal dynamics of rabies virus variantsin big brown bat populations across Canada: Footprints of an emerging zoonosis. Molecular Ecology, 19(10), 2120–2136. https:// doi.org/10.1111/j.1365-294X.2010.04630.x Nadin-Davis, S. A., Guerrero, E., Knowles, M. K., & Feng, Y. (2012a). DNA barcoding facilitates bat species identification for improved surveillance of bat-associated rabies across Canada. The Open Zoology Journal, 5(Suppl. 1-M5), 27–37. Retrieved from https:// benthamopen.com/contents/pdf/TOZJ/TOZJ-5-27.pdf Nadin-Davis, S. A., Sheen, M., & Wandeler, A. I. (2012b). Recent emergence of the Arctic rabies virus lineage. Virus Research, 163(10), 352–362. https://doi.org/10.1016/j.virusres.2011.10.026 Nadin-Davis, S., Alnabelseya, N., & Knowles, M. K. (2017a). The phylogeography of Myotis bat-associated rabies viruses across Canada. PLoS, 11(5), e0005541. https://doi.org/10.1371/journal.pntd.0005541 Nadin-Davis, S.A., Colville, A., Trewby, H., Biek, R. & Real, L. A. (2017b). Application of high-throughput sequencing to whole rabies viral genome characterisation and its use for phylogenetic re-evaluation of a raccoon strain incursion into the province of Ontario. Virus Research, 232, 123–133. https://doi.org/10.1016/j.virusres.2017.02.007 Nadin-Davis, S. A., Fu, Q., Trewby, H., Biek, R., Johnson, R. H., & Real, L. (2018). Geography but not alternative host species explain the spread of raccoon rabies virus in Vermont. Epidemiology and Infection, 146, 1977–1986. https://doi.org/10.1017/S0950268818001759 Nettles, V. F., Shaddock, J. H., Sikes, R. K., & Reyes, R. C. (1979). Rabies in translocated raccoons. 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Ecology and Epizootiology of Wildlife Rabies Real, L. A., Henderson, J. C., Biek, R., Snaman, J., Jack, T. L., Childs, J. E., ... Nadin-Davis, S. (2005). Unifying the spatial population ­dynamics and molecular evolution of epidemic rabies virus. Proceedings of the National Academy of Sciences USA, 102(34), 12107–12111. https://doi.org/10.1073/pnas.0500057102 Rosatte, R., Donavan D., Allan, M., Howes, L.-A., Silver, A., Bennett, K., ... Radford, B. (2001). Emergency response to raccoon rabies introduction into Ontario. Journal of Wildlife Diseases, 37(2), 265–279. https://doi.org/10.7589/0090-3558-37.2.265 Smith, J. S. (2002). Molecular epidemiology. In A. C. Jackson & W. H. Wunner (Eds.), Rabies (pp. 79–111). New York, NY: Academic Press Inc. Smith, J. S., Sumner, J. W., Roumillat, L. F., Baer, G. M., & Winkler, W. (1984). Antigenic characteristics of isolates associated with a new epizootic of raccoon rabies in the United States. Journal of Infectious Diseases, 149(5), 769–774. https://doi.org/10.1093/infdis /149.5.769 Smith, J. S., Orciari, L. A., Yager, P. A., Seidel, H. D., & Warner, C. K. (1992). Epidemic and historical relationships among 87 rabies v­ irus isolates as determined by limited sequence analysis. Journal of Infectious Diseases, 166(2), 296–307. https://doi.org/10.1093/infdis /166.2.296 Szanto, A. G., Nadin-Davis, S. A., & White, B. N. (2008). Complete genome sequence of a raccoon rabies virus isolate. Virus Research, 136(1–2), 130–139. https://doi.org/10.1016/j.virusres.2008.04.029 Szanto, A. G., Nadin-Davis, S. A., Rosatte, R. C., & White, B. N. (2011). Genetic tracking of the raccoon variant of rabies virus in ­eastern North America. Epidemics, 3(2), 76–87. https://doi.org/10.1016/j.epidem.2011.02.002 Tinline, R. R., & MacInnes, C. D. (2004). Ecogeographic patterns of rabies in southern Ontario based on time series analysis. Journal of Wildlife Diseases, 40(2), 212–221. https://doi.org/10.7589/0090-3558-40.2.212 Trewby, H., Nadin-Davis, S. A., Real, L. A., & Biek, R. (2017). Processes underlying rabies virus incursions across US–Canada border as revealed by whole-genome phylogeography. Emerging Infectious Diseases, 23(9), 1454–1461. https://dx.doi.org/10.3201 /eid2309.170325. Wandeler, A. I., & Salsberg, E. (1999). Raccoon rabies in eastern Ontario. Canadian Veterinary Journal, 40, 731. Retrieved from https:// www.ncbi.nlm.nih.gov/pmc/articles/PMC1539819/pdf/canvetj00143-0045.pdf Webster, W. A., Casey, G. A., Charlton, K. M., & Wiktor, T. J. (1985). Antigenic variants of rabies virus in isolates from eastern, central and northern Canada. Canadian Journal of Comparative Medicine, 49, 186–188. Retrieved from https://www.ncbi.nlm.nih.gov/pubmed /3893660 Webster, W. A., Casey, G. A., & Charlton, K. M. (1986). Major antigenic groups of rabies virus in Canada determined by anti-nucleocapsid monoclonal antibodies. Comparative Immunology, Microbiology and Infectious Diseases, 9(1), 59–69. https://doi.org/10.1016/0147 -9571(86)90076-7 Webster, W. A., Casey, G. A., Charlton, K. M., Sayson, R. C., McLaughlin, B., & Noble, M. A. (1987). A case of human rabies in western Canada. Canadian Journal of Public Health, 78, 412–413. Retrieved from https://www.jstor.org/stable/41990509 Webster, W. A., Casey, G. A., & Charlton, K. M. (1989). Bat-induced rabies in terrestrial mammals in Nova Scotia and N ­ ewfoundland. Canadian Veterinary Journal, 30, 679. Retrieved from https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1681141/pdf/canvetj00561 -0069a.pdf

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30 Understanding Host Dynamics: Applications of Molecular Ecology Cathy I. Cullingham Carleton University, Ontario, Canada

Introduction The use of molecular methods in understanding rabies dynamics in Canada has a long history. Diagnostic methods and sequencing of the virus have led to a greater understanding of how the virus is structured and among which populations it is transmitted, as described in Chapter 29 (Nadin-Davis). These applications have always focused on the virus, with very little attention given to the host. Historically, this probably stems from a lack of appropriate methods available to apply to host populations. However, with the rise in molecular ecology and landscape genetics, there has been an increased focus on host populations (Nadin-Davis et al., 2010; DeYoung et al., 2009; Root et al., 2009; Cullingham et al., 2008a, 2009). Molecular ecology is the application of population genetics and molecular phylogenetics to questions in ecology; examples include assessing diversity, defining species and subspecies, assigning parentage, and understanding dispersal and population connectivity (Freeland et al., 2011). Applications characterize the diversity of the deoxyribonucleic acid (DNA) in a portion of the genome or organelle genome of an individual or a population of individuals. Historically allozymes (protein variants) were characterized, but as technology and knowledge have advanced, we have been able to look at variations at the DNA sequence level. Many applications today make use of either microsatellites or single nucleotide polymophisms (SNPs), which are both co-dominant markers, where there are two alleles, one from each parent (Figure 30.1).

Landscape genetics is an extension of molecular ecology where genetic population structure is related to geographic and environmental attributes that may be the cause of the structure while accounting for the species biology (Manel et  al., 2003; Storfer et  al., 2007). With improved methodological frameworks and access to technologies comes an ability to learn about individuals, populations, and how they interact. To understand how we can use these advanced molecular methods to investigate questions of ecological importance, consider the simple example in Figure 30.2. Here, a river restricts the movement of a species, allowing for population differentiation; however, there are some opportunities for movement and migration across the river. Using a sufficient number of molecular markers, such as microsatellites or SNPs, would allow us to detect these migrants.

Figure 30.1: Microsatellites are simple sequences of two to six base pairs. The number of repeats can differ within and between individuals. Here, Ind. A is a homozygote for a five AT repeat, while Ind. B is a heterozygote for seven and three AT repeats. An SNP is a single base pair change. Ind. A is a homozygote for the A allele, while Ind. B is a heterozygote for the A and C alleles. The lines represent conserved sequences that allow us to characterize the repeat using the polymerase chain reaction. Source: illustration prepared by the author.

Ecology and Epizootiology of Wildlife Rabies

Figure 30.2: In panel A, a population becomes separated into two populations by the formation of a large river. Over time (panel B) the genetic composition of these populations changes in different directions because of selection and drift. Anthropogenic changes (the bridge in this illustration) result in the opportunity for dispersal across the river (panel C). With additional dispersal and mating, the genetic lineages mix (panel D). We can use microsatellite genotyping (or other methods of genetic analysis) to determine the genetic population structure and infer the processes. In panel A there is one genetic population, and genetic analysis would show one genetic population, with most variation between individuals. In panel B the river has restricted dispersal and gene flow. Over time this has resulted in two genetic populations; therefore, if we were to characterize them genetically, we would find different variations (or different frequencies of those variations) on each side of the river, distinguishing them as two populations. In panel C the bridge has allowed for dispersal, and a genetic analysis in this situation would detect two populations and identify migrants on each side of the river. In panel D the dispersal across the river has allowed for breeding between the two populations, and genetic analysis would find two populations with a large proportion of admixed individuals. Source: illustration prepared by the author.

Knowing the movement of a host species can be extremely useful for managing a disease (Hess et al., 2002; Sterner & Smith, 2006). For instance, if there is a disease spreading across the spatial distribution of a species, we can use landscape genetics to assess the spread probability given the dispersal patterns of the host. As well, an understanding of their dispersal capability can contribute to the development of control strategies by knowing when animals move and how far they move. Understanding population histories can also contribute, where the host may comprise different historical lineages and potentially exhibit differences in the response to disease. This chapter explores some examples

of how these methods have been applied to rabies research and how, in this context, Canada has been a leader in using these methodologies. Finally, the chapter briefly discusses new advances in the field and how these can further contribute to our understanding and managing of rabies spread.

Phylogeography Phylogeography looks at the historical processes that resulted in the geographic distribution of species

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genealogical lineages (Avise, 2000). Through analysing either host or disease populations within this framework, we can gain insight into disease dynamics. If populations of host species have been separated in the past, it is possible that they have different evolutionary trajectories and therefore may respond differently to disease. For instance, Cullingham et al. (2008b) used a phylogeographic approach to investigate the subspecies designation of raccoons across eastern and portions of central North America to determine if lineage diversification existed and what impacts that would have on rabies management. Based on morphological classification of raccoons (Hall, 1981; Goldman, 1950), four subspecies of raccoon exist within the range studied by Cullingham and her colleagues. However, their analyses of these subspecies using mitochondrial (mt)

DNA found limited support for these designations, with only one lineage showing geographic isolation in Florida (Procyon lotor elucus) and considerable mixing of lineages across the rest of the range, with the exception of some evidence of restricted gene flow across the Mississippi River (Figure 30.3). These results complement observations made by other researchers. First, rabies epizootics in Florida are smaller, less frequent, and not as well defined compared to epizootics in more northerly states along the eastern coast of North America (Childs et al., 2001). This, coupled with the geographic isolation of the raccoon lineage in Florida, suggests that dispersal is limited and, therefore, plays a lesser role in rabies dynamics in that state. Second, the Appalachian Mountain ridge, often cited as a barrier to rabies spread

Figure 30.3: Map of central and eastern North America illustrating the three raccoon (Procyon lotor) lineage groups identified using mtDNA sequence data. The first group is primarily restricted to Florida (▲), the second (●) is to the west of the Mississippi River (highlighted in black for reference), and the third are (○) cover the majority of eastern North America. Source: Reprinted from Cullingham et al. (2008) with permission from NRC.

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(Slate et al., 2005), did not correspond to limited mtDNA gene flow, which is consistent with the later findings of Root et al. (2009) who investigated the effects of ridges and valleys in Pennsylvania. The only landscape feature that was consistent with reduced dispersal was the Mississippi River. These results highlight the need for managers to be cognizant of the risks for westward spread across the Appalachians and to identify a potential river barrier that could be used if spread were to continue westward. Phylogeographic inference can also provide insight into transmission dynamics. Nadin-Davis et  al. (2010) found contrasting patterns between the phylogeographic and population genetic structure of big brown bats that allowed them to make inferences regarding transmission of different viral variants. In their analysis they found strong evidence of female philopatry (individuals that breed near their place of birth) and long distance male dispersal. As well they found that there were five different lineages of rabies virus; four of these were very geographically restricted while the fifth was geographically widespread (see Chapter 29). The author concluded that the geographically restricted lineages were likely associated with transmission within the nurseries and reflected the female philopatric structure, whereas the fifth lineage was transmitted by dispersing males. Knowing that there are different transmission patterns is useful for targeted management of rabies spread among and within bat populations.

analysed). Using these data, they were able to generate a dispersal distribution for each area. Based on the distribution a large majority of offspring moved less than 1 kilometre, but a small portion moved upwards of 20 kilometres. These data have obvious implications for management and identify the distances at which disease-founding events could occur. To understand more about the dispersal behaviours in raccoons, Cullingham et  al. (2008a) also looked at the relationship between genetic relatedness and geographic distance, similar to an autocorrelation analysis (Fortin & Dale, 2005) for each age-sex class (adult male, adult female, juvenile male, juvenile female). Here they found that adult females, and juvenile females and males were significantly more genetically related than by chance at distances up to three kilometres, suggesting female philopatry and kin structure. Given these samples were primarily collected in the fall indicates that many male juveniles potentially disperse in the spring. Any baiting programs aimed at inoculating dispersive raccoons should consider this as a peak dispersal time. Both the distribution of dispersal distances and the autocorrelation analysis indicated the majority of movements were less than three kilometres, making this an appropriate distance for the population-infection-control programs as described in Chapter 10. Estimates of individual-based dispersal are necessary for effective disease management, but factors affecting population level movements can also be an important contribution. Using a landscape genetic approach, Cullingham et al. (2009) investigated population connectivity of raccoon populations in the Niagara and St Lawrence regions in Ontario and New York to assess the proportion of migration occurring across these two rivers. These areas are extremely important as they present the only direct opportunities for rabies spread into Ontario from New York. Their analysis of population structure identified two populations corresponding to the Ontario and New York sides of the Niagara River but no population structure across the St Lawrence River. This was an interesting finding since rabies incidence was correlated with this, where there had been a number of rabies incursions in the Ontario side of the St Lawrence, yet none across the Niagara River despite longer rabies prevalence in New York in the Niagara region. This study highlighted an important barrier to use for rabies control but a geographic feature that did not consistently represent a barrier to dispersal, suggesting additional factors could be contributing to these differences (Rees et al. 2009). As a result, managers will not be able to make assumptions about the permeability of landscape features without empirical evaluation.

Population Genetics Dispersal is a key behaviour that will determine the spread of disease (Anderson & May, 1978; Coyne et  al., 1989; Macdonald & Laurenson, 2006) and what management scenarios are going to be most effective for disease control and eradication, yet this parameter is extremely difficult to measure, especially when considering both distance and frequency. While this can be measured in the field using either capture-mark-recapture or telemetry/radiotracking, both methods have limitations. These include practical restrictions on study size and sample size, and ascertainment bias (Koenig et al., 1996; Proctor et al., 2004; Ogutu et al., 2006). To overcome these issues, Cullingham et  al. (2008a) used molecular parentage assignment to assess the dispersal of raccoon offspring. They analysed a large number of individuals from two different populations with a sufficient number of microsatellite markers to be able to resolve mother-offspring relationships (e.g. offspring will share at a minimum one allele with their parent at every microsatellite

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Discussion

More recently Paquette et al. (2014) used a landscape genetic approach to identify the most likely pathway of raccoon rabies spread in southern Quebec by examining two different hosts of the rabies vector, raccoons and skunks. They incorporated circuit theory (McRae, 2006), which views the landscape as a surface where features are assigned different levels of electrical resistance. This model of movement is a better predictor of how animals move on the landscape, provided resistance surfaces are optimized (McRae & Beier, 2007). While they did not find significant landscape barriers to overall movement of raccoons, the application of circuit theory demonstrated the potential routes of transmission, which provides wildlife managers a prediction of spread in variable landscapes.

The research discussed in this chapter demonstrates the broad utility of molecular ecology in understanding host dynamics and how this can contribute to rabies control. This approach has provided insight into processes that would not have been possible with field studies alone. For instance, the logistics, time, and effort involved in measuring dispersal across a large geographic feature, such as the Niagara River, would be too prohibitive to attempt. As well, a detailed dispersal distribution that includes enough samples to account for distances and frequencies would again require considerably more effort if we were to rely on capture-mark-recapture. However, the contributions from the field to the examples here are invaluable in interpreting and understanding the results obtained. For example, knowing the age class was an important component to the dispersal study; without this information having been collected from the field, there would be no way to identify the important differences between male adults and juveniles. Based on the findings presented in this chapter, there are additional areas for investigation. The phylogeographic analysis of raccoon subspecies identified strong mtDNA structuring in Florida, which suggests there may be different population dynamics here, such as strong female philopatry or reduced dispersal overall. Whatever these factors are, they might be driving the differences in temporal and spatial spread of rabies; therefore, identifying these could provide valuable insight for accurate disease modelling and effective management. Phylogeographic analysis of the raccoon suggests that the Mississippi River did act as a semi-permeable barrier to gene flow, similar to the analysis of the Niagara River, yet the St Lawrence River was not a major barrier. Rees et al. (2009) modelled the population dynamics of raccoons in this region and found the landscape constriction contributed to the structure found in Niagara. While this does not explain why the Mississippi River acts as a barrier, it does indicate that there are different landscapes that will restrict raccoon movement; however, they are not consistent and will need to be investigated before managers can assume their permeability. In terms of management, some results can be directly applied and others can be used in developing accurate models to assess spread risk (see Chapters 23 and 24d). Dispersal results can be directly applied to management. Both the dispersal distribution and the spatial autocorrelation analyses demonstrated that three kilometres was a critical distance for raccoons and is an appropriate minimum distance to use for infection control, while

Functional Genetics The above studies have been looking at what is considered neutral genetic variation, which simply means that no selection is acting on the frequencies of genetic variants; they are affected only by population processes such as immigration, drift, and mutation (Hedrick, 2005). Because rabies causes reduced fitness of the host, primarily through mortality, there is the potential for selection of more resistant genotypes, if they exist. Recently, Castillo et al. (2010) characterized a locus of the major histocompatibility complex (MHC) in raccoons and found the locus was duplicated and exhibited very high diversity (66 variants among 264 individuals). This region is important for immune response and antigen binding: if there are variants in the raccoon populations that can effectively recognize rabies and mount an immediate immune response, then these individuals will survive and increase the proportion of resistant alleles in the population. Based on this, Srithayakumar et al. (2011) extended the work of Castillo et  al. (2010) and characterized raccoon populations with varied exposure times to the rabies virus (e.g., 10, 20, 40, and more than 70 years). They found evidence of positive selection suggestive of a rapidly evolving region, and more importantly they found associations of susceptibility and resistance to rabies in this region. Given their limited sampling size, some of these were weak associations and increased sampling should increase the associations they did find. Knowing the alleles that are associated with the disease can be very beneficial for predicting the likelihood of spread to new areas, and the impact that spread would have on novel populations.

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upwards of 20 kilometres should be considered for the maximum. Estimates of landscape permeability can be used in modelling to assess the risk of spread of rabies into a novel environment (Rees et al., 2008) without control and with different control scenarios, which will allow for the development of control plans that maximize efficiency and resources while minimizing risk. Defining functional variation that is associated with disease within the genome can make important contributions to developing accurate spread-risk models. Knowing what alleles exhibit decreased or increased disease risk and their allele frequencies in the populations at risk of rabies exposure can help to determine the rate of transmission and levels of population mortality. The contributions that have been made to our understanding of rabies transmission and spread are invaluable in our continued efforts to improve control strategies and management options. Canada has been at the forefront in applying molecular ecological methodology to understand more about the host populations and how their population demographics affect rabies spread and persistence. Since the work of Cullingham et al. (2008a, 2009), the use of molecular ecology to study host populations, including raccoon (Dharmarajan et al., 2009; Root et al., 2009; Côté et al., 2012; Paquette et al., 2014), fox (DeYoung et al., 2009), skunk (Talbot et al. 2012), and bat (Nadin-Davis et al., 2010; Smith et al., 2011) has increased. As well, review articles have addressed the way forward for disease research

and focused on the use of molecular ecology (Archie et al., 2008; Biek & Real, 2010, Fitak et al. 2019).

Future Directions The field of molecular ecology has been rapidly changing with increasing access to data and improved models for analysis. One recent breakthrough has been advances in sequencing technology with the advent of a number of next-generation sequencing (NGS) methods (Mardis, 2008; see Chapter 29). These technologies are giving average research labs access to whole genome sequence data for non-model organisms at reasonable costs (Mardis, 2008; Ekblom & Galindo, 2011). These data can be used in multiple ways. First, functional variation in genes important to disease susceptibility and risk can be identified using a genome-wide association approach (GWAS; e.g. Fitak et al. 2019). Identification of genetic variants that are associated with disease can be used to understand the susceptibility of vulnerable populations, and may also provide a deeper understanding of an organism’s response to the disease. This information could then be used to better understand human etiology for developing new approaches to prevention/treatment (Videvall et al. 2015). Finally, being able to assess thousands of loci throughout the genome would provide increased resolution to be used for investigating landscape genetics.

References Anderson, R. M., & May, R. M. (1978). Regulation and stability of host-parasite populations interactions. I. Regulatory processes. ­Journal of Animal Ecology, 47(1), 219–247. https://doi.org/10.2307/3933 Archie, E. A., Luikart, G., & Ezenwa, V. O. (2008). Infecting epidemiology with genetics: A new frontier in disease ecology. Trends in Ecology and Evolution, 24(1), 21–30. https://doi.org/10.1016/j.tree.2008.08.008 Avise, J. C. (2000). Phylogeography: The history and formation of species. Cambridge, MA: Harvard University Press. Biek, R., & Real, L. A. (2010). The landscape genetics of infectious disease emergence and spread. Molecular Ecology, 19(17), 3515–3531. https://doi.org/10.1111/j.1365-294X.2010.04679.x Castillo, S., Srithayakumar, V., Meunier, V., & Kyle, C. J. (2010). Characterization of major histocompatibility complex (MHC) DRB Exon 2 and DRA Exon 3 fragments in a primary terrestrial rabies vector (Procyon lotor). PLoS ONE, 5(8), e12066. https://doi.org /10.1371/journal.pone.0012066 Childs, J. E., Curns, A. T., Dey, M. E., Real, L. A., Rupprecht, C., & Krebs, J. (2001). Rabies epizootics among raccoons vary along a north-south gradient in the eastern United States. Vector Borne and Zoonotic Disease, 1(4), 253–267. https://doi.org/10.1089 /15303660160025895 Côté, H., Garant, D., Robert, K., Mainguy, J., & Pelletier F. (2012). Genetic structure and rabies spread potential in raccoons: The role of landscape barriers and sex-biased dispersal. Evolutionary Applications, 5(4), 393–404. https://doi.org/10.1111/j.1752-4571.2012.00238.x Coyne, M. J., Smith, G., & McAllister, F. E. (1989). Mathematic model of the population biology of rabies in raccoons in the m ­ id-Atlantic States. American Journal of Veterinary Research, 50, 2148–2154. Retrieved from https://www.ncbi.nlm.nih.gov/pubmed/2610445

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R., Moore, G., Honeycutt, R., & Root, J. J. (2009). Landscape-genetic analysis of population structure in the Texas gray fox oral rabies vaccination zone. Journal of Wildlife Management, 73(8), 1292–1299. https://doi.org/10.2193/2008-336 Dharmarajan, G, Beasley, J. C., Fike, J. A., & Rhodes, O. E. (2009). Population genetic structure of raccoons (Procyon lotor) inhabiting a highly fragmented landscape. Canadian Journal of Zoology, 87(9), 814–824. https://doi.org/10.1139/Z09-072 Ekblom, R., & Galindo, J. (2011). Applications of next generation sequencing in molecular ecology of non-model organisms. Heredity, 107(1), 1–15. https://doi.org/10.1038/hdy.2010.152 Fitak, R. R., Antonides, J. D., Baitchman, E. J., Bonaccorso, E., Braun, J., Kubiski, S., ... Pecon-Slattery, J. (2019). The expectations and challenges of wildlife disease research in the era of genomics: Forecasting with a horizon scan-like exercise. Journal of Heredity, 110(3), 261–274. Retrieved from https://evogentas.files.wordpress.com/2019/05/fitak-et-al-2019.pdf Fortin, M. J., & Dale, M. R. T. (2005). Spatial analysis: A guide for ecologists. Cambridge, England: Cambridge University Press. Freeland, J. R., Kirk, H., & Peterson, S. D. (2011). Molecular Ecology (2nd ed.). West Sussex, England: John Wiley & Sons. Goldman, E. A. (1950). Raccoons of the North and Middle America. Washington, DC: United States Government Printing Office. Hall, E. R. (1981). The mammals of North America (2nd ed.). New York, NY: John Wiley & Sons. Hedrick, P. W. (2005). Genetics of populations (4th ed.). Sudbury, MA: Jones and Bartlett Publishers. Hess, G. R., Randolph, S. E., Arneberg, P., Chemini, C., Furlanello, J., Harwood, J., ... Swinton, J. (2002). Spatial aspects of disease ­dynamics. In P. J. Hudson, A. Rizooli, B. Grenfell, H. Heesterbeek, & A. Dobson (Eds.), The ecology of wildlife diseases (pp. 102–118). New York, NY: Oxford University Press. Macdonald, D. W., & Laurenson, M. K. (2006). Infectious disease: Inextricable linkages between human and ecosystem health. B ­ iological Conservation, 131(2), 143–150. https://doi.org/10.1016/j.biocon.2006.05.007 Manel, S., Schwartz, M. K., Luikart, G., & Taberlet, P. (2003). Landscape genetics: Combining landscape ecology and population genetics. Trends in Ecology and Evolution, 18(4), 189–197. https://doi.org/10.1016/S0169-5347(03)00008-9 Mardis, E. R. (2008). The impact of next-generation sequencing technology on genetics. Trends in Genetics, 24(3), 133–141. https:// doi.org/10.1016/j.tig.2007.12.007 McRae, B. H. (2006). Isolation by resistance. Evolution, 60(8), 1551–1561. https://doi.org/10.1554/05-321.1 McRae, B. H., & Beier, P. (2007). Circuit theory predicts gene flow in plant and animal populations. Proceedings of the National ­Academy of Sciences of the United States of America, 104(50),19885–19890. https://doi.org/10.1073/pnas.0706568104 Nadin-Davis, S. A., Feng, Y., Mousse, D., Wandeler, A. I., & Aris-Brosou, S. (2010). Spatial and temporal dynamics of rabies virus ­variants in big brown bat populations across Canada: Footprints of an emerging zoonosis. Molecular Ecology, 19(10), 2120–2136. https://doi.org/10.1111/j.1365-294X.2010.04630.x Paquette, S. R., Talbot, B., Garant, D., Mainguy, J., & Pelletier, F. (2014). Modelling the dispersal of the two main hosts of the raccoon rabies variant in heterogenous environments with landscape genetics. Evolutionary Applications, 7(7), 734–749. https://doi. org/10.1111/eva.12161 Rees, E. E., Pond, B. A., Cullingham, C. I., Tinline, R. R., Ball, D., Kyle, C., & White, B. (2008). Assessing a landscape barrier using genetic simulation modelling: Implications for raccoon rabies management. Preventative Veterinary Medicine, 86(1–2), 107–123. https://doi.org/10.1016/j.prevetmed.2008.03.007 Rees, E. E., Pond, B. A., Cullingham, C. I., Tinline, R. R., Ball, D., Kyle, C., & White, B. (2009). Landscape modelling spatial bottlenecks: Implications for raccoon rabies disease spread. Biology Letters, 5(3), 387–390. https://doi.org/10.1098/rsbl.2009.0094 Root, J. J., Puskas, R. B., Fischer, J. W., Swope, C. B., Neubaum, M., Reeder, S., & Paggio, A. (2009). Landscape genetics of raccoons (Procyon lotor) associated with ridges and valleys of Pennsylvania: Implications for oral rabies vaccination programs. Vector-Borne and Zoonotic Diseases, 9, 583–588. https://doi.org/10.1089/vbz.2008.0110 Slate, D., Rupprecht, C. E., Rooney, J. A., Donovan, D., & Lein, D., & Chipman, R. (2005). Status of oral rabies vaccination in wild ­carnivores in the United States. Virus Research, 111(1), 68–76. https://doi.org/10.1016/j.virusres.2005.03.012 Smith, G. C., Aegerter, J. N., Allnutt, T. R., MacNicoll, A. D., Learmount, L., Hutson, A. M., & Aterby, H. (2011). Bat p ­ opulation genetics and Lyssavirus presence in Great Britain. 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PART 7

Prevention and Management of Rabies in Domestic Animals and Humans

Overview The chapters in Part 7 examine how various federal and provincial or territorial agencies manage to prevent and control rabies. Canada is an example of a federal structure where both the federal and the provincial or territorial (state, region, district, etc.) levels of government have responsibility for similar and often conflicting roles in the management of a program. Historically, the major distinction between these levels of government in rabies management in Canada has been that the federal role concentrated on rabies in domestic animals while the provincial and territorial role focused on treating and preventing rabies in humans. Historically, the major federal agency was Agriculture Canada (now the Canadian Food Inspection Agency or CFIA), and at the provincial and territorial level, the major agencies dealing with rabies tend to be associated with public health and wildlife. The response to rabies could not be neatly compartmentalized, so, over time, the roles and responsibilities of federal and provincial agencies have become intertwined. To make clear the structure of rabies management in Canada before 2014, Chapter 31 examines (1)  how each of the two major federal agencies discussed in Part 2 of this book (CFIA and PHAC) handle their mandates to manage or prevent incidents of rabies in domestic animals and humans; and (2) how the reporting and treatment aspects of rabies management have become interlinked among federal and provincial and territorial agencies. As an example, Chapter 32 discusses Ontario to demonstrate how a provincial or territorial public health responds to the reporting, treatment and prevention of rabies. Provincial and territorial health responses to rabies outbreaks in provinces and territories other than Ontario are discussed in the chapters in Part 3. Chapter 33 extends the comparison of federal and provincial or territorial agency roles by discussing the communications strategies employed at each level of government to inform the public and other agencies about the nature of rabies, treatment options, and preventive measures. Once again, Ontario serves as the example for response at the provincial and territorial level. Chapter 34, the final chapter in this Part, examines the costs involved in managing rabies at the federal and provincial or territorial levels. Given the complicated and interlinked

Prevention and Management of Rabies in Canada

organizational structures dealing with rabies, this is a daunting task. Chapter 34 attempts this by concentrating on Ontario, the province with the largest number of rabies cases in Canada and the leader among provinces and territories in terms of developing wildlife control programs, the major contributor to the costs of rabies management in Canada. Chapter 34 further limits the scope of its enquiry by dealing solely with the three agencies that contributed the most resources to rabies management in Ontario: the CFIA, the Ontario Ministry of Health (MOH), and the Ontario Ministry of Natural Resources (OMNR, now OMNRF). The results are surprising. Even with generous allowances for cost estimates within the examined agencies and for additional costs in other agencies, rabies control in Canada costs less than one dollar per citizen per year.

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31 Prevention and Management in Domestic Animals David J. Gregory Canadian Food Inspection Agency (Retired), Ottawa, Ontario, Canada

Introduction The great economic value of veterinary preventive medicine is receiving each year a more full and appreciative recognition by the governments of all civilized countries, and it behoves us, living as we do, in a country rich in flocks and herds to see that our system is modern and our service efficient. – Report of the Veterinary Director General (1904, pp. 55–56)

From its genesis as the Dominion’s Bureau of Agriculture in the 1800s, Agriculture Canada’s (now the Canadian Food Inspection Agency or CFIA) mission has always been that of disease prevention and control for domestic animals and reducing the probability of human exposure to potentially diseased animals. This was predicated on the British, European, and American settlers and their animals arriving in Canada. They had the potential to bring diseases such as hog cholera, Glanders, dourine, tuberculosis, and bovine contagious pleuro-pneumonia with them. These diseases were controlled to an extent by the act of 1865 to prevent the import of animals with disease. This was followed by the Contagious Diseases of Animals Act of 1869 (Dukes & McAninch, 1992), which, because of a lack of quarantine stations also had limitations. But because of the passion, foresight, and determination of Dr Duncan McEachran (Sayers, 1983; see Chapter 20), the first station was built at Levis in Quebec. This veterinarian was a leader in disease control and a strong voice for the improved standards of education for veterinarians. He appointed Dr J. R. Rutherford to the position of veterinary director general, the first in the Dominion. Because of these two veterinarians and many

others who followed them, Canada now has become a world leader in animal disease prevention and control. The following sections deal with rabies management in Canada by the CFIA before the devolution of its field services to provincial and territorial agencies on 1 April 2014. CFIA has retained its diagnostic and reporting services since that date. An update of the provincial and territorial programs as they exist today can be found in the chapters in Part 3 of this book.

Prevention, Control, and Management of Rabies By virtue of the Animal Contagious Diseases Act of 1903, rabies became a reportable disease in 1905 (Report of the Veterinary Director General, 1905). This allowed for better control of rabies through investigation of all suspect cases and establishment of dog control measures. Following the introduction of diagnostic tests for rabies by 1905, through the inoculation of live animals or the determination of Negri bodies in brain tissue, control measures allowed for the identification of positive animals and the more immediate determination of treatment for human contacts. With the introduction of domestic animal vaccination in 1953, control measures for rabies included establishing a reporting system, thoroughly investigating all suspect cases and diagnosing submission of specimens to a federal laboratory, determining the number of wildlife in the area, establishing dog control measures, and vaccinating dogs for free. Through the payment of an indemnity, farmers were

Prevention and Management of Rabies in Canada

encouraged to report cases of rabid cattle, horses, swine, goats, and sheep beginning in 1961. This also provided for some compensation for the loss of their animals. The district office, at that time, was the hub of rabies prevention and control activities. The district veterinarian was supervised from the regional office and guided by the rabies section in the Manual of Procedures (Agriculture Canada, 1987), written in 1987 and updated on a regular basis (Canadian Food Inspection Agency [CFIA], 2013). Reporting suspect rabies cases to the district veterinarian, investigating these cases, liaising with health officials and private veterinary practitioners, and distributing information on case-positives were part of the duties and can be found in the Manual of Procedures. Discussions of rabies cases in Canada and their distribution are found in Chapters 2, 3, and 21, and a breakdown of data for each province and territory is found in the chapters in Part 3. Today, more than 100 years after it was made a reportable disease, rabies, despite improved control methods and reduced numbers of cases, remains a potential threat in Canada (see Chapter 39). Its control and management program remains mandated and regulated by parts of the Health of Animals Act, Health of Animals Regulations, Reportable Diseases Regulations, and Rabies Indemnification Regulations. The main objective of the program is to prevent the transmission of rabies from domestic animals to humans, and the program meets its objective by carrying out the activities described in the Manual of Procedures (Agriculture Canada, 1987; CFIA, 2013). This chapter deals with the actions of Agriculture Canada (now the CFIA) in rabies management. The other agencies involved in this cooperative “one health” management program were dealt with in previous chapters (Figure 31.1). For example, the Public Health Agency of Canada (PHAC) was discussed in Chapter 5; the Ontario provincial health roles, in Chapter 32; and the wildlife rabies control program in Chapters 10, 11, 17, and 19.

PHAC and Agriculture Canada (now known as the CFIA) are the two federal agencies most involved with rabies management today. Provincially, wildlife ministries such as the Ontario Ministry of Natural Resources and Forestry (OMNRF) and the Ministry of Health and Long-Term Care provide the links (Figure 31.1) between the federal agencies and the provinces and territories in the management of animal and human rabies. As Ontario’s health and wildlife agencies bore the brunt of the rabies epizootic during the 1950s and 1980s, with most rabies cases reported and most humans treated for post-exposure contact, their examples are given in detail in Chapters 10 and 34. The other provincial and territorial health and wildlife agencies dealing with rabies control are discussed in Part 3 in detail.

Federal Agencies Public Health Agency of Canada The PHAC manages cases of human rabies and their treatment. Development of vaccination protocols for treatment pre- and post-exposure come under its mandate. Human vaccines are also regulated by this agency. Research and communication of these standards are essential actions. The PHAC initiated and was one of the signatories to the CRMP and NARMP. Pre- and post-exposure treatment data are collected and disseminated by this federal body. The role of Health Canada (now PHAC) in rabies management is discussed in Chapter 5 and its vaccination protocols in Chapter 15a.

Canadian Food Inspection Agency The CFIA is one of several organizations that fall under the mandate of the Department of Agriculture and Agri-Food Canada and is responsible for policies governing agriculture production, farming income, research and development, inspection, and the regulation of animals and plants. CFIA reports to the minister of agriculture and agri-food through its president and is dedicated to the safeguarding of food, animals, and plants that enhance the health and well-being of Canadians, their environment, and economy. The mandate of the CFIA’s rabies control program is the reduction or elimination of the disease in domestic animals and investigation of all human or domestic animal exposure to rabies, suspect or confirmed in domestic or wild animals. The actions of CFIA in rabies management are developed

Canadian Agencies Involved in Rabies Management Rabies management has involved the cooperative actions of many agencies since 1905. Figure 31.1 illustrates the close link between some of these federal and provincial or territorial agencies in the overall management of rabies. These links were strengthened with signing of the Canadian Rabies Management Plan (CRMP) in October 2009 (Tataryn & Buck, 2016) with the Canadian agencies and the signing of the North American Rabies Management Plan (NARMP) in October 2008 (Planning Team, 2008) providing for international cooperation with the United States.

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Figure 31.1: Canadian agencies involved in rabies management as of 2014. Note that underlined titles in the boxes indicate agencies, and responsibilities are listed in the boxes. Source: author.

and regulated through three levels – ­headquarters, regional offices (now called area offices), and district offices – as well as its federal diagnostic laboratories at Ottawa Laboratory Fallowfield (OLF) and Lethbridge, Alberta (LET) (see Chapter 20). A history of the laboratories and the basic tests for rabies are discussed in Chapter 20. The ultimate decisions on the rabies program direction rests with the minister of agriculture.

CFIA HEADQUARTERS

Located in Ottawa, Ontario, CFIA’s headquarters (HQ) is the administrative centre for Canada’s disease control programs, including that of the rabies control program. Its management activities are closely linked to the CFIA area offices; the area district offices; the Rabies Centre of Expertise in Ottawa; other federal agencies, such as PHAC; provincial and territorial agencies managing wildlife

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rabies, such as the OMNRF; and international agencies, such as the World Organisation for Animal Health (OIE) and the World Health Organization (WHO). The overall management of the rabies control program resides with the Health of Animals Division at HQ in Ottawa. Its activities in rabies management are divided into two broad categories; the field activities and the diagnostic and research activities. The four main elements of the CFIA’s field program against rabies carried out by the area district offices included:

the production of wildlife vaccines and their licensing, as well as providing funding to the baiting program. CFIA AREA OFFICES

Before 1995, Agriculture Canada maintained seven regional offices in British Columbia, Alberta, Saskatchewan, Manitoba, Ontario, Quebec, and the Maritimes. Each regional office had its own district offices, which totalled 110 in 1990 (Agriculture Canada, 1990). Today, these regional offices have amalgamated administratively into four area offices. For the Atlantic area, the main office is in Moncton, New Brunswick, with local offices in Fredericton (New Brunswick), Dartmouth (Nova Scotia), Charlottetown (PEI), and St John’s (Newfoundland and Labrador). For Ontario, the main office is in Guelph, with local offices in Guelph, London (South-West Ontario), Nepean (North-East Ontario), and Toronto. For the Quebec area, the main office is in Montreal, with local offices in Anjou (Montreal East), Ste Foy (Quebec), Montreal (Montreal West), and St Hyacinthe. For the Western and northen areas, Calgary (Alberta) is the main office, with local offices in Edmonton (Alberta North, Northwest Territories), Burnaby (BC Coastal), Winnipeg (Manitoba), Calgary (Alberta South), Burnaby (BC Mainland and Interior and Yukon) and Regina (Saskatchewan). Nunavut is serviced by a district office. The area offices provide the link for distribution of program information and policies between HQ, the area district offices, OLF and provincial and territorial wildlife and health ministries. Policies to suit local conditions may be set from here. The area offices in Ontario, Quebec, and Manitoba have been responsible for the payment of indemnity to the provincial governments since 1 July 1994. Under an agreement with each participating province, CFIA contributes 40% of the maximum amount paid per animal under the Rabies Indemnification Regulations: for cattle, $400; for horses, $200; and for sheep, goats, and swine, $80. Through audits of its district offices, the area offices supervise the actions required by the Manual of Procedures (CFIA, 2013) to maintain a high degree of efficiency within the control program.

(a) investigating all suspect rabies cases in domestic animals by CFIA district office veterinarians and when a positive diagnosis of rabies with human contact is determined, notifying public health authorities; (b) imposing quarantines on all domestic animals suspected of being exposed to a confirmed or suspect ­rabid domestic or wild animal; (c) collecting specimens and sending them to one of the two federal laboratories for testing and sending the results of a positive diagnosis to the health authorities when there has been human contact; and (d) providing data, statistics, and educational brochures on rabies, its dangers, and the CFIA’s policies to the g­ eneral public. Changes to the Health of Animals Act and Regulations are promulgated at HQ and the rabies program is reviewed on a regular basis. Policy changes are developed and issued from here and become incorporated within the Manual of Procedures on a timely basis and disseminated to CFIA area and district offices, other agencies, and individuals through the Access to Information Act. The minister of agriculture is apprised of all diseases that may affect Canada’s animal population, especially those affecting human safety or those affecting international trade agreements. Rabies is no exception, with the minister being updated on a regular basis. The CFIA provides the media and provincial, territorial, and international agencies with updates on Canada’s disease situation, brochures are printed and disseminated (see Chapters 33a and 33b) as required, and policies, procedures, and ­statistics on positive rabies cases are made available on the CFIA website. CFIA is also responsible for the import and export of animals, and these regulations are on the website as well. Rabies vaccines for domestic pets are regulated by the Veterinary Biologics Section of CFIA and are discussed in Chapter 16. CFIA maintains a voluntary presence on the Rabies Advisory Committee of the OMNRF, advising on

CFIA AREA DISTRICT OFFICES

The number of CFIA district offices (DOs) has varied over the years, rising to 119 in 1985, perhaps because of the outbreak of rabies, and falling to 110 in 1990 (see Chapter 4). With successful animal health programs in brucellosis, tuberculosis, and rabies, this number has decreased, in part because of a declining need for resources with decreases in the number of affected animals. The number of district offices, regional offices, and laboratories in 1990 is shown in Figure 4.2 of Chapter 4. 522

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The area district offices are the hubs of the field-related rabies management activities, and these are discussed below. Note that CFIA does not have a presence in Arctic Canada (Yukon, Northwest Territories, Nunavut, Nunavik, or Labrador) but district offices in other provinces provide the support needed for regulating the program in these areas. For example, the Burnaby office in BC supports Yukon, or the Edmonton office in Alberta supports the Northwest Territories.

Quarantines

Following the initial investigation, quarantines maybe imposed on domestic pets or livestock. This may precede the receipt of a positive rabies diagnosis. In 2005 CFIA changed its policy in the management of pets exposed to a rabies-suspect or rabies-confirmed animal. Pets in this case include cats, dogs, and ferrets, and the owner of a vaccinated or non-vaccinated animal is given several options in dealing with exposure to a suspected rabid animal. Besides the options of quarantine or euthanasia, the owner may have the animal revaccinated or tested to determine its titre of rabies neutralizing antibody (RNA), within five days post-exposure. This is followed by a 45-day observation period by the owner in the case of vaccinated pets. Pets not meeting the requirement of having been vaccinated previously or that have an inadequate RNA titre or are unvaccinated are subject to six months’ quarantine and revaccination at the end of the period at the owner’s cost (Manual of Procedures, CFIA, 2013). In the case of domestic livestock such as horses, cattle, or sheep with previous rabies vaccination, the quarantine requirements are the same but the duration maybe different. In the case of an unvaccinated herd of livestock, the duration of quarantine depends on the index case: 40 days for the total herd if the index case was from within the herd, and 60 days if the index case is from outside the herd.

INVESTIGATIONS

Under the mandate of the Health of Animals Act and Regulations, and applying the policies set out in the Manual of Procedures (CFIA, 2013), district veterinarians are responsible for investigating all suspect rabies cases and providing information on rabies, the quarantine of animals, specimen collection, and the submission to the two federal laboratories of all cases of rabies reported in their area. Where human involvement is part of the case investigation, the local Public Health Unit (PHU) (Figure 31.1) is advised of the investigation and the results of the diagnosis when a specimen is submitted. The CFIA does not investigate wildlife rabies situations unless domestic animals or humans have been exposed. The district veterinarian makes a risk assessment on the submission of any specimen for rabies diagnosis based on a number of criteria: the case history of human contact with the animal suspected of being rabid, the reported rabies cases in the area or on the farm, the vaccination status of the dog or cat, if involved, and consultation with the local medical physician or health unit. The CFIA inspector will collect specimens from any diseased animal in contact with humans or domestic animals when the possibility of rabies exists. Where an assessment concludes that there has been no risk, no specimen is taken. Quarantines may be imposed on the farm or domestic pet as warranted according to the Manual of Procedures (CFIA, 2013). When a specimen is collected it is submitted by air or road transport to the nearest federal laboratory in the area under the guidance of the Transport of Dangerous Goods Regulations usually as an “exempt animal specimen” (see Chapter 22). The submitter is always the district veterinarian, except for specimens from remote areas without a district office; then a third party, such as the Royal Canadian Mounted Police (RCMP) has been designated to carry out this task under the guidance of a CFIA officer in the nearest office. Disposal of the carcass or body remains can be done by the CFIA officer, the farmer or owner of the animal, the municipality, academic laboratories, veterinary clinics, or the CFIA laboratory involved in the diagnosis and disposal of the specimen.

Indemnity

Under the mandate of the Rabies Indemnification Regulations, federal-provincial agreements provide financial assistance to owners of certain domestic species that die as a result of rabies. This agreement, begun in the early 1960s with four participating provinces (Ontario, Quebec, Manitoba, and New Brunswick) continues today without New Brunswick (see Chapter 34). The federal share of the indemnity is 40% of an assessed market value up to a maximum amount for the species outlined in the regulations. Participating provinces are responsible for the remaining share. These maximums varied over the years, and before 1981, the amount that a farmer could receive was $500 for cattle; $350 for horses; and $100 for sheep, swine, and goats. After 1981 these increased to $1000 for cattle; $500 for horses; and $200 for sheep, swine, and goats. Today, these values are $400 for cattle; $200 for horses; and $80 for sheep, swine, and goats. In the provinces where an indemnity is paid, rabies is confirmed either by laboratory diagnosis or a veterinary clinical diagnosis. Since 2014 an indemnity is no longer paid federally. 523

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clinics. A regulation change made under the Health and Protection Act of Ontario in 1994 ensured that all pet owners vaccinated their animals against rabies and sponsored low-cost clinics of their own until the private practitioners started to provide clinics as well. The last rabies clinic held in the Ontario region by the federal government was in April 1996 at the Moose Factory Indian Reserve (E. Salsberg, personal communication, 7 April 1998). Although the first rabies clinics were free and carried out by Agriculture Canada personnel only, by 1960 vaccination of pets was also allowed by private practitioners (see Chapter 34). Today, municipalities and townships in all provinces and territories have by-laws appended to the licensing of pets requiring rabies vaccination. However, this requirement is not followed up by the authorities. In accordance with the employer’s health and safety standards, any employee or group at risk, including CFIA veterinarians and primary products inspectors, as well as biology and research scientists, must be immunized against rabies where there is a risk of contacting a suspected rabid animal.

Vaccination Clinics RABIES VACCINATION EXTENDED TO NEW AREAS Vaccination will be done free of charge by departmental veterinarians of the Health of Animals Division. The purpose of this vaccination program is to establish immunity to the disease in the dog and cat population of those communities before rabies infection becomes established through contacts of these animals with wildlife in the areas.

Agriculture Canada/CFIA has provided rabies vaccine and vaccination clinics for rabies prevention since the introduction of rabies vaccine in 1948 (see Chapter 15b) for domestic animals. The vaccinations were carried out by Agriculture Canada veterinarians or a third party in the far north, such as the RCMP or trained lay vaccinators. As rabies spread from the Northwest Territories through Alberta and eastwards into Saskatchewan and Manitoba in the late 1940s and early 1950s, vaccination of dogs became a priority. Perhaps the earliest clinics were those carried out by Dr Ross Singleton in 1952 (R. Singleton, personal communication, 2003). He travelled from Swan Lake in Manitoba to The Pas and Flin Flon, to Churchill and Keewatin (in what is now Nunavut) vaccinating dogs. As rabies moved eastwards into northern Ontario requests were received from northern county communities for rabies clinics. Requests for vaccination clinics received by Agriculture Canada from municipalities, townships, and Indigenous reserves were approved, depending on previous clinics held in the area, the prevalence of rabies in the area, pet control in the area, the anticipated cost of supplies, and the staff available. Those requesting clinics were asked to provide a clinic location, animal handlers, and clerical staff, and carry the costs of advertising. It was an enormous undertaking given that the first clinics in 1955 and 1956 were provided in winter in the northern county communities (see Chapter 34). For example, between December 1955 and February 1960 some 124,280 dogs, 62,772 cats, and numerous other pets, including rabbits, ferrets, squirrels, raccoons, a pony, a monkey, sheep, and skunks, were vaccinated at no cost to the owner in 33 counties of Ontario. In the same period, 1955 to 1961, nearly 10,000 dogs were vaccinated in the Northwest Territories and Yukon. Clinics continued to be held through the years and in 1958–1959, 61,446 dogs and 30,574 cats were vaccinated in 17 counties. By 1985 the requesting party agreed to pay Agriculture Canada $3 per animal in advance for a government-sponsored clinic. Following the successful rabies oral baiting program in 1989, the federal government virtually stopped sponsoring

Biting Incidents

Dog control has been an essential part of Agriculture Canada’s rabies control program since the earliest reports of rabies in Canada. District outbreaks of rabies in dogs occurred in 1907, 1930, and between 1943 and 1946. Control was achieved by restriction of movement, muzzling, destruction of strays, and pet vaccination (after 1950). Before 2003 biting incidents were evaluated with the risk of rabies being present or not. Where the risk of rabies was extremely unlikely following a discussion with the owner, a 10-day observation was suggested, with changes in behaviour reported. Where the vaccination history was unknown for the pet or the history of the attack assumed that rabies could not be ruled out, the owner may have been offered the options of a legal quarantine or euthanasia. However, a survey between 1999 and 2004 showed that a large percentage of animals destroyed presented minimal risk. Of 8093 dogs and 6773 cats euthanized for a biting incident, only 9 dogs (0.11%) and 13 cats (0.19%) tested positive for rabies. Following this survey, CFIA suggested that euthanasia be carried out as a last resort and a 10-day observation period be implemented (Kumor, 2005). In 2003 CFIA withdrew from initial involvement in the investigation of reported animal (dog, cat, and ferret) bites with the appropriate provincial or territorial authority taking responsibility. The initial investigation of animal bites by the provincial and territorial public health authorities occurs in all provinces and territories but Quebec.

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Communications

All diagnosticians working in the two federal laboratories receive extensive training and proficiency testing. Support is provided by the laboratories (OLF and LET) to all CFIA inspectors and veterinarians and program specialists, as well as the PHU, for the interpretation of the test results (Figure 31.1). With its expertise, OLF has become an OIE Reference Laboratory for rabies, as well as a WHO/ PAHO Collaborating Centre for the Control, Pathogenesis and Epidemiology of Rabies in Carnivores.

The district office and its veterinarian is the link between the area office, the federal laboratory that receives the specimens, local veterinary associations, private practitioners, the local medical physician, the PHU, and the general public. As such, the district veterinarian is able to provide updates on the rabies situation in the area; provide information on rabies through meetings, the CFIA website, and pamphlets (see Chapter 33a); provide updates on quarantines in process; and consult with the PHU to assess immunizing humans contacting suspect rabid animals.

RESEARCH ACTIVITIES

In addition to its diagnostic and information activities, the Centre for Expertise (OLF and LET) conducts research in three main areas: the biology of the rabies virus, oral rabies vaccine research, and developments to improve diagnostic methods. A great deal of effort has gone into supporting Ontario’s rabies control efforts. This includes providing the location coordinates of positive rabies specimens for its baiting activities; conducting collaborative research on oral vaccines for wildlife (ERA, V-RG, ONRAB), including safety and efficacy trials, vaccine stability, and immune response; and typing of variants to identify emerging epizootics and vaccine-induced cases (C. Fehlner-Gardiner, personal communication, 2012).

CFIA Rabies Laboratories The present CFIA rabies laboratories are located in Ottawa (OLF) and Lethbridge (LET) (see Chapter 20). These two laboratories undertake all official rabies testing of mandated samples, that is, human or domestic animal involvement with a rabies-suspect animal. The fluorescent antibody test (FAT) is the test of choice (see Chapter 20), as recommended by the WHO and the OIE. When wildlife surveillance testing is carried out by non-CFIA laboratories (direct rapid immunohistochemical test, dRIT; see Chapter 24c), positive result samples with possible human involvement must be submitted to OLF for confirmatory testing (CFIA, 2013).

NATIONAL AND INTERNATIONAL ACTIVITIES

As an OIE Reference Laboratory and WHO/PAHO Collaborating Centre, OLF provides scientific and technical expertise to both the CFIA and its outside clients. This includes training visiting scientists in diagnostic and research initiatives and maintaining reference virus and monoclonal antibody collections. Other activities include participation in international rabies initiatives, such as the characterization of lyssa viruses distributed globally, and participation in national and international committees, such as the NARMP and Rabies in the Americas (RITA). OLF supports and participates in programs to raise the awareness of rabies in other countries, such as World Rabies Day and RITA. World Rabies Day is an international campaign coordinated by the Global Alliance for Rabies Control, a nonprofit organization with headquarters in the United States and the United Kingdom. The day is celebrated each year since 2007 on September 28, the day Louis Pasteur died. Its aim is to raise the awareness about the impact of rabies on humans and animals, provide information and advice on how to prevent the disease, and provide information on how individuals and organizations can strive towards eliminating the main global sources (Global Alliance for Rabies Control, 2019). RITA is an annual meeting that has been held since 1990 and has been hosted by many countries in the Americas. Canada hosted

RABIES DIAGNOSIS AND STRAIN IDENTIFICATION

Upon arrival at one of the two federal laboratories, the rabies specimen is entered into the laboratory specimen tracking system and the FAT is carried out. After a result is determined, the district office is informed by telephone or email. The information is entered into the database for the month and area, and later transferred to the CFIA website. The district office then conveys the result to the individual, the physician, and the PHU in cases requiring immunization. The data are also used to guide control programs in various provinces and territories. As part of ongoing research into virus strains within areas of Canada and its wildlife species, variant typing by antigenic and molecular methods is ­carried out (see Chapters 18 and 23). The immunohistochemical (IHC) test may be performed on formalin fixed tissues and molecular methods such as reverse transcription polymerase chain reaction (RT-PCR) for human ­suspect cases; see Chapter 20). Confirmatory tests are carried out on the IHC tests by Saskatchewan’s Prairie Diagnostic Services. Specimens from provincial enhanced surveillance projects may be diagnosed for rabies under contractual arrangements (see Chapters 24c and 21).

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in 1991, 1994, 1997, 2001, 2005, 2009, and 2013. The 2020 meeting is being hosted by Colombia. The meeting provides a venue for researchers; health professionals; international, national, and local managers of rabies programs; wildlife biologists; laboratory personnel; and other people interested in the advancement of knowledge on subjects such as rabies surveillance, prevention, and control to meet to discuss their successes and ways to meet future challenges.

brought together the expertise of Canadian and international groups and agencies interested in rabies management. Rabies is reportable in all provinces and territories, which allowed CFIA to take the lead role regarding domestic animals, while health agencies took the lead role for human contacts (see Chapter 32) and provincial and territorial agencies took the lead in wildlife control (see Chapters 6 to 14). As of 1 April 2014, CFIA withdrew from all field activities but maintains its laboratory expertise. The field programs were down loaded to the provincial and territorial agencies and ministries (see Chapter 21) with some cost recovery elements available to the provinces and territories. All rabies cases with human contact are still directed to the responsible agency. In the case of wildlife specimens identified as positive by provincial or territorial agencies, these too are directed to CFIA for confirmation. It remains to be seen what effect these changes will have on the management of rabies in Canada.

Summary Rabies control in Canada over the years has had the cooperative help and expertise of a diverse group of agencies, laboratories, universities, drug companies, individuals, scientists, private practitioners and physicians, trappers, Indigenous and provincial and territorial biologists, and health officials in all provinces and territories. It has

Acknowledgments The author wishes to acknowledge the invaluable help provided by Dr Kim Knight-Picketts (CFIA, retired) with the information on the CFIA rabies control program. Information on the human health involvement in the rabies management program was provided by the Ministry of Health and Long-Term Care (Dr Catherine Filejski).

References Agriculture Canada. (1987). Rabies. In Disease control: Manual of procedures – Animal health (section 14). Ottawa, ON: Food ­Production and Inspection Branch. Agriculture Canada. (1990). Health of animals: Overview (6th ed.). Ottawa, ON: Author. Retrieved from http://publications.gc.ca /collections/collection_2012/agr/A61-13-1990-eng.pdf Canadian Food Inspection Agency. (2013). Rabies. In Disease control: Manual of procedures – Animal health. Ottawa, ON: Author. Dukes, T., & McAninch, N. (1992). Health of Animals Branch, Agriculture Canada: A look at the past. Canadian Veterinary Journal, 33(1), 58–64. Retrieved from https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1481176/pdf/canvetj00050-0060.pdf Global Alliance for Rabies Control. (2019). World Rabies Day. Retrieved from https://rabiesalliance.org/world-rabies-day Kumor, L. (2005). Canadian Food Inspection Agency’s notice to private veterinary practitioners. Canadian Veterinary Journal, 46(10), 917. Retrieved from https://www.ncbi.nlm.nih.gov/pmc/issues/123098/ Planning Team. (2008). North American rabies management plan: A partnership for effective management. Retrieved from US Animal and Plant Health Inspection Services website, https://www.aphis.usda.gov/wildlife_damage/oral_rabies/downloads /Final%20NARMP%209-30-2008%20(ENGLISH).pdf Report of the veterinary director general for the year ending March 31, 1904. (1904). Ottawa, ON: Department of Agriculture. Available from Library and Archives Canada, https://bac-lac.on.worldcat.org/oclc/29657040 Report of the veterinary director general for the year ending March 31, 1905. (1905). Ottawa, ON: Department of Agriculture. Available from Library and Archives Canada, https://bac-lac.on.worldcat.org/oclc/29657040 Sayers, C. W. (1983). Early history of the Animal Pathology Division of Agriculture Canada. Canadian Veterinary Journal, 24(8), 262–267. Retrieved from https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1790385/pdf/canvetj00273-0042.pdf Tataryn, J., & Buck, P. A. (2016). The Canadian rabies management plan: An integrated approach to the coordination of rabies activities in Canada. Canada Communicable Disease Report, 42(6), 135–136. https://doi.org/10.14745/ccdr.v42i06a05

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32 Rabies and Practice in Public Health in Ontario Ian Gemmill Medical Officer of Health (Retired), Kingston, Frontenac, and Lennox and Addington Public Health, Ontario, Canada

Introduction Beginning in the late 1950s, and continuing into the 1990s, Ontario had a higher incidence of rabies in wildlife than any other place in North America. Originating in arctic foxes from the north, rabies moved through the geographic funnel that extends from Georgian Bay in the west, to the Ottawa River in the east, through a horizontal line that runs through French River and North Bay (see Chapter 10). Once in southern Ontario, this strain of rabies became enzootic in the red fox population, and consequently, rabies became a serious threat to the health and safety of both humans and other animals. Farmers had to fear not only for their own safety but also for the safety of their livestock in which they had invested and on which they depended for their livelihoods. Spillover to skunks worsened this already problematic situation, as skunks became another reservoir for the virus. Further, because of the interaction between fox and skunk populations with domestic animals, the risk of exposure to humans through these domestic animals increased. The challenge for public health was immense and, as this chapter will describe, the response has been widespread and innovative, and has led to quite a different picture for rabies and public health today.

Historical Perspectives First Interventions Despite the fact that rabies was at an all-time high in the ­second half of the twentieth century, it had been a threat to human health in Ontario for decades before (see Chapters 2,

3b, and 10). Rabies was already a concern in the late nineteenth century in Ontario, when rabid dogs posed a risk to human health, and outbreaks of the disease occurred in the canine population from time to time. Several people who were bitten by rabid or possibly rabid dogs travelled to New York City to the Pasteur Institute for preventive therapy – the serum – to abort an incubating infection (see Chapter 3b). At that time, the cost of both the travel and the care were borne by the affected person, which clearly was a financial hardship for much of the population. Mercifully, the municipal council and sometimes the provincial Board of Health, the predecessor of Ontario’s Ministry of Health, subsidized part or all of these costs. By 1910 with a major outbreak of rabies in dogs in southwestern Ontario, the issue had become so crucial and the follow-up so cumbersome that the provincial government negotiated with the Pasteur Institute in New York to provide next day delivery of the human vaccine to Toronto General Hospital or to the Hospital for Sick Children when requested, and to train physicians at those hospitals in the administration of the vaccine. This agreement simplified the receipt of rabies vaccine by affected persons and led the way to the production of the vaccine locally by 1913. In 1916 for the first time, this vaccine was made available free to all persons at risk of rabies through possible exposure to a rabid animal, a major change in an era in which the burden of health care was borne by individuals or by charities. The expectation that municipalities would pay for transportation of persons requiring post-exposure prophylaxis (PEP) continued, even after the vaccine was made available to all. The outbreak of 1910 in fact started two to three years before, when a dog from New York state incubating rabies

Prevention and Management of Rabies in Canada

crossed the Niagara River over a suspension bridge near Queenston, Ontario. This importation of rabies led to ever-increasing disease in dogs over the subsequent years in southwestern Ontario (see Chapter 2). Not only humans were affected; the disease also posed a risk to livestock. The public demanded action, and in addition to improved access to PEP, regulations were implemented to control the canine population (see Chapter 4). These provisions included the tethering and muzzling of dogs, the isolation of dogs suspected of having rabies, and the euthanasia of rabid dogs. Originally, the regulations were enacted by municipalities, creating a patchwork of control that was ineffective. Therefore, in February 1910, the federal Department of Agriculture issued an order under the Animal Contagious Diseases Act that all dogs in western Ontario (what is now southwestern Ontario; northern Ontario had not yet been ceded to the province by the federal government, an event that took place in 1912) be tied and muzzled. A parallel provincial Order in Council made similar requirements, and the provincial Board of Health requested that all local public health agencies enforce these regulations. Although there was some opposition to these provisions, they largely were supported by municipalities because of the serious situation in the province at that time. Although these provisions did not eliminate rabies from southern Ontario, they presumably did reduce the risk to humans, thereby mitigating the impact of this epizootic. In its report for 1910, the provincial Board of Health reported that “that the (muzzling) order has been fairly well obeyed as well as thousands of dogs being killed all of which has aided very materially in stamping out the disease” (Ontario Department of Health, 1910, p. 42). When the Public Health Act was amended in 1912, ­rabies was explicitly included in the specific definition of communicable disease for the first time. The amendments did not contain any provisions specific to rabies, and thus, the regulations of the provincial Board of Health concerning the isolation of animals suspected of having rabies, euthanasia of diseased animals, and PEP for humans were not changed but only reinforced by the inclusion of rabies in the Public Health Act. After the replacement of the provincial Board of Health by the Department of Health, with its own minister, the issue became political. The minister, Dr Forbes Godfrey, blamed renewed activity of rabies in dogs on the federal government because it allowed the importation of hunting dogs into the province. The event in question involved a dog from a kennel in Vermont that became rabid while hunting in Quebec, an event that subsequently led to spread in Ontario. Seymour and Bell (1928) reported that

Godfrey had asked for more stringent quarantine and muzzling orders and for an embargo at the international border to prevent the further importation of possibly rabid dogs. When the disease began to affect the feline population in the late 1920s, there was significant concern, because cats tended to roam freely and were not subject to the control of by-laws in most municipalities. This unenviable situation for health officials in Ontario continued for several decades. As the prevalence of the disease increased in animals, the risk of exposure to humans increased in a parallel. Vaccine against rabies for animals had been available since 1950s, but it was not seen as necessary by owners for the health of their pets. In fact, the most common reason for having a pet vaccinated was not to protect it or the humans with which it interacted but to allow entry to the United States. The underuse of vaccine for pets continued to be a problem, addressed finally by veterinarians who took it upon themselves to set up low cost clinics to promote wider vaccination of pets (see Chapter 15b). Further, some municipalities required owners to have their pets vaccinated before a licence would be issued. Since by-laws normally did not require the licensing of cats, these provisions had a reduced effect. Even at reduced costs, farmers did not line up to have their barn cats immunized, even though they were possibly the animals most at risk because of their increased likelihood of interacting with wild animals. Another measure under the Public Health Act allowed the medical officer of health (MOH) to place into quarantine any animal suspected of having rabies. Some MOHs expressed frustration at being criticized or even sued for causing an animal to be quarantined for 14 days, especially if it turned out not to have this disease.

Using Vaccines for Human Exposure Pet vaccinations and PEP for humans via vaccination has been the first line of defence against rabies since the development of rabies vaccine by Louis Pasteur in France in the nineteenth century. In humans, vaccination was done with the goal of preventing the incubating infection. Over the years there were several variations in the vaccine, such as the rabbit brain vaccine and the duck embryo vaccine, among others (see Chapter 15a). All these vaccines had serious side effects, which either made the treated person ill or, in rarer circumstances, caused their death (Rubin et al., 1973; Warrell et al., 2014). Because rabies is an almost invariably fatal disease, when the risk of exposure to rabies was real, the use of vaccine was welcomed, despite its shortcomings. The real issue with these vaccines was that one needed to

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be sure of the risk of rabies in the exposed person. If the potential for rabies was at all in doubt, providing a person with vaccine was one of the most difficult decisions in public health. PEP for a confirmed exposure to a fatal disease was an easy decision, but when it was uncertain, it was an unenviable decision to make. By the early 1980s, however, a safer and more effective vaccine became available (see Chapter 15a). Human diploid cell vaccine (HDCV) revolutionized the treatment of rabies (Parija, 2009). It worked well, avoiding most of the treatment failures associated with the previous types of rabies vaccine, and it could be given largely without fear of harm to the patient. While this vaccine did nothing to ameliorate the significant endemic of rabies in wild animals in southern Ontario, it finally provided an alternative effective PEP that removed most of the anxiety that complicated the decision to treat animal bites or not. After the arrival of wildlife rabies to southern Ontario in the late 1950s, the treatment of bites by potentially rabid animals became a fundamental part of public health practice. Public health professionals had to be available at all times to assess and to advise on bites to humans by animals. They needed to understand the dynamics of this disease, both in wild and domestic populations, and how various types of exposure either did or did not pose a risk of infection to humans, if the biting animal was rabid. It meant that a public health professional could not stray far from a telephone when on call, and that she or he sometimes had to postpone the day’s work if one or more persons were exposed to a potentially rabid animal. It was a significant part of the work and responsibility of a professional in public health and, since bites to humans by animals were very common, a very time-consuming part of the job. It was a responsibility that was taken extremely seriously. In the follow-up of possible exposures to rabies, among one of the most important partners of local practitioners in public health were the local veterinary colleagues from Agriculture Canada, now known as the Canadian Food Inspection Agency (CFIA). Like public health professionals, these district veterinary officers (DVOs) and their technicians worked for the benefit of people who had had potential exposures to rabies. If the biting animal was available for testing, these professionals were available on weekends and holidays to analyse tissue and to provide the critically important information of whether the biting animal was infected with rabies. Since rabies virus doesn’t migrate to the salivary glands until an animal has developed encephalitis, it could be concluded with certainty that an animal that did not have rabies encephalitis was not infectious at

the time of the bite, even if the animal was incubating the disease. Without the invaluable assistance of the veterinary colleagues, follow-up of potential exposures would have been much less precise, and there would have been significantly more vaccine used, as the default decision often was to provide PEP in the absence of definitive information on the status of the biting animal. They were extremely helpful colleagues and could not have provided better service. The recent loss of this service, which will be discussed at the conclusion of this chapter, has complicated the follow-up of potential exposures considerably.

The Structure of Rabies Management As background, it is helpful to know how public health in Ontario was structured, and how the federal, provincial, and local public health authorities collaborated (see Chapter 31). By the early 1980s, the hundreds of local boards of health had been amalgamated to just 42. Most boards of health were autonomous, non-governmental organizations under the Public Health Act of 1882, the most notable exception being the city of Toronto, which reported to city council. They were funded in variable ratios by the Ministry of Health and the local municipalities. All were responsible under the Public Health Act, however, for the control of communicable diseases generally and of rabies specifically. Within each local public health agency (LPHA), the MOH and associate MOHs held this responsibility, although in some LPHAs the responsibility was delegated to public health inspectors or public health nurses. The bottom line was that rabies was so prevalent in southern Ontario that every animal bite was reportable to local public health by law, and an assessment had to be done by a public health professional, usually in consultation with the DVO, who provided the testing of the animal that was so important to precision in decision-making. Rabies prevention and control were an essential part of public health practice. Eventually, the follow-up of rabies became a shared responsibility among the three levels of government. Figure 31.1 in Chapter 31 illustrates the various partners and their connections. The laboratories at Agriculture Canada/CFIA did the testing of suspect animals and provided data for surveillance to the Public Health Agency of Canada (PHAC). The district office of Agriculture Canada facilitated testing of the animal, often euthanizing the animal and transporting it to its facilities for testing, and reporting results back to the local MOH. These services were essential to local public health practice, as they

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provided the status of the animal that was needed for a correct decision on PEP. The district office of Agriculture Canada/CFIA also conducted the quarantine of animals. The PHAC and its various predecessors used data from CFIA’s lab to keep track of the epidemiology nationally so that local epidemiology was available to practitioners at the local level. Provinces purchased vaccine for PEP and provided guidelines to LPHAs for the follow-up of cases, and collaborated with both CFIA and PHAC on approaches to policy and surveillance. The local physician depended on the local MOH for both advice on the right course of action and the vaccine. The collaboration amongst all of these partners was the key to the success of an effective program of follow-up to protect the public.

initiating PEP, as the status of the animal was never certain, unless the animal could be examined pathologically. For domestic animals, the decision was more difficult. If the animal was owned by an identified person, it could be quarantined to assess whether it was rabid at the time of exposure. Since all dogs and cats (and later it was identified as true for ferrets as well) die within 10 days of the developing rabies and becoming infectious, if the one under quarantine was still alive after that period, the animal was not rabid at the time of the potential exposure. Everyone was reassured, and no vaccine was needed. If the owner of the animal could not be identified, and the animal escaped or could not be located, the decision became more problematic. Such assessments were even more common than assessments for contact with wild animals, since humans have more contact with domestic animals than with wild ones. The risk in domestic animals tended to be lower, but if the biting animal could not be identified, most of these cases were given PEP because the possibility of rabies could not be ruled out. The immunization status of the animal in some cases mitigated the risk, and PEP was deemed unnecessary, but other factors, such as the behaviour of the domestic animal, may have negated that factor. Today, however, the likelihood of those animals being infected and infectious with rabies is small; against the background of years of caution in recommending PEP, these cases are much more difficult, leading to slower than expected reduction in the use of PEP (see Chapter 34). This is especially true in cases in which the dog or cat is not ill and seems cared for, but no owner or address is available. And then there is every case in between. The next factor needed to assess the risk of rabies is the type of exposure. If a bite clearly has occurred, a rabid animal can transmit rabies. What about a lick on intact skin, however, or even on an old wound, especially if the animal is known to be rabid? Only a professional with nerves of steel would back away from the use of a safe and effective vaccine, even when the risk is small. It is easy to see why the default might be to use a newer, safer, and more effective vaccine against rabies, rather than to wait it out on tenterhooks, hoping for the best. The behaviour of the animal, whether wild or domestic, was another key factor. If an animal was mangy and thin, one might be more inclined to recommend PEP, even though many feral cats fit this description and were not rabid. It was important to determine whether the animal behaved in the highly aggressive way that is characteristic of some cases of rabies, or was completely passive and withdrawn, as happens in dumb rabies. If a domestic animal did

The Public Health Approach to Rabies The Decision Process The sole and unique responsibility for rabies treatment by public health professionals has been the assessment of human exposures and the prevention of disease in humans. All activity in public health regarding rabies has this single goal, whether it is promoting the immunization of domestic animals, quarantining animals suspected of being rabid, or providing vaccine to primary care physicians when a potential exposure has occurred. The approach to rabies prevention in individuals always has been complex, but, in the end, it is a binary decision: does the person in question require PEP or can they be reassured that the risk of developing rabies is zero or negligible. It is the latter that is problematic in public health practice, made even more difficult as the risk has diminished over time. This binary decision has several components. First, and most important, is the species of the animal to which a human has been exposed. Exposure to a fox or skunk was considered de facto grounds to immunize against rabies, if the type of exposure made transmission to the human in question possible and the animal could not be tested. This recommendation is the policy of the Ministry of Health in Ontario. Bats were also considered a high-risk species, and in the era of immunized populations of foxes and skunks, bats have emerged as the highest risk animal for rabies, not because more of them are now infected but because rabies in the other species has dropped, with the exception of the current epizootic in raccoons near Hamilton, Ontario (see Chapter 10). Notwithstanding, a significant exposure to almost any wild animal would be grounds for

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Rabies and Practice in Public Health in Ontario

not appear unwell but was not available for testing, some professionals, under patient pressure, still had difficulty not recommending PEP, even when the risk of rabies in animals had plummeted. In the days of prevalent rabies, the geographical location of the possible exposure was also important. Rabid foxes and skunks were more common in rural areas, but most professionals in public health knew of cases of rabid animals in towns. So while it pointed towards PEP when the exposure occurred in rural areas, it was never considered zero risk if a potential exposure occurred in a suburban or even an urban area. Next, the anatomical location of the bite or scratch on the infected person influenced how quickly PEP was needed. If the exposure was on the head or neck, the practice was to implement PEP quickly, even while the animal was being observed or tested. For other bites, immunoprophylaxis was postponed until results were available. If testing showed that the animal was rabid, immunoprophylaxis was started immediately. If the animal tested negative, immunoprophylaxis for the bites on the head and neck were discontinued. This approach was taken because the incubation period, the time from exposure to the first signs of disease, was much shorter when the bite was near the brain. The shorter incubation period resulted from the decreased distance from the bite to the brain that rabies virus had to travel when the bite was on the head and neck. Finally, the status of the biting animal was critically important. No matter what the species, no matter the location of the bite, no matter what the behaviour of the animal, a public health professional could say with certainty that there was no risk from a bite if it was shown that the animal was not infected. The essential role of the DVO in providing these results in a timely way helped to prevent needless PEP, and in addition to the always helpful advice they provided, helped saved the system the cost of the vaccine and medical visits to administer it. It often was the difference between having to give PEP or not. The purpose of outlining these factors considered in assessing whether a possibly exposed person should receive PEP is to show how complex this decision is and how much the judgment of the professional influences this decision. It is a yes or no decision and clearly influenced by the possibility of a fatal outcome. It was among the most difficult everyday decision that professionals in public health had to make. This level of complexity and responsibility raised the issue of what type of professional should be responsible for these difficult decisions. It could be argued that the decision

must be a medical one, but it could also be argued that an experienced public health inspector might be more adept at such decisions than an inexperienced public health physician. The practice therefore varied across the system. In some LPHAs, physicians were given this job exclusively. In others, other professionals in public health were delegated this responsibility. In the end, there were no situations in recent history in which the training and qualifications of the decision-maker led to a preventable case and consequent death. This, of course, may be owing to the fact that there was an easy default position with little risk: when in doubt, PEP with HDCV was given. Regardless of who made the decision about PEP, one thing was certain: it was absolutely essential that there be a system of reporting that ensured that every case was dealt with expeditiously. Cases had to be assessed and decisions made quickly to ensure that if rabies virus was present, it was arrested by PEP early in the incubation period. Early intervention was necessary to ensure that the immune globulin infiltrated around the portal of entry would immobilize the progression of the virus while the vaccine over a period of weeks induced the development of antibodies in the affected person. Time was of the essence, especially in cases in which the bite occurred on the head and neck, and no animal specimen was available. The person responsible could not let a four-day weekend pass and deal with a report on the next business day. As a result, LPHAs had to arrange for coverage on call. Since most public health inspectors were unionized, a cost was attached to their availability. In many LPHAs, however, it was the practice to put public health physicians on call, since an extra cost was not necessarily attached. This last anomaly was finally corrected by the Ontario Medical Association and the government of Ontario in 2008, when a stipend for being on call was instituted for public health physicians. It is important to comment on the precautionary principle in public health, as it applied to rabies investigations. It long had been the modus operandi in the investigation of possible rabies exposure, and it was appropriate. It was invoked in cases in which exposure to rabies could not be ruled out, and while vaccine may have been overused, most professionals in the system believed that this approach was the right one, to ensure that no person suffered from and succumbed to rabies in Ontario. Some believe that the precautionary principle is more appropriate for rabies than for other issues for which people outside public health think it should be used. For example, some people believe that the most protective approach should always be taken, even when it would paralyze some systems in society, in

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Prevention and Management of Rabies in Canada

the absence of data that show harm. Environmental issues are examples – the placing of towers to transmit signals for mobile phones or to house wind turbines. Some argue that they not be allowed, because there might be a health effect determined at some point in the future. For the follow-up of possible exposure to rabies, when it was uncertain whether exposure had occurred, the health effect, though unlikely, was known: the exposed person would die if rabies exposure had occurred. This use of the precautionary principle made sense and was the right way to follow up reported potential exposures. Finally, it is important to emphasize how the advent of HDCV changed public health practice and the approach that public health professionals adopted for PEP. Before HDCV’s development, public health officials had to make difficult choices, balancing the risks of the previous vaccines against the risk of exposure to a fatal infection. HDCV made the decision easier, because side effects were so minimal. The only downside was the cost, so the decision to give the vaccine was much easier and more vaccine was used. The vaccine was so safe, in fact, that in 15 years in the Ottawa area, only one adverse reaction was reported. The adverse effect was urticaria, an allergic reaction of the skin that may be a harbinger of anaphylaxis, a potentially fatal systemic reaction (Sanofi Pasteur, 2006). The urticaria occurred after the second dose, but it was mild, so a third dose was given. When the urticaria recurred after the third dose and was worse, it was decided that the final two doses to complete the series should be withheld. The risk of exposure had been assessed as low, and thus the risk of withholding the final doses of vaccine was also deemed to be low. In addition, the doses that patient had received already may have provided some protection, although that possibility could not be relied upon, and the decision to withhold vaccine was independent of that fact. Professionals in public health work with many other partners in the community on rabies: family and emergency room physicians; veterinarians, both local private and DVOs; police forces; Agriculture Canada (now CFIA); and others. While others are concerned about the well-being of animals, such as observation for disease if animals are exposed, the focus by public health is highly specific: reducing to the lowest possible level the chance of a human case of rabies. This focus is reinforced by the fact that rabies, although rare in humans, is virtually a universally fatal disease, and every precaution must be taken to ensure that the right decision is made. This approach has ensured that, despite Ontario having had the highest prevalence of rabies in animals in North America, human deaths

have been extremely infrequent (see Chapter 3b). In fact, rabies is the rarest of communicable diseases in humans, partly for this reason. Between 1810 and 2017, a total of 49 people in six provinces and one territory died of rabies in Canada: British Columbia (2), Alberta (1), Saskatchewan (2), Ontario (25), Quebec (16), Nova Scotia (1) and Yukon (2) (see Chapter 3b). But when the incidence of rabies in animals began to decline in the 1990s because of the oral vaccination of wildlife, the decrease of the use of vaccine lagged behind. We are still haunted by the prospect of being the professional who allows a case of rabies to occur, despite the markedly diminishing risk to humans in Ontario over the last two decades. The tension between using a safe vaccine to prevent a fatal disease and making changes to practice to reflect new circumstances is difficult. It would be nice, however, to reap the rewards of decreasing the risk of this disease and to realize the savings of not having to provide PEP to reassure ourselves.

Some Interesting Cases It is illustrative to relate the more unusual stories that present themselves in professional practice. They also are interesting cases, providing the human face to what might otherwise seem a highly clinical decision. Over the years, several cases occurred that challenged the principles that guided professionals in their assessments. The last death in the Ottawa area occurred in 1967. A barn cat attacked a girl and did not release her leg until her father beat the cat with a shovel (see Chapter 3b). The tragedy of this case, of course, was that the affected girl still succumbed to rabies, despite the best available treatment and the most competent care by public health professionals. Had the more effective and safer HDCV been available, it is possible that she might have survived, as treatment failures with the formerly used vaccines occurred. We are privileged to live in an era when not only has scientific ingenuity reduced our risk of exposure through vaccinating high-risk species but the PEP also works so well and can be used with so much less fear of serious, unwelcomed complications. Ontario also had cases in which people unknowingly ate beef from an infected cow. Although these people were given PEP, based on the precautionary principle, some made the argument that rabies virus concentrates in nervous tissue and is unlikely to cause disease through ingestion of flesh, especially if it had been thoroughly cooked. Cooking would have destroyed this virus, which cannot live long outside mammalian hosts, but could safety be guaranteed, when the administration of a safe and effective vaccine really had

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Rabies and Practice in Public Health in Ontario

no downside except the cost to the taxpayer? There was no criticism voiced over this awkward professional decision. Rabies vaccine is purchased by provinces and territories for the PEP program in their jurisdictions. It is made available to LPHAs, primary care physicians, and health care nurses in a variety of ways (Figure 31.1, Chapter 31). In some places, because the HDCV initially was relatively expensive, it was kept in the LPHA and released to primary care physicians only when a mutual decision had been made to provide PEP. In others, vaccine was made available to emergency departments so that PEP was more readily available. The latter approach provides more convenient access to PEP when it is necessary but may lack the controls needed to ensure that vaccine is used appropriately in every case. It is a double-edged sword and may have led to the overuse of PEP in an era when the risk of exposure to rabies has plummeted. Once in a while, a case came to light in which limiting the extent of use of PEP was difficult. In the early 1980s, a long-term-care home was the site of a major initiative of assessment and PEP when a rabid puppy exposed dozens of elderly people. The puppy was taken to the home to entertain residents. The report stated that the visiting pup saw most, if not all, of the residents, and licked most of them. When the pup subsequently died and was found to be rabid, the public health professionals in this area had a major task to undertake: the risk assessment of every resident and some of the staff in this long-term-care home. In the end, most people received PEP, putting a huge strain on supply. As often happens in public health, the people who definitely need PEP are obvious, but assessing those for whom it becomes less clear with less well defined exposures is more difficult. Professionals know where to start, but a burden that we all bear is that it is often difficult to know where to stop. Some of the cases were fanciful. In at least two cases reported to one LPHA, exposures in residents of Canada travelling abroad occurred. One involved an exposure by a bear in Turkey. The other was a bite by a monkey in the Far East. Were those animals rabid? How could anyone ever find enough accurate information to reassure the person who was bitten abroad? Unfortunately, these travellers did not seek advice from the people in the best position to advise them: public health professionals in the countries in which they were exposed. They also delayed their assessment by waiting, sometimes for several days, until their return to Canada. In the end, because of the enormous difficulty in getting good information, the outcome of these cases was easily determined through the invocation of the precautionary principle, and PEP was normally

given, an appropriate decision in the absence of information from distant locales (see Chapter 6). These individuals all received PEP, simply because no one could never know the status of the animal. Another interesting case occurred in the 1980s in Ottawa, when a thoughtless person decided that, rather than paying the veterinary bills, he would drop his sick dog off in downtown Ottawa. Because the dog was both unwell and aggressive, it was remarkable to passers-by, who called the Humane Society to collect the animal. Before the dog could be apprehended, however, observers witnessed the dog biting a man. The man in question boarded a bus before he could be identified. The Humane Society sent the animal for testing, the testing showed that it was rabid, and the LPHA was duly notified. The difficulty, however, was that no one had any idea who the bitten man was or how to reach him. There was no identifying information and the LPHA had to resort to other means to find him. It was decided that the only effective and efficient means of locating the affected person was to go to the media. A press release was drafted and released, and interviews with the media were duly provided. Luckily, the affected individual saw the piece on the evening news on television, and called the LPHA to report that he had been wearing gloves, and that the rabid dog had not broken through the leather. Sometimes, public health officials went to great lengths to determine whether a person actually had had an exposure to rabies. On one occasion, a person rang the office of public health in Ottawa to report that he had been bitten by a dog in Sudbury. When asked to place the dog under observation, he reported that he had shot and buried the dog in Sudbury. They could simply have used the HDCV, but there was an opportunity to avoid doing so. It was agreed that, since the animal was available, albeit 800 kilometres away, the bitten person would return to Sudbury, exhume the canine corpse, and take it to Ottawa for testing at the laboratory at Agriculture Canada. This laborious process turned out to bear fruit, as the testing was negative, and the bitten person was able to avoid PEP. Odd circumstances often present themselves. When vaccine was in short supply, the Ontario Provincial Police kindly accommodated Ottawa Public Health and the persons in need of vaccine by delivering it from another LPHA. On another occasion, a resident who had had contact with a bat called in on a weekend, some days after an exposure, to report it. He said that the bat was still in his possession, in his garage. When a public health inspector went to collect the bat, he noted that the bat was moving. It was not alive, however; its head was full of writhing maggots that

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Prevention and Management of Rabies in Canada

gave it that appearance. Clearly, the brain was not suitable for testing, and the decision to provide PEP had to be based on the other circumstances in the case.

eliminated in the near future as there have been no effective ways developed to immunize bats. The concern that domestic animals were exposed to rabies by foxes and skunks and then developed the disease, putting their owners and others at risk, was also addressed by the control measures in animals. Although the disease was far more prevalent in the population of wild animals, the exposure to humans was largely from their pets or domestic animals with which they came in contact more frequently. While there is still concern about exposure to domestic animals, the likelihood that a domestic animal will be exposed to rabies also has been lowered by these wildlife control programs, together with more widespread immunization of pets, thereby reducing the concern to humans of bites from dogs and cats that otherwise seem healthy. While control programs have helped in almost every aspect of assessing the risk of exposure to rabies, there continues to be a need for immunization of pets that travel with their owners outside Ontario. One of the anticipated benefits of controlling rabies in wildlife was to save money on PEP, a hope that has yet to fully materialize. Although some authors have argued that there has been a modest cost saving in PEPs (Shwiff et al., 2011), others (Nunan et al., 2002) have noted that PEPs have not declined in proportion to the reduction in r­ abies-positives. For instance, in 1958, at the peak of the invasion of the arctic fox strain of rabies, there were 1647 PEPs in Ontario and 2493 rabies-positives, a ratio of 0.66 human treatments for every diagnosed case of rabies (Table 32.1). In 2012, however, there were only 29 rabies-positives but 1809 PEPs, a ratio of 62.3 at a time when the threat of wildlife rabies had been largely removed (see Chapters 10 and 34). The dramatic increase in the ratio of PEP/positive since 1989 is demonstrated in Figure 32.1. Note that PEPs in the 1980s had increased about 68% over PEPs in the 1970s following the 1980 introduction of a safer vaccine, but this increase was overshadowed by events following the introduction of wildlife control programs. Overall, public health officials continue to practice with the mindset of the era before the ORAVAX aerial baiting control program, perhaps fearful of erring on the side of withholding vaccine, even when the risk is very low. It is important for this benefit to be realized, and public health practice must change before that benefit can occur. Practitioners in public health need to leave behind the fears of the last half-century so that these resources can be devoted to new priorities in public health. One recent development has made the follow-up of potential exposure to rabies more difficult. Because of

The Impact of Rabies Control in Wildlife on Public Health Practice Geography and animal behaviour conspired to make the incidence of rabies in southern Ontario a major concern in the last half of the twentieth century. This situation ensured that follow-up of potential exposures to rabies was a fundamental part of public health practice. The introduction of a safer vaccine for PEP in 1980 helped since the decision to provide it was much less ­nerve-wracking. However, PEP kept individuals who were potentially exposed from becoming ill, but it did not address the source of the problem: enzootic rabies in the populations of foxes and skunks. That issue was addressed definitively by the initiation of control programs in populations of animals, described in Chapter 10. Control of rabies in wildlife, including the aerial distribution of oral vaccine baits (ORAVAX), the trap-vaccinate-release (TVR) program, and the euthanizing of some species to restrict spread (point infection control or PIC) had, in combination, a remarkable effect on the decreasing the incidence of rabies in wildlife. Indeed, from 2013 until the outbreak in raccoons in December 2015 (see Chapter 1) there were no terrestrial rabies cases in southern Ontario. Like John Snow’s lock on the pump in Broad Street in England, the aerial oral vaccine baiting program stopped exposure of rabies to humans from these species and altered the risk to humans of rabies correspondingly. Threats remain, however, as the continuing epizootic of raccoon rabies surrounding Hamilton, Ontario (see Chapter 10) demonstrates. As well, rabies remains in the arctic fox population in the north, and another southwards invasion remains a possibility. The risk of human exposure to rabies in southern Ontario is now largely confined to a species that also poses risk in other parts of Canada, namely, bats. Rabies in bats has not increased substantially but it has become the leading source of rabies exposure now that the disease is being controlled in foxes, skunks, and raccoons (see Chapters 10 and 27). Although current protocols for immunization after interactions with bats have been effective in reducing the use of PEP (see Chapters 6 and 10), bats commonly co-habit with humans in homes. Hence, this important activity in public health will not be

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Rabies and Practice in Public Health in Ontario

reductions in federal spending, CFIA (the successor to Agriculture Canada) and the agency with the responsibility for testing animals for rabies, decided in 2014 to discontinue the field activities of collection and transport of specimens for testing and take DVOs out of the process. While testing continues, the job of getting the specimens to CFIA has fallen to LPHAs and other provincial and territorial agencies. Provinces and territories are working to find ways to facilitate these processes, but training people locally in these specialized skills and finding transportation from some places that are distant from the labs has been daunting. The result is that just when the use of vaccine could be reduced, it will increase because less testing is possible. Without the benefit of that assistance from DVOs, public health professionals will have no choice in some cases but to recommend vaccine in the absence of testing results, thereby putting more people through unnecessary PEP with the attendant costs. It is hoped that a solution will be found soon, so that the use of PEP, which should be decreasing at this point in history, will not increase at considerable cost to the taxpayer.

Table 32.1 Rabies-positives and post-exposure prophylaxis treatments in Ontario, 1958 to 2012. A safer vaccine was introduced in 1980 and wildlife control programs began in 1989. Year

Positives

PEPs

PEP/Positive

PEPs/100,000

1958 1959 1960 1961 1962 1963 1964 1965 1966 1967 1968 1969 1970 1971 1972 1973 1974 1975 1976 1977 1978 1979 1980 1981 1982 1983 1984 1985 1986 1987 1988 1989 1990 1991 1992 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012

2493 638 227 862 790 870 1148 1021 1002 1048 1730 1719 1187 1777 1480 1318 1229 1722 1273 1162 1357 1407 1416 1557 2107 1860 1382 1984 3273 2007 1832 1905 1634 1238 1305 1254 611 328 158 97 81 100 187 212 202 126 106 96 82 106 80 49 38 26 29

1647 479 566 790 991 965 852 1367 1168 1461 1539 1187 1164 960 1252 1020 974 1050 935 957 816 1002 1096 1833 2402 2481 2027 2150 4212 2621 2266 2640 1991 1739 2186 2581 1437 1182 937 1079 1048 890 1073 1640 1728 1498 1426 1526 1988 2257 2692 1678 1542 1512 1806

0.66 0.75 2.49 0.92 1.25 1.11 0.74 1.34 1.16 1.39 0.89 0.69 0.98 0.54 0.85 0.77 0.79 0.61 0.73 0.82 0.60 0.72 0.77 1.18 1.14 1.33 1.47 1.08 1.29 1.31 1.24 1.39 1.22 1.40 1.67 2.06 2.35 3.60 5.93 11.12 10.99 8.90 5.75 7.73 8.55 11.88 13.45 15.89 24.24 21.29 33.65 34.24 40.58 58.15 62.27

28.3 8.0 9.3 12.7 15.6 14.9 12.9 20.2 16.8 20.5 212.0 16.1 15.4 12.4 15.8 12.7 11.9 12.6 11.1 11.3 9.5 12.0 11.6 20.8 27.0 27.5 22.1 23.2 44.7 27.2 23.1 26.2 19.4 16.7 20.7 24.2 13.3 10.8 8.5 9.6 9.2 7.7 9.2 13.79 14.29 12.24 11.51 12.12 15.7 17.95 20.88 12.92 11.74 11.4 13.47

Discussion The practice of public health has been assisted hugely by the people who developed and executed the programs to control rabies in animals. Much is owed to this group of innovative scientists, who quietly and behind the scenes made a huge contribution to the health of Ontarians and to the practice of public health in the province by reducing the incidence of this disease in animals. Like the engineers, who provided clean water and sanitation, and who made water-borne illness an uncommon event in society, thereby saving countless lives, this group has contributed significantly by controlling rabies in animals. Public health owes a great deal of thanks to them for the strategic thinking that they brought to a serious public health problem. They intervened innovatively and effectively to eliminate this important source of risk to health. The great challenge now for public health professionals is to learn to alter their practice appropriately for the new conditions and epizootiology of this disease in southern Ontario. The payoff for the control program is great in terms of reduced risk to health, but further gains can be made in realizing savings from reduced use of vaccine by assessing cases more appropriately based on lower risk, changing practice to provide vaccine only when it is clearly indicated, and redirecting

Source: compiled from CFIA and Ontario Ministry of Health and Long-Term Care data.

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Prevention and Management of Rabies in Canada

Figure 32.1: The annual ratio of PEPs to rabies-positives. Wildlife rabies control programs began in 1989. Source: created from CFIA and Ontario Ministry of Health and Long-Term Care data.

resources from rabies follow-up to other needed public health services. Two important issues remain. The first is that public health professionals need to learn to practise in the new environment, in which the risk of rabies has diminished significantly through control of the disease in all animals. This program, brilliant in its conception, has the potential to save public monies if practice can change. These monetary benefits cannot be realized, however, if the use of PEP continues as it has for the last six decades, despite the change in risk. Practices change in other fields of medicine as technology makes more effective practice possible. Practice similarly needs to change in public health, adjusted

for the new and better circumstances that have been made possible by the control of rabies in wildlife. The second issue that needs to be front of mind is that we must never be complacent. The veterinarians, biologists, virologists, epidemiologists, and geographers have given a gift of reduced risk to the people of Ontario. To keep that risk at the lowest possible level, programs to control rabies in wildlife need to remain robust and effective, and surveillance of this disease in animals needs to be maintained. No one wants to return to the days when people and pets alike were at significant risk of a potentially fatal disease. Much has been gained by the control of rabies in wildlife; we have to protect these important gains.

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Acknowledgments The author would like to thank Dr Catherine Filejski for the very helpful background information on the history of rabies in Ontario that contributed to the writing of this chapter. The author would also like to thank the colleagues who helped so much with the follow-up of potential exposures to rabies in the days when rabies was a major threat, and whose imagination and innovation made those days a memory.

References Nunan, C. P., Tinline, R. R., Honig, J. M, Ball, D., Hauschildt, P., & LeBer, C. (2002). Postexposure treatment and animal rabies, O ­ ntario, 1958–2000. Emerging Infectious Disease, 8(2), 214–217. https://doi.org/10.3201/eid0802.010177 Ontario Department of Health. (1910). 29th annual report of the Provincial Board of Health. Retrieved from https://archive.org/details /ontariodepthealth1910ontauoft/page/n1 Parija, S. C. (2009.) Textbook of microbiology and immunology. Gurgaon, India: Elsevier India. Rubin, R. H., Hattwick, M. A. W., Jones, S., Gregg, M. B., & Schwartz, V. D. (1973). Adverse reactions to duck embryo rabies vaccine: Range and incidence. Annals of Internal Medicine, 78(5), 643–649. https://doi.org/10.7326/0003-4819-78-5-643 Sanofi Pasteur. (2006) Product Monograph IMOVAX® Rabies Vaccine Inactivated. Seymour, M., & Bell, W. (1928). Public health administration: The rabies situation. Public Health Journal, 19(6), 279–281. Retrieved from https://www.jstor.org/stable/41973831 Shwiff, S. A., Nunan, C. P., Kirkpatrick, K. N., & Shwiff, S. S. (2011). A retrospective economic analysis of the Ontario red fox oral ­rabies vaccination programme. Zoonoses and Public Health, 58(3), 169–177. https://doi.org/10.1111/j.1863-2378.2010.01335.x Warrell, D. A., Cox, T. M., & Firth, J. D. (Eds.) (2014). Oxford textbook of medicine. New York, NY: Oxford University Press.

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33a Communication Strategies FEDERAL LEVEL

David J. Gregory Canadian Food Inspection Agency (Retired), Ottawa, Ontario, Canada

Introduction The knowledge of the general public as to the true nature of rabies and its manifestations is so defective and so much clouded by tradition and nervous dread, that any dog acting in a peculiar manner is very apt to become an object of suspicion and to be hunted down and killed as mad. Under ordinary circumstances, the death of the animal in this way destroys all possibility of confirming the facts as to the existence or non-existence of the disease. This lack of definite evidence constitutes one of the greatest difficulties encountered in dealing officially with reported outbreaks, and it is with the view of enlightening the public as to what rabies really is and how to deal with suspected animals, that this bulletin has been prepared for general circulation. It is hoped that its distribution in Canada will assist in dispelling from the minds of some exceedingly well-disposed and humane persons the hallucination that there is no such disease as rabies and that the officers of this department are guilty of heartless cruelty in ordering the destruction of affected animals and the tying up or muzzling of dogs which have or may have been exposed to infection. – J. G. Rutherford (1909)

The chapter epigraph is a part of the foreword by the veterinary director general, J. G. Rutherford, to his minister of agriculture. It appeared in Bulletin No. 14: Rabies, written by George Hilton, the chief veterinary inspector. It is probably the first attempt at a meaningful communications activity directed at the general public as to the true dangers

of rabies. We do not know the size of audience it reached but it was intended for general circulation and initiated by the rabies outbreaks in Ontario, Manitoba, Saskatchewan, and Alberta at the time. Interestingly, it was released in both official languages and dealt with the clinical signs of the disease, its manifestations in a number of animals, instructions on the submission of specimens to the laboratory, and the Rabies Regulations of the Dominion of Canada, under the Animal Contagious Diseases Act, 1903. Although current communications efforts are more sophisticated, costly, and aimed at a larger, better informed audience, the old fears about rabies remain and sometimes results in the destruction of animals without definite proof of disease. By 1926 improvements to laboratory diagnosis of rabies, mandated reporting on a regular basis, regulated control of the disease through the Animal Contagious Diseases Act, 1903, and cooperation between veterinary and health officials at all levels of government led to far better communications between agencies and the public. It also emphasized the need for a standard plan when a rabies issue developed. Far too often, action was after the fact and an outbreak resulted in a panic reaction among the public.

Strategy at the Federal Level Objectives The objective of current communication strategies, as it was in the 1900s, is to raise rabies awareness among all citizens in Canada with the aim of preventing contact with

Communication Strategies: Federal Level

rabid animals by their families and pets. Typically, communications are case by case and fit the needs of the situation. Awareness is accomplished through a number of communications methods and involves several levels of government and all provinces and territories. The issue is ongoing as an outbreak of rabies can occur at any time, and prolonged low incidence in an area tends to lead to apathy or indifference in the general public and government agencies.

and territorial health authorities the responsibilities of investigating rabies and submitting samples for testing. It maintains its two testing laboratories and the mandate for reporting all positive diagnoses with human contact to provincial or territorial health authorities. CFIA also continues to provide rabies advice and guidance to the general public through its website, http://www.inspection.gc.ca; thorough collaborative education and management programs with its provincial and territorial counterparts; and through direct education efforts internally and externally.

Background

Target Audience

We can never hope to stamp out rabies in wildlife. It is much too complicated a problem.

The key messages in a communications strategy will depend on the audience for which it is intended and will influence the communication’s approach and activity carried out to support that message. The target audience can be infinite but for practical purposes the target audience for CFIA communications can be divided into two:

– Dr Kenneth Wells as cited by John Schmidt (1963)

Until rabies eradication is a reality, rabies will continue to be an ongoing issue and must be managed on case by case. People need to be reminded that rabies is a viral disease that affects the central nervous system of warm-blooded animals, including humans. It is transmitted through the saliva, very often after a bite of an animal and can be spread by infected saliva coming into contact with an open wound or scratch or through the mucous membranes of the mouth, nasal cavity, and eyes. Once symptoms appear in a host, rabies is usually fatal. Rabies is preventable in domestic animals through ongoing vaccination for pets. The dog was the animal most affected by rabies in the early seventeenth and eighteenth centuries in Canada, but stringent controls including quarantine and vaccination have drastically reduced incidence in domestic animals. At present, the major rabies vectors in Canada are wildlife – bats, foxes, skunks, and raccoons – and this poses additional problems for rabies prevention and control.

1. A specific, ongoing internal audience with a day-to-day communications need 2. A more variable and larger external audience that requires an information package on an ongoing basis Internal communications are those that provide the CFIA personnel with rabies information. This includes field ­veterinarians, department heads. and, more important, the minister of agriculture. External communications are those used to inform the general public and other local, provincial or territorial, and international agencies as to the rabies situation in Canada. INTERNAL AUDIENCES

From 1900 to 1940, the veterinary director(s) general wrote annual reports for internal distribution. These reports usually contained updates of disease issues but were often a year or two late in content. The rabies reports were also by fiscal and calendar year, but because the diagnostic laboratories for rabies were connected by telephone, telegram, fax, and now by electronic mail to the national, area (regional), and district offices, all communications were, and are, readily available. Between 1957 and 1970, the Health of Animals Division published Newsletter in an effort to keep Division veterinarians apprised of Agriculture Canada activities, as well as providing updates on rabies-positive diagnoses. This monthly publication was followed by Communication between 1974 and 1983, a quarterly printing by the Education and Development Division distributed to all Branch veterinarians. This was

Strategic Considerations With the passage of the Animal Contagious Diseases Act in 1903, and the Rabies Regulations of 1905, the authority and responsibility for rabies prevention and control in domestic animals has been with the Canadian Food Inspection Agency (CFIA). The CFIA supports other federal, provincial and territorial, and municipal jurisdictions in reducing the risk of exposure of human populations to rabies in domestic animals and wildlife. Prior to 2014 CFIA veterinarians investigated rabies incidents and submitted samples for laboratory testing when domestic livestock and pets were reported to have been exposed to or show symptoms of rabies. In 2014 CFIA relinquished to provincial

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then superseded by the Health of Animals: Overview, a yearly report of the Food Production and Inspection Branch between 1984 and 1990 that reported on Branch activities for the previous year. As a result of resource cuts and the transformation of the Health of Animals (Agriculture Canada) into the CFIA, the department became more business orientated and the report was discontinued (Figure 33a.1). In the 1980s Agriculture Canada’s Communications Branch provided Health of Animals veterinarians with courses on how to deal with the media. It was customary for local media to interview the federal veterinarian on the latest disease problem, often just fishing for information. The courses were designed to give the veterinarian some

experience in handling media questions. On one notable occasion, the Communications Branch “invaded” the Animal Diseases Research Institute in Ottawa to test the security system. This was a time of animal activists. After entering the laboratory without any real effort, visiting the animal pens, and taking photographs, they called the director and asked how he felt about the security for the laboratory. He assured them all was well secured, only to have a rude awakening. By the end of the year, a perimeter fence and guard house had been erected to protect the laboratory. During 1993 the minister of agriculture was apprised of the possible emergence of raccoon rabies in Canada by his officials in Agriculture and Agri-Food Canada. He

Figure 33a.1: ­Communication methods: Report of the ­Veterinary Director General (1905), C ­ ommunication (1982), ­Newsletter (1961), Health of ­Animals: Overview (1990). Source: Canadian Food Inspection Agency. Used with permission.

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was provided with information on the possible outbreak, the preparations in place to meet the threat of an outbreak, the lead agency, and the part its officials would play in an outbreak. This enabled the minister to answer many of the questions he was asked about the threat in Parliament. This is just as important today.

(CFIA, 2019) for private practitioners. Both manuals are on the CFIA website and provide up-to-date information on rabies policies and procedures to carry out investigations of reported cases. The district veterinarian also spreads awareness through brochures and public service announcements on radio and television and in newspapers and informs private practitioners of rabies quarantines in their area. Presentations at local, provincial and territorial, and international meetings update the world on the progress of the rabies management program in Canada. The Canadian Veterinary Medical Association played a key role in the dissemination of information for Agriculture Canada over the years. Through the Canadian Veterinary Journal, members received updates on rabies outbreaks, regulation changes, vaccine availability, and articles of regulatory interest. At its annual meetings, presentations were made to the veterinary members on the role of Agriculture Canada in rabies control during the regulatory sessions. Through the years, CFIA veterinarians played an important role in the dissemination of information about the regulatory process for reportable diseases such as rabies, making presentations at municipal, provincial and territorial, and international meetings, as well as to the five Canadian veterinary colleges: Ste Hyacinthe in Quebec; Western College in Saskatoon; Faculty of Veterinary Medicine in Calgary, Alberta; Atlantic Veterinary College at Prince Edward Island; and Ontario Veterinary College at Guelph, Ontario. More recent presentations included information on rabies data in Canada, regulation changes, and the progress of the aerial baiting program in Ontario, Quebec, and the Atlantic provinces. The presentations at the veterinary colleges discussed reportable diseases such as rabies, to whom to report cases of possible rabid animal contacts, where to take suspect animals if brought in by a private person, how the dissemination of reports will occur, and the implications of a positive diagnosis. This was also a good time to advise the students on getting vaccinated against rabies and maintaining a rabies titre with revaccination. Most colleges offer vaccination clinics with checks on titres before their students enter clinical studies. The few who decline vaccination must sign a waiver when doing field work.

EXTERNAL AUDIENCES

While the key message for the internal audience was designed mainly for CFIA employees use, often the communication approach and activity were shared with other levels of government, with provincial and territorial agencies, and internationally. Using the standards set out and agreed to in the sanitary and phyto-sanitary measures, and as a member of the World Trade Organization, Canada reports on its disease status to the World Organisation for Animal Health (OIE) on a regular basis. Through sharing of its disease status with other countries, CFIA maintains its high level of animal health credibility. For example, in 2004 CFIA produced a report entitled Canada’s Zoosanitary Situation for the OIE. Rabies incidence in Canada is one of the diseases tracked by the World Animal Health Information System. This provides the animal health disease status of many countries on an ongoing basis to its member delegates and is important for international trade. One of the earliest examples of a shared activity by Agriculture Canada for an external audience was the black-and-white movie called Rabies in Canada produced by the veterinary director general in 1958. This was to be viewed by all veterinarians. By the 1960s television had made its debut as a communications media, and in February 1966 Dr K. F. Wells participated in a television program called This Land of Ours about rabies. It was a great success and interviews have been used often since then. The key message for external audiences is one of awareness and protection. “Rabies is a viral disease affecting all warm-blooded animals and is usually fatal. Avoid wild animals that act strangely, prevent your pet from roaming free, and vaccinate it as recommended by your private practitioner”: this message is found in everything from films (Figure 33a.2) to illustrated brochures (Plate 25). Pamphlets are distributed through CFIA’s national, area (regional), and district offices, as well as provincial and territorial agencies and private veterinarians. Other examples of shared messages to external audiences are found in the Agriculture Canada’s (1987) Disease Control: Manual of Procedures for internal use by field veterinarians and the Accredited Veterinarian’s Manual

Budget Many activities of CFIA are subject to cost recovery for services. However, rabies as a reportable disease with human health ramifications was not considered for cost recovery. All messages and activities for internal audiences are part of the operating budget from year to year. All materials

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Figure 33a.2: RUFUS 1988. ­Certificate of Merit for the ­Production of an Animated Cartoon by Agriculture Canada’s Communications Branch.

Source: CFIA. Used with permission.

produced are in English and French. Seminar attendance and travel to meetings for rabies must be evaluated and approved. With a rabies outbreak and a need to raise the public’s awareness and reinforce prevention activities for them, additional funding is sought, sometimes using a shared activity with another agency. It is often said that “it takes a dog bite to shake the trees for money.” Information on CFIA regulations, policies, and positive rabies diagnosis for the general public can now be found by

telephone or email and on the website. The CFIA’s 1-800 number (1-800-442-2342) was made available 8 May 2006 and is available from Monday to Friday from 8 a.m. to 8 p.m. These are the most frequent types of calls received by the agents: • people reporting their pets or someone they know was bitten by an animal • pets bitten by a wild animal and referred by a veterinarian

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• sightings of bats in backyards or cellars • foxes wandering in the neighbourhood and acting abnormally

submitted to these CFIA laboratories and either disposed of or sent to some of the regional laboratories run by the Canadian Wildlife Health Cooperatives (see Chapters 21 and 24c). These were usually active surveillance specimens and tested by the direct rapid immunohistochemical test (dRIT) with indeterminate and positive results with human contact (Chapter 24c) being sent to OLF for confirmation. Where there was one policy for regulatory field activities, there are now policies for each province and territory in Canada. This has placed an added burden on the provincial and territorial medical offices and on the veterinary colleges to provide the regulatory information required. As well, the colleges often have students from more than one province attending class and the problem becomes how to prepare students for working in a particular province or territory. When CFIA was in charge of providing the field services, each rabies investigation was immediately followed by an investigation report from the district veterinarian to all parties involved and the distribution of a CFIA brochure on rabies. This procedure is now up to the provincial and territorial agency departments, an added expense to their already stretched finances and resources. Hopefully, these changes will provide the same level of follow-up that the CFIA and its provincial and territorial partners had ­provided before 2014.

The callers are individuals, hospital staff, and veterinarians. The CFIA website, http://www.inspection.gc.ca, was launched on 1 April 2007. Contacts from this site are often people looking for vaccination requirements when travelling. These media are also used to evaluate the success of the rabies awareness program. As of 1 April 2014 CFIA withdrew from field activities but maintained its ­diagnostic capabilities. These field activities have been redirected to ­ various provincial and territorial medical agencies. Further discussion of this action and its implications are made in Chapters 21 and 39.

The Future? The change in CFIA’s mandate in 2014 changed rabies reporting across Canada. Now provincial and territorial authorities were responsible for investigating rabid case reports, taking samples, and shipping them to a laboratory. In the case of human contact specimens, these were still to be shipped to the CFIA laboratories at Lethbridge, Alberta, or Ottawa Laboratory Fallowfield (OLF) at Nepean. Specimens with no human contact were not to be

Acknowledgments The author would like to thank the Communications Branch of CFIA for its assistance during the writing of this chapter.

References Agriculture Canada. (1987). Rabies. In Disease control: Manual of procedures – Animal health (section 14). Ottawa, ON: Food ­Production and Inspection Branch. Canadian Food Inspection Agency. (2019). Accredited veterinarian’s manual. Retrieved from https://www.inspection.gc.ca/animals /terrestrial-animals/diseases/accredited-veterinarian-s-manual/eng/1343915611518/1343915703253 Rutherford, J. G. (1909). Foreword. In G. Hilton, Bulletin No. 14: Rabies (pp. 3–4). Ottawa, ON: Department of Agriculture, Health of Animals Branch. Retrieved from http://publications.gc.ca/collections/collection_2016/aac-aafc/agrhist/A12-5-14-1909-eng.pdf Schmidt, J. (1963, March 12). Agricultural Alberta. The Calgary Herald, p. 9. Retrieved from https://www.newspapers.com/image /481609456

543

33b Communication Strategies PROVINCIAL LEVEL – ONTARIO

Beverly Stevenson Ontario Ministry of Natural Resources and Forestry, Peterborough, Ontario, Canada

Introduction Arctic fox strain rabies has been endemic in Ontario since the late 1950s. With a human population of approximately 10 million in Ontario, of which approximately 14% live in rural areas, when rabies control programs were implemented, it was necessary to communicate to the public the threat that rabies posed to humans, domestic animals, and wildlife and the control programs that were being implemented. Two of the biggest challenges for any program to be successful are to have sufficient funding and to have public support. When the program is being conducted by the provincial government, these two are intertwined because funding is allocated from taxpayer dollars. Generally, programs that the public perceive as being important receive more funding; programs that the public does not support receive little or no funding. The key phrase here is public perception. The best program in the world will face challenges if the public thinks it is a bad idea; it won’t have the public support that it needs, and funding will be an issue. This is especially critical to long-term programs. Not only is the support of the public essential when the program is initiated, but that support must also be maintained for the duration of the program. It would be pointless to initiate a program to eliminate rabies if it was expected to take a decade or more while knowing that funding would only be available for one year. Public support is also a requirement for programs that are being conducted on the ground on a large geographical scale. On the ground programs require landowner

permission; if the public does not think the program is worthwhile, they are unlikely to give permission to be on their property. So how do you communicate a program to the public, persuade them that it is to their benefit, and have them continue to support and want to allocate their taxes to that program? This chapter examines the evolution of communications strategies for rabies and rabies control programs in Ontario. This includes the teaching packages and an educational video that were developed when rabies control programs were being initiated and information had to be distributed to the uninformed public. This chapter also examines the benefits and drawbacks of media coverage. It covers the present-day use of newsletters, websites, presentations, and workshops. The development of contingency plans and a rabies hotline is also reviewed.

Communications Historical Communications, 1900s to 1960s Historically, communications only had to be conducted at a very local level. Individuals generally only travelled within a few kilometres of their home, and they focused on news that affected them. If it was important, everyone was talking about it at the local store and it made the front page of the local newspaper. Individuals read local newspapers, listened to the local radio station, and watched the local television channel (or, if they were lucky, channels). Although national news

Communication Strategies: Provincial Level

working for government (including public health) and veterinarians is a worldwide issue for rabies control (Steele, 1988). The Ontario Ministry of Natural Resources (now the Ontario Ministry of Natural Resources and Forestry (OMNRF)), Ontario Ministry of Agriculture and Food (OMAFRA), and Ontario Ministry of Health (MOH) staff were most likely to receive calls or questions from the public, and it was important that they be able to knowledgably answer on rabies and its control programs (D. Smith, personal communication, 17 December 2010). A good example of this occurred when OMNRF’s Mike Power was involved in the trap-vaccinate-release (TVR) program (Rosatte et al., 1992). He was approached by two women who were out for a walk. He took the time to explain what he was doing and why the program was being conducted. When our coordinator received a notice shortly after that commending his staff for their excellent public relations, it was revealed that one of the ladies was the assistant deputy minister’s wife. It’s important to treat every member of the public equally because you never know to whom you might be talking! Sometimes public relations are not quite as effective though. This was the case when OMNRF’s Rob Warren was live trapping in Scarborough in the late 1990s. The couple whose property Warren was trapping on asked him about coyotes and whether or not they posed a threat. Warren assured the couple that there were coyotes in the nearby ravine but they need not worry about an attack since coyotes are normally timid animals. The words had barely left Warren’s mouth when a coyote lunged out of some nearby bushes, grabbed the couple’s pet poodle, and disappeared into the ravine (R. Warren, personal communication, 1997). During the late 1980s, meetings were held with local government staff. These meetings were opportunities to educate district staff about rabies and its control programs, provide messages to be delivered to the public, and open discussions on the best methods to communicate with the public (C. Hogenkamp, personal communication, 17 January 2011). OMNR’s Daryl Smith believes that this encompassing approach, along with the follow-up information distributed to staff on the success of the research programs, was one of the keys to the success of the program. With staff being kept informed on the progress of rabies control, they felt that they were part of the program and stayed enthusiastic about communicating rabies information. In 1989, everything changed. OMNRF switched from doing localized research to doing a broad-scale aerial rabies vaccination bait drop. It was no longer possible to meet with every group that wanted to know more about the program. And to complicate things, all of the previous research

was interesting, the local happenings were what mattered most. It was more important to know which one of their neighbours had passed away of natural causes than it was to know that someone they had never met was murdered in a city hundreds or thousands of kilometres away. Generally, historical communications about rabies were in the form of quarantines or muzzle orders (Tabel et al., 1974; Rosatte, 1988). Muzzle orders required dogs from specific households or specific areas to be muzzled while outdoors. This would prevent the dogs from biting other animals or people, which would prevent them from spreading rabies. The problems with muzzle orders were that they had to be applied at a landscape level to be effective; dogs could escape from houses while they were not muzzled; determined dogs could remove the muzzle regardless of how well it was fastened; and numerous un-owned dogs were wandering the countryside (Carpenter, 1890; Hansard, 1890). Quarantines were even more localized than muzzle orders – applying only to homes or farms where a rabid animal had been discovered – and required the animals to be confined for up to six months (Rosatte, 1988). As with any control strategy, if people decided to disregard the orders, the strategy would be ineffective.

Communicating in the Modern Era, 1970s and 1980s When the Ontario government began its rabies control programs for arctic fox strain rabies, most of the research activities were localized. By contacting one or two special interest groups, such as a trapper’s council or fox hunting association, everyone that was affected by the program was contacted (D. Smith, personal communication, 17 December 2010). Although the research was important, it did not affect the general public and as a result, there was no need to notify newspapers, television, or radio stations. The only individuals that needed to know about it were the ones who were likely to help with the research. Since it was such a small number of individuals to contact, staff would contact the special interest group and offer to meet with them (C. Hogenkamp, personal communication, 17 January 2011). This frequently involved giving a presentation, showing a video, and answering questions. This grassroots approach not only educated a specific group but also provided an opportunity to garner additional public support for the program. One of the most important groups to inform was provincial government staff from the areas where the programs were being conducted (B. Murch, personal communication, 16 December 2010). Proper education of individuals

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public, including news releases, fact sheets, educational videos, and educational kits (Figure 33b.1) (Rosatte et al., 1990). In addition to these methods, specialized communication plans (such as canvassing households within the TVR area) were also carried out to further educate specific audiences. As part of the comprehensive communication plan, an educational video called Casper’s Mail was developed in 1988. This eight-minute video featured a basset hound that educated children about rabies and the dangers of petting stray or wild animals. The catchy and addictive jingle “Don’t touch the bait” reinforced the idea that children should leave rabies vaccine baits alone if they found one. That simple message was so effective that there were no reports of children handling baits during the first few rabies bait drops (C. Hogenkamp, personal communication, 17 January 2011). An entertaining and educational rabies video that targeted children and was also distributed to schools in target areas was a highly effective and novel communications strategy.

activities had been conducted in southwestern Ontario while the rabies bait drop was being done in eastern and northern Ontario. All the individuals who already knew something about the program were not going to be involved in it and the program would no longer spread by word of mouth from them to the farmers on whose land the baits would be distributed. The challenge then was to figure out how to ensure that all landowners within a 14,660 km2 area were notified (MacInnes et al., 2001). And that area would expand in the following years until it included almost all of southern Ontario (approximately 100,000 km2). To prepare for this change from localized programs to programs covering a large geographic area, OMNRF’s Communications Services Branch prepared a comprehensive communication plan (Rosatte et al., 1990). The purpose of the plan was to inform the public about the objectives of the various parts of the rabies control programs. The plan incorporated numerous strategies to communicate with the

Figure 33b.1: OMNRF educational poster developed to tell the story of rabies to children. Source: OMNRF.

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demonstrations on the ground, which gave opportunities for video footage without the side effect of becoming airsick. The bait machine was loaded with baits and a box or Rubbermaid tub was placed under the chute (egress) in the bottom of the aircraft to catch the baits. The camera operators would carefully aim their camera so that it wasn’t obvious to viewers that they were not flying. Most television stations would then use stock footage of scenery from previous years or from other aerial stories that they had done to provide good coverage of the program. These staged shootings were easier to organize, gave the reporters more room to move around the aircraft for the perfect angle since there would be fewer staff and baits in the way, had zero turbulence, and allowed the reporters to get back to the station sooner so they could air the story sooner or spend more time editing the footage. It was a win-win situation for both parties. After all, the better the reporter feels, the more positive the news story will be that gets aired. And it is very important that reporters both support and understand the work if you are going to maintain public support. A supportive reporter can ensure that the program receives more than the standard 30 to 60 seconds of television coverage. Conversely, negative media coverage can have a huge impact on public opinion (Figure 33b.2). This could have been the case in 1990 in eastern Ontario when the headlines of the Ottawa Citizen declared “Rabies vaccination project fails – discriminating foxes turn noses up at 260,000 baits dropped across region.” Individuals who read only the headline would assume that the government had wasted taxpayer’s dollars. They had to read the entire article to realize that 50% of the foxes examined had eaten a bait and that OMNRF was working on developing a more attractive bait. Headlines in such a significant newspaper stating that the program was a failure could have resulted in a huge reduction in public support. Fortunately, this never happened – whether this was

The 1990s The communications strategies developed in the 1980s provided the basis for communications for the much larger rabies control programs that would be conducted in the 1990s. During the first few years of the large-scale oral rabies vaccination (ORV) program, communications efforts focused on mainstream media (newspaper, radio, and television) (J. Sirois, personal communication, 17 December 2010). This was accomplished by distributing news releases and hosting media days at each of the airports at which OMNRF was baiting. Reporters would be invited to the airport, which gave them an opportunity to interview researchers and take photos and video footage of the staff and equipment in action. The few brave reporters who dared to participate in an ORV baiting flight had an opportunity to take some scenic footage of the areas that were to be baited. Since ORV normally occurred in late September or early October, the fall colours were spectacular and the flights appeared vacation-like. In reality, the camera operators rarely fared well. They would eagerly spend the first few minutes of the flight looking through the camera lens at the rotating drum on the bait machine as it dropped baits through a hole in the floor of the aircraft and taking panoramic shots out the window of the aircraft flying at 250 kilometres an hour. Of course, while they were doing that, they had to work around the staff and equipment in the aircraft, handle the turbulence that occurs with low-level flying, and deal with the odours of the baits. After the first 15 or 20 minutes, their enthusiastic attitude was frequently overcome by feelings of nausea and wishing that someone else had handled the assignment. OMNRF quickly learned to plan special flights for the media that were only about 30 minutes long instead of making them endure the standard three-hour baiting flights. As years passed and as the reputation for torturing camera operators spread, OMNRF adapted to providing

Figure 33b.2: Headline from the Ottawa Citizen declaring OMNRF’s first rabies bait drop in eastern Ontario a failure. Source: author.

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a result of effective pre-baiting communications, the rapid drop in rabies cases over the next three years (MacInnes et al., 2001), or something else will never be known. Media relations were also important for the ongoing TVR programs (see Chapter 10). Because TVR was localized, the media coverage required was much less extensive. News releases only had to be distributed to a handful of newspapers, and local reporters could be invited to accompany a trapper to cover the story. By the mid-1990s, the ORV and TVR programs were well established and annual communication was becoming routine. To maintain rabies awareness and provide a focus for annual events, the Ontario Parliament declared May as Rabies Awareness Month (Rosatte et al., 1997).

from all levels of government and their associated agencies (i.e. Humane Societies and animal control companies) to discuss the risks associated with raccoon rabies and consider the course of action (O. Williams, personal communication, 17 December 2010). In Ontario at least four ministries in the provincial and federal governments (Canadian Food Inspection Agency (CFIA), MOH, OMAFRA, and OMNRF) had some key jurisdiction, but none owned the leadership role, and many other organizations had associated roles to play in rabies control. The provincial and federal government departments were either trying to cope with recently losing up to half of their staff or they were just in the process of downsizing because of government financial constraints. The municipal representatives were very vocal about the impact of provincial and federal downloading of responsibilities and costs to them (O. Williams, personal communication, 17 December 2010). After four hours of presentations and discussions, everyone agreed that there was a critical need for decisive action, yet each representative was adamant that they were not in a position to help. The prevailing opinion was summarized by the representative from one of the potential lead government departments who indicated that they appreciated the problem and the need for definitive action but financial constraints prevented them from doing so. They suggested we call back when raccoon rabies was actually present in Ontario. With that summation, people began closing their notebooks and reaching for their coats. The meeting facilitator appealed to everyone to consider what each organization in the room was required to do by law. The facilitator pointed out that if in the coming months each organization began to take action on the aspects that it was legally required to do (or for which a public expectation existed) then we would collectively be responding to the risk of raccoon rabies (O. Williams, personal communication, 17 December 2010). As representatives were settling back in their chairs to ponder this, the facilitator provided a short, colourful description of the public’s view of the threat as they pictured hordes of rabid raccoons snarling across the bridges from the United States. Each organization clarified the basic actions that it could feasibly undertake and the framework of a strategy was developed. The four key government ministries would assign a task force to provide the leadership that would engage the wider network of organizations across the province. The focus for engagement at the municipal level was the development of a contingency plan that was specific to

Proactive Communications Unfortunately, new rabies concerns were threatening Ontario, which would require different communications strategies. The mid-Atlantic raccoon strain of rabies was spreading northward through the eastern United States and it could arrive in Ontario at any time (Winkler & Jenkins, 1991; Torrence et al., 1992; Torrence et al., 1995; Broadfoot et al., 2001). In anticipation of its arrival, an interagency Raccoon Rabies Task Force was established in 1991 (Rosatte et  al., 1997). The task force was composed of provincial and federal specialists assigned to provide leadership to all organizations that had a mandate or interest in the prevention and control of raccoon rabies (O. Williams, task force chairman, personal communication, 17 December 2010). One of the goals of the Task Force was to develop a contingency plan that would provide the framework for giving information to the public about raccoon rabies (Rosatte et al., 1993; Rosatte et al., 1997). Raccoon rabies was a major public relations concern because raccoons live much more closely with humans than foxes do. Healthy foxes try to avoid people but raccoons go through our garbage, live in our attics, and will even eat out of dog food dishes if the dishes are left outdoors. And of course, there is an abundance of raccoons in urban areas. It is estimated that approximately one million raccoons live in southern Ontario, with densities in Toronto exceeding 100 raccoons/km2 in prime habitat (Rosatte, 2000). If raccoon rabies were to become established in a major metropolitan area such as Toronto, Niagara, or Ottawa, it would be a public relations and public health nightmare. Before the establishment of the task force, a meeting was held in the Niagara region with about 50 representatives

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each municipality (i.e., county or regional municipality). In addition, it was recognized that in this constrained environment, it would be essential to have strong leadership, not just by the assigned task force, but by every lead person within every organization throughout the network (O. Williams, personal communication, 17 December 2010). Excellence in communications was agreed to be essential, yet it had to be efficient, requiring each organizations’ best communicators to collaborate. The meeting ended with each representative returning to their organization with an important message: raccoon rabies was a critical threat that needed immediate action; the required response is a daunting task, but our organization has to deliver only a key action (that is within our legal mandate) to achieve public protection. Within a week, the Provincial Raccoon Rabies Task Force was established with seven representatives from Canadian Food Inspection Agency (CFIA), MOH, OMAFRA, and OMNRF. They developed and led a process of contingency planning across the province over the next few years. Each municipality was provided with a workshop for its leaders and assistance in preparing their own contingency plan that specified how they would keep raccoon rabies out of their area (and thus out of Ontario), how they would contain an outbreak, should it occur, and the actions needed to help people protect themselves and their communities. The task force worked closely with the Niagara municipality (where the first outbreak was anticipated to occur) to develop the first contingency plan. That plan was then used to prepare a “fill-in-the-blanks” template to be used by others. Background material and presentation packages were prepared, and representatives from the task force went to every upper-tier municipality in the province to deliver a six-hour workshop. Workshops typically involved representatives from every organization that had some role to play in rabies control: the local health unit (who ended up taking the lead for the plans), police department, clerk’s office, animal control companies and/or trappers’ council, and local offices of the OMNRF, OMAFRA, MOH, and CFIA. The contingency plan template was twelve pages and was provided in digital format (relatively new technology that enabled a person to prepare a document on a computer, typing in their specific details in the blanks provided!). It covered prevention, detection, containment, and ­communications/education. In each section, the planners were asked to identify specific actions to take relative to the potential needs and risks, and then name the person or office (along with their contact information) with responsibility for the action.

At the provincial level, the task force prepared and followed a transfer plan and a communication plan. The communication plan covered a complete range of actions from news releases to development of curriculum support materials for school teachers (O. Williams, personal communication, 17 December 2010). Each municipality was encouraged to prepare a communication plan as well, using the materials that were prepared for them by the provincial team. The transfer plan covered the process of relationship building, conflict resolution, education/training, and ownership development. In addition to this planning, one of the key messages that had to be communicated to the public was to not relocate wildlife. The relocation of raccoons in the United States was responsible for long-distance movements of rabies into previously uninfected areas (Nettles et al., 1979; Slate, 1985). In Ontario raccoons have been intentionally and unintentionally relocated by wildlife rehabilitators, nuisance animal control companies, homeowners, truckers, and boaters (Rosatte et al., 1997). Providing that the message was communicated effectively, the public being convinced of the importance of not relocating wildlife (even if it appeared healthy), would be a positive step towards prevention.

Entering the Technological Era In today’s technological world, information needs to be made available as soon as possible. Individuals want to find the information they are looking for in a matter of seconds. If it is not immediately available, they give up looking or get side-tracked. Texting, tweeting, and blogging has made it possible for good news stories and misinformation to spread at lightning speed. It’s essential for individuals to be able to find factual information first as it can be difficult to correct misinformation after it has become popular belief.

The 2000s While both ORV and TVR control programs continued, the technological era progressed and the job of communicating quickly became easier. To meet the requirements of the Environmental Bill of Rights, it was essential to provide 30 days’ notice to the public for any programs being conducted on private property. Historically, this used to involve a few staff determining which municipalities were going to be affected and which municipalities were immediately adjacent to the planned area (the ORV area might need to be expanded at the last minute). After this list was determined, an information package that contained a letter

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Prevention and Management of Rabies in Canada

outlining the program, a fact sheet on the rabies bait and vaccine, and a map of the proposed area had to be mailed to each of the municipalities involved (J. Sirois, personal communication, 17 December 2010). The adjacent municipalities were also sent an information package after the main mailout was completed. This was a very labour intensive and time-consuming task. Today, however, mass communication is a simpler process. A one- or two-page electronic document is prepared that outlines the program and provides links on where to find more information on the baits and vaccine and where to find an up-to-date map of the ORV area. This document is then sent by electronic mail to all municipalities in the province. What used to take five days is now accomplished in just a few minutes. With municipalities, other government agencies and special interest groups must be notified. Historically, an information package for each representative within these organizations was prepared, but this same information is now distributed electronically via email. Not only is this method faster and easier, but it is also more economical; there are no costs for photocopying or postage and fewer staff are required. In many cases, only one individual within an organization needs to be contacted, and they pass the information along to other staff. A good example of this is the Ontario Ministry of Health and Long-Term Care (MOHLTC). The main contact forwards the email to all of the medical officers of health in the health units that are affected. The medical officer of health will then forward it to all the pertinent staff in that health unit. With the ease, speed, and simplicity of this method, an early notification of upcoming rabies control programs can be sent and a follow-up reminder notice can be resent to each agency a week or two before the program begins (a shared communications plan between Ontario Ministry of Natural Resources and Forestry [OMNRF] and MOHLTC). Communicating with reporters is now much easier. With the localized programs such as TVR, an email can be sent to reporters containing a couple of relevant facts about the program to peak their interest, one or two photos, and an invitation to do an interview. This gives smaller media outlets the opportunity to provide coverage of our programs. By receiving high-quality photos or video for their use, they are able to complete a story simply by doing a telephone interview and using the stock images provided. This greatly reduces costs for the smaller media outlets as they do not have to cover travel costs for a reporter or photographer, and it results in much better coverage by smaller media than occurred previously.

Other Communications Methods While many media options are available to the public today, it is not always possible to ensure that all media provide coverage of a specific program. It is still necessary to do on the ground communication methods using fact sheets, warning labels (Figures 33b.3 and 33b.4), signs (Figures  33b.5 and 33b.6), and pamphlets (Figure 33b.7). All baits and live traps are labelled with a sticker providing a toll-free number that individuals can call for more information. Pamphlets and fact sheets (also providing the toll-free number) are distributed to landowners that we come in contact with. The toll-free number continues to be an inexpensive and easy way to encourage questions and comments from the public. People are much more likely to ask a question if they don’t have to pay long-distance charges. This toll-free number is continually monitored during periods when field programs are underway or have just finished. At other times of the year, the voice-mail for this information hotline is monitored at least once a day. People who have questions about rabies or the rabies control programs can call this number to speak directly to a person or leave a voice-mail to have their call returned. On occasion, voicemail messages proved very useful to OMNRF staff. One such message left by a caller was a message regarding bedbugs and rabies. Toronto Public Health had been doing an awareness campaign on bedbugs. The caller was quite concerned about the probability of a bedbug eating a rabid bat and then biting him while he slept. Answering this call directly by OMNRF staff would have presented a laughable image of this gigantic bedbug consuming a bat and then hiding in the caller’s bed. Questions like this emphasize the need for continued public education. Another modern tool for communicating is the Rabies in Ontario website (http://www.ontario.ca/rabies), which provides comprehensive information on everything rabies related as well as links to other relevant websites. The website can be updated quickly whenever required, and it includes a link to a webmail account where individuals can submit questions on rabies directly to OMNRF staff. The Rabies Reporter was another useful tool for communication. This newsletter was published quarterly and provided information on the status of rabies in Ontario, rabies control programs, and other stories of interests for individuals that work with rabies or rabies vectors. The newsletter was distributed free to anyone who wanted to subscribe. When the newsletter was first published in 1990, it was in hard copy. In 1999 it became available online on the Rabies

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Communication Strategies: Provincial Level

Figure 33b.3: Warning label attached to live traps to advise members of the public that a trap-vaccinate-release program is being conducted in the area. Source: OMNRF.

Figure 33b.4: Warning label on rabies vaccine baits distributed by air and by ground in Ontario.

Figure 33b.5: Signs posted around perimeter of airports during early ORV programs.

Source: OMNRF.

Source: OMNRF.

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Prevention and Management of Rabies in Canada

Figure 33b.6: Warning posted in areas where foxes were being trapped to be affixed with radio-collars. Source: OMNRF.

in Ontario website, a change that significantly increased its circulation. Several reporters subscribed to the Rabies Reporter to stay current and have a ready source of information for their own articles. Currently the Rabies Reporter is still printed in hard copy semi-annually. Online information is available through the Rabies in Ontario website mentioned above. Sometimes, despite the latest technology available, there is a need to use old-fashioned but proven methods, such as door-to-door campaigns, informational display booths, or educational workshops to target specific audiences. No matter what methods are used, some individuals will always be missed. This was the case with a woman from Kitchener in 2008 who saw low-flying aircraft. This individual did not

Figure 33b.7: Rabies pamphlet distributed to members of the public. Source: OMNRF.

have a computer and only subscribed to one small, local newspaper, so she had never heard of the ORV programs. After raccoon rabies was diagnosed in Ontario, OMNRF staff did a door-to-door campaign to distribute fact sheets

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Communication Strategies: Provincial Level

to the landowners in the areas surrounding the confirmed cases (L. Bruce, personal communication, 2009). This campaign not only educated the public but provided an opportunity to gather information on whether any individuals had observed ill raccoons in the area. Flyers were also distributed to all households in the areas where baits containing ONRAB rabies vaccine were distributed in 2006 and 2007 (see Chapter 17 for more information on ONRAB). The flyers were a requirement of the permit to release the vaccine bait, and they notified the public that the vaccine was being distributed and that follow-up live-trapping programs would be conducted to assess the effectiveness of ONRAB. This helped facilitate landowner permission for the live trapping. Workshops can also be especially effective when you are educating a very specific group of individuals, such as the workshop that was held in Ottawa for wildlife rehabilitators, animal control agencies, and enforcement personnel. In response to raccoon rabies being confirmed in Ontario, a high-risk area was established in 2000 prohibiting the relocation of rabies vector species (raccoons, skunks, and foxes) (Rosatte, et  al, 2009). Subsequent to these new rules on relocation was a new requirement for wildlife rehabilitators to complete a course on rabies vector species before being permitted to rehabilitate those species (T. Gomer, personal communication, 2005). To help explain these new rules to the people who were affected by them and to the people who would be enforcing them, a one-day educational workshop was held in 2002. The workshop not only explained the new rules but also provided the science on why the rules were necessary; this education was essential because wildlife rehabilitators had been vocal in their opposition to the new rules. Information booths can also target specific audiences. For example, booths were set up at the Ontario Fur Manager’s Federation Rendez-vous, which is attended almost exclusively by fur harvesters and their families. These booths can also provide information to a large number of people;

such as at the Toronto Sportsmen’s Show, Hunting Show, or International Plowing Match. These exhibits are multi-day events attended by thousands of individuals – mostly people who love the outdoors and rural landowners in southern Ontario who are the individuals most affected by rabies control programs.

Discussion There is no perfect recipe for communications but good communication depends on a few fundamental things: the message is simple, the information is correct, and communications are targeted. Ignoring one of these basic principles can result in wasted efforts. The best communication methods are different for every situation but sufficient advanced preparation is essential to ensuring that the message is delivered effectively. Poor planning can result in something being common knowledge in one area but unknown a few kilometres away because a particular newspaper or radio station was not notified. And of course, timing is everything. Daily newspapers are restricted to large, urban areas, so notifying rural newspapers a few days before a program begins could result in them publishing the story after the fact, when the news is already history. Recognizing the scale of the program is necessary. For large programs that target a cross-section of society, it is important to develop a communications strategy that targets the entire cross-section. This may require working with other agencies and determining which agency should be the team leader. As with any communication, the information to be relayed needs to come from a credible source – someone who has the experience and skills to influence the public. Good communications also build on existing relationships. All agencies must be committed to providing the resources required to communicate effectively, and their leadership must commit to those efforts. After all, the leaders are the ones who control staff time and budgets.

References Broadfoot, J., Rosatte, R., & O’Leary, D. (2001). Raccoon and skunk models for urban disease control planning in Ontario, Canada. ­Ecological Applications, 11(1), 295–303. https://doi.org/10.1890/1051-0761(2001)011[0295:RASPMF]2.0.CO;2 Carpenter, A. (1890, September). Rabies and the muzzling order. British Medical Journal, 767. Retrieved from https://www.jstor.org /stable/25278126

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Prevention and Management of Rabies in Canada Hansard. (1890, May 5). House of Commons Debates, 344, 142–144. MacInnes, C. D., Smith, S., Tinline, R., Ayers, N. R., Bachmann, P., Ball, D., ... Voigt, D. R. (2001). Elimination of rabies from red foxes in eastern Ontario. Journal of Wildlife Diseases, 37(1), 119–132. https://doi.org/10.7589/0090-3558-37.1.119 Nettles, V., Shaddock, J., Sikes, R., & Reyes, C. (1979). Rabies in trans-located raccoons. American Journal of Public Health, 69(6), 601–602. https://doi.org/10.2105/AJPH.69.6.601 Rosatte, R. (1988). Rabies in Canada: History, epidemiology and control. Canadian Veterinary Journal, 29, 362–365. Retrieved from https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1680921/ Rosatte, R. (2000). Management of raccoons (Procyon lotor) in Ontario, Canada: Do human intervention and disease have significant impact on raccoon populations? Mammalia, 64(4), 369–390. https://doi.org/10.1515/mamm.2000.64.4.369 Rosatte, R., Power, M., MacInnes, C., & Lawson, K. F. (1990). Rabies control for urban foxes, skunks and raccoons. In L. R. Davis & R. E. Marsh (Eds.), Proceedings of 14th Vertebrate Pest Conference (pp. 160–167). Sacramento, CA: University of California. Rosatte, R., Power, M., MacInnes, C., & Campbell, J. (1992). Trap-vaccinate-release and oral vaccination for rabies control in urban skunks, raccoons and foxes. Journal of Wildlife Diseases, 28(4), 562–571. https://doi.org/10.7589/0090-3558-28.4.562 Rosatte, R., MacInnes, C., Power, M. J., Johnston, D. H., Bachmann, P., Nunan, C., ... Calder, L. (1993). Tactics for the control of wildlife rabies in Ontario (Canada). Revue Scientifique et Technique (International Office of Epizootics), 12(1), 95–98. https://doi.org/10.20506 /rst.12.1.670 Rosatte, R., MacInnes, C., Williams, R., & Williams, O. (1997). A proactive prevention strategy for raccoon rabies in Ontario, Canada. Wildlife Society Bulletin, 25, 110–116. Retrieved from https://www.jstor.org/stable/3783292 Rosatte, R., Donovan, D., Allan, M., Bruce, L., Buchanan, T., Sobey, K., ... Wandeler, A. (2009). The control of raccoon rabies in Ontario, Canada: proactive and reactive tactics, 1994–2007. Journal of Wildlife Diseases, 45(3), 772–784. https://doi.org/10.7589/0090-3558 -45.3.772 Slate, D. (1985). Movement, activity and home range patterns among members of a high density suburban raccoon population (­Unpublished doctoral dissertation). Rutgers University, New Brunswick, New Jersey. Steele, J. (1988). Rabies in the Americas and remarks on global aspects. Reviews of Infectious Diseases, 10(Suppl. 4), s585–s597. https:// doi.org/10.1093/clinids/10.Supplement_4.S585 Tabel, H., Corner, A., Webster, W., & Casey, C. (1974). History and epizootiology of rabies in Canada. Canadian Veterinary Journal, 15(10), 271–281. Retrieved from https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1696688/ Torrence, M., Jenkins, S., & Glickman, L. (1992). Epidemiology of raccoon rabies in Virginia, 1984–1989. Journal of Wildlife Diseases, 28(3), 369–376. https://doi.org/10.7589/0090-3558-28.3.369 Torrence, M., Beck, A., Glickman, L., Perez, C., & Samuels, M. L. (1995). Raccoon rabies in the mid-Atlantic (epidemic) and s­ outheastern states (endemic), 1970–1986: An evaluation of reporting methods. Preventative Veterinary Medicine, 22(3), 197–211. https://doi.org /10.1016/0167-5877(94)00410-K Winkler, W. G., & Jenkins, S. (1991). Raccoon rabies. In G. M. Baer (Ed.), The natural history of rabies (2nd ed., pp. 325–340). Boca ­Raton, FL: CRC Press.

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34 Costs of Rabies Management David J. Gregory1 and Beverly Stevenson2 1

Canadian Food Inspection Agency (Retired), Ottawa, Ontario, Canada Ontario Ministry of Natural Resources and Forestry, Peterborough, Ontario, Canada

2

Introduction Preventing rabies in humans is at the core of the rabies control programs in Canada. This chapter outlines some of the program costs associated with reducing the risk of human exposure to rabies. Submissions data have been reported in Canada since 1985. Beginning in 1989–90, when rabies control programs for wildlife began in Ontario and were subsequently instituted in several other provinces, submissions have steadily declined and the percentage of submissions positive for rabies has also declined, from over 20% annually to about 6% annually in 2018 (Table 34.1). Furthermore, no human cases of rabies occurred between 1970 and 2018 as a result of exposure to domestic animals with rabies in Canada. Compared to many other countries, such as the United States (Centers for Disease Control and Prevention, 2014) and Africa and Asia (Fooks, 2014), this measure of success is exceptional. This success can be attributed to a number of factors: (1) the development of a multidisciplinary program under the umbrella of the Health of Animals Act and Regulations since 1905; (2) the development of new and improved diagnostic tests for rabies; (3) the development of human and animal vaccines to protect against rabies, resulting in lowered incidence in pets and a gradual decrease in post-exposure treatments for humans; (4) the elimination of fox rabies in southern Ontario by a highly successful wildlife oral baiting program, resulting in fewer sample submissions and therefore lower costs for testing; (5) the successful control of raccoon invasions from south

Table 34.1 Annual specimen submissions in Canada. Year

Positive

Negative

Total

1985 1986 1987 1988 1989 1990 1991 1992 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012 2013 2014 2015 2016 2017 2018

2,335 3,871 2,741 2,264 2,197 2,299 2,073 2,262 1,890 856 444 293 234 371 500 664 441 343 266 254 248 229 274 235 145 123 115 142 115 95 155 403 245 183

10,691 12,916 12,020 10,334 10,094 10,474 10,224 10,720 10,853 8,737 7,837 7,414 11,034 8,170 7,208 8,052 9,078 8,150 8,096 7,394 6,621 7,715 7,433 7,101 5,370 4,775 4,289 3,709 3,351 1,823 2,144 2,664 2,536 2,727

13,026 16,787 14,761 12,598 12,291 12,773 12,297 12,982 12,743 9,593 8,281 7,707 11,268 8,541 7,708 8,716 9,519 8,493 8,362 7,648 6,869 7,944 7,707 7336 5,515 4,898 4,404 3,851 3,466 1,918 2,299 3,067 2,781 2,842

Source: compiled from CFIA data.

% Positive 21.84 29.97 22.80 21.91 21.77 21.95 20.28 21.10 17.41 9.80 5.67 3.95 2.12 4.54 6.94 8.25 4.86 4.21 3.29 3.44 3.75 2.97 3.69 3.31 2.70 2.57 2.61 3.69 3.30 5.00 6.70 13.10 8.80 6.40

Prevention and Management of Rabies in Canada

Table 34.2 Government agencies from which cost data was available. Each source of data is discussed in the chapter. Government

Agency

Costs Associated With

Federal

Pet vaccination Canadian Food Inspection Agency

Provincial

Indemnity (federal and provincial) Salary Quarantine Specimen testing PEP Wildlife rabies program

Public Health Ontario (now Ministry of Health) Ontario Ministry of Natural Resources and Forestry

Table 34.3 Positive rabies results in Canada, 1985 to 2012, survey samples included. Prov./Terr. BC AB SK MB ON QC NB NS PE NL NT NU YK  Total   % Total

Total 321 250 2,632 2,032 19,146 3,175 79 14 5 119 117 294 0 28,184

Cat/Dog 4 13 104 99 1,473 413 1 2 1 6 24 52 0 2,192 7.8

Bat

Raccoon

Skunk

Fox

Other

Live

Wild

% Total

311 114 152 28 1,020 151 12 7 1 1 0 0 0 1,797 6.4

0 0 5 5 294 145 55 0 0 0 0 0 0 504 1.8

4 116 2,211 1,623 4,466 260 10 0 0 0 0 0 0 8,690 30.8

0 1 1 33 8,820 1,788 0 3 3 102 87 226 0 11,064 39.3

2 1 6 12 57 12 0 0 0 0 2 0 0 92 0.3

0 5 153 228 2,812 353 1 2 0 3 0 0 0 3,557 12.6

0 0 0 4 204 53 0 0 0 7 4 16 0 288 1

1.1 0.9 9.3 7.2 67.9 11.3 0.3 0 0 0.4 0.4 1 0 100

Live = livestock, Wild = coyote and wolf, Other = all other animals Source: compiled from CFIA data.

of the border; (6) research into new diagnostic methods and new control methods; (7) a better understanding of the animal biology of the important vector species of rabies; and (8) a Canada-wide improved and far reaching public health communications network. Cost estimates for rabies control have often been limited to dog vaccination programs or human ­post-exposure prophylaxis (PEP) (Anderson & Shwiff, 2013; Shwiff et al., 2007). Meltzer and Rupprecht (1998a, 1998b) point out that controlling rabies in animal populations is often a multiyear program involving many disciplines, but few papers recognize this fact and do not allow for other costs and benefits. This chapter deals with the costs of rabies management in Canada using information available between 1985 and 2012 from various agencies, outlined in Table 34.2. With the exception of indemnity data Ontario data are used although all provinces and territories participated at their own level in the program. The decision was made to use data on costs from only two Ontario agencies because

Ontario carried the brunt of the rabies outbreak between 1985 and 2012 in terms of submissions and rabies cases (Tables 34.3 and 34.4). No attempt was made to determine the costs of the many other federal, provincial, and territorial programs involved in rabies control, but reference to their programs can be found in the chapters on the provinces and territories in Part 3.

General Considerations Rabies control and management in Canada is mandated under the Health of Animals Act and Regulations at the federal level, making rabies a reportable disease since 1905. With this mandate, Agriculture Canada (now the Canadian Food Inspection Agency or CFIA) has provided an umbrella under which provincial and territorial rabies management programs acted, using an integrated, cooperative approach involving public and private human and animal health professionals from many agencies, an

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Table 34.4 Submissions, Canada, 1985 to 2012, survey samples included. Prov./Terr. BC AB SK MB ON QC NB NS PE NL NT NU YK  Total   % Total

Total

Cat/Dog

Bat

Raccoon

Skunk

Fox

Other

Live

Wild

% Total

8,103 16,968 18,757 13,849 150,603 50,821 3,463 1,356 330 1,291 541 678 35 258,692

2,009 6,107 7,557 6,629 47,540 30,072 926 349 120 277 226 277 22 100,102 38.7

4,788 3,433 2,074 264 20,340 5,568 430 520 108 73 11 0 3 32,824 12.7

192 206 488 618 22,112 4,151 1,291 205 14 0 0 0 0 29,085 11.2

136 4,400 4,685 3,027 11,865 1,107 166 19 10 0 1 0 0 25,280 9.8

22 182 584 412 17,402 3,650 206 85 28 825 177 348 3 23,902 9.2

688 1,230 989 718 15,948 3,199 191 57 18 60 18 20 0 22,448 8.7

158 780 1,747 1,942 14,273 2,688 229 98 31 18 0 0 4 21,968 8.5

110 630 633 239 1,123 386 24 23 1 38 108 33 3 3,241 1.3

3.1 6.6 7.3 5.4 58.2 19.6 1.3 0.5 0.1 0.5 0.2 0.3 0.0 100.0

Live = livestock, Wild = coyote and wolf, Other = all other animals. Source: compiled from CFIA data.

approach often referred to as “one health.” The costs of this multidisciplinary program have never been fully itemized and, in many cases, little is known of the actual costs. An attempt to bring together all the known and itemized costs goes beyond the scope of this chapter. Instead, this chapter attempts to document what is known about some of the costs of the rabies management program in Canada between 1985 and 2012, with a focus on Ontario in the case of health and wildlife. Data are presented for two time frames: (1) 1950 to 1984, before the initiation of the vaccination programs against wildlife in various provinces; and (2) 1985 to 2012, following the initiation of the vaccination program for wildlife and the beginning (in 1985) of CFIA’s lab sample control system, which provided consolidated data on the submissions of rabies specimens for testing. Furthermore, the total cost of the rabies program is only estimated for the second period for which three major datasets were available (Table 34.2): (1) CFIA and its domestic animal control; (2) the Ontario Ministry of Health and post-exposure treatment of humans; and (3) the Ontario Ministry of Natural Resources (and Forestry in 2014) with the aerial baiting of wildlife. This chapter also identifies some of the problems associated with obtaining these data. The problems of determining the costs were compounded by (1) multidisciplinary involvement, with differing mandates and budgets, such as CFIA being involved with domestic animal rabies and preventing contact with humans; health authorities preventing human rabies by pre- and post-exposure vaccination; and wildlife agencies involved with managing wildlife but becoming involved in

rabies control; (2) changing programs over the years, with additional methods of control, including vaccination of dogs and wildlife; (3) changing costs through time, including indemnity payments for livestock and human vaccine costs; (4) archiving data or destroying them after 10 years, with the remaining archival data accessible only through Access to Information permits; (5) multidisciplinary jurisdictions requiring different types of data and having differing modes and programs for data collection and, in the case of CFIA, changing data collection and recording systems, sample location data, and fiscal versus annual recording; and (6) each province and territory having its own budget for management of rabies, which included trapping and depopulation of species, data dispersal, vaccination clinics and public health programs, and communication delivery.

Cost of Rabies Management in Canada Costs to Agriculture Canada/Canadian Food Inspection Agency The reported and estimated CFIA costs are discussed under five categories: (1) vaccination of domestic animals, (2) indemnity, (3) CFIA budget and salaries, (4) quarantines, and (5) rabies test costs. Some of the undetermined costs for CFIA are the salaries associated with clerical and non-veterinary inspection staff; maintenance of laboratories for research and diagnosis; maintenance of field offices (national, area, and district offices); training and education of all staff; maintenance of vehicles; educational materials; attendance at

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Prevention and Management of Rabies in Canada

meetings; communications; and estimates of costs incurred by the public during program operations (attending public information sessions, investigations, transportation, liability claims, farm quarantines, and loss of production).

epizootic in northern Canada and provides the following details of vaccine production: in 1950, 3300 doses of vaccine distributed; in 1951, 5952 doses of vaccine distributed; and in 1952, 3000 doses distributed, most being sent to the Northwest Territories. In a letter in 1956, Dr K. F. Wells, veterinary director general, alluded to the effectiveness of vaccination use in the north, noting that of 15,000 dogs vaccinated during the outbreak at that time in northern Ontario, no cases of rabies had occurred (Wells, 1956).

VACCINATION OF DOMESTIC ANIMALS

Background

Early control of rabies in domestic pets depended on clinical diagnosis and dog control (quarantines, muzzling, and elimination of strays) to prevent its spread to humans. Vaccination of pets against rabies using Canadian-produced vaccine beginning in 1948 ushered in a new era of control (Defries, 1968). The demand for rabies vaccine for preventing rabies in dogs probably began in 1947 with a push by Dr Charles A. Mitchell, Dominion animal pathologist, to have a Canadian company produce rabies vaccine. This occurred for two reasons: a change in regulations requiring vaccinations of all dogs before entering Canada and their shipment to the United States, and a threat of rabies invasion from the north through wildlife vectors. Dr P. J. G. Plummer, Animal Disease Research Institute (ADRI), Hull, Quebec had been sent to the Northwest Territories to investigate a disease resembling rabies, diagnosed rabies using staining of Negri bodies in April 1947, and brought tissue specimens to ADRI for inoculation with virus culture. The test was successful. Subsequently, Dr Mitchell wrote to Dr R. D. Defries, director of Connaught Medical Research Laboratories in Toronto, with a request for vaccine as soon as possible (Mitchell, 1947a). Lederele Laboratories Division, North American Cyanamid Limited, had also been consulted to provide information on their rabies vaccine as it appears that the RCMP had been vaccinating dogs in the Northwest Territories using the Lederele vaccine (Mitchell, 1948). Dr Mitchell, however, did not want to issue import permits for vaccine from a US company, preferring to have better control with a Canadian company (Mitchell, 1947b). In 1914 Connaught Laboratory had begun research to produce products for the prevention and treatment of diseases, first in the human medical field, and then by 1935 in the veterinary field. Further correspondence from Dr Mitchell on 30 January 1948 indicates that the use of vaccine to prevent rabies in dogs in the Northwest Territories was being encouraged as it was the only method shown to have any promise in controlling the disease (Mitchell, 1948). The minutes of the Committee on Veterinary Production at Connaught Laboratories on 25 February 1952 (Dr C.  J.  Rutty, personal communication, 16 October 2019) reports on renewed interest in rabies vaccine given the

Clinics

As wildlife rabies spread from the north to the south and east of Canada, vaccination clinics for dogs and cats were held extensively to prevent human rabies. In Ontario the clinics, often provided after the disease had been reported in an area, were provided free to the public by the Agriculture Canada (AC). Some costs to the government to provide these clinics are listed below. Until 1953 the use of rabies vaccines in Canada was restricted to AC officers, with the exception of authorized personnel in the north and private practitioners certifying dogs for export to the United States and working in areas surrounding quarantines in the northern part of the western provinces. Following requests from national and provincial veterinary associations, Dr T. Childs, veterinary director general for the Department of Agriculture, changed the policy in 28 February 1953 to permit sale to and use by private practitioners of rabies vaccine (Childs, 1953). The vaccine used in the early vaccination clinics was the chick embryo origin vaccine produced by Connaught Medical Research Laboratories at the University of Toronto (Connaught Medical Research Laboratories and University of Toronto, 1956). By 1965 this had been replaced by the ERA rabies vaccine, also produced by Connaught, a modified live virus porcine tissue culture origin vaccine (Connaught Medical Research Laboratories, 1965). The listed price (suggested retail price to veterinarians) in 1956 was 80 cents for a one-dose vial of chick embryo origin vaccine. This was probably sold to the federal officers for the free vaccination clinics for the net price of 60 cents for a one-dose vial. Given the need for syringes, diluent, tags, and so on, for the vaccination, the overall cost was probably about $1 per pet vaccinated (Connaught Medical Research Laboratories and University of Toronto, 1956). Using the total number of pets vaccinated in Quebec, Ontario, and the Northwest Territories between 1955 and 1986 (870,282  + 9856 = 880,138) using archived CFIA documents, a minimum cost of $880,138 is realized (Table 34.5). The “Other”

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Costs of Rabies Management

Table 34.5 Number of dogs, cats, and other animals vaccinated between 1955 and 1986 in Ontario and Quebec.

1754 dogs and 330 cats were vaccinated at 18 clinics during five and a half days. Itemized costs were as follows:

Year

Dog

Cat

Other

Total

1955 1956 1957 1958 1959 1960 1961 1962 1963 1964 1965 1966 1967 1968 1969 1970 1971 1972 1973 1974 1975 1976 1977 1978 1979 1980 1981 1982 1983 1984 1985 1986  Total

9,374 48,430 1,963 53,356 16,527 2,604 – – – – – – 3,429 0 3,751 12,580 14,384 121,913 55,531 409 48,925 30,108 18,852 22,542 14,532 16,449 6,152 24,853 4,147 5,409 0 249 546,492

165 23,450 105 23,337 16,046 0 – – – – – – 2,215 0 2,275 7,303 8,673 65,524 29,898 98 26,711 14,121 10,400 14,592 8,262 10,090 4,163 14,258 3,902 4,620 0 109 298,643

0 36 1 363 139 0 – – – – – – 44 0 49 31 57 56 0 0 0 0 0 0 0 0 0 0 0 0 0 0 835

9,539 71,916 2,069 77,056 32,712 2,604 129 1,213 985 585 5,377 16,023 5,688 0 6,075 19,914 23,114 187,493 85,429 507 75,636 44,229 29,152 37,134 22,794 26,539 10,315 39,111 8,049 10,029 0 358 870,282

Mileage, private car: 594 miles at eight cents a mile Mileage, a government car: 1204 miles – f­ ederal cost Meals Radio advertising Television advertising Newspaper advertising Casual veterinarians

$47.52 $19.45 $30.75 $50.00 $50.00 $42.18 $240.00 $429.90

A second example comes from Bruce County, where 4892 dogs and 3491 cats were vaccinated at 33 clinics during 14 days with the following costs: Casual veterinarians, 13 days at $30.00 Room and meals, full-time veterinarian Mileage, private car: 790 miles at eight cents a mile Mileage for federal veterinarian: 3463 miles – federal cost Newspaper advertising Radio advertising Telephone

$390.00 $410.00 $63.20 N/A $402.14 $30.00 $15.00 $1310.34

While the costs provided are those for federally funded clinics, by 1953 vaccine had become available to private veterinarians. This would have had additional costs for vaccination of pets throughout Canada, though no figures are available. The examples given were for clinics in Ontario but the costs of vaccination were for Ontario, Quebec, and the Northwest Territories (Table 34.4). A cost to vaccinate pets during the same time frame would have also occurred in the other provinces but were not determined. The 1982 clinic cost $118,628 ($2 per vaccine) while the cost per pet at the Dufferin County clinic was about 10 cents and that for the Bruce County clinic about 16 cents, given the available data. An estimate of pet vaccination is provided later in the chapter.

Note: While the vaccine was listed as safe for use in dogs, cats, cattle, and swine, two dogs died during one clinic. Between 1961 and 1966 archival data gives only total of animals. No data were available in 1968 and 1985, possibly because vaccinations were then done by private practitioners. Source: compiled from CFIA data.

category (Table 34.5) included animals such as rabbits, fox, skunks, pony, sheep, monkey, guinea pig, and raccoons. A  report by Ontario’s Inter-ministerial Committee on Rabies (1976), noted a cost of $82,995 for 46,108 animals vaccinated at free clinics by AC. Further, a report of vaccination clinics held in 1982 in 10 counties of Ontario, at 217 sites during 118 clinic days, gave a total of 59,314 dogs and cats vaccinated at a cost of $118,628 (using a $2 cost per pet). The premises used, the advertising, and the clinical assistance were provided by the township requesting the clinic (an undetermined cost). In all cases salaries of the federal veterinarians were not included in the costs. AC reports (1958) provide two examples of clinicassociated costs. The first was in Dufferin County, where

INDEMNITY

Background

Indemnification of domestic livestock dying of rabies began in the mid-1950s, not as a disease control measure but as an emergency program designed to defray the losses by farmers for their livestock as the northern rabies epizootic affected Ontario. By 1 April 1958 the federal government had paid

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Prevention and Management of Rabies in Canada

Table 34.6 Maximums paid ($) for rabies under the Rabies Indemnification Regulations, by year of regulation change.

Year

Cattle

Horse

1958 1963 1973 1980 1982 2009

250 100 200 500 1000 400

100 40 140 350 500 200

Table 34.7 Annual rabies-positives, clinicals, and indemnity for Ontario, Quebec, Manitoba, and New Brunswick, 1960 to 2012.

Sheep, Swine, Goats 40 16 40 100 200 80

Source: compiled from CFIA data.

out $109,662 to Ontario farmers in indemnity. This Ontario program was cancelled and then replaced in 1958 with a federal-provincial cost-sharing program under the Rabies Indemnification Regulations (under the Appropriations Act). Under this program, farmers could be reimbursed for livestock dying of rabies, the federal portion was 40% and the provincial share 60% of certain maximums set by the minister for cattle, horses, sheep, swine, and goats. Four provinces, Manitoba, Ontario, Quebec, and New Brunswick joined the program. The maximums were subject to a Memorandum of Understanding between participating provinces and the federal authority and changed over time (Table 34.6). It is not known why the changes occurred but may have been due to changing economic conditions. Payment was authorized by the federal district veterinarians based on a positive rabies diagnosis. The indemnity defrayed the cost of losses to farmers and encouraged them to report rabid animals on their farm. However, with a large increase in submitted specimens during the outbreak of 1986, a policy of clinicals was instituted. If a farm had more than one positive rabies diagnosis, the district veterinarian presumed that any further animals showing clinical signs of rabies on the same farm were positive and authorized payment of indemnity, deeming them “clinical.” Note that while clinical cases were reimbursed, they were not added to the data for laboratorydiagnosed positive cases until the 2000s.

Payments

While four provinces signed on to the indemnification agreement, archival data show that in several years Saskatchewan reported clinicals and an indemnity was paid (1964, 1967, 1968, 1970, 1972, 1975, and 1976). These costs for Saskatchewan are not included in Table 34.7. No explanation was found for the payment to a non-participating province. Table 34.7 provides a breakdown of indemnities paid between 1960 and 2012. Between 1960 and 1984, the total indemnity paid amounted to $3,351,052 and, between 1985 and 2012, $3,520,309. Ontario farmers received the largest share of payments, followed by Quebec. Note that up to

Year

Positives Clinicals Federal ($) Provincial ($)

1960 1961 1962 1963 1964 1965 1966 1967 1968 1969 1970 1971 1972 1973 1974 1975 1976 1977 1978 1979 1980 1981 1982 1983 1984 1985 1986 1987 1988 1989 1990 1991 1992 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012  Total

285 1,057 955 1,125 1,370 1,281 1,220 1,343 2,088 2,069 1,354 2,027 1,881 1,641 1,487 1,953 1,400 1,314 1,511 1,539 1,506 1,737 2,244 1,937 1,486 2,064 3,404 2,096 2,002 2,082 2,189 1,972 2,128 1,725 804 388 244 196 267 337 459 333 277 198 197 191 162 227 169 97 87 64 73 62,242

28 74 106 110 240 238 163 165 280 262 205 244 215 255 199 95 134 247 148 102 147 130 173 124 84 166 253 156 129 160 172 97 107 109 87 25 4 4 2 0 7 4 6 1 7 0 0 0 0 0 0 0 0 5,664

8,135 7,366 12,814 20,447 21,831 18,989 45,499 34,999 22,900 55,997 59,131 45,895 41,639 59,224 58,387 85,000 89,729 84,208 64,111 67,171 57,260 71,470 123,210 95,623 89,389 74,317 129,700 175,778 123,124 118,041 122,309 132,854 108,845 125,892 114,878 51,638 23,578 9,888 9,466 3,950 11,691 15,278 12,473 6,360 8,813 4,802 2,132 6,010 7,816 4,640 2,441 705 690 2,740,398

12,202 11,049 19,221 30,670 32,746 28,483 68,248 52,498 34,350 83,995 88,696 68,842 62,458 88,836 87,580 127,500 134,593 126,312 96,166 100,756 85890 107,205 184,815 143,434 134,083 111,475 194,550 263,667 184,686 177,061 183,463 199,281 163,267 188,838 172,347 77,457 35,368 14,832 14,199 5,925 17,536 22,917 18,709 9,540 13,219 7,214 3,198 9,015 11,723 6,960 3,661 1,057 1,035 4,110,626

Total ($) 20,337 18,415 32,035 51,117 54,577 47,472 113,747 87,497 57,250 139,992 147,827 114,737 104,097 148,060 145,967 212,500 224,322 210,520 160,277 167,927 143,150 178,675 308,025 239,057 223,472 185,792 324,250 439,445 307,810 295,102 305,772 332,135 272,112 314,730 287,225 129,095 58,946 24720 23,665 9,875 29,227 38,195 31,182 15,900 22,032 12,016 5,330 15,025 19,539 11,600 6,102 1762 1725 6,851,024

Source: compiled from CFIA and Agriculture Canada data.

1995, any payments of less than $5000 by a province were not listed in the archived data, thus Ontario was always noted while the others may not have been recorded. Federal payments were always reported. The expenditures in the 560

Costs of Rabies Management

archival data are often rounded so that $41,639 (1972) was recorded as $42,000 on the summary sheet for Public Accounts in 1971–1972; New Brunswick appeared three times with indemnity payments in 1967–1968, 1968–1969, and 1969–1970, and with one clinical report in 1970–1971 but no indemnity was recorded by the archives. The height of indemnity payments in 1986 (Figure 34.1) was the result of two factors: positive rabies cases in Canada (3872 cases) peaked, and in the four participating provinces (3404 cases), indemnity payments had been raised in 1982 (Table 34.6). Table 34.7 also shows the decreasing number of clinical cases. By 2005, none were reported and there were no indemnity payments for 2012–2013. Indemnity data for this section were obtained from two sources: (1) between 1959 and 1995, from Library Archives Canada, Ottawa, online data set under Federal-Provincial Shared-Cost Programs by Province/Public Accounts; and (2) Access to Information (ATIP) requests to CFIA’s Financial Planning and Management Services in Ottawa.

The initial effect of the Ontario oral baiting program on indemnity costs is striking (Figure 34.1). Between 1990 and 2000 there was an 8.7-fold decrease in annual costs. Between 1990 and 2010, when the control programs in New Brunswick and Quebec were activated, there was a 188-fold decrease in payments. Table 34.8 illustrates the effect of the oral baiting programs on the payments to provinces, which started in 1995. The table gives a breakdown by species affected by rabies and compensated under the Memorandum of Understanding mentioned previously. BUDGETS AND SALARIES

Background

The Health of Animals budget was part of CFIA’s annual estimates submitted by the Minister of Agriculture for approval by the Treasury Board at Cabinet. Once approved, the budget was issued to the president of CFIA for allotment to the different sections. Indemnity

Figure 34.1: Annual total indemnity payments (black line) compared with the total number of rabies-positive animals (dots) and “clinicals” (grey line). The vertical grey lines represent years in which indemnity maximums changed (see Table 34.3). Source: created from CFIA data.

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Prevention and Management of Rabies in Canada

Table 34.8 Federal and provincial indemnity payments for four years, by species and province. Federal Share, 40% ($)

Provincial Share, 60% ($)

Total Fed. Year Province Bovine Equine Porcine Ovine Caprine Share Bovine ON 1983 QU MB

ON 1995 QU MB

ON 2000 MB

ON 2010 MB

84,433 4,384 295 24 800 2 2,730 200 11 1

188 3

40,876 740 125 4 1,200 200 3 1 4,700 1,000 13 5 4,904 14 6,787 20 1.951 5 490 2

80 1

1,988 900 32 16

2.751 504 38 8 160 2 36 2

91,893 370 800 2 2,930 12 95,623 384 44,871 175 1,560 6 5,816 21 52,247 202 4,904 14 6,787 20 11,691 34 1,951 5 490 2 2,441 7

Total Provincial Total of Both Equine Porcine Ovine Caprine Share Shares

126,649 6,576 295 24 1,200 2 4,095 300 11 1 61,314 125 1,803

282 3

1,110 4 300

7,053 1,500 13 5

2,982 1,350 32 16

4,165 38 240 120 1

7,353 14 10,180

2,926 5 735 2

756 8 54 2

137.839 370 1,200 2 4,395 12 143,434 384 67,345 175 2,340 6 8,724 21 78.409 202 7,356 14 10,180 20 17,536 34 2,926 5 735 2 3.661 7

229,732 2,000 7,325 239,057 112216 3,900 14,540 130,656 12,260 16,967 29,227 4,877 1,225 6,102

Source: compiled from CFIA data.

was a separate allotment provided by the Appropriations Act. For 2006–2007, the CFIA main estimates to Cabinet totalled $637.6 million, with $353.5 million allotted to the program activity Food Safety and Public Health animal diseases that are transmissible to humans are effectively controlled within animal populations. This includes activities such as disease surveillance; inspection and monitoring; compliance and enforcement; emergency response to disease outbreaks; eradication activities; and program design and redesign. From the president’s office the allotments were passed to the Health of Animals headquarters, area offices and district offices, and the three laboratories for delivery of the programs. While district staff had time standards allotted to work on activities such as specimen collection and quarantines for rabies (RMS – Resource Management System/MARS – Management Resources and Results Structure), time-tracking of spending at most program levels was not carried out. Control programs for reportable diseases such as rabies in Canada are reviewed regularly and promulgated from the headquarters level of CFIA in Ottawa, managed at the regional office level (now area offices; see Chapter 32)

level, and acted on at the district office level. Veterinarians at these levels would spend a work day involved in more than one program and not dedicated to a single disease. Imports, exports, and eradication programs for brucellosis and tuberculosis, salmonellosis, poultry diseases, rabies, and others occupied their 37.5-plus work hours each week. This section deals with the salaries of the federal veterinary officers determined from the negotiated collective agreement between the CFIA and the Professional Institute of the Public Service of Canada (2014). These salaries are used to determine some costs at the headquarters, area offices, and district offices. No attempt has been made to include costs of other staff members who also played a part in the rabies equation. From these salaries and using RMS/MARS (time standards) for program delivery, costs for specimen collection and transport, and, monitoring of rabies quarantines were estimated. The specimen collection and transport section include submissions and laboratory test costs.

Veterinary Salaries

In 1984 AC (now CFIA) had 117 district offices in all provinces but none in the territories (Agriculture Canada, 1984). 562

Costs of Rabies Management

The number of offices increased in 1985 to 119, with the greatest increase in Ontario because of the rabies outbreak. This number decreased to 111 by 1989, and in 2013 the number of offices operating had been reduced to 72. Assuming headquarters (HQ) and each regional office/area office (RO) had one veterinary officer at VM-04 level and each district office (DO) had two veterinary officers, one at the VM-02 level and one at the lower VM-01 level, the salary cost for veterinarians for the rabies program can be estimated. Additional veterinarians at the levels VM-03 and VM-05 may also manage rabies for part of their work day. Assuming that the veterinarians at the VM-04 level spent 20% of their work week carrying out rabies management duties (the ­calculations take in to account that there is one VM-04 at headquarters), the following salary-based costs were determined: from 1997 to 2012 when there were five VM-04s (one at HQ and four in ROs) salary costs = $1,556,290. Using CFIA VM salary figures for 2012 (see the Appendix to this chapter), an hourly rate for VM-01 and VM-02 level veterinarians was calculated (Professional Institute of the Public Service of Canada [PIPSC], 2014). For simplicity, the two salary levels were averaged since it is not known what veterinarians were present to carry out rabies investigations. The value of $45.17 (VM-01) was used for quarantines and inspection times in collecting samples for submission. If offices used a VM-02 to carry out the rabies investigations, then an additional 15% value was added.

in the Appendix assume that this was done and usually by a district veterinarian (VM-01 or VM-02 level). Nunavut had seven quarantines but was not included in the calculations as the inspections were carried out by non-veterinary ­personnel. The calculations are in the “Quarantines” section. For this one year, the cost came to less than a v­ eterinarian’s annual salary. RABIES TEST COSTS

The overall cost of a rabies test includes (1) the collection of the specimen from the field, (2) the transport of the specimen to the laboratory, and (3) the cost of the testing. These are dealt with separately using RMS/MARS inspection times with veterinary salaries discussed in the Appendix; freight cost for air and ground transport to the laboratory; and a cost per test for 1997 provided by CFIA’s Centre of Expertise in Ottawa (cost assumed for all calculations for test). The costing also includes the surcharge added by delivery companies for transport of dangerous goods under the Transportation of Dangerous Goods Act of Transport Canada between 1980 and 2006. Rabies specimens were deemed dangerous goods up to 2006. After that rabies specimens sent for diagnosis were placed in a lesser risk category and shipped as non-infectious “exempt animal specimen” (see Chapter 22).

Collection of the Specimen

A submission to the Cabinet Committee on Resources Development from the Inter-ministerial Committee on Rabies (1976) estimated the direct costs to the Ontario Government, including estimates from AC for Ontario for 1976 were $775,015:

QUARANTINES

Quarantines are an integral part of the rabies management program. This includes on-farm quarantine of livestock and kennel quarantines for dogs and cats. Import quarantines for cats and dogs are now the responsibility of private veterinarians. Quarantine data were recorded by HQ but later became the responsibility of the area offices. Little data were available at archives, most being disposed of every 10 years. One entry was found for 1982–1983 in which 1743 premises were quarantined province-wide, with 26,215 animals of various species under observation for varying times. Extrapolation of present inspection times to that data was not possible given the large number of differences in the recording process over time. During 2012 CFIA collected quarantine data for all domestic animals in each province and territory, including Nunavut. These data were divided into three categories: three-month quarantine, six-month quarantine, and ten-day observation. Animals under quarantine for these periods were subject to four to eight veterinary inspections for quarantines and three visits for observation. While these inspection visits were not always carried out by veterinary personnel the calculations

Field investigation and laboratory diagnosis for 4914 submissions Free public rabies clinics for 46,108 animals Research and administration

$638,820 $82,995 $53,200

This was one of the earliest reports of laboratory diagnostic costs. For the period under consideration the costs of field investigation and retrieval of specimens were estimated using RMS/MARS time standards (national averages for the investigation) and three hours of the veterinarian’s salary as follows: Attending the premises (phone call, appointment, etc.) Rabies on the farm and possible quarantine Obtaining the sample Travel time 563

30 mins 60 mins 30 mins 60 mins

Prevention and Management of Rabies in Canada

FAT became available in 1968 (Bradley, 1979), replacing the rabies diagnosis by Negri body brain smears. The mouse inoculation test was replaced by the rabies tissue culture infection test (RTCIT) in 1987 (which was less costly and more humane) and discontinued in 2011, after MAbs became available in 1989. The TC test was compared against FAT between 1995 and 2010 as a confirmatory test (n = 66,099, FAT-negative samples with human exposure) but was then discontinued, with FAT being an equally sensitive test but less expensive. The total cost of a specimen diagnostic test result (excluding indirect costs of data communication, etc.), assuming a minimum freight charge of $25.00 and a transport of dangerous goods surcharge of $25.00 (from 1980 to 2006) was as follows:

Packaging and Transport to the Laboratory

At the DO, the specimen was packaged and sent to the nearest Agriculture Canada laboratory by road or air or a combination of both. Packing took 30 minutes, so assuming a VM-01 collected, packaged, and shipped the specimen, the cost was 3.5 × $41.17 = $158.10 (Appendix). The transport cost is then added. Several examples are given, recalling that between 1980 and 2006 a surcharge was added to the specimen container for the transport of dangerous goods. This amount was an extra $15 in Ontario and $45 from the Atlantic region. The cost for the specimen can be assumed to be part of the operating and materials laboratory costs of the specimen test. Transport costs were variable and often depended on the weight of the specimen container and the distance to the laboratory. Specimens from the Northwest Territories, Yukon, and part of Nunavut were sent by air to the Lethbridge Laboratory, which meant a stop in Edmonton, Alberta, and a bus trip to complete the journey. Specimens from BC, Alberta, and Saskatchewan were routed to Lethbridge, usually by bus. Specimens from Baker Lake, Nunavut, Nunavik, and the other provinces were routed to Ottawa Laboratory Fallowfield (OLF). Examples of specimen transport costs by road and air for 2012 are listed below: By air Goose Bay, Labrador, to Ottawa St John’s, NL, to Ottawa Inuvik or Yellowknife, NT, to Edmonton Cambridge Bay or Rankin Inlet, NU  Priority  Normal By ground Vancouver, BC, to Lethbridge Edmonton, AB, to Lethbridge ON locations and Atlantic locations

Collection and packaging of specimen by a VM0A Transport and surcharge cost ($25.00 + $25.00)

$50.00

FA Test

$30.25

Total cost

$238.35

These specimen cost values may be higher or lower depending on the location from which the specimens are shipped and whether a veterinarian carries out all the collecting and packaging. Table 34.9 provides two scenarios for the total test cost of rabies specimens in a given period: (1) 1993 to 2006 when transport of dangerous goods regulations were in effect, and 2007 to 2010 when regulations changed and the transport surcharge of $25 was removed; and (2) 1985 to 2012, using the number of submissions (CFIA data) and FAT only, including survey samples in both cases, and using VM-01cost of $238.35 in both scenarios. Plate 26 shows that submissions fell steadily with the introduction of the wildlife vaccination programs in Ontario in 1989. Ontario, however, continued to be at the centre of the rabies outbreak, with more submission-positives and rabies cases from 1985 to 2012 (Tables 34.3 and 34.4) than any other province. Ontario had 67.9% of the total ­rabies-positive cases, thus accounting for the higher cost for testing, as well as for indemnity, quarantines, and investigations. Quebec, as Plate 26 shows, was a distant second but consistently higher than other provinces.

$100 $71 $45 $80 $40 $25 $22 $10 to $30

To these freight charges were added the transport of dangerous goods surcharge of $15 to $30 (sometimes no charge).

Diagnostic Costs

The costs of rabies diagnostic tests for 1997 provided by CFIA (C. Fehlner-Gardiner, personal communication, 2012) were as follows: Fluorescent antibody test (FAT) Tissue culture (TC) Immunohistochemistry Long panel monoclonal antibody typing MAb-typing (smears)

$158.10

Public Health Ontario

$30.25 $30.25 $158.82 $226.89 $34.03

BACKGROUND

Several chapters in this book deal with rabies management under the provincial and territorial health programs

564

Costs of Rabies Management

Table 34.10 Estimated total costs for PEP in Ontario, 1958 to 2012. In 1980 the human diploid cell vaccine (HDCV) became available. In 1985 the first field trials were held for the ERA vaccine in Ontario, and 1989 was the start of large-scale vaccine releases in eastern Ontario.

Table 34.9 The total cost of testing rabies specimens for given time periods.

Period

Transport Charge ($25)

Samples (n)

Cost VM-01 ($)

Sampling 1993–2006 2007–2010  Total

Yes No

202,017 44,110 246,127

48,150,752 10,513,619 58,664,371

FA Testing 1985–2006 2007–2010  Total

Yes No

239,721 33,581 273,302

57,113,528 8,004,031 65,117,559

Year 1958 1959 1960 1961 1962 1963 1964 1965 1966 1967 1968 1969 1970 1971 1972 1973 1974 1975 1976 1977 1978 1979 1980 1981 1982 1983 1984 1985 1986 1987 1988 1989 1990 1991 1992 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012  Total

Data source: estimated from CFIA data.

(Part  3), but none deal directly with any costs associated with treatment of patients contacting rabid animals. Each province or territory tabulates data on human contacts with suspect rabid animals, the resulting number of PEP treatments, and their cost. These data were collected by Health Canada (now Public Health Agency of Canada) to provide an annual report. Often, erroneous reports or no reports were sent in by provinces or territories. This section will deal specifically with the estimated costs of PEP of humans in Ontario using data derived from Public Health Ontario (PHO), the CFIA, and the Ontario Ministry of Natural Resources (OMNR), now known as Ontario Ministry of Natural Resources and Forestry (OMNRF). COSTS

Several assumptions were made to estimate the costs for the PEP treatments to develop Table 34.10 from 1985 to 2012 in Ontario (see the Appendix). The human population estimates for Ontario were obtained from Statistics Canada estimates for Canada, provinces and territories, 1958 to 2012. The values used to determine the PEP dollar values include public health staff time for investigating the exposure, the nurse’s and physician’s time to assess the exposure and administer the rabies immunoglobulin, and each of the five doses of rabies vaccine (Middleton et al., 2014). Two important advances in rabies prevention had an impact on the number of PEP treatments and the number of rabies-positive cases: the introduction of human diploid cell rabies vaccine (HDCV) in 1980 (Nunan et al., 2002), and the initiation of the oral rabies vaccination program in wildlife in 1989. The effect of these two advances can be seen in Table 34.10 and Plate 27. The introduction of HDVC resulted in an immediate increase in the number of PEP treatments after 1980 (Nunan et al., 2002). Between 1958 and 1980 the ratio of PEP to ­rabies-positives remained steadily less than one. By 1981 the ratio was

Positives PEPs 2,493 638 227 862 790 870 1,148 1,021 1,002 1,048 1,730 1,719 1,187 1,777 1,480 1,318 1,229 1,722 1,273 1,162 1,357 1,407 1,416 1,557 2,107 1,860 1,382 1,984 3,273 2,007 1,832 1,905 1,634 1,238 1,305 1,254 611 328 158 97 81 100 187 212 202 126 106 96 82 106 80 49 38 26 29 54,928

1,647 479 566 790 991 965 852 1,367 1,168 1,461 1,539 1,187 1,164 960 1,252 1,020 974 1,050 935 957 816 1,002 1,096 1,833 2,402 2,481 2,027 2,150 4,212 2,621 2,266 2,640 1,991 1,739 2,186 2,581 1,437 1,182 937 1,079 1,048 890 1,073 1,640 1,728 1,498 1,426 1,526 1,988 2,257 2,692 1,678 1,542 1,512 1,806 84,306

PEP/+ve PEP/100,000 0.66 075 2.49 0.92 1.25 1.11 0 74 1.34 1.16 1.39 0.89 0.69 0.98 0.54 0.85 0.77 0.79 0.61 0.73 0.82 0.60 0.72 0.77 1.18 1.14 1.33 1.47 1.08 1.29 1.31 1.24 1.39 1.22 1.40 1.67 2.06 2.35 3.60 5.93 11.12 10.99 8.90 5.75 7.73 8.55 11.88 13.45 15.89 24.24 21.29 33.65 34.24 40.58 58.15 62.27

28.3 8.0 9.3 12.7 15.6 14.9 12.9 20.2 16.8 20.5 21.2 16.1 15.4 12.4 15.8 12.7 11.9 12.6 11.1 11.3 9.5 12.0 11.6 20.8 27.0 27.5 22.1 23.2 44.7 27.2 23.1 26.2 19.4 16.7 20.7 24.2 13.3 10.8 8.5 9.6 9.2 7.7 9.2 13.79 14.29 12.24 11.51 12.12 15.7 17.95 20.88 12.92 11.74 11.4 13.47

PEP ($) 1,359,599 395,415 467,233 652,145 818,071 796,608 703,326 1,128,459 964,184 1,206,056 1,270,445 979,869 960,882 792,480 1,033,526 842,010 804,037 866,775 771,843 790,004 673,608 827,151 904,748 2,219,763 2,908,822 3,004,491 2,454,697 2,603,650 5,100,732 3,174,031 2,744,126 3,197,040 2,411,101 2,105,929 2,647,246 3,125,591 1,740,207 1,431,402 1,134,707 1,306,669 1,269,128 1,077,790 1,299,403 1,986,040 2,092,608 1,814,078 1,726,886 2,289,000 2,982,000 3,385.500 4,038,000 2,517,000 2,313,000 2,268,000 2,709,000 97,086,111

Source: compiled from CFIA, PHO, and OMNRF data. Notes: PEPs = number of rabies post-exposure prophylaxis given.

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greater than one, and the rate of PEP per 100,000 people doubled and continues at a high level today. By 1985, when small-scale field trials with ERA v­ accine were initiated in Ontario, rabies-positive cases were high and peaked in 1986. There was a corresponding increase in submissions, from 9529 in 1985 to 11,790 in 1986. With the initiation of the oral vaccination program in 1989, rabies cases started to decrease as the program took effect, but PEP treatments remained high and out of proportion to the rabies case decrease. The level remained high to 2012 (Table 34.10), even with fewer rabies cases, and in 2013 the number of PEP treatments increased slightly. The ratio for PEP to positives increased dramatically from 2000 as the oral vaccination program took effect.

The most dramatic effects on this program was the annual cost of the vaccine treatments and the increasing budget for treatments, the total cost which for 2012 was estimated at $2,709,000. The estimated cost from 1958 to 2012 for the human side of the rabies program was $64,383,935 for direct costs, but it would be much higher if the indirect costs (death of a patient, travel time for treatments, litigation, animal exposure investigations, etc.) were considered. Using the Bank of Canada’s Inflation Calculator (Bank of Canada, 2014), the PEP costs were estimated in 2014 dollars. Hence, the non-adjusted cost (total) for 1985–2012 was $64,980,182 (derived from Table 34.10). Adjusted to 2014 dollar value this would be $93,398,845. Figure 34.2 shows a downwards trend for adjusted PEP costs. The adjusted

Figure 34.2: Comparison of adjusted PEP values (black line) and normal values (dashed line) for PEP, 1958 to 2012. The Inflation Calculator uses monthly consumer price index (CPI) data from 1914 to the present to show changes in the cost of a fixed basket of consumer goods. These include food, shelter, furniture, clothing, transportation, and recreation. Source: created from CPI, PHO, and OMNRF data.

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costs demonstrate effectively the sensitivity to rabies events: the spike in costs during the rabies invasion in 1958; the decrease and then increase in the 1960s as rabies incidence rebounded after the initial invasion; the effect of the introduction of the HDCV in the 1980s, which made vaccination easier and safer and, therefore, easier to prescribe; the increase in 2000 as raccoon rabies invaded Ontario; and the increase with the bat scare in the first decade of this century and the subsequent decrease as studies of risk led to the adjustment of treatment protocols (see Chapters 6, 10, and 11 for British Columbia, Ontario, and Quebec).

data to describe a long-term program. Aubert (1999) is perhaps one of the few who compared the costs of depopulation of foxes against oral vaccination of foxes in France from 1988 to 1998. These costs included the vaccination of domestic animals, improved surveillance and diagnostic capabilities, costs associated with loss of livestock from rabies, and the costs of preventive vaccination and post-exposure treatment of humans. Like MacInnes and LeBer (2000), Meltzer and Rupprecht (1998a, 1998b) found that the preventive vaccination of domestic animals accounted for the greatest proportion of these costs (72%). Depopulation of foxes only delayed rabies entering an area while oral vaccination of wildlife proved beneficial to the management of rabies compared to depopulation (Aubert, 1999). This chapter has attempted to estimate the costs of the rabies management program in Canada using the three available sources (Table 34.12) of data that cover some of the costs. The estimates for the costs from 1985 to 2012 for the three federal/provincial areas of rabies management discussed in the above sections are shown in Table 34.12. For the 27-year period (1985–2012) this means an annual cost of about $4.8 million for the federal government and $6 million for Ontario, without taking into account all other costs mentioned previously or inflation costs (except for PEP). Assuming that the costs of rabies control have been proportional to number of positives over the 27-year period, then Ontario’s costs represent 68% of all provincial costs. Extrapolating this number for all provinces yields an estimate of $238,114,619 for all provincial costs. If we estimate costs on the basis of submissions, Ontario represents about 56% of all provincial costs so the estimate for total costs for all provinces would be $289,139,169. Thus, exclusive of the costs that have not been measured adequately (see the next section), an estimate of the combined cost of rabies control for all Canada would be in the range of $361,071,154 to $418,095,704, or approximately $13.4 million to $15.5 million annually from 1985 to 2012. Finally, assuming the costs of rabies control are proportional to provincial population, and using Ontario’s costs calculated on a per capita basis, yields an annual estimate of $20.4 million for rabies control in Canada or a per capita cost of just over 57 cents.

Ontario Ministry of Natural Resources and Forestry OMNRF is one of the few agencies to have maintained a tracking system to record the dollars spent for rabies management over time. First, in 1976 the Inter-ministerial Committee on Rabies provided a costing of rabies in Ontario as shared by four agencies: the OMNRF, the Ontario Ministry of Agriculture and Food, the Ontario Ministry of Health, and AC. This amounted to $4,691,770 in 1976, and the figures were used to seek funding for vaccine and bait development. Second, the Inter-ministerial Committee on Rabies, which went on to become the Rabies Advisory Committee in 1979, required costing figures for Cabinet submission to obtain approval for $113 million over three years for research into rabies control. Table 34.11 provides information on the costing of all aspects of the OMNRF rabies control program, beginning in fiscal 1979–1980 and extending to 2011–2012. The total cost to OMNRF during that same period for its part of the total Canadian rabies control program was $102,063,500. The OMNRF costs were adjusted using the Inflation Calculator index as for the Ontario Ministry of Health costs (see Figure 34.2). The result was a nearly 50% increase in the costs over the period 1979– 2012, from $102,063,500 to $142,026,100.

Discussion Estimating Total Costs Consideration of the cost and objectives of the rabies management program should include all elements that go towards preventing the spread of rabies from wildlife to domestic animals and possibly to humans. The Canadian rabies management program in animals is a multi-agency and multidimensional program evolving and being maintained over a long period. In estimating the costs of rabies management, few authors have taken the time or have the

Additional Costs Five costs were not included in the Table 34.12 estimates above. 1. The CFIA made contributions to the oral rabies vaccination program for raccoons, an effort to contain 567

Prevention and Management of Rabies in Canada

Table 34.11 Fiscal costs for OMNRF rabies control program, 1979–1980 to 2011–2012 (in C$000). Date

OMNRF

Seas

Con-1

Con-2

1979–1980 1980–1981 1981–1982 1982–1983 1983–1984 1984–1985 1985–1986 1986–1987 1987–1988 1988–1989 1989–1990 1990–1991 1991–1992 1992–1993 1993–1994 1994–1995 1995–1996 1996–1997 1997–1998 1998–1999 1999–1920 2000–2001 2001–2002 2002–2003 2003–2004 2004–2005 2005–2006 2006–2007 2007–2008 2008–2009 2009–2010 2010–2011 2011–2012  Total

150.0 231.0 79.0 127.5 98.4 125.4 95.0 113.5 67.4 71.1 355.3 1,141.8 918.7 424.0 364.9 792.5 836.7 917.9 881.3 821.0 845.9 1,243.4 1,220.2 952.1 893.8 868.6 1,062.4 1,017.1 966.9 786.5 756.0 682.4 349.0 20,256.7

65.0 68.0 56.0 94.0 90.0 106.0 117.0 142.0 157.0 185.0 307.2 360.0 314.5 392.3 390.0 580.0 654.2 641.4 650.1 690.3 694.7 850.0 910.0 811.2 550.0 496.7 579.0 548.9 401.5 259.8 215.4 33.5 12,410.7

84.4 190.3 506.5 552.0 551.4 617.0 586.0 592.4 617.0 730.0 747.0 3,377.7 1,032.1 994.6 806.0 670.0 1,501.0 1,376.3 1,419.3 1,261.0 1,516.3 2,452.8 2,048.8 1,927.8 2,750.0 1,929.0 1,668.0 1,335.0 1,981.8 1,182.0 2,238.0 1,355.0 631.5 41,228.0

38.5 59.2 103.8 145.9 155.0 101.2 89.8 63.3 70.0 90.0 805.5 1,583.0 893.8 794.2 356.0 769.2 629.5 638.0 644.0 507.0 558.0 152.0 152.0 152.0 5.0 5.0 6.0 5.0 22.3 76.2 69.0 93.0 53.0 9,885.4

Con-3

1.3 7.0 7.0

40.2 10.0 10.0 10.0 10.0 160.0 160.0 10.0 10.0

435.5

Bait-M

Various

154.0 82.0 3.5 13.7 8.6 6.3 55.0 54.9 56.4 131.2 24.4 26.5 140.4 455.1 200.1 60.0 97.9 95.0 67.0 67.0 67.0 67.0 67.0 25.0 2,025.0

122.9 257.1 189.0 304.5 295.5 412.5 500.7 458.7 446.7 334.2 255.0 503.3 1,591.2 171.0 246.0 320.0 320.0 445.0 521.3 470.0 545.0 970.0 1,010.0 890.0 1,060.0 1,060.0 818.4 592.4 205.0 46.0 46.0 46.0 10.0 15,463.4

Grads

7.0 27.0 3.0 17.3 24.0

8.0 96.0 96.0 80.5

358.8

Total 395.8 802.6 946.3 1,185.9 1,194.3 1,346.1 1,377.5 1,344.9 1,343.1 1,536.3 2,438.1 6,950.5 4,819.5 2,706.9 2,188.8 3,020.7 3,922.1 4,087.8 4,278.7 3,743.5 4,200.0 5,663.3 5,842.0 5,288.0 5,820.5 4,520.0 4,156.5 3,595.5 3,791.9 2,559.2 3,435.8 2,454.8 1,102.0 102,063.5

Notes: Seas = Seasonal costs Con-1= Contracts – vaccine bait manufacture, includes Connaught Labs, Langford Labs, Artemis Inc, Merial-VRG bulk, Merial Con-2 = Contracts – vaccine studies: Connaught Labs, University of Guelph, University of Saskatchewan, University of Toronto, Adenovirus, University of Ottawa, adenovirus, adenovirus (Microbix) Con-3 = Contracts – bait studies, includes biomarkers, raccoon/skunk (Ken Lawson), sachet comparative bait, blister-pack research Bait-M = Bait machinery, includes bait manufacturing machine, equipment move to Artemis, Artemis machines extras, bait machine – Robert Redford, bait machine – demand maintenance, bait machine – OES, bait machine – other, bait machine – ARNAV Various = Various contracts include: University of Toronto, ADRI,OLF,CFIA, Queen’s University, Cornell University, the United States Department of Agriculture (USDA), density study, model (Jim Broadfoot), trap studies (FIC), additional contracts Grads = graduate students, includes University of Guelph, Trent University, Queen’s University (Schubert), Queen’s University (Adkins) Source: compiled from OMNRF data.

2. The cost of pet vaccination in Canada is considered to be large but is mostly unknown. Determination of the number of vaccines sold in Canada is subject to drug company rules. A study by MacInnes & LeBer (2000) estimated that there were 800,000 unvaccinated dogs in southern Ontario and slightly more cats. With an average vaccination cost of $40, the estimate came to $50 million annually. The Canadian Animal Health Institute estimated that in 2016 there were 6.4 million dogs in Canada and 8.3 million cats. About 41% of

the raccoons within the US borders. This included an extensive baiting program along the New York, New Hampshire/Ontario, and Quebec borders in 2002 ­ ($200,000) and Maine–New Brunswick border in 2003 ($200,000). A previous contribution in 1998 and 1999 of $100,000 (see Chapter 11) supported the University of Cornell’s baiting program in southern Quebec. The total of both contributions was $500,000 to develop and coordinate oral vaccination to combat raccoon rabies (L. Kumor, personal communication, 2005).

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Costs of Rabies Management

on affected animals. This often led to the unnecessary euthanasia of these animals since the owners did not want to assume responsibility or the cost of the ­observation period. Only Quebec maintained these observation periods using CFIA personnel. It was not possible to determine the number of these biting incidents and estimate costs using the veterinary costs determined in earlier in this chapter. ­Assuming that the quarantine numbers and costs given for 2012 above remained the same from 1985 to 2012 (27 years), $1,595,224 could be added to estimated costs in Table 34.12. 5. Communications is an unknown cost. AC (CFIA) and health and wildlife agencies in provinces and territories produced films, pamphlets, and data reports each year. Some of these expenses may have been included in operating budgets but the communication projects were often contracted out. As well, the cost of items such as newspaper, radio and film announcements are not known.

Table 34.12 Estimated costs for rabies management for CFIA and Ontario, 1985 to 2012. Agency CFIA CFIA CFIA   CFIA CFIA   PHO OMNR(F)  

Cost area Indemnity (federal) Indemnity (provincial) Quarantines Quarantines × 27 Testing (FA) Testing (FA +) CFIA Total PEP Baiting   Ontario Total

Cost $1,408,109 $2,112,200 $59,082 $1,595,214 $65,117,559 $58,664,371 $128,956,535 $64,383,935 $97,534,000 $161,917,935

Data source: CFIA, PHO, and OMNRF.

households had a least one dog and 38% of households had a least on cat (Canadian Animal Health Institute, 2019). Probably fewer than 50% of these pets receive an annual rabies vaccination. Assuming a cost of $50 per vaccination, this gives an estimated cost of $335 million annually. Further, if the cost of pet vaccinations and the number of pets given above remained the same during the period 1985 to 2012, the estimated cost of pet vaccination over 27 years would be just over $9 billion. 3. Pre-exposure rabies vaccination is recommended for all persons at risk for rabies through work or travel in Canada. Pre-exposure vaccination should be less than PEP because fewer vaccinations are required, and the neutralizing antibodies produced negate the requirement for immunoglobulin (Meltzer & Rupprecht, 1998a). Three independent studies comparing pre-exposure prophylaxis to PEP found it was not cost effective unless the probability of exposure to rabies was 18% to 20% or higher (Mann, 1984; LeGuerrier et al., 1996; Bernard & Fishbein, 1991). The study by LeGuerrier et al. (1996) found the cost of pre-exposure prophylaxis for travellers to be $250, which included the medical and administrative costs. To save one life, it would be necessary to vaccinate 18.5 million travellers at a cost of $5 billion. The threshold at which pre-exposure prophylaxis was as cost effective as PEP occurred when 37.5% of travellers were exposed to rabies (Meltzer & Rupprecht, 1998a). No determination was made of the number of Canadians vaccinated pre-exposure. 4. The CFIA withdrew from its involvement in the investigation of reported animal (cat, dog, and ferret) bites in 2013, with the appropriate provincial and territorial authorities taking over responsibility. Before that date, CFIA monitored 10-day observation quarantines

Additional Benefits of the Rabies Program The previous sections have identified some of the costs of managing the rabies program. Even if the estimated annual costs of $13.4 million to $15.5 million noted above are doubled, the cost per Canadian remains less than one dollar per year. The result has been a markedly reduced threat of rabies in wildlife and domestic animals and consequently to humans. The mandate to make rabies a named disease in 1905 was the beginning of control efforts in the field. It was followed by the introduction of diagnostic procedures by 1910; the production of rabies vaccine for humans in 1914 in Ontario and for domestic animals by 1948 in Canada; the mandatory reporting of the disease cases by 1925; the realization by 1947 that rabies was not just a canine disease but one of all animals; and continued passive surveillance. It all eventually led to the huge effort to orally vaccinate wildlife by aerial baiting and the continuing efforts to improve diagnostic tests. Everything contributed to the success of the total program. Several authors have described the potential economics of controlling terrestrial rabies with an emphasis on canine rabies (Meltzer & Rupprecht, 1998a, 1998b; Recuenco et  al., 2007; Shwiff et  al., 2013). Certainly, the introduction of vaccines for domestic pets in 1950 removed the threat of canine variant rabies with a resulting decrease in dog to human rabies transmission.

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Prevention and Management of Rabies in Canada

Comparing the annual cost of pet vaccination against the estimated annual costs for the management of the rabies program ($13.4 million to $15.5 million), it could be argued that the current management programs are a feasible alternative to the problem of trying to have all domestic animals vaccinated. The continuing vaccination of dogs, cats, and ferrets by private veterinarians has helped to ensure the disappearance of canine rabies from Canada since 1950. This remains a very expensive but valuable part of rabies control. The success of the oral rabies vaccination program in several provinces has brought huge relief to all sectors of the total program. Decreasing wildlife rabies has led to decreased need for field activities by CFIA staff and resulted in savings through fewer inspections, quarantines, and specimen submissions and decreased testing costs. While this chapter deals with costs up to 2012, it should be noted that the field activities carried out by CFIA were downloaded to the provincial and territorial agencies and laboratories in 2014. The decrease in rabies cases led to a gradual decrease in PEP by health authorities. This decrease has levelled off but continues to be influenced by rabies incidents. This decrease in rabies cases has also produced a levelling off in specimen submissions. Any biting incident or contact with bats or other animals often brings about a PEP response following a risk assessment. This is particularly true for the ever-present threat of bat rabies and their contact with humans (Chapters 27 and 39), and again the possible rabies virus mutation and cross-species transmission is an increasing worry to health care officials. Reducing rabies cases also brings about a decreased awareness in the human population as to the risks of rabies. However

small this risk, medical authorities are under pressure to treat their patient on request (see Chapter 32). A study by Huot et al. (2008) provided some relief to the over use of PEP as a result of occult bat exposure. Their findings allowed for a re-examination of PEP by the US Advisory Committee on Immunization Practice and a cost saving in the use of PEP across provinces and territories. OMNRF costs for the development of wildlife rabies vaccines and their delivery have also decreased. Vaccine production is done through a private company as aerial delivery of oral vaccine will always be needed to prevent recurrences of rabies hot spots and incursions from the United States. Given that a recurrent invasion may happen, it would be prudent to store a quantity of vaccine. With virus mutation and possible rabies virus cross-transmission among terrestrial and aerial animals continuing to be a potential threat, active surveillance using genetic tools is needed. A spinoff from the success of the baiting program for Canada has been the requests from around the world for the technology and expertise found in the Ontario program. In April 2014 CFIA relinquished its involvement with field activities but maintained its laboratory function of research, diagnosis, and reporting. The diagnosis of specimens submitted is only for those specimens where human or domestic animal contact was involved with the animal of concern. Any other tests are performed on a cost-recovery basis. The field activities were downloaded to the agencies and laboratories in the provinces and territories. Estimates of future costs associated with these activities will become more difficult to obtain and it remains to be seen how the provinces will manage this new approach.

Acknowledgments With profound gratitude the authors acknowledge the many agencies and people who helped make this chapter possible. The Canadian Food Inspection Agency (CFIA) and Dr Fehlner-Gardiner (OLF); the Ontario Ministry of Natural Resources and Forestry (OMNRF) and Chris Davies (retired), Dennis Donovan (retired), and Tore Buchanan for their continued support for the publication of this book; Peter Bachmann (retired), who provided the data on the OMNRF rabies program; the Provincial Health Department of Ontario and Dr Dean Middleton for post-exposure treatment data; Health Heritage Research Services and Dr Chris Rutty for data from Connaught Laboratories; Libraries of Agriculture and Agri-Food Canada with Lynne Thacker and Dorothy Drew for their patience in providing requested materials; Library and Archives Canada, Ottawa with Julia McIntosh and Michelle Guitard for uncovering the indemnity payments, clinicals and vaccination records; and Dr Rowland Tinline, Professor Emeritus, Queen’s University, Kingston, for the graphics and statistical analysis of data discussed in this chapter.

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Costs of Rabies Management

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Ontario Ministry of Natural Resources. Copy in possession of David Gregory. Inter-ministerial Committee on Rabies. (1976). [Submission to the Cabinet Committee on Resources Development, Animal Control, Rehabilitation and Rabies Control]. Copy in possession of David Gregory. LeGuerrier, P., Pilon, P. A., Deshaies, D., & Allard, R. (1996). Pre-exposure rabies prophylaxis for the international traveller: A decision analysis. Vaccine, 14(2), 167–176. https://doi.org/10.1016/0264-410X(95)00110-M MacInnes, C. D., & LeBer, C. A. (2000). Wildlife management agencies should participate in rabies control. Wildlife Society Bulletin, 28(4), 1156–1167. Retrieved from https://www.researchgate.net/ publication/261825472_Wildlife_Management_Agencies_Should_Participate_in_Rabies_Control Mann, J. M. (1984). Routine pre-exposure rabies prophylaxis: A reassessment. American Journal of Public Health, 74(7), 720–722. ­Retrieved from https://ajph.aphapublications.org/doi/pdf/10.2105/AJPH.74.7.720 Meltzer, M. I., & Rupprecht, C. E. (1998a). A review of the economics of the prevention and control of rabies. Part 1: Global impact and human rabies in humans. PharmacoEconomics, 14(4), 365–383. https://doi.org/10.2165/00019053-199814040-00004 Meltzer, M. I., & Rupprecht, C. E. (1998b). A review of the economics of the prevention and control of rabies. Part 2: Rabies in dogs, livestock and wildlife. PharmacoEconomics, 14(5), 481–97. https://doi.org/10.2165/00019053-199814050-00003 Middleton. D., Johnson, K. O., Rosatte, R. C., Hobbs, J. L., Moore, S. R., & Rosella, L. (2014). Human rabies post-exposure prophylaxis and animal rabies in Ontario, Canada, 2001–2012. Zoonoses and Public Health, 62(5), 356–364. https://doi.org/10/1111/zph.12155. Mitchell, C. A. (1947a, May 7). [Letter to Dr R. D. Defries, director, Connaught Laboratories, University of Toronto]. Copy in possession of David Gregory. Mitchell, C. A. (1947b, May 30). [Letter Dr R. D. Defries, director, Connaught Laboratories, University of Toronto]. Copy in possession of David Gregory. Mitchell, C. A. (1948, January 30). [Letter to Dr A. C. R. Walker, School of Hygiene, University of Toronto]. Copy in possession of ­David Gregory. Nunan, C. P., Tinline, R. R., Honig, J. M., Ball, D. G. A., Hauschildt, P., & LeBer, C. (2002). Postexposure treatment and animal r­ abies, Ontario, 1958–2000. Emerging Infectious Diseases, 8(2), 214–217. Retrieved from https://www.ncbi.nlm.nih.gov/pmc/articles /PMC2732448/

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Prevention and Management of Rabies in Canada Professional Institute of the Public Service of Canada. (2014). Collective agreement between the Canadian Food Inspection Agency and the Professional Institute of the Public Service of Canada regarding the Veterinary Medicine (VM) Group Bargaining Unit. Retrieved from http://www.inspection.gc.ca/english/hrrh/col/vm/appae.shtml Recuenco, S., Cherry, B., & Eidson, M. (2007). Potential cost savings with terrestrial rabies control. BMC Public Health, 7(1), 47. https:// doi.org/10.1186/1471-2458-7-47 Shwiff, S. A., Sterner, R. T., Jay, M. T., Parikh, S., Bellomy, A., Meltzer, M., ... Slate, D. (2007). Direct and indirect costs of rabies e­ xposure: a retrospective study in southern California (1998–2002). Journal of Wildlife Diseases, 43(2), 251–257. https://doi.org/10.7589 /0090-3558-43.2.251 Shwiff, S., Hampson, K., & Anderson, A. (2013). Potential economic benefits of eliminating canine rabies. Antiviral Research, 98(2), 352–356. https://doi.org/10.1016/j.antiviral.2013.03.004 Wallace, R. M., Gilbert, A., Slate, D., Chipman, R., Singh, A., Wedd, C., & Blanton, J. D. (2014). Right place, wrong species: A 20-year ­review of rabies virus cross species transmission among terrestrial mammals in the United States. PLOS ONE, 9(10), e107539. https://doi.org/10.1371/journal.pone.0107539 Wells, K. F. (1956, February 2) [Letter]. Copy in possession of David Gregory.

Appendix Salaries For VM-01 @ $81,254 ÷ 1957 = $41.52 per hour For VM-02 @ $95,548 ÷ 1957 = $48.82 per hour Average of two levels = $45.17 per hour (VM0A)

Quarantines Assuming that each visit takes 90 minutes (30 minutes for inspection and 60 minutes travel time): Six-month quarantines require 90 × 8 ­minutes = 720 minutes Three-month quarantines require 90 × 4 minutes = 360 minutes 10-day observations require 90 × 3 minutes = 270 minutes The total quarantine times for all provinces during 2012 (number of quarantines × time): Six-month quarantines = 60,930 minutes Three-month quarantines = 2160 minutes 10-day observation = 15,390 minutes Grand total = 78,480 minutes or 1308 hours The veterinary salary for 2012 (VM-01 and VM-02 levels) was divided by the full-time equivalent (which is equal to the number of hours the veterinarian can work in one year), that is, 1957.0 hours (PIPSC, 2014). This provides an estimate of the salary dollars per hour. Two estimates given in the salaries section of this Appendix were averaged and the hourly rate of $45.17 was used to determine the 2012 cost of the Canada-wide quarantines assuming that a veterinarian carried out all the inspections throughout the provinces. VM0A at $45.17 per hour × 1,308 = $59,082.36. This value is less than the annual salary for either level of a VM-01 or VM-02 veterinarian for 2012. Quarantine costs are further discussed in the chapter.

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PHO Assumptions 1. Between 1964 and 1980, the annual PEP cost was $913,000 and the average number of PEPs per year was 1106. The average annual cost per PEP was $913,000 ÷ 1106 = $825.50. This value was used to estimate the PEP $ value per year. 2. Between 1981 and 1988, the annual PEP cost was $3,027,000 and the average number of PEPs per year was 2499. The average annual cost per PEP was $3,027,000 ÷ 2499 = $1211.29. The value $1211 was used to estimate the PEP $ value per year between 1981 and 2005. These values varied from year to year and so an average PEP was used for consistency (P. Bachmann, personal communication, 14 March 2014). 3. A value of $1500 was used for calculations between 1989 and 2012.

OMNRF Budget Details Note: The Ontario Ministry of Natural Resources (OMNR) became the Ontario Ministry of Natural Resources and Forestry (OMNRF) in 2015. Because of the complexity of the original data table, Table 34.11 does not show resources allocated to certain sectors of the table for a time, withdrawn, and then allocated to other sections of the budget. For example, under Contracts (vaccine bait manufacture), Connaught Laboratories was contracted for 1979–1980 to 1993–1994, then Langford laboratories from 1990–1991 and 1994–1995, and finally Artemis Inc from 1994–1995 to 2012. As a second example, under contracts (bait studies) resources were allocated to biomarkers between 1988–1989 and 1991–1992 while the sachet comparative trials were allocated budget between 2002–2003 and 2003–2004. Each of these timelines corresponds to some specific aspect of the process to develop a viable vaccine, a bait and carrier, and a machine (airplane adapted) to deliver the vaccine from the air.

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PART 8

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Overview The chapters in Part 8 are novel as they describe the involvement of various groups that, in the editors’ opinion, have never been properly acknowledged in terms of the history of rabies and its control in wildlife. Chapter 35 discusses the importance of trappers, especially in Ontario, in the surveillance and testing of wildlife control strategies and techniques. Chapter 36 presents a snapshot of Indigenous peoples’ view of rabies and how they have contributed to rabies control along the Canadian–US border. Chapter 37 examines the possibility that the spread of rabies into North America followed the migration of peoples from Siberia eastwards across northern Canada and into Greenland. It discusses whether the spread of the virus was associated with the marked increase use of sled dogs as the eastward movement of the Thule (modern day Inuit) displaced the more sedentary Dorset peoples, a concept that has received little attention in the literature.

35 Trapper Participation in Rabies Control in Canada Beverly Stevenson Ontario Ministry of Natural Resources and Forestry, Wildlife Research and Development Section, Trent University, Ontario, Canada

Introduction

Trapper Utility

Trappers and the fur industry were central to North America’s settlement and early governance (Dolin, 2010; Royle, 2010). Trappers were also fundamental to the Ontario Ministry of Natural Resources’ (recently renamed Ontario Ministry of Natural Resources and Forestry (OMNRF)) efforts to control wildlife rabies. Trappers from across Canada have been involved since the notion to control rabies in wildlife was conceived to the present day. Their knowledge and passion to participate in the rabies control program was invaluable to the efforts to control and almost eliminate rabies in southern Ontario. Trappers contributed in a variety of ways, including helping to radio-collar foxes so more could be learned about their ecology, locating fox dens so baits could be hand placed near them, taking blood samples in the field to determine whether foxes (Vulpes vulpes) and skunks (Mephitis mephitis) had developed rabies antibodies, and providing carcasses to determine whether animals were ingesting the rabies vaccine baits or not. This chapter describes the involvement of trappers in rabies control programs in Ontario, as well as Alberta, Quebec, New Brunswick, Nova Scotia, and Newfoundland and Labrador. Trapper participation in vector depopulation, specimen sampling, radio-collaring wildlife, bait distribution, oral rabies vaccination, trap-vaccinate-release, and evaluation programs is also discussed.

Trappers and Trapping When OMNRF created the Rabies Research and Development Unit to determine ways to control terrestrial rabies, it quickly realized that more information was needed about fox ecology and that it would require significant research and outside help. After rabies was introduced into Ontario by arctic foxes from northern Canada during the mid-1950s, red foxes became the main reservoir and vector of the disease in southern Ontario (Tabel et al., 1974; see Chapters 2 and 10). It was crucial to the understanding of the disease and any rabies control options to gain knowledge of fox movements, behaviour, and population dynamics. OMNRF’s David Johnston appreciated that they would require the support of trappers and hunters for the program to be successful. At that time, not enough information was known about the density, movements, or feeding behaviour of red foxes in southern Ontario. The trappers who made their living from trapping, however, had intimate knowledge of local populations and fox behaviour from years of experience. Not only did trappers understand fox movements, but they also knew about attractants and feeding behaviour (Giroux, 1999). This was the type of information that researchers needed to develop an effective rabies control program. Before the rabies control program, the only information available on fox density in Ontario was based on the

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Figure 35.1: Number of red foxes harvested by trappers and hunters in Ontario from 1919 to 2009. Source: created from unpublished OMNRF data.

number of foxes harvested by hunters and trappers each year. Unfortunately, one of the problems with using this information is that the effort put into trapping and hunting depends greatly on the market value of the pelt and not solely on the abundance of foxes in the area (Voigt, 1999). When pelt prices are low, trappers and hunters put less effort into harvesting even though fox populations may be high. Furthermore, it is not clear what the relationship is between harvest per unit effort and very high or low populations. As well, three- to five-year cyclical fluctuations in fox populations (see Chapter 10) complicated understanding the relationship between harvest and density (Daigle, 1998; Siemer et  al., 1994). Figure 35.1 shows the red fox harvest in Ontario and Figure 35.2 shows the average pelt price for a red fox. When pelt prices are high (Figure 35.2), a great deal more effort is put into harvesting the animals (Payne, 1980; MacInnes & LeBer, 2000). Relying on harvest information to estimate the abundance of foxes in Ontario could lead to the mistaken belief that the population is either declining or increasing significantly from year to year when in fact the population may be stable. The best way to get an accurate estimate of the density of foxes in Ontario was to do extensive fieldwork. Although Ontario had approximately 9000 licensed trappers in Ontario when OMNRF began its rabies control efforts in 1967 (Figure 35.3), Huron County

(located in southwestern Ontario) had more trappers and hunters per capita than the rest of Ontario (D. Johnston, personal communication, October 1993). The area also had regular rabies outbreaks and, according to Huron County trapper Len Baird, it was one of the few areas where trappers were actively trapping foxes at the time. In the late 1960s when OMNR was beginning its rabies research, approximately 5000 red foxes a year were being harvested in Ontario. This was down substantially from the average of almost 21,000 foxes harvested per year in Ontario for the 35 years before rabies became established in the province and from the peak of almost 60,000 foxes harvested during the 1943–1944 trapping season (Figure 35.1). Although, the pelt prices were approximately the same in 1943–1944 and 1968–1969 ($13–$14 each), the profit from these pelts was much less in the late 1960s than it was 25 years earlier; pelt prices had not increased with inflation rates but expenses to trap the foxes had increased (Figure 35.2). In addition to having a large number of trappers, southwestern Ontario was easily accessible to OMNR’s research staff and had a good road network for radio-tracking foxes. In addition, southern Ontario was known as the rabies capital of North America (MacInnes et al., 1988; MacInnes & LeBer, 2000; MacInnes et al., 2001). Studies by Verts (1966) indicated that rabies prevalence is directly related to the density of susceptible hosts.

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Figure 35.2: Average prices received by fur harvesters for foxes trapped and hunted in Ontario from 1919 to 2009. Source: created from unpublished OMNRF data.

Figure 35.3: Number of trapping licences issued in Ontario from 1950 to 2009. Source: created from unpublished OMNRF data.

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Johnston contacted the Huron County and Grey-Bruce trappers associations to enlist the support of their members for the preliminary research needed. Trappers were eager to participate because of extra financial incentive, and if the program was successful, it would reduce the threat of rabies to their families, livestock, and pets. They also believed that populations of foxes (which were so important to the trapping industry) would be more stable and densities higher. During rabies epizootics, fox populations can be decimated in localized areas (Gier, 1948). Trappers like Ross Taylor, who once trapped 14 foxes in a single day and 75 foxes in 15 days, wanted to see the fox population return to what it was before rabies became established in Ontario (Figure 35.4). Once rabies became enzootic, or permanently established, the fox population remained low in Ontario, and Taylor was no longer able to trap large numbers of foxes in a short time. One of the fundamental goals of conservation followed by trappers is to have sustainable wildlife populations. Rabies control would help ensure the maximum sustainable population of foxes as fox densities declined significantly after rabies became established in southern Ontario.

Fox Ecology A fundamental need was to develop a better understanding of foxes, the principle rabies vector in Ontario, particularly with respect to movements, home ranges, population fluctuations, mortality causes, den use, and so on (MacInnes, 1999). This information was also needed for the striped skunk, the other main rabies vector in Ontario. This knowledge of basic population dynamics was necessary to be able to develop effective control strategies. At that time, detailed information for foxes and skunks in Ontario had not been collected over a long term or on a large scale (MacInnes & LeBer, 2000). Little information was available on fox population dynamics other than anecdotal observations from trappers, hunters, and other individuals who are in the field on a regular basis. One of the first rabies control strategies considered was population control (P. Bachmann, personal communication, October 2010). OMNR’s Johnston contacted trappers in eastern Ontario to distribute baits containing reproductive inhibitors. These baits were distributed in response to the death of Donna Featherstone in Richmond (near

Figure 35.4: Huron County trapper Ross Taylor displays 75 foxes that he captured during a two-week period before rabies become ­established in Ontario. The foxes were trapped within a 12-kilometre radius of Ross’s house. Source: courtesy of Ross Taylor.

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Ottawa) in 1967 (D. Johnston, personal communication, October 2010; see Chapter 3b). Another control strategy being considered was oral rabies vaccination (ORV) (see Chapters 17, 18, and 19). ORV is the distribution of baits containing rabies vaccine to immunize target species of wildlife against rabies. If a sufficient percentage of the rabies vectors can be vaccinated in an area, then the contact rate among infective vectors would limit rabies spread and perhaps lead to the elimination of rabies (MacInnes, 1999). Before an educated guess could be made on the requirements for baiting density, spacing, or the percentage of the population that would have to be vaccinated, it was vital to understand certain aspects of the species involved. One key piece of information needed was to determine the home ranges and movements for these rabies vectors. Southwestern Ontario trappers were asked to assist with trapping rabies vectors so that OMNRF staff could affix radio-collars to them before release. Although most of the foxes were eventually trapped by OMNRF staff, the trappers assisted with developing and teaching the best techniques for live capture without injuring foxes. OMNRF researcher Dennis Voigt worked with trappers to develop modified leg-hold traps and foot snares that would capture foxes, coyotes, and skunks and hold them securely but safely without injury. These efforts became internationally recognized as others in the United States, Australia, and England were in turn taught by Voigt. He recalls that instruction was not always without incident. His most memorable fox was dubbed “Mr. Boots” when it firmly latched onto British researcher David MacDonald’s boot and wouldn’t let go for a very long time. The participating trappers in Ontario tell many stories about foxes latched onto gloves, fingers, shirt sleeves, and even hats. Some foxes were live-captured numerous times for radio-collaring and each time had some new trick! From 1972 to 1981, a total of 169 radio-collars were affixed to 125 foxes, 21 skunks, 15 raccoons, and 8 coyotes (P. Bachmann, personal communication, October 2010). Trapping foxes and skunks was just the beginning of the effort. The real work involved tracking these animals on a regular basis to see where they were going and how far they were moving. OMNRF staff spent thousands of hours following foxes in their home range or on cross-country trips when juveniles began dispersing in late summer and during the fall. Trappers often captured radio-collared foxes when the trapping season was open. This was expected and part of the assessment for OMNRF on various mortality causes and their rates. One young, dispersing, wayward fox was

radio-collared near Barrie (Simcoe County) and dispersed to the Bruce Peninsula (a distance of 135 kilometres). OMNRF staff tracked this fox for a week on the peninsula before discovering the signal coming from a house. OMNRF’s Johnston knocked on the door and asked the owner if he had trapped a fox recently with a collar on it. The trapper, who was unaware of the program, was astonished at the question but was very interested to learn about OMNRF’s rabies control programs and discover how he had been tracked down (I. Watt, personal communication, October 2010). This fox encountered a number of rabies outbreak areas during its trek. The information on this animal’s movements was used to simulate possible rabies transfer from area to area and to understand rabies dynamics in southern Ontario (P. Bachmann, personal communication, October 2010). From these research projects, it was estimated that an average of one to two foxes and one to two skunks per square kilometre lived throughout most of southern Ontario (MacInnes et al., 1988; Rosatte, 1999; Voigt, 1999; Rosatte & Larivière, 2003). The detailed study by OMNRF of movements, population dynamics, and density coupled, with the contribution of knowledge and samples by trappers, were essential to the eventual success of the rabies control program.

Bait Development and Distribution While OMNRF was studying home ranges and movements of rabies vectors, development had begun on a bait that would be attractive to foxes, as well as a method to distribute the baits. Although foxes and skunks accounted for approximately two-thirds of all rabies cases in Ontario, the bait and vaccine were going to target foxes because they were the single most important species accounting for approximately 45% of all diagnosed cases (MacInnes et  al., 1988; Rosatte et  al., 2007). OMNRF had hoped that once rabies was controlled in foxes, it would die out naturally in skunks (MacInnes et al., 2001). One of the first steps was to test different attractants and bait compositions to see what foxes would readily consume. Knowing that the primary way that foxes would find these baits would be by using their olfactory senses, the bait development focused on attractant scents. The very first bait formulas were composed of fragrant cheeses (limburger, gorgonzola, and Roquefort). To determine how attractive these baits were to wildlife, trappers were enlisted to distribute baits by hand. The trappers either worked by themselves or were asked to accompany the OMNRF staff to the

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location of any fox dens of which they were aware. OMNRF’s Watt recalls the intense negotiations that were required to convince the trappers to do this once they smelled the baits. It seems that the trappers were very concerned that these baits would repel the foxes instead of attracting them! In the end, the desire to contribute to the program prevailed and the trappers volunteered a great deal of their time to show the OMNRF staff where the fox dens were located. It was during one of these expeditions that a Huron County trapper accompanied two OMNRF staff to a den site. The young female staff evidently had not been advised to dress appropriately for work in the field. When they came to a stream that needed to be crossed, the trapper gallantly offered to carry her across the stream while the other OMNRF staff was going to leave her to cope on her own. But no good deed goes unpunished and when the trapper was halfway across the stream, he stumbled and nearly dropped her in the water. It required the help of the other OMNRF staff to ensure that both of them made it safely to shore (C. Stevenson, personal communication, October 2010). The largest number of baits hand distributed by trappers occurred in the Cambridge area from 1988 to 1991 (P. Bachmann, personal communication, October 2010). In 1988 approximately 60 trappers distributed 14,300 placebo baits in two days. Although these baits did not contain a vaccine, they did contain a biomarker so teeth from carcasses could be analysed to determine bait uptake rates. From 1989 to 1991, the baits distributed by these trappers contained both a rabies vaccine (targeting foxes) and a biomarker. In those three years, Cambridge-area trappers distributed 78,000 baits. Approximately 100 trappers volunteered their time to distribute the baits over two days each year. Cambridge-area trapper Don Brittain fondly recalls participating with the hand distribution of baits. The highlight of his experience was interrupting individuals who were harvesting marijuana and watching police cruisers patrol the area. Evidently the swarm of people descending on the area caused some concern with local residents who were not aware of what was happening. After a few years of development, the baits were refined and the bait of choice was a meatball bait enclosed in a plastic bag. The distribution method was also refined so that these baits could now be distributed by aircraft instead of having to be delivered by hand to known den sites. However, the baits had to be hand-bombed out of the window of the aircraft. The downside of aerial distribution of baits from a small aircraft was that a small percentage of the baits had a distinct aroma of vomit to them when they left the aircraft (I. Watt, personal communication, October 2010).

No research was conducted to see whether this new aroma acted as a better attractant or not. To assess how well the baits were being chewed or eaten by wildlife, it was necessary to try to recover some of the bait bags after they were distributed. OMNRF once again approached the trappers in southwestern Ontario and asked them to recover any bags that they might find while they were out trapping. By examining the bags, OMNRF researchers would be able to determine how well foxes were chewing the bags and how likely they would be to be exposed to the vaccine or consume the bait. Each bag that was recovered would provide valuable information. However, OMNRF was realistic and thought it unlikely that the trappers would be able to find more than a couple of dozen bait bags in total so nothing was set aside in the budget. They underestimated Huron County trapper Charlie Stevenson though. Stevenson did his best to help out this research project and recovered 200 bait bags on his own. At 10 cents each, it was a nice little bonus for picking up bags while he was already out in the field!

Aerial Baiting The preliminary aerial baiting flights to test mechanized bait dispersal methods relied heavily on volunteers. Since the program was still in its developmental years, not enough funding was available to hire all the staff needed for the aerial bait drops. Huron County trappers Doug Vincent and Tim Moon, and Bruce County trapper Don Dodds were some of the individuals that volunteered to help out. These trappers had been involved with the rabies research programs since the early years and were eager to participate in the next phase of rabies research and control. The flights were based out of Goderich airport in southwestern Ontario during 1990 and 1991. The trappers worked with other volunteers and OMNRF staff to help load baits onto the conveyor belt of the bait machine and keep the bait machine clean so that it didn’t jam. The baits were being distributed over experimental plots to assess bait density, flight-line spacing, and bait attractants. The perspective from the aircraft was incredibly different from what they were used to seeing on the ground. Although they were used to trapping in and walking through the areas that they were flying over and could have found their way out of any forest in the area, they were now looking at it from a bird’s-eye view and had to rely on occasional familiar landmarks to determine their location. These trappers agreed unanimously that participating in an aerial rabies baiting flight was an unforgettable experience

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(although some of the volunteers would gladly forget the ill feeling that they acquired while flying). As bait distribution methods were further improved, trappers were still encouraged to participate in the baiting flights to promote good public relations. Volunteers were no longer as necessary to the flights since operations were more streamlined. Eastern Ontario trappers Bill Mather and Brian McDougall were two of the individuals who participated in the baiting program. They were hired on shortterm contracts and discovered that they enjoyed flying so much that they returned every summer for several years to assist with the aerial bait drops. According to both Mather and McDougall, the highlight of their flying experience was participating in a helicopter baiting program in Toronto. As a result of some rabid skunks in the Greater Toronto Area, baits were distributed along all the rivers and ravine areas there to prevent rabies from re-occurring in the city (Rosatte et al., 2007). Doing low-level flying over Toronto (including the Toronto Zoo) gave them a novel look at city that few people ever experience. It was during one of these flights that they had the rare opportunity to circle the CN Tower and take photographs.

skunks. When the carcasses of the foxes and skunks were submitted to OMNRF, a hemolyzed blood sample would then be collected from the same animals. The lab would test and compare both of these blood samples to develop an effective test for analysing hemolyzed blood samples. Although taking a fresh blood sample sounds simple, things are not always as easy as they seem. Jake McDougall, a former Huron County trapper, can attest to that. McDougall was willing to take blood samples from the animals he trapped before killing them. In exchange, he was compensated for the blood sample and the information he provided on the animal. In addition to his payment, he received pre-exposure rabies vaccination free. Obtaining a blood sample from foxes was fairly straightforward. The trapper approached the trapped animal, tapped it on the end of the nose with a stick to knock it out, and then took a blood sample by cardiac puncture, before killing the fox. This is slightly more complicated with a skunk as another trapper, Doug Vincent, found out when he was assisting McDougall. With a fox, if the first tap doesn’t knock the animal out, you try again. With a skunk, if the first tap doesn’t knock it out, you end up wearing some incredibly pungent perfume and are forced (by your spouse) to undress outside when you return home. Despite incidents like these, trappers were so enthusiastic about assisting OMNRF and obtaining the research samples that the ministry had to limit the number of animals it would accept from any one trapper. Without this limit, OMNRF would have been inundated with samples that it could not afford to analyse. The type of assistance required from the trappers varied with the type of information being sought by OMNRF. Sometimes blood samples were required; at other times the head or the carcass of the trapped animal was needed. In all cases, the trapper was required to record information on the date, location, sex, and method of mortality for the captured animal. This was a mutually beneficial partnership for OMNRF and the trappers. OMNRF, as the wildlife management agency, received the information necessary to make informed decisions on rabies control methods. And this information was obtained more economically and easily than if OMNRF had to send staff out to collect specimens. In exchange, the trappers assisted with wildlife management and knew they were providing reliable, scientific information. And as a bonus, they received financial compensation. All the animals that were collected from the trappers were tested for rabies. As a result of that, Huron County trapper Stevenson learned a thing or two about health

Assessing the Success of Rabies Control Programs To determine how successful the rabies control programs were, once again licensed trappers and hunters were enlisted to support the program. Since rabies incidence tends to be cyclical because of the population crash and the resultant recovery of vector populations, it was difficult to determine whether a decrease in rabies cases was the result of rabies control programs or just a natural fluctuation in wildlife populations (Schubert et al., 1998). During the development of a bait, and accompanying oral vaccine use, trappers from southwestern Ontario (and later from across the southern Ontario rabies control areas) were invited to help OMNRF assess the success of rabies control programs. Their assistance ranged from submitting carcasses of animals they had trapped for rabies testing through analysis of bait acceptance to collecting blood samples from live-trapped animals. The Canadian Food Inspection Agency laboratory in Nepean was able to test fresh blood samples to determine rabies antibody levels. However, no similar test was available to test hemolyzed blood from frozen carcasses. Under normal circumstances, the only blood samples available to OMNRF were from the frozen carcasses. To develop a test to determine the antibody levels of these hemolyzed blood samples, fresh blood samples were required from foxes and

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and safety while assisting with the rabies surveillance programs. Stevenson believed in keeping things simple. When he caught a skunk in a trap, he cut the head off the skunk at the trap site. Stevenson then placed the head in a plastic bread bag and put in the pocket of his coveralls until he returned to his truck. At the truck, Stevenson removed the head from his pocket and filled out the data tag that would accompany the head when it was submitted. Then he would take the head and tag home and place them in the freezer until they were picked up by OMNRF staff. After receiving the report on his specimens one year, Stevenson quickly changed his routine. Seven of the skunks he had collected the previous fall had been rabid. Although there was little risk since Stevenson had been vaccinated against rabies when he first started assisting OMNRF, this was enough of a wakeup call for him to adopt better health and safety practices. OMNRF staff learned some good lessons working with trappers. OMNRF’s Johnston used to travel to the trappers’ houses in the early days to pick up the carcasses they had collected. Carcasses were picked up regularly in fall and winter during the trapping season. The major collection area in Huron County was in a snow belt, and winter conditions were common. Johnston was called to pick up a freezer full of carcasses right after a recent snowstorm. The deep snow meant Johnston was forced to carry the carcasses from the barn, where the carcasses were stored, to his truck, which remained parked on the road. Since this was one of the early years of the program, the plastic bags provided to the trappers had not been thoroughly tested for durability. Johnston loaded a toboggan (suggested and supplied by the trapper) with the carcasses and began to trudge through the deep snow to his truck. As it turns out, not all plastic remains flexible when frozen. With the jostling, the carcasses broke through the brittle plastic bags and spilled out into the deep snow across the yard. Eventually, Johnston had to traipse back and forth through the snow with one or two carcasses at a time (D. Johnston, personal communication, September 1993). As the rabies control programs expanded throughout southern Ontario, trappers from across the entire rabies control areas were solicited to help. Even trappers from adjacent Quebec and New York were asked to provide samples; these samples would allow OMNRF to determine whether movement of animals occurred between baited and non-baited areas. Eventually, a new lab test was developed by using all the blood samples previously obtained by the trappers. This test allowed the lab to examine blood samples from frozen

carcasses. There was no longer a need for the trappers to collect fresh blood in the field or for OMNRF staff to visit the trappers every few days to pick up the blood samples. Instead, OMNRF could switch to visiting trappers every few weeks or once a month to pick up specimens. This reduced the staff time requirement and the costs associated with this surveillance program.

Trap-Vaccinate-Release Another of the rabies control programs that trappers participated in was Ontario’s trap-vaccinate-release (TVR) program (Rosatte et al., 1992). TVR involves live trapping raccoons (Procyon lotor) and skunks, vaccinating them against rabies, ear-tagging them to uniquely identify them, and then releasing them at the point of capture (Figures 35.5 and 35.6). Although it was not a requirement to be a licensed trapper to participate in the TVR program, some of the best were licensed trappers. Their trapping expertise and knowledge of wildlife was invaluable; they were familiar with species’ behaviour, and they knew where to set the traps to catch the animals they were after. The biggest difference between traditional raccoon trapping (where the animal is normally killed by the trap) and TVR (where the animal is caught in a live-capture box trap and is not happy about being in the trap), according to eastern Ontario trapper Brian McDougall, is learning how to deal with caged animals. With TVR, you have to remember to keep your fingers out of the trap and you have to watch for claws reaching through the wire of the trap to grab your arm or leg. This can give new TVR trappers quite a surprise the first time they are grabbed by a raccoon! TVR trappers quickly learn to identify what is in the trap before they get too close to it. The sight of a white stripe in the live trap can make many people stop in their tracks. A black-and-white animal in your trap is a good reminder to slow down, take your time, and approach with caution. Many trappers have felt the effects of being sprayed in the face by a skunk when they try to rush things and have commented that skunk spray tastes much worse than it smells! Not only do the trappers have to get close enough to pick up the trap, but they also have to vaccinate the animal and affix two ear tags (Figures 35.5 and 35.6), as well as identify the gender of the animal captured. With a recaptured animal, they have to get close enough to the animal to read the tiny ear tags (Figure 35.7). It is necessary to verify the eartag numbers because some animals may have been trapped in that area in past years. The trapper needs to know whether the animal was vaccinated in the current year or

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Figure 35.5: Photograph of a trapper vaccinating a ­live-trapped raccoon against rabies before releasing it at the point of capture during TVR. Source: OMNRF.

Figure 35.6: Photo of a raccoon being ear-tagged. Each ear tag is uniquely numbered so the animal can be identified. After being vaccinated against rabies and ear-tagged, the raccoon will be released at the point of capture. Source: OMNRF.

in a previous one. If the animal had been vaccinated that year, it was released without further processing; if it had been vaccinated in a previous year, it required a booster vaccination. Recaptured animals also provide information on animal movements. Each time an animal is captured, the location is recorded, allowing researchers to map how

far individual animals are moving from week to week or from year to year. Sometimes, trappers were too good at their jobs. It was possible, especially when juvenile animals are involved, to capture more than one animal at a time in the live trap. Juveniles frequently stay close to each other and also stay

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Figure 35.7: Photo of a skunk displaying its new ear tag. ­Trappers must record the ear-tag number of recaptured skunks, which requires them to get quite close to the animal. Source: OMNRF.

close to mom. With raccoons, this is not too much of an issue. You simply transfer one of the raccoons to a second live trap and then you can process each animal separately. With skunks, this is a little more complicated, according to eastern Ontario trapper Mather. You still have to separate the skunks so that there is one animal per live trap. However, juvenile skunks tend to be easily frightened and spray whenever they are stressed. And as Mather says, “They like to spray and spray and spray.” Another aspect of TVR that can lead to interesting experiences is the requirement to get landowner permission before setting live traps on their property. The TVR trapper never knows what type of person they will encounter when they approach the landowner. It could be anyone – a nice older woman who reminds you of your grandmother and invites you in for tea, a farmer who wants to tell you his entire life history, a drug dealer growing marijuana on his property who really doesn’t want someone from the government finding his grow-op. McDougall has met them all. He’s encountered people from all walks of life and has met a lot of people that have misconceptions about wildlife. Some people are convinced that all fishers are bad because their pet cat has gone missing, that coyotes will eat little children, or that all skunks are rabid. But trappers know that all animals play an important role in the ecosystem, and the trappers are willing to take the time to try to dispel

these wildlife myths while they are talking to landowners. It takes all kinds of people and animals to keep the world interesting, and that’s one of the reasons why McDougall loved his job and couldn’t wait to get to work when he woke up each morning.

Point Infection Control Point infection control (PIC) is used to combat a focal outbreak of rabies in a new area (Rosatte et al., 2009). Initially, PIC was essentially a modified TVR program. With PIC, the area immediately surrounding the rabies outbreak is live-trapped, and all rabies vectors captured are humanely euthanized (unless they have already been vaccinated against rabies that year). This is called the depopulation zone. The area surrounding the depopulation zone receives regular TVR and all rabies vectors are vaccinated against rabies. The first PIC was implemented in Ontario in 1999 after the first case of the mid-Atlantic strain of raccoon rabies was discovered in Ontario. Since that time, PIC design has evolved to include the use of vaccine baits, as well as TVR and depopulation. Because of the serious threat posed by raccoon rabies, OMNRF’s Rick Rosatte felt that it was vital to involve local trappers in the PIC program. Local trappers were more familiar with the habitat and also knew many of

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the landowners already, which made it easier to obtain permission to set live traps on private property. Darcy Alkerton, president of the Grenville Area Fur Harvesters when the first PIC was conducted, was surprised when he was approached by OMNRF to ask for his council’s assistance. Most people had treated Alkerton like he was “just a trapper” but OMNRF valued the trappers’ assistance and gave them the recognition they deserved. This was the start of a successful relationship with OMNRF which still exists today. Alkerton realized that raccoon rabies was too close for comfort and was glad to help with rabies control programs in any way that he could – including encouraging the other members of the trapper’s council to do their part. Even when the trappers weren’t specifically involved in the PIC, they still helped out by reporting rabies-suspect animals and educating the public about raccoon rabies. Alkerton recalls an interesting phone call from a man in Brockville who made some muffins and left them to cool on the kitchen counter. A raccoon smelled the muffins, entered the kitchen through the patio door, and proceeded to eat some of the muffins. Since Alkerton also owned a nuisance animal control business, the man called Alkerton the following day for assistance. During the conversation, Alkerton determined that the caller had not been able to scare the sick-looking raccoon out of the kitchen but had managed to rescue some of his muffins from the raccoon. After being directed by Alkerton to contact his doctor, the individual was started on post-exposure rabies prophylaxis. One of the most significant differences between TVR and population reduction, PIC (from the trapper’s viewpoint) is that all animals have to be taken to a central location for processing. Normally, during TVR, the trapper vaccinates the animal at the trap site and then it is immediately released. With PIC, because the animals are going to be euthanized, they must be taken to a central site for processing as only certain staff are authorized to euthanize animals. Transporting raccoons and skunks in live traps in the back of a truck can be tricky. Bob Moir, a trapper from eastern Ontario, had an interesting experience, when he was pulled over on the 401. The female officer who pulled him over asked Moir why he was in such a hurry. Moir’s reply was that he had to get the animals in the back of his truck to the laboratory for processing. Being trained to check details, the officer looked in the back of the truck and found two skunks staring back at her. Her response was to jump away from the truck into the middle of the 401 (a major freeway), tell Moir to speed on, and then quickly depart the scene.

Trappers’ Involved in Other Rabies Control Programs in Canada Licensed trappers were also involved in rabies control programs in many other provinces in Canada. However, their involvement was at different times and not as extensive as in Ontario.

Alberta The involvement of licensed trappers in Alberta’s rabies control programs was limited. During the 1950s, trappers were used to depopulate wildlife in areas where rabies was present (Ballantyne & O’Donoghue, 1954; Gunson et al., 1978; Pybus, 1988). More information on their involvement can be found in Chapters 7 and 28. This depopulation program was the only time that licensed trappers were specifically used for rabies control in Alberta.

Quebec In Quebec, trappers have been a major component of the Ministère des Ressources Naturelles et de la Faune’s (MRNF) raccoon rabies control programs. Trappers have also been vital to the post-baiting active surveillance programs. Since 2007, commercial trappers have provided thousands of carcasses for testing, which have provided valuable information on rabies incidence, bait acceptance, and rabies antibody levels. In 2006 when raccoon rabies was confirmed in Quebec, and again in 2007, trappers were the cornerstone of the PIC program. From July to August 2007, a maximum of 43 trappers set up to 3,000 live traps each night and conducted a PIC (incorporating both TVR and population reduction) over an 1800 km2 area (P. Canac-Marquis, personal communication, December 2010). This was a very extensive operation which was only possible through the successful collaboration with the Fédération des Trappeurs Gestionnaires du Québec (FTGQ) – Quebec’s organized trapping federation. Without the help of these professionals, the successful results would have been impossible to obtain. The FTGQ also assisted MRNF by administering the salaries and expenses for all of the trappers participating in raccoon rabies control programs. In 2008 the use of live traps was replaced with the distribution of rabies vaccine baits. Trappers were asked again to participate in the hand placement of baits. Trappers used their knowledge of skunks and raccoons to specifically target the habitats where these species would be present.

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This approach gave excellent results and was adopted as a fundamental part of raccoon rabies control programs. The professionalism and dedication of the trappers was the key to the success of this approach. Trapper Pierre Martin has been involved in all of Quebec’s rabies control programs, from TVR and PIC to aerial and hand baiting and post-baiting surveillance. During his trapping efforts, Martin has frequently recaptured eartagged animals – including animals ear-tagged in New York and Vermont states. One of his most memorable recaptures was a grey fox that had been ear-tagged in New York. Grey foxes are not known to occur in Quebec. Since the animal was alive and unharmed, Martin released it but was not able to record the ear-tag numbers, which would have let him determine how far the fox had travelled. Trapper Marc Dussault has also been involved in Quebec’s raccoon rabies control programs since 2006 and has many interesting stories of unusual animals he has captured, including a few opossums – another species which is not very common in Quebec. But Dussault’s least favourite animal to capture is the porcupine. When a large porcupine walks into the live trap and gets captured, it is too big to turn around in the trap and it is unable to back out. The quills get caught in the wire mesh which prevents the animal from reversing out of the trap. When this happens, Dussault had to resort to cutting the trap apart to release the porcupine. This can be quite stressful both to Dussault and to the porcupine as neither of them wants to get too close to the other! Martin and Dussault are just two of the many trappers that have been pivotal to the successful raccoon rabies control programs. Along with their efforts to create a vaccinated population of raccoons and skunks, they have each played important roles in detecting the extent of raccoon rabies in Quebec with each of them having captured at least two rabid animals while they were trapping.

communication, December 2010). For more information on the involvement of trappers in their rabies control programs see Chapter 13.

Nova Scotia In April 2009, the Nova Scotia Department of Natural Resources enlisted the support of a trapper to assist with rabies surveillance efforts (Government of Nova Scotia, 2009). The trapper was tasked with trapping foxes in an area where rabies had been detected in December 2007. The objective of this increased active surveillance program was to ensure that rabies had not spread and was no longer present in the area.

New Brunswick In the fall of 2001, trappers from across New Brunswick participated in the province’s first TVR program (Fur Institute of Canada, 2003). TVR was implemented in response to the first case of raccoon strain rabies, which was detected in 2000. The trappers were tasked with creating a vaccinated buffer of raccoons and skunks in the area of the rabies cases. This barrier of immunized animals was crucial to the successful elimination of raccoon strain rabies from New Brunswick. For more information on New Brunswick’s rabies control programs and the role that trappers played, refer to Chapter 12. New Brunswick trappers were so enthusiastic about the rabies control programs that they even have a favourite recipe from their work. Mixing one litre of hydrogen peroxide, one cup of baking soda, and one tablespoon of liquid dish soap will give you a with solution that is more effective at neutralizing skunk odours than most commercially available products (New Brunswick Trappers and Fur Harvesters Federation, 2019).

Newfoundland and Labrador

Conclusions

Newfoundland has also benefited from the use of licensed trappers. Trappers inside and outside of the rabies control area were requested to submit fox carcasses as part of Newfoundland’s active surveillance program. Trappers received financial compensation for these carcasses which were used to analyse rabies incidence and bait acceptance. Trappers were also used to depopulate foxes in the area where rabies had been confirmed. The localized depopulation and surveillance programs were both integral to the successful control of rabies in Newfoundland (H. Whitney, personal

Trappers from across Canada have been involved in controlling rabies since before formal rabies control programs were even developed. Historically, when sick or aggressive animals were encountered, trappers and hunters were frequently called on to capture or dispatch the animals in question. Once rabies control programs were developed, trappers were called on for their expertise. They have assisted with learning more about the ecology of foxes and skunks; developing attractants for baits; assessing bait

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dispersal; providing specimens for testing for rabies, rabies antibody levels, and bait ingestion rates; and assisting with bait distribution. Trappers have participated in all aspects of rabies control and their contributions have been invaluable.

My father was one of the original trappers approached by OMNRF’s Johnston to help with its research. I grew up seeing the rabies technicians visit my house every fall to pick up carcasses and blood samples. And the one thing that I kept thinking was, “That’s such a cool job. I want to do that when I grow up.” Despite numerous technicians advising me that there was no future in wildlife research and I’d never be able to get work in the wildlife field, I went to university to study wildlife biology. And here I am, working for the OMNRF’s rabies program and still interacting with trappers throughout Ontario.

Epilogue Work with trappers has produced some unexpected contributions and results. I am one of those unexpected results.

References Ballantyne, E., & O’Donoghue, J. (1954). Rabies control in Alberta. Journal of the American Veterinary Medical Association, 125, 316–326. Daigle, J., Muth, R., Zwick, R., & Glass R. (1998). Socio-cultural dimensions of trapping: A factor analytic study of trappers in six northeastern states. Wildlife Society Bulletin, 26(3), 614–625. Dolin, E. J. (2010). Fur, fortune and empire. New York, NY: W. W. Norton. Fur Institute of Canada. (2003). Trappers: Stewards of the land. Ottawa, ON: Fur Institute of Canada. Gier, H. T. (1948). Rabies in the wild. Journal of Wildlife Management, 12(2), 142–153. https://doi.org/10.2307/3796409 Giroux, A. (1999). The role of the trapper today. In M. Novak, J. Baker, M. Obbard, & B. Malloch (Eds.), Wild furbearer management and conservation in North America (pp. 228–243). Sault St. Marie, ON: Ontario Fur Managers Federation. Government of Nova Scotia. (2009, April 6). Fox trapping program in Mulgrave (Press release). Natural Resources/Health Promotion and Protection. Gunson, J., Dorward, W., & Schowalter, D. (1978). An evaluation of rabies control in skunks in Alberta. Canadian Veterinary Journal, 19, 214–220. Retrieved from https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1789425/pdf/canvetj00333-0016.pdf MacInnes, C. D. (1999). Rabies. In M. Novak, J. Baker, M. Obbard, & B. Malloch (Eds.), Wild furbearer management and conservation in North America (pp. 910–929). Sault St. Marie, ON: Ontario Fur Managers Federation. MacInnes, C. D., & LeBer, C. (2000). Wildlife management agencies should participate in rabies control. Wildlife Society Bulletin, 28(4), 1156–1167. Retrieved from https://www.jstor.org/stable/3783876 MacInnes, C. D., Tinline, R., Voigt, D., Broekhoven, L., & Rosatte, R. (1988). Planning for rabies control in Ontario. Reviews of Infectious Diseases, 10(S4), 665–669. Retrieved from https://www.ncbi.nlm.nih.gov/pubmed/3060956 MacInnes, C. D., Smith, S., Tinline, R., Ayers, N. R., Bachmann, P., Ball, D., ... Voigt, D. R. (2001). Elimination of rabies from red foxes in eastern Ontario. Journal of Wildlife Diseases, 7(1), 119–132. https://doi.org/10.7589/0090-3558-37.1.119 New Brunswick Trappers and Fur Harvesters Federation. (2019). Striped skunk. Retrieved from http://www.nbtrappers.ca/skunk.html Payne, N. (1980). Furbearer management and trapping. Wildlife Society Bulletin, 8(4), 345–348. Retrieved from https://www.jstor.org/ stable/3781188 Pybus, M. (1988). Rabies and rabies control in striped skunks (Mephitis mephitis) in three prairie regions of western North America. Journal of Wildlife Diseases, 24(3), 434–449. https://doi.org/10.7589/0090-3558-24.3.434 Rosatte, R. C. (1999). Striped, spotted, hooded, and hog-nosed skunk. In M. Novak, J. Baker, M. Obbard, & B. Malloch, Wild furbearer management and conservation in North America (pp. 599–613). Sault St. Marie, ON: Ontario Fur Managers Federation. Rosatte, R. C., & Larivière, S. (2003). Skunks. In G. A. Feldhamer, B. C. Thompson, & J. A. Chapman (Eds.), Wild mammals of North America: Biology, management, and conservation (2nd ed., pp. 692–707). Baltimore, MD: Johns Hopkins University Press. Rosatte, R., Power, M., MacInnes, C., & Campbell, J. (1992). Trap-vaccinate-release and oral vaccination for rabies control in urban skunks, raccoons and foxes. Journal of Wildlife Diseases, 28(4), 562–571. https://doi.org/10.7589/0090-3558-28.4.562 Rosatte, R., Power, M., Donovan, D., Davies, J. C., Allan. M., Bachmann, P., ... Muldoon, F. (2007). The elimination of the arctic variant of rabies in red foxes in metropolitan Toronto, Ontario, Canada. Emerging Infectious Diseases, 13(1), 25–27. https://doi.org/10.3201/ eid1301.060622

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Special Interest Groups Rosatte, R., Donovan, D., Allan, M., Bruce, L., Buchanan, T., Soby, K., ... Wandeler, A. (2009). The control of raccoon rabies in Ontario, Canada: Proactive and reactive tactics, 1994–2007. Journal of Wildlife Diseases, 45(3), 772–784. https://doi. org/10.7589/0090-3558-45.3.772 Royle, S. (2010). Company, crown and colony: The Hudson’s Bay Company and territorial endeavour in western Canada. New York, NY: J. B. Tauris. Schubert, C., Rosatte, R., MacInnes, C., & Nudds, T. (1998). Rabies control: An adaptive management approach. Journal of Wildlife Management, 62(2), 622–629. https://doi.org/10.2307/3802338 Siemer, W., Batcheller, G., Glass, R., & Brown, T. (1994). Characteristics of trappers and trapping participation in New York. Wildlife Society Bulletin, 22(1), 100–111. Retrieved from https://www.jstor.org/stable/3783230 Tabel, H., Corner, A. H. Webster W. A., & Casey, C. A. (1974). History and epizootiology of rabies in Canada. Canadian Veterinary Journal, 15(10), 271–281. Retrieved from https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1696688/pdf/canvetj00419-0015.pdf Verts, B., & Storm, G. (1966). A local study of prevalence of rabies among foxes and striped skunks. Journal of Wildlife Management, 30(2), 419–421. https://doi.org/10.2307/3797831 Voigt, D. (1999). Red fox. In M. Novak, J. Baker, M. Obbard, & B. Malloch (Eds.), Wild furbearer management and conservation in North America (pp. 228–243). Sault St. Marie, ON: Ontario Fur Managers Federation.

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36 First Nations People and Rabies Henry Lickers1 and Michael T. Francis Jr.2 1

Environmental Science Officer, Mohawk Council of Akwesasne, Ontario, Canada 2 Conservation Officer, Mohawk Council of Akwesasne, Ontario, Canada

Place The Mohawk Nation at Akwesasne is a Kanien’kehá:ka territory that straddles the intersection of the United States and Canadian borders and the Ontario and Quebec boundaries on both banks of the St Lawrence River (Figure 36.1). Although divided by an international border, the residents consider themselves to be one community. It was founded in the mid-eighteenth century by people from Kahnawake, a Catholic Mohawk village south of Montreal. It has 12,000 residents, with the largest population and land area (85.89 km2) of any Kanien’kehá:ke community. The name Kanien’kahá in the Mohawk language means “Land Where the Ruffed Grouse Drums,” referring to the rich wildlife in the area.

The territory incorporates part of the St Lawrence River, the mouths of the Raquette and St Regis rivers, and a number of islands in each of these three rivers. The nation is divided north-south by an international boundary, with the northern portion further divided by the provincial boundary between Ontario and Quebec. The Three Nations Crossing connects Cornwall Island, Ontario, to the city of Cornwall in the north and New York in the south.

Introduction Native peoples have occupied the area of the St Lawrence River that we now call Akwesasne for the past 10,000 years.

Figure 36.1: Map of Akwesasne showing the boundaries with Ontario, Quebec, and the United States. Source: map modified from original obtained from www.akwehsg.org.

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Mohawk people came to the St Lawrence, because of the abundance of fish, animals, and plants. Major animal corridors existed through the Akwesasne area. The area also had good farmlands that could be used to grow corn, beans, and squashes, staples of the Haudenosaunee. The islands of the St Lawrence were occupied by fishing camps and archaeological evidence can be found on all the islands. In the St Lawrence River Valley, evidence can be found of the Anishnabek nation. They clearly saw the riches of the area and formed alliances and agreements with the ­Mohawk people so that all could share in the benefits of the region. A wampum belt was made and buried on the shore of the St Lawrence to signify this agreement. This “friendship” belt has been honoured in modern time in that the First Nations People of Golden Lake, direct descendants of these early Anishnabek people, do not claim the St ­Lawrence ­Watershed as part of their land claims. The peace of the area was disturbed when Europeans began fur trading. A conflict developed between the First Nations peoples in the area but the peace of the “friendship” belt was still honoured. With the introduction of the fur trade there is evidence that rabies or the “madness” was introduced into the populations of animals of Akwesasne. Today, rabies is known by many names among First Nations peoples in Canada, but the disease was relatively unknown before European contact. The first recorded case of rabies in North America was by a priest in Mexico to his superiors in Spain. He was reprimanded for raising the problem. By the mid-1700, rabies was reported throughout the eastern United States and eastern Canada. The First Nations people who encountered this disease knew the symptoms and its final outcome: death. It was usually described in the First Nations language by its symptoms as mind altering, raging, and fear of water. They also knew its sources to be dogs, foxes, coyotes, wolves, and bats. Legends also speak of shapeshifters and skinwalkers as having rabies-like symptoms. Today, talking to elders, it is hard to find accurate translations of rabies and very old stories about the disease, but it is feared by all communities. Dogs have been companions of First Nations people in time out of memory, with legends describing the domestication of dogs as mutually beneficial to both animals and people. Therefore rabies was seen as a horrible disease that affected not only the animals but also the relationship between dogs and the people. In communities, First Nations people are concerned about the Dog Problem. Children are more likely to be bitten on reserves than outside in the non-native communities and in most cases these are not well reported.

Little is known about rabies in Akwesasne – perhaps its isolation by rivers kept it immune from the outbreaks in Ontario and Quebec. However, when raccoon rabies moved up the east coast of the United States, threatening Canada, First Nations people became involved in prevention and treatment of the disease. While other groups may have been involved with rabies, the actions taken by the Akwesasne peoples helped in large part to prevent raccoon rabies from entering into Canada across their lands. Raccoon rabies in other parts of Ontario, Quebec, and the Maritimes is described in Chapters 10, 11, and 12.

Rabies Considerations In 1791 the British colony known as Canada was divided into Upper and Lower Canada. The area around Akwesasne was not included in the division because the Mohawk Peoples of Akwesasne were viewed as allies to the Crown. The border of the territory between Quebec and Ontario was not established until 1978 by a proclamation of the two provinces. Many bridges were built to improve access between the Nations but that also increased animal passage. The scientific literature is discouraging: many articles and research reports discuss Canada-wide outbreaks of rabies, but very few concentrate on First Nations communities and the incidence of rabies there. Health Canada and First Nations Community records of reported rabies are rare. The complex jurisdiction between the provincial and federal Governments may cloud a clear understanding of these issues in First Nations communities. By 1980 the Mohawk Council of Akwesasne began to formulate a code that became the Wildlife Conservation Community Law. In 1981 the Department of the Environment was the first department to take on the Conservation Program and begin enforcing the Wildlife Conservation Community Law. The Mohawk Council of Akwesasne needed to form their own court system to try people who violated the law. In 1985 the Wildlife Conservation Community Law was passed by the Mohawk Nation Council of Chiefs as a community law for the Mohawk Council of Akwesasne. Enforcement of that law was assigned to the Conservation Program and its officers. The Canada Department of Indian Affairs revoked the Wildlife Conservation Community Law as a by-law as established under the Indian Act, however the Mohawk Council of Akwesasne continues to enforce the law through its own court system.

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In 1987 the Conservation Program was transferred to the Mohawk Police Department, and the conservation officers were armed. In 1995 the provincial government charged an Akwesasne conservation officer with carrying a handgun but the judge dismissed that charge on a technicality. In 1996 the Adams case (R v Adams, [1996] 3 SCR 101) was finally decided in favour of the rights of the Mohawk to hunt and fish on the St Lawrence River. The Adams case became a keystone similar to the Marshal case in establishing native rights to resources.

Participation From 1996 to 2009, the Mohawk Department of the Environment administered the Conservation Program. That program and the Department of the Environment began to build positive relationships with what was then the Ontario Ministry of Natural Resources (OMNR). This development led to the Mohawk Council helping OMNR with yellow perch regulations, eel population research, and raccoon rabies and West Nile studies. The Ministry of Natural Resources cooperated with the Mohawk Conservation Program to patrol the St Lawrence and developed a working relationship with the Department. At the same time, the Department has made a concerted effort to inform and involve local non-native hunt and game clubs to understand Mohawk wildlife issues. Various local hunting clubs look to the Conservation Program for guidance. While the work of the Conservation Program is essential for the survival of the natural resources of the St Lawrence River, funding for this program has always been insufficient since the Mohawk Council of Akwesasne receives no funding for it. At present, the Conservation Department is administered by the Justice Program. In 1990 raccoon rabies advancing from the south had crossed New York State and was threatening to invade Canada. Akwesasne became part of the frontline to keep raccoon rabies from entering Canada. The Mohawk People of Akwesasne charged their Environmental people to understand and work with Ontario authorities to stop the spread of raccoon rabies. During 1990 and 1991 several meetings were held between the OMNR and the Department of the Environment of the Mohawk Council of Akwesasne. Civil unrest in the communities caused a hiatus in the negotiations. In 1994 the Conservation Department began to work with OMNR to understand the problem and then identify actions that could be carried out in Akwesasne. The Mohawk Council of Akwesasne, Department of the ­Environment (Figures 36.2a and 36.2b), began to inform

Figure 36.2a: Environmental Science Officer Henry Lickers, Akwesasne. Source: courtesy of Henry Lickers.

Figure 36.2b: Environmental O ­ fficer Michael Francis, Akwesasne. Source: courtesy of Henry Lickers.

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Special Interest Groups

Figure 36.3: Trapped raccoons to be vaccinated and released. Source: authors.

other ­Mohawk Communities about the dangers of raccoon rabies: Six ­Nations near Brantford, Kahnawake near Montreal, Tyendinaga near Belleville, and the St Regis Tribal Council were just a few. By 1995 the islands in the St Lawrence River were identified as a possible gap in the frontline defences and the Conservation Department began hand placing raccoon rabies baits on all of the islands. They also assisted Kahnawake and St Regis Mohawk Tribe with a baiting project. Information packages for the community of Akwesasne was developed informing the community about the baiting program and the need to vaccinate the local pet population against rabies. By 2000–2004, the Conservation Department was actively trapping, vaccinating, and releasing raccoons and skunks on the island and main lands of the community of Akwesasne. OMNR, per Rick Rosatte, supplied Imrab rabies vaccine, live traps, and other support. While this work was integral to the Ontario, New York, and Quebec programs, Akwesasne’s involvement was not mentioned in the government reports. In 2002 the Mohawk Council of Akwesasne passed the Mohawk Council of Akwesasne Rabies Protocol and Agreement, which outlined the procedures that the Conservation Department would use to curtail the spread of raccoon rabies. It also established the responsibilities of the Mohawk Council of Akwesasne, Department of Environment, and Department of Conservation, and OMNR if an outbreak should occur. That agreement continues today. The Departments of Environment and Conservation reported our insights and activities on the

raccoon rabies issues at the Raccoon Rabies Colloquium in June 2003. Our information was well received by the participants. From 2004 to 2007, the trap, vaccination, and release project (Figure 36.3) continued, and 300 raccoons, 200 skunks, 2 fishers, and 10 foxes on the St Lawrence River islands were trapped, vaccinated, and released. The Mohawk Council of Akwesasne continued to inform the community concerning raccoon rabies, and their conservation officers made numerous presentations to local schools, elders committees, homemakers associations, and public meetings. During this time, the conservation officers participated in aerial baiting drops (Figures 36.4, 36.5, and 36.6) along with conservation officers from Kahnawake and the St Regis Tribal Council. Conservation officers also collected hair samples from captured raccoons as part of a study coordinated by OMNRF to examine the genetic characteristics of raccoons in the area. The cooperation between OMNR and Mohawk communities in Canada and the United States has led to a protected border. The influence of raccoon rabies was even included in the design of the new Three Nations Bridge at Cornwall. The Mohawk Council of Akwesasne and the Department of the Environment asked that a closed girder system be used for the new bridge to prevent raccoons from crossing the river via the bridge. Cameras are used to help monitor for hitchhiking animals on trucks and other vehicles. The Department of the Environment and Conservation also reported on First Nations activities and findings to

594

First Nations People and Rabies

Figure 36.4: Environment ­officers from Akwesasne ­preparing for a bait drop. Source: authors.

Figure 36.5: Monitoring the bait machine in flight – an ­Akwesasne volunteer (left) with an OMNRF member of the ­rabies team. Source: authors.

protection of First Nations people. Funds for the development of dog control and veterinary infrastructure are mandated by sections of the Indian Act and through several provincial acts. First Nations need these regulations and have asked for these programs but have received little response. A few First Nations communities have animal welfare or dog management programs but that is changing. As a community that lives on the border, Akwesasne has to contend with many problems that other communities

the Canadian Food Inspection Agency’s World Rabies Day Symposium in 2007.

Discussion Many First Nations communities are developing animal welfare and dog management strategies. The Indian Act gives discretionary power to band councils to act in the

595

Special Interest Groups

Figure 36.6: Loading the bait machine – an Akwesasne ­volunteer (left) with an OMNRF member of the rabies team. Source: authors.

do not have. Canada Border Services Agency must also be vigilant to prevent the spread of raccoon rabies. A unique problem for First Nations is the practice of abandoning unwanted pets and young wildlife on First Nations lands. It is not unusual for the conservation officers to respond to 200 to 300 animal nuisance reports a year. Many of these incidents involve abandoned kittens and puppies left by the road or dropped into drainage ditches. They have had to respond to exotic pets like boas and other snakes that have been left in the marshes. Since Akwesasne still has pristine lands and islands, many people believe they can harvest what they want from our lands. The harvesting of wild garlic, turtles, and snakes has increased over the past decades. These illegal abandonments and harvests have a direct bearing on the ability to protect our lands and people. Raccoon rabies control, while very important, must compete with the problems of dealing with exotic and noxious species that invade Akwesasne. The Mohawk People of Akwesasne will continue to work for the protection of their lands, animals, and people

because it is their responsibility to do so. They are thankful to their friends and neighbours who have helped over the years and send them our sincere greetings and gratitude. We thank you for hearing our story. Now our minds are one – Naiwen kowa.

Note This chapter is a good example of the cooperation between First Nations people and the rabies control efforts in Ontario. Many of the other First Nations participated in the aerial baiting or the distribution of baits by hand in specific areas. Table 36.1 lists the First Nations that worked with OMNR and details the time and nature of their involvement. The table was provided by the OMNR (now Ontario Ministry of Natural Resources and Forestry) and covers the period from the beginning of Ontario’s control program in 1989 to 2012. There were no control efforts on First Nations land in 2013 and 2014.

596

Table 36.1  First Nations that worked with the Ontario Ministry of Natural Resources, the time and nature of their involvement, 1989 to 2012. Year

Reserve Name

Reserve Number

Nation

Area (km2)

County 

OMNR District

1 9 8 9

Chippewas of Saugeen

Saugeen Hunting Ground

60A

Chippewa

6

Bruce

Midhurst

-

-

-

-

-

-

-

-

 

 

-

-

-

-

 

-

 

 

 

 

 

 

 

 

Chippewas of Nawash

Cape Croker Hunting Ground

60B

Chippewa

9

Bruce

Midhurst

-

-

-

-

-

-

-

-

 

 

-

-

-

-

 

-

 

 

 

 

 

 

 

 

Chippewas of Nawash

Cape Croker

27

Chippewa

63

Bruce

Midhurst

-

-

-

-

-

-

-

-

 

 

-

 

-

-

 

 

 

 

 

X X  

 

G

Chippewas of Saugeen

Chief’s Point

28

Chippewa

5

Bruce

Midhurst

-

-

-

-

-

 

 

 

 

 

 

 

 

 

 

 

 

 

 

X X  

X X

Chippewas of Saugeen

Saugeen

29

Chippewa

37

Bruce

Midhurst

-

-

-

-

-

 

 

 

 

 

 

 

 

 

 

 

 

 

 

X X  

X X

Chippewas of Nawash

Saugeen & Cape Croker Fishing Island

 

Chippewa

 

Bruce

Midhurst

-

-

-

-

-

-

-

-

-

-

-

-

-

-

-

-

 

 

 

 

 

 

 

 

Beausoleil First Nation

Christian Island

30

Chippewa

54

Simcoe

Midhurst

-

-

-

-

-

-

-

-

-

-

-

-

-

-

-

-

 

 

 

 

 

 

 

 

Beausoleil First Nation

Christian Island Wharf

30A

Chippewa

1

Simcoe

Midhurst

-

-

-

-

-

-

-

-

-

-

-

-

-

-

-

-

 

 

 

 

 

 

 

 

Chippewas of Mnjikaning Rama

32

Chippewa

9

Simcoe

Aurora

-

-

-

-

 

 

 

 

 

 

-

-

-

-

-

-

 

 

 

 

 

 

 

 

Six Nations of the Grand River Territory Mississaugas of New Credit Six Nations of the Grand River Territory Munsee-Delaware First Nation Onyota’a:ka First Nation

Six Nations

40

Six Nations

157

Brant

Guelph

-

-

-

-

-

 

 

 

 

 

 

 

 

 

 

-

 

 

 

X X X  

 

New Credit

40A

 

19

Brant

Guelph

-

-

-

-

-

 

 

 

 

 

-

 

 

 

 

-

 

 

 

 

 

Glebe Farm

40B

Mississauga

1

Brant

Guelph

-

-

-

-

-

 

 

 

 

 

 

 

 

 

 

 

 

 

 

X X X  

 

Muncey

 

1

Middlesex

Aylmer

-

-

-

-

-

-

 

 

 

 

 

-

-

-

-

 

 

 

 

 

 

 

 

 

Oneida

41

MunseeDelaware Oneida

21

Middlesex

Aylmer

-

-

-

-

-

-

 

 

 

 

 

-

-

-

-

 

 

 

 

 

 

 

 

 

Caradoc

42

Chippewa

44

Middlesex

Aylmer

-

-

-

-

-

-

 

 

 

 

 

-

-

-

-

 

 

 

 

 

 

 

 

 

Chippewas of Kettle and Kettle Point Stony Point (Ipperwash)

44

Chippewa

19

Lambton

Aylmer

-

-

-

-

-

-

 

 

-

-

-

-

-

-

-

-

 

 

 

 

 

 

 

 

Chippewas of Aamjiwnaang

Sarnia

45

Chippewa

25

Lambton

Aylmer

-

-

-

-

-

-

 

-

-

-

-

-

-

-

-

-

 

 

 

 

 

 

 

 

Bkwejwanong Territory

Walpole Island

46

Chippewa

164

Lambton-Kent

Aylmer

-

-

-

-

-

-

 

-

-

-

-

-

-

-

-

-

 

 

 

 

 

 

 

 

Delaware First Nation

Moravian

47

Moravian

12

Kent

Aylmer

-

-

-

-

-

-

 

 

 

 

 

-

-

-

-

-

 

 

 

 

 

 

 

 

Chippewas of Georgina Island

Georgina Island

33

Chippewa

15

York

Aurora

-

-

-

-

-

-

-

-

-

-

-

-

-

-

-

-

 

 

 

 

 

 

 

 

First Nations Name

Chippewas of the Thames

1 9 9 0

1 9 9 1

1 9 9 2

1 9 9 3

1 9 9 4

1 9 9 5

1 9 9 6

1 9 9 7

1 9 9 8

1 9 9 9

2 0 0 0

2 0 0 1

2 0 0 2

2 0 0 3

2 0 0 4

2 0 0 5

2 0 0 6

2 0 0 7

2 0 0 8

2 0 0 9

2 0 1 0

2 0 1 1

2 0 1 2

(Continued)

35

Curve Lake

Curve Lake Island

Curve Lake First Nation

Curve Lake First Nation

37 37A

Alderville

Sugar Island

Tyendinaga

Alderville First Nation

Alderville First Nation

Mohawks of the Bay of Quinte

36

Whitefish Lake

Dokis

Nippissing

Whitefish Lake First Nation

Dokis First Nation

Nippissing First Nation

10

9  

 

 

 

Iroquois

Mohawk

Mississauga

Mississauga

Mississauga

Mississauga

Mississauga

Mississauga

Mississauga

Chippewa

Nation

-

 

 

 

 

8

1

Nipissing

Nipissing

Sudbury

Renfrew

Stormont

Hastings

Northumberland

Northumberland

Peterborough

Peterborough

Peterborough

Peterborough

Durham

York

County 

North Bay

North Bay

Sudbury

Pembrooke

Kemptville

Peterborough

Peterborough

Peterborough

Peterborough

Peterborough

Peterborough

Peterborough

Aurora

Aurora

OMNR District

-

-

-

-

-

 

-

-

-

-

-

-

-

-

-

-

 

-

-

-

-

-

-

-

-

-

-

1 9 9 0

-

-

-

 

-

-

-

-

-

-

-

-

-

-

1 9 9 1

-

-

-

 

-

 

-

-

-

-

-

-

-

-

1 9 9 2

-

-

-

 

-

-

-

-

-

-

-

 

 

-

1 9 9 3

-

-

-

-

-

 

-

 

-

 

-

 

 

-

1 9 9 4

ERA planned drop, but not certain if area was baited that year

13

1

8

5

7

3

 

Area (km2)

Note: All rows represent aerial baiting except shaded rows, which were hand baited.

G Ground baited by First Nations band

Golden Lake

6

59 39

Mohawks of Akwesasne Akwesasne Island

Algonquines of Pikwakanagan First Nation

38

36A

Hiawatha

Island in the Trent waters

Hiawatha First Nation

Hiawatha First Nation

35A

34

ERA

Reserve Number

Georgina Island Wharf 33A

Reserve Name

Mississaugas of Scugog Scugog

Chippewas of Georgina Island

First Nations Name

1 9 8 9

-

-

-

-

-

 

-

 

-

 

-

 

 

-

1 9 9 5

-

-

-

-

-

 

-

 

-

 

-

 

 

-

1 9 9 6

X

-

-

-

-

-

 

-

 

-

 

-

 

 

-

1 9 9 7

-

-

-

-

-

 

-

 

-

 

-

 

 

-

1 9 9 9

-

-

-

-

-

 

-

 

-

 

-

 

 

-

2 0 0 0

ONRAB

-

-

-

-

-

 

-

 

-

 

-

 

 

-

1 9 9 8

-

-

-

-

-

-

-

 

-

 

-

 

 

-

2 0 0 1

Year

 

 

-

-

-

-

-

 

-

 

-

 

 

-

2 0 0 2

 

 

 

-

-

-

-

 

-

 

-

 

 

-

2 0 0 3

 

-

-

-

-

-

-

-

-

 

-

-

-

-

-

-

-

-

 

 

 

 

   

 

 

2 0 0 6

 

 

2 0 0 5

V-RG

-

-

-

-

-

-

-

-

-

 

-

 

 

-

2 0 0 4

-

-

-

-

-

-

-

-

 

 

 

 

 

 

2 0 0 7

-

-

-

-

-

-

-

-

 

 

 

 

 

 

2 0 0 8

-

-

-

-

-

-

-

-

 

 

 

 

 

 

2 0 0 9

-

-

-

-

-

-

-

-

 

 

 

 

 

 

2 0 1 0

-

-

-

-

-

-

-

-

 

 

 

 

 

 

2 0 1 1

-

-

-

-

-

-

-

-

 

 

 

 

 

 

2 0 1 2

37 Inuit and Rabies David J. Gregory,1 Susan Nadin-Davis,2 and Maanasa Raghavan3 1

Canadian Food Inspection Agency (Retired), Ottawa, Ontario, Canada Ottawa Laboratory Fallowfield, Canadian Food Inspection Agency (Retired), Ottawa, Ontario, Canada 3 Assistant Professor, Department of Human Genetics, University of Chicago, Illinois, United States

2

Introduction It is clear from the chapters dealing with rabies in southern Canada (Chapter 2 and Chapters 6 to 12) that the distribution of rabies has been influenced by human settlement and land use patterns as well as human association with pets and livestock that are affected by rabies. In the north, however, the implicit assumption seems to be that the sparse human population has had little impact on the distribution of rabies, save that population centres were sample locations for observing the disease. Indeed, most of the speculation about the persistence of rabies in the Arctic (see Chapter 26b) centres on the ecology of the arctic fox and says little about the impact of the peoples of the north on the disease. Approximately 1000 years ago, Thule culture and technology developed in the Bering Strait area and swept eastwards across Arctic Canada reaching Greenland a few hundred years later (McGhee, 1996; Friesen et  al., 2008; Morrison, 1999). The Thule are the cultural and biological ancestors of Inuit who inhabit the North American Arctic today (McGhee, 1984a; Raghavan et al., 2014). Along the way, the Thule displaced or eliminated the Dorset culture that had populated the area previously. Although the exact trigger behind the eastwards Thule expansion is debated, hypotheses include Thule hunters following an increased bowhead whale range (McGhee, 1996; Maxwell, 1985), which might have occurred in tandem with the warming of the North American Arctic during the Medieval Warm Period (Taylor, 1963), or, alternatively, the Thule being in

search of metal further east in Greenland (McGhee, 1984b). The Thule technology made them more mobile compared to previous groups that had inhabited the region such as the Dorset; the Thule used dog sleds, larger boats at sea, and kayaks that made travel and hunting on land and sea more effective (McGhee, 1996; Maxwell, 1985). Improved technology meant better food resources, and the Thule lived in much larger settlements, typically dozens of people, rather than the scattered smaller Dorset settlements. Could this combination of mobility, use of dogs, and land settlement have affected the spread of rabies? Recent evidence that rabies spread to the Arctic from northern Asia (Nadin-Davis et  al., 2007) and that this movement may have been facilitated by human activity (Bourhy et al., 2008) supports speculation that peoples of the north have had at least some influence on the spread and persistence of rabies in the Arctic. Hence, this chapter discusses what is known about ­Inuit settlements and their association with rabies and how these might relate to recent evidence about the nature of the rabies virus in the north and its origins. Unfortunately, the history of Inuit themselves consists of limited archaeological evidence, some stories handed down from one generation to another, the scattered reports of explorers, a few observations from various northern administrators, and recent DNA evidence (see Chapter 29). While this chapter is often speculative, it does provide another viewpoint on why the virus persists in the north and the extent to which human settlement patterns are associated with rabies.

Special Interest Groups

to survive the harsh climate of Alaska, Arctic Canada, and Greenland over the past 5000 to 6000 years, However, there is little consensus in the archaeological literature as to how these different peoples were related to one another and to the current inhabitants of the region: Inuit (Raghavan et al., 2014; Park, 2014). The Arctic Small Tool tradition (3000–800 BCE), or the Early Paleo-Inuit, included the Denbigh Flint complex of Northern Alaska, the Pre-Dorset culture in Arctic Canada, and the Independence I and the Saqqaq cultures in Greenland (Irving, 1962; Maxwell, 1984, 1985; Dixon, 2013). The Pre-Dorset, Independence I, and the Saqqaq cultures were the earliest cultures to inhabit the Canadian Arctic and Greenland as they migrated eastwards along the northern coast from Alaska some 5000 years ago, reaching ­Greenland around 4000 years ago. They possessed toolkits similar to those of the northeastern Siberian Neolithic cultures, and their primary subsistence sources included musk ox, caribou, and seals (McGhee, 1996). The Arctic Small Tool tradition was succeeded by the Late Paleo-Inuit, who were represented by two groups: one in Alaska named the Norton tradition (about 1000 BC–800 CE), and the Dorset culture, consisting of Early, Middle, and Late Dorset cultures (800 BC–1300 AD), which developed in Arctic Canada (Dixon, 2013; Maxwell, 1984). Most Norton archaeological sites are noted for subterranean homes, pottery, oil lamps, and elaborate ivory carvings (Ipuiutak carvings) (Dixon, 2013). The Dorset culture (Tuniit in Inuktitut) adapted well to conditions in the Arctic, flourishing for 2000 years and occupying large areas in their dispersal. They had the technology to build snow houses (igloos) allowing them to spend the long winter months on the sea ice hunting sea mammals (McGhee, 1996). They are well known for their ­miniature carvings and perhaps the use of shamans (­McGhee, 1996). Around 800 CE, the climate warmed, interfering with their winter hunting, and around 1300 CE, they disappeared from the archaeological record, aided, perhaps by the a­ rrival of the Thule culture and other unknown factors (Park, 2014). An exception were the now-extinct ­ Sadlermiut people, who occupied the Southampton Island in the Hudson Bay ­between the fifteenth and nineteenth centuries AD and were considered to be descendants of the Dorset people based on cultural and genetic similarities. The Thule culture, part of the Neo-Inuit tradition (about 200 BCE–1700 CE), is thought to have developed in Alaska around 1000 years ago from the preceding Beringian cultures, such as Punuk, Birnirk, and Ipiutak, and rapidly spread eastwards into Greenland about 1300 years ago (Friesen & Arnold, 2008; Morrison, 1999; Mason, 2007).

Inuit – Past and Present What are the origins of the Canadian Arctic peoples and their dogs? And did they bring a rabies virus with them? In simple terms, the Paleo-Inuit (Pre-Dorset and Dorset cultures, also Paleo-Eskimos), the earliest tradition to inhabit the North American Arctic, archaeologically show little use of dogs (Morey & Aaris-Sorensen, 2002). They were succeeded by the Thule culture, part of the Inuit (also Neo-Eskimo) tradition, who made extensive use of dogs for transport, a tradition that still exists among present-day Inuit. The following sections will trace the archaeological and DNA evidence of the various Arctic cultures, focusing on the Thule culture and their dogs, and speculate on the origins of the rabies virus in the Arctic north from Siberia to Greenland.

Archaeological Evidence The earliest documented human presence in the North American Arctic dates back about 14,000 years ago in present-day Alaska. These Paleoindians, a term given to the people who entered and eventually inhabited the American continent during the final glacial stage of the Pleistocene period, eventually developed a tradition that became known as the Nenana Complex. Named after the Nenana valley in Central Alaska and dating between 12,000 and 11,000 years ago, this tradition was distinct from succeeding cultures in that it did not develop the use of microblades (Goebel & Buvit, 2011). Sometime after 11,000 years ago, the prehistoric Bering land bridge connecting Alaska and Siberia was inundated by the rising sea level (Elias et  al., 1996). Around this time, people from the Diuktai culture with origins in Siberia inhabited Alaska. Other cultures followed these Paleoindians in Alaska and were given various names (e.g., Northwest microblade tradition, Denali Complex or Beringian tradition) but fall under a general term of Paleo-Arctic tradition. They were known for their stone technology, including microblades used for hunting (Fagan, 2005). Although the earliest documented evidence of humans in the North American Arctic is from Alaska about 14,000 years ago (Goebel & Buvit, 2011), the evidence of humans spreading east into Arctic Canada and Greenland is not until much later, around 6000 years ago, with the Paleo-Arctic tradition in Alaska giving way to the Arctic Small Tool tradition (Harritt, 1998). Archaeological evidence shows that several traditions and cultures, identifiable by their distinct tool making, art, and hunting expertise, were able

600

Inuit and Rabies

Figure 37.1. Eskimo is used for some Native populations living in parts of Alaska and Siberia (Park, 2014). While there are northward and southward migrations of the Thule in the North American Arctic, this chapter deals only with the northern migrations along the north coast of Alaska in the formation of the present Inuit culture.

As the Thule spread across the Canadian Arctic, they left archaeological evidence of their stay, with some Thule sites being found as far as Labrador’s Killinek Island, Staffe Island, and Saglet Bay (1500) (Pastore, 1998). The Thule adapted to the Arctic environment by hunting large sea mammals in open water, using drag floats attached to their harpoon lines, large skin boats or umiaks used for transporting goods and people, and kayaks for hunting, and the introduction of dogs to pull large sleds (Maxwell, 1985; McGhee, 1996). Between 1400 CE and 1600 CE, the Little Ice Age shortened the season for open-water whale hunting, and by the sixteenth century, umaik and kayak whale hunting had ceased. The Thule communities dispersed and the people became known as historical Inuit (McGhee, 1984b). This led to the modern day Inuit culture with new survival tools. The terms Inuit and Eskimo are often confused in use. Today, Inuit refers to Indigenous people who live in the Canadian Arctic, Greenland, and Alaska as shown in

INUIT CONTACT WITH THE VIKINGS AND OTHER HISTORICAL EUROPEANS

When the Vikings arrived in the Arctic in the tenth century, they encountered the Dorset – or skraelings, as they called them – noting that they did not use iron but were adept at hunting with walrus tusks and used sharpened stones in place of knives. More puzzling was the fact that when hit with the Vikings’ iron weapons, the people did not bleed. This was probably due to the more blade-­resistant animal skins worn by the Dorset hiding the wound ­(Gamble, 2011).

Figure 37.1: Modern day Inuit regions of Arctic Canada.

601

Special Interest Groups

The first Europeans the Thule had contact with were the Vikings, who had settled in Greenland and referred to them, as they had the Dorset, as skraelings. In 1576 the Thule met Martin Frobisher off Baffin Island in his quest for the Northwest Passage (McGhee, 2005). The Thule culture had already spread out across the Canadian Arctic and eventually to Greenland and Labrador by 1200–1300. A hundred years after contact with Frobisher, the Labrador Inuit met with the Basque whalers and fisherman who were already working the Labrador coast and establishing whaling stations. The Thule were using iron tools long before post-Viking European contact, obtained either from meteoric sources or trade with the Vikings. Climate change forced Inuit to subsist on a poorer diet and lose access to essential raw materials for tools. They were forced to move south using marginal niches along the edges of the treeline. Evidence suggests that they were still moving southward in Labrador when they first met Europeans in the seventeenth century.

Inuit in both Canada and Greenland, and are genetically related to or descendants of the Siberian Birnirk culture (Raghavan et al., 2014). Moreover, on the basis of both mitochondrial and nuclear DNA markers, the authors found no evidence for the extinct historical Sadlermiut people as Dorset remnants and instead observed that this population was closely related to the Thule and present-day Inuit. The study sheds light on the peopling of the North American Arctic and the origins of Inuit by showing that (1) Paleo-Inuit and the Thule/Inuit constituted different migrations from one another, as well as from other Indigenous populations across the Americas; (2) all Paleo-Inuit (Saqqaq, Pre-Dorset, and Dorset) represent a single genetic lineage that survived in the North American Arctic for over 4000 years; (3) there is genetic continuity over the last 1000 years of Greenlandic and ­Canadian Thule and present-day Inuit populations; (4) there is a close genetic relationship between Siberian Birnirk and the Thule, suggesting the former was not only culturally but possibly also genetically ancestral to the Thule; (5) individuals from the Sadlermuit site on Southampton Island, Canada, were either genetically derived from or related to Thule rather than to the Paleo-Inuit; and (6) potential genetic admixture between the Paleo-Inuit and Thule cannot be discounted. Overall, the Paleo-Inuit and Thule peoples appear to have occupied the North American Arctic for close to 5000 years, with a single population replacement by the Thule some 750 years ago.

DNA Evidence Arctic-adapted Inuit live in the regions extending from Alaska to Greenland. In terms of biological, linguistic, and archaeological evidence, they are distinct from all other aboriginal populations of the Americas and derive from a more recent migration from East Asia (McGhee, 1996; Greenberg et al., 1986; Gilbert et al., 2008; Raghavan et al., 2014). Recently, Raghavan et  al. (2014) analysed nuclear and mitochondrial DNA markers from a large number of ancient human bones, teeth, and hair from field and museum collections from Arctic Siberia, Alaska, Canada, and Greenland. Some of these ancient samples were radiocarbon dated for accurate cultural assignment (Raghavan et  al., 2014). Their results show two separate migrations from Siberia into the North American Arctic, including Greenland, the first being the Paleo-Inuit tradition, including the Pre-Dorset and Dorset cultures, and the second being the Neo-Inuit tradition, including the Thule culture (Plate 28). The study further shows that all Paleo-Inuit are genetically closer to each other than to any present-day populations, suggesting that the Early Paleo-Inuit (Pre-Dorset and Saqqaq) and the Late Paleo-Inuit (Dorset) were part of the same migration into the North American Arctic (Raghavan et  al., 2014). Among present-day populations, the PaleoInuit are observed to share some level of ancestry with northeast Siberians (e.g., Chukchi) and Inuit. Additionally, the Thule are genetic and cultural ancestors of modern day

Inuit Sled Dog Humans have been closely linked to their canine companion since dogs’ domestication some 15,000 years ago (Brown et al., 2013). A study by Leonard et al. (2002) throws some light on the origin of dogs in the Americas before European colonization led to the dilution of the original gene pool. The authors conclude that Eurasian and American domestic dogs originate from Old World grey wolves (Canis lupis), and the earliest migrants into the Americas brought multiple domestic dog lineages with them some 12,000 to 14,000 years ago. Canadian Eskimo dogs have been known residents of the Arctic for at least 4000 years (Figure 37.2). First bred by the Thule, they are known by several names: Canadian Husky, Canadian Inuit dog, Canis familiaris borealis, Kingmik, Esquimaux Husky, and Qimmiq, the territorial animal symbol of Nunavut. They have been used by Canadian Inuit as a multi-purpose dog, for hunting seals and other Arctic

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Figure 37.2: Modern Inuit dog team with fan hitch.

Photograph by Nick Newbery (Government of Nunavut) and used with his permission.

game and for hunting polar bears. They play an integral part in the annual Inuit routine, in summer as pack animals and in winter as teams pulling sleds. Their fur was prized for its resistance to wear and in times of famine, the dogs were used as an emergency food source (Bogoras, 1904). Archaeological sites in the Arctic have uncovered dog remains, sled parts, and different accessory items of equipment from eastern Arctic Thule sites (Morey & Aaris-Sorensen, 2002). Going back 1000 years to the beginning of Thule culture, dog remains have been recovered at nearly every Thule archaeological site from Siberia to Greenland, many of these site remains being associated with dog sled traction (Brown et  al., 2013). Dog remains have also been found at three Early Paleo-Inuit sites in West Greenland representing the Saqqaq culture, the Greenlandic variant of the Arctic Small Tool Tradition (Morey & Aaris-Sorensen, 2002). This stands in sharp contrast to the almost complete absence of dog

remains from the Dorset and Canadian Pre-Dorset cultures. Dogs only became important in Arctic life after sledding became a means of transport seasonally for the movement of peoples and their materials over long distances. Who then first harnessed dogs to the sled for transport? Historical records of the use of sled dogs in the Siberian subarctic appear in the tenth century and in the writings of Marco Polo in the thirteenth century and Francesco de Kollo in the sixteenth century (Swanny, 2008). The Siberian Birnirk people did use sleds of the same basic design as those later used with dog teams. Bogoras (1904) describes the different dog types, types of sleds, and the different harnesses used by Eastern and Western Siberian Chukchi people. Sleds and sled dog teams have often been used by polar explorers and expeditions (Barr, 2009); they are used today by the Inuit but to a lesser extent, with dogs often now replaced by snowmobiles.

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What are the origins of the Qimmiq or Inuit Husky sled dog? Did Inuit develop a breed for transportation using dogs and wolves? Several archaeological sites in Alaska have yielded dog remains from cultures such as the Ipiutak and Old Bering Sea, and Brown et al. (2013) suggest that, at the end of the Birnirk phase at Barrow in Alaska, a larger, sturdier breed of dog was introduced into Arctic America from Siberia. The study by Brown et al. (2013) analysed mitochondrial DNA from dog bone and teeth samples to determine the genetic continuity of ancient and modern dogs from the North American Arctic. The sampled areas included Cape Espenberg in Alaska and Inglefield Land in Greenland. Inglefield Land is thought to be the main entry point for the prehistoric Indigenous populations of Greenland who originated in Alaska and made their way across the Canadian Arctic. Comparing 20 archaeological (about 1250–1910 CE) and 3 surface-collected recent (about 1910–1930 CE) Canis bone and teeth samples with 51 modern Inuit Sled Dogs to determine evidence of either gene replacement or continuity over time, a common haplotype A31 was found in the ancient samples and modern samples from Greenland. It is thought that the remoteness and isolation of Greenland contributed to the preservation of indigenous dogs’ gene pool in the eastern Arctic, with this haplotype serving as a common thread tying the archaeological and modern eastern Arctic breed dogs together (Brown et al., 2013). Additionally, haplotype A31 was found to be present in archaeological samples from both Alaska and Greenland, indicating geographical continuity across the North American Arctic, in addition to the temporal continuity in the eastern Arctic. This result is also important in the context of human migrations. The language spoken from northern Alaska to Arctic Canada and Greenland is part of the Inuktitut language (Brown et al., 2013). Members of the Fifth Thule Expedition of 1920 found that their Greenlandic language could be understood all the way to northwestern Alaska (McGhee, 2005). Linguistic, archaeological and genetic evidence in the form of a common genetic signature across time and space among North American arctic dogs altogether could be used as proxy for the Thule migration in the region. Recently, Brown et al. (2015) have used autosomal, mitochondrial, and Y chromosome markers to test the hypothesis that Inuit dogs retained their indigenous ancestry. Over most of North America, post-colonial dogs have largely erased the genetic signatures of prehistoric dogs. It was hypothesized and hoped that the North American arctic dogs had retained their genetic makeup as they were

thought to have descended from Inuit dogs from Canada and Greenland associated with Thule peoples about 750 years ago (Brown, 2015). The results supported the theory of indigenous ancestry of Inuit dogs. Also, the results indicated that there was no detectable genomic differentiation between Inuit dogs from Canada and Greenland and that they were distinct from Siberian Huskies, Alaskan Huskies, and Malamutes.

Inuit Rabies History Rabies, differently called crazy fox disease, Polar madness, Eskimo dog disease, arctic dog disease, and dikovanic or dikusha in Russian (Kuzmin, 2008), has been reported from Arctic Canada since the nineteenth century as a disease of arctic mammals. These reports are either oral or part of polar explorers’ expedition reports. Though Inuit were threatened by the disease of their dogs, there are few reports to indicate that Inuit suffered from the disease (Bogoras, 1904; Freuchen, 1935). All these reports are relatively recent, after the nineteenth century, with no indication as to whether rabies existed before that time. The following sections will deal with some of the reports of rabies disease in dogs.

Inuit Stories Four sources of Inuit association with rabies can be found: (1) the Canadian Broadcasting Corporation (CBC) translation of interviews conducted with Inuit; (2) an article by Hugh Whitney; (3) a survey by Charles Elton completed in 1931; and (4) accounts by several polar explorers. Unfortunately, these accounts only extend back to 1845. CBC INTERVIEWS

1. Peter Nerke Airo comes from Kangirsuk, a community in northern Nunavik. His story: “Sometimes dogs became rabid, and the dogs which became rabid had to be killed because there is not case for rabies. Dogs which became rabid have a habit of fighting with other dogs, so they had to be killed. Peter and Sammy had a total of four dogs left and they had to borrow someone else’s dogs to travel to hunt caribou” (CBC, 2002–2009). 2. Paulossie Shauk comes from Kuujjuarapik, a community near the mouth of the Great Whale River. His story: “Sometimes dogs became rabid in the past, but he has not heard of any dog getting rabies recently” (CBC, 1990).

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people, particularly in the Northern Greenland area, where many of the expeditions began because it had a good source of dogs. Following the disappearance of John Franklin’s expedition aboard the Erebus and Terror in 1845, several expeditions went in search of Franklin and his crews (Barr, 2009). It would seem that in most of the expeditions, both men and dogs were starving, going as far as to feed the dogs old moccasins, torn gloves, or a piece of buffalo robe with hair on it so that the men could keep the pemmican. Barr (2009), writing of McClintock as commander of the Intrepid during the journey of Dr Scott to the pole in 1852–1854, describes one of the dogs as having “fits,” running away, and not returning. Later, aboard the Fox in 1859, he describes some of his dogs as having “fits,” falling down, and then running away not to return. In his memoirs Journey of Pullen aboard the North Star, Captain Pullen describes several dogs as having “fits” and suggests that the dogs he obtained from Godhaven (now Qeqertarsuag on the south end of Disco Island off Greenland) were more susceptible to disease. While none of the writers give details of the dogs’ disease, it would seem that they were suffering from rabies. It is interesting to note that Flemming (1875) received a communication from the Danish government about the dogs at Disco, and in his reply to other explorers, he warns of obtaining dogs from Northern Greenland as he feared that this expedition, like all previous ones to Smith’s Sound, would lose many of its dog teams to this “mysterious malady.” Dr I. I. Hayes on board the schooner United States knew of the problems with dogs from South Greenland and went to great lengths to move his dogs away from the DanishEsquimau settlements from where he obtained them to prevent any contact with infection (Hayes, 1867). Heavy losses were described in dogs from Whale Sound from what was thought to be distemper. During his voyage one dog came down with a disease and was shot. A few hours later a second dog began to act strangely, running around the boat, barking, having fits, and finally succumbing to the disease. Hayes carried out a post-mortem and assumed that the disease could not be rabies since the dog had an affinity for water and not a dislike, but he remarked that it had all the symptoms of rabies. He lost 18 dogs in the first two weeks of December and three more in another week. To continue his endeavour he sought animals from the north end of Greenland. Winter had set in, so he decided to wait until the end of the year before deciding on a course of action. Bogoras (1904) described what he called a peculiar Arctic form of rabies occurring most often in the spring, usually associated with long sled drives on the open tundra, which,

HUGH WHITNEY

These stories are contained in “Rabies in Labrador” (Whitney, 1992). 1. Mrs. Bella Lyall from Nain remembers back in 1948– 1950 rabid red foxes were so common in Nutak (Okak Island) that children were kept inside to prevent them from being bitten. Many dogs became ill and had to be shot. Nutak was a bad area for rabies, which cycled every three to four years. She recalls the summer of 1919 when a young boy from Hebron was bitten by a local dog, eventually became ill, and died, probably from rabies. Her uncle had to kill a lot of dogs that year because of rabies. 2. Mrs. Susie Andersen of Makkovik remembers travelling back to Makkovik from Mary’s Harbour in January of 1934 when their sled team was attacked by a young dog. As it persisted in its attack, the driver shot it. Back in 1920, when she was living in Flower’s Bay, a small dog attacked the window of their cabin. It was weak in the hind end and dragging itself around. It was shot on suspicion of rabies. 3. Mr. Jim Andersen recalls the spring of 1941 when all the dogs along the coast were dying. Many were frothing and vicious. 4. Mr. Leonard McNeill, living at Island Harbour between 1943 and 1945 often had to travel to Hopedale for supplies. Stories were told of many dogs, from Hebron to Port Hope Simpson, becoming sick and dying, often frothing at the mouth, turning nasty, running around, and biting at everything. CHARLES ELTON

Two articles by Charles Elton contain references to rabies in dogs and foxes. The first describes his meeting with W. O. Douglas of the Hudson Bay Company while in London. He suggests that the disease in dogs came from the foxes, was cyclical and was disrupting the fur trade (Elton, 1942). This led to Elton’s survey questionnaire in 1925 to determine the extent of the epidemics in the sled dogs of the Baffin Island, Hudson Strait, and Hudson Bay areas (Elton, 1931). While some of the stories go back to the 1890s there is confusion in some instances about whether some of the dog deaths were due to distemper.

Polar Explorers Several authors describe rabies in dogs during their polar explorations, which in some cases delayed the expeditions and created a void in available sled dogs for the Arctic

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according to the natives, resulted from excessive exposure of the brain to the sun. No one was reported to have died from the bite of a rabid dog, though they did when bitten by a wolf. A rabid dog biting a teammate caused that dog to go mad. On a long journey, the drivers would muzzle the rabid dog and continue to drive it for several days. On short journeys the affected dog was shot. Bogoras describes a palsy of northern dogs, affecting their walking, which can also kill the dog in 24 hours. Arctic rabies has only generally been reported in the last 160 years. Its origins before then are open to speculation, and its probable source is discussed in the next sections.

interspecies transmission events, referred to as spillovers, do occur sporadically; much more rarely such an event leads to a host shift in which the virus is able to persist and spread within the new host. The most compelling example of such a host shift occurred in Arizona, where the striped skunk has become a reservoir host for a rabies virus variant that circulates sympatrically in big brown bats (Leslie et al., 2006; Kuzmin et al., 2012). The phenomenon of rabies virus host shifts has been studied extensively in bats of the United States, where multiple bat species harbour several distinct viral variants. For this group of viruses, increased opportunity for physical contact between host species (e.g., use of the same roosts and or habitats) correlated with spillover frequency, while cross-species host shifts were impacted by the phylogenetic distance between the donor and receiving species; that is, the greater the evolutionary distance between the two bat species, the less likely a successful host shift could occur (Streicker et al., 2010). Such observations have stimulated discussion of the relative importance of host ecology and viral evolution in the emergence of new viral variants (Mollentze et al., 2014). It has long been assumed that the association of viral variants with particular hosts requires some viral adaptation to allow the virus to replicate to appropriate levels and optimize its chances for transmission to the next individual. As observed in the bat studies, such a strategy could severely limit successful transmission to an alternative host species if there is a large taxonomic divide between the two hosts; the corollary of this is that a virus could be transmitted between genetically related hosts more easily. Viral features that might facilitate such host adaptation have yet to be identified but, despite our lack of understanding of the evolutionary mechanisms at play on the virus during a host shift, phylogenetic studies provide evidence for several instances of such events in the past, particularly between canid species. For example, despite emerging relatively recently, the cosmopolitan rabies virus lineage occurs over an extensive geographical area and in multiple host species (Nadin-Davis & Bingham, 2004), a phenomenon that could only have occurred following several host shifts. Several reports suggest that spillovers in non-flying terrestrial hosts frequently involve spread from dogs to other canid species. The westwards spread of rabies across Europe in the twentieth century was accompanied by host shifts from dogs to both red foxes and raccoon dogs (Bourhy et al., 1999), while emergence of fox rabies in Turkey during 2000–2001 may have evolved following a host shift from dogs (Johnson et  al., 2003); the coyote rabies outbreak in Texas in the late 1980s was due to a canid viral

Arctic Rabies: Evolution and Reservoir Hosts The Importance of the Dog as a Rabies Reservoir Globally Historically the dog has been the animal most closely associated with the disease of rabies around the world; indeed the danger of “mad dogs” was recognized in ancient times (Jackson, 2013). Dogs still play a central role in maintaining most extant rabies virus lineages and are responsible for the vast majority of human rabies exposures in the developing world. However, molecular epidemiological evidence suggests that all these viruses have evolved from a common ancestor within the last 1500 years (Bourhy et al., 2008). Assuming that the anecdotal information is correct, then all current rabies viruses must have emerged as an evolutionary branch of the Lyssavirus genus distinct from the viruses that circulated in ancient times. The prominent role of dogs as rabies hosts suggests that all the rabies viruses presently circulating in non-flying terrestrial hosts emerged from a virus originally associated with domestic dogs. Of course, the close association of dogs with people could obscure the importance of other species as rabies reservoirs. It is well documented that, as dog rabies has been controlled in certain parts of the world, the role of wildlife in maintaining the disease has become far more evident; we need look no further than the situation in North America to observe this phenomenon (Hanlon, 2013). In addition to improving knowledge of the temporal and spatial phylodynamics of rabies outbreaks, current studies seek to use viral sequence data to improve our understanding of viral evolution and the processes that operate to limit cross-species transmission of the disease. There is an increasing body of evidence that while a particular viral strain is usually associated with a particular host species,

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variant (Clark et al., 1994); foxes harbour a subgroup of the viruses associated with dogs in northern Brazil (Bernardi et al., 2005; Carnieli et al., 2009); and many African wildlife species are reservoirs for viruses closely related to canid strains (Sabeta et al., 2003). While these studies all suggest that the direction of transmission was from dog to wild canid, the possibility that transmission events can sometimes happen in the reverse direction cannot be discounted. The role of human activities on rabies spread in many parts of the world has also been significant. Since livestock and companion animals have often accompanied humans engaged in long distance travel and the incubation period of rabies can be many weeks or even months, clearly human-mediated movement of animals provides opportunity for spread of disease to new areas. Indeed, the colonization of new lands by Europeans was a major factor in the spread of the cosmopolitan rabies virus lineage (Nadin-Davis & Bingham, 2004) while anthropogenic factors were identified as playing a significant role in rabies spread in North Africa (Talbi et al., 2010) and to the island nation of Indonesia (Susetya et al., 2008). In this respect the Arctic may not be so different from other parts of the world. As detailed above, there have been changes in the distribution and settlement of human populations inhabiting the Arctic over the last several hundred years, with the arrival of the Thule in North America. Domestic animals, particularly dogs, which are used for transportation and hunting, accompanied these ancestral Inuit populations; canid diseases, including rabies, could thus have been spread during this period. Indeed, Bourhy et al. (2008) suggested a role for human activities in the spread of rabies from Russia to Canada and Greenland.

much broader range across many Asian countries, including the Indian subcontinent, Korea, and parts of the Middle East (Nadin-Davis et al., 2012; see Chapter 29). A number of studies have employed coalescent methods of phylogenetic tree prediction to estimate the mean age of the AL lineage and its Arctic-type descendants; some of these estimates are summarized in Table 37.1. These data indicate that the AL lineage emerged between 200 and 500 years ago while the current arctic branch of this lineage emerged more r­ecently, most likely in the early twentieth century. The evidence from studies of the AL lineage (Kuzmin et al., 2008; Nadin-Davis et al., 2012; Pant et al., 2013) suggests that the evolution of the arctic viral group has involved (1) a host shift from dog to fox and (2) spread from Asia, possibly via Siberia, where the oldest known true arctic strain isolates were recovered, into all circumpolar areas. The emergence of the arctic strain of rabies in the early twentieth century is consistent with the reporting of an outbreak of Arctic rabies in Canada in the late 1940s (Nadin-Davis et al., 2012; see Chapter 29). The current arctic group of viruses comprises four distinct subtypes (A1 to A4). The A1 subtype, collected from Ontario and Quebec only, represents the remnants of the wave of infection that spread into southern Canada from the north in the mid1900s and is generally regarded as the most distinctive and outlying branch of the arctic group (see Chapters 10, 23, and 29). The A2 subtype has circulated extensively, having been recovered from Siberia, Alaska, and western Canada, Table 37.1  Age of the rabies virus AL lineage and the current arctic branch of this lineage.

Evolution of the Arctic Group of Rabies Viruses As the rabies virus propagates and spreads, it is constantly undergoing mutation because of the lack of proofreading capability by its polymerase. This is true of all RNA viruses. Many mutants get lost along the way because of purifying selection, loss of fitness, or chance, while others survive and propagate. Those variants that are successful spread throughout their host population to generate viral lineages; the stochastic processes of genetic drift and population subdivision are the most important factors that have shaped the global phylogeography of all canid rabies viruses including those of the Arctic (Bourhy et al., 2008). The arctic rabies viruses that currently circulate across the northern circumpolar region, including North America, form a distinct branch of the arctic-like (AL) lineage, which has a

Description of Date of dataset of AL TMRCA* – samples AL lineage

Date of TMRCA* – Arctic branch

Reference

212 partial N gene sequences 32 N gene sequences

1826 (1738–1900)

1951 (1929–1967)

Nadin-Davis et al., 2012

1524 (1255–1786)

1921 (1874–1959)

Kuzmin et al., 2008

67 N gene sequences 67 N&G gene sequences 29 Whole genome sequences

1823 (1686–1924) 1729 (1630–1817) 1739 (1669–1807)

1939 (1897–1970) 1925 (1900–1948) 1934 (1918–1949)

Pant et al., 2013 Nadin-Davis, unpublished data Nadin-Davis, unpublished data

*Based on the mean age of each viral group, the year in which the most recent common ancestor (TMRCA) of the group circulated is provided; values in brackets are the 95% highest posterior density values determined from each analysis that indicate the 95% probability range of the date for TMRCA. Source: Susan Nadin-Davis.

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but it has not been observed in Canada since the early 1990s. The A3 subtype is the variant presently circulating over vast regions of the north, including Alaska, Siberia, Greenland, and northern Canada, from where it moves southwards into Labrador and northern Quebec periodically. The A4 subtype has been found only in Alaska, and its distinct geophysical distribution may reflect a major physical barrier shared with the Nenana Complex humans who resided in the Nenana Valley of Central Alaska some 12,000 years ago. Indeed, the emergence of these subtypes suggests that there are some barriers to dispersal of the virus across the northern landscape (see Chapter 30). Factors such as geographical features and habitat that limit host range and density could significantly restrict viral spread and lead to extinctions of specific viral subtypes when transmission chains cannot be maintained. In such an extreme environment as the Arctic, where food sources and animal densities can be highly variable, frequent viral extinction events would be anticipated. On the other hand, the recent extensive dispersal of the A3 subtype does demonstrate that successful variants can be widely dispersed across the polar region. Although the arctic fox is recognized as an important host for arctic rabies, the disease also spreads easily to the red fox. Recent studies have failed to identify any consistent genetic differences in the viruses recovered from both fox species within a restricted geographical region, thus suggesting that interspecies transmission events between arctic and red foxes are common and may contribute to disease maintenance. Other wild canids (e.g., wolves) are occasionally also diagnosed as rabid but their role in disease maintenance is less clear. Dogs are the one domestic species that are reported with rabies relatively frequently. It is not clear if this frequency is a result of their close relationship with people, and hence a higher incidence of testing and reporting, or whether this could be indicative of a maintenance role in the disease.

the question of how Inuit came to be in the Arctic. Hall’s statement was logical as Frobisher had been looking for the passageway to Asia and assumed he was there. It has since been proven that culturally and linguistically, those Inuit people were similar in features and language to the many peoples of Arctic Siberia, Alaska, Canada, and Greenland. Archaeological and DNA evidence shows that the ancestors of present-day Inuit came from Siberia by boat across the Bering Strait and dispersed as far as Greenland less than a thousand years ago (Park, 2014; Raghavan et al., 2014). The Thule lived in large communities (Park, 2014), possessed sled dogs and sleds, and were very mobile, moving their communities from Alaska to Greenland in about 200 or 300 years, although dates in the Arctic are still debated due to uncertainties in radiocarbon dating (Friesen & Arnold, 2008). This movement was also necessitated by their need for sourcing food supplies and iron for their use and facilitated by the lack of any major physical barriers. Genetic evidence supports the view that the Thule were instrumental in the introduction of current sled dog populations across the north from Alaska to Greenland. While the origins of the Inuit have been mostly resolved (Park, 2014; Raghavan et al., 2014) and the lineage of their sled dogs determined (Brown et al., 2013; Brown et al., 2015), the history of rabies in the Arctic remains less clear because of inconsistences between anecdotal and phylogenetic evidence, both of which have their drawbacks.

Historical Origins of Arctic Rabies There are many reports by Basque whalers and European settlers that a disease clinically consistent with rabies was present in the far north as early as the nineteenth century; in addition polar explorers mention the incidence of rabies in dogs, but not foxes, in Greenland in the mid-nineteenth century (Hayes, 1867; Barr, 2009). While these reports appear compelling at this time, no means of confirming the nature of such diseases was available and in some cases confusion with other diseases, such as distemper, is a possibility. Phylogenetic evidence strongly suggests that the arctic group of rabies viruses, which emerged from the AL lineage that has circulated across much of Asia for several hundred years, first spread into Siberia and then into North America and Greenland. All estimates of the age of the most recent common ancestor of Arctic rabies viruses suggest that this group emerged in the nineteenth century, well after the spread of the Thule culture and establishment of human populations across the Arctic. It is assumed that at some

Discussion They bee like to Tartars, with long blacke haire, broad faces, and flatte noses, and tawnie in colour, wearing Seale skinnes, and so doe the women, not different in fashion, but the women are marked in the face with blewe streekes downe the cheeks, and around the eyes. (McGhee, 2005)

The quote by Christopher Hall, a seaman aboard Martin Frobisher’s ship in 1576 (McGhee, 2005), introduces

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point during the emergence of the arctic lineage from the AL lineage, at least one or more host shifts from the dog to fox species occurred, ultimately resulting in the spread of the disease throughout northern fox populations. However, such studies can include only those viral lineages for which samples can be recovered and studied. In some situations rabies outbreaks can die out naturally, without any human intervention, as shown by fox rabies in Quebec (see Chapter 11), so it is possible that rabies was introduced either from Asia or from Europe into the Arctic before the nineteenth century and that such lineages subsequently died out and were replaced with the current arctic lineage. Such a scenario would be consistent with the historical anecdotal evidence describing the presence of rabies in the Arctic before 1900. While animal-to-animal transmission might have been responsible for the spread of the current arctic rabies lineage into North America, Bourhy et al. (2008) found significant evidence to support human-mediated spread of the disease from Russia into Canada and Greenland; trading across the Bering Strait up until the time of the Stalin era could have facilitated movement of rabies-infected animals to North America (Morrison, 1991). In conclusion, while it appears that the current arctic rabies strain was introduced from Asia relatively recently, the existence of previous circumpolar epizootics cannot be ruled out. The role of human activity, and by inference the movement of their domestic animals (i.e., dogs) in this process remains speculative but certainly a possibility.

where their ranges overlap. As a result, the virus could be maintained in the red fox population during periods of low arctic fox population density and then be reintroduced into arctic foxes during periods of population rebound. In this way both fox species might serve a significant maintenance role for the virus. Dogs are of course another potential maintenance host given their important reservoir role in other parts of the world. High levels of dog vaccination against rabies in northern Canada would mitigate this concern, but as detailed in Chapter 34, vaccination rates generally fall below what would provide pack immunity. Persistence of the virus could in part be explained by what Wandeler et  al. (1994) refer to as “oral immunization by cannibalism.” Bogoras (1904) described the use of dogs as food with perhaps the remnants going to the living animals. He also described the muzzling of rabid dogs to fill the complement of the team for the sleds. Freuchen (1935) commented that the people told him that eating the diseased and starving dogs has caused a plague among them. A report by the Royal Canadian Mounted Police in 1951 (see Chapter 14d) on Nunavik describes the feeding of rabid dogs and foxes by the Inuit to their healthy dogs. All these examples could have led to rabies persistence in dog populations in the area. Moreover, all cultures, including the Thule and present-day Inuit, had garbage dumps, which allowed for contact of dogs and wildlife and thus provide an opportunity for ongoing cross-species rabies transmission and viral persistence. Another factor that may impact rabies persistence in extreme environments such as the Arctic is the virulence of the circulating strain. Interestingly, in 1881 Dr Colan, deputy inspector general of hospitals and fleets, and fleet surgeon in the Late Arctic Expedition of 1875–1876 aboard the Alert, commented on rabies and its effect on dogs in different polar expeditions stating that “the disease gradually declined in extent and virulence” (Colan, 1881, p. 325). He noted a difference in the length of the attack of the disease in dogs from the south and north of Greenland. “Is it not possible that the dog disease of the Arctic Regions is but ripening Rabies, which to the southward of 70° north shows itself in the Rabies which causes Hydrophobia? Or is it that Hydrophobia is modified in passing through the bodies of carnivorous animals going north, such as foxes and wolves, and becomes the disease we see in North Greenland? It is worthy to note, that when Rabies first appeared in some countries it was less virulent than after a number of years: if so, might it not now be ripening in Greenland?” (Colan, 1881, p. 325).

Arctic Rabies Maintenance Another controversial issue is the mechanism of rabies persistence in the Arctic. The commonly held belief is that rabies in the Arctic is maintained solely by the arctic fox. Studies of the population genetics of this species have found low levels of differentiation of foxes from across North America, Greenland, and Siberia (Norén et al., 2011), consistent with the high mobility and wide range of this opportunistic carnivore. Such a lifestyle would facilitate extensive spread of diseases such as rabies across much of the arctic fox’s circumpolar range. However, the fact that fox population levels vary dramatically with food source availability has led to suggestions that the arctic fox may not be the sole maintenance host for this virus (A. Wandeler, personal communication, 2015). Red foxes are highly susceptible to rabies virus infection and are frequently infected with the arctic strain; there is strong support for frequent transmission of rabies viruses between red and arctic foxes in areas

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Wandeler et al. (1994) point out that some mutations of rabies virus are sub-lethal while others are highly neurovirulent for specific hosts and lead to a rapid death; if the host is killed too quickly then the virus may lose the opportunity to reach an exit portal and be successfully transmitted to its next victim. It has often been speculated that the lack of human rabies cases in northern regions could be due to limited pathogenicity of the virus, an immunity in the person from previous contacts, or simply a consequence of the heavy clothing worn by the Inuit most of the time (Freuchen, 1935; Bogoras, 1904; Colan, 1881; Kuzmin et al., 2008). While mechanisms by which the rabies virus adapts to its host are poorly understood, we have some understanding of the features of the virus that contribute to its pathogenicity. It has been known for some time that the viral glycoprotein is an important determinant of neurovirulence and pathogenicity as certain amino acid substitutions within this protein significantly impact these properties (Dietzschold et al., 2008). However, many other viral genes, including the L gene and the G-L intergenic region, have an impact on pathogenicity in experimentally infected mice, and it appears that the pathogenicity of a rabies virus

within a host may depend on the complex interactions of many viral products with a variety of host components ­(Dietzschold et al., 2008). Currently, it is unknown whether subtle differences between circulating viral variants significantly alter their virulence in a particular mammalian species, although it is known that some hosts are generally more susceptible to rabies viruses than are others (Wandeler et al., 1994). Given the current global warming trend, changing weather patterns may alter the range and distribution of many mammalian species and impact their role as rabies reservoirs. How this will affect the frequency and extent of the spread of rabies outbreaks southwards remains to be seen but there is real potential for significant change to this phenomenon. Improved knowledge of what role, if any, dogs play in the maintenance of rabies in the Arctic may suggest novel control strategies to mitigate this threat. This chapter has speculated on the role of the dog in its travels as a source of rabies virus infections and its potential role in persistence of rabies in the far north. Hopefully, this discussion will promote further exploration of how rabies persists in the Arctic.

Acknowledgments The authors would like to acknowledge the help and direction provided in writing this important and difficult chapter by the following people: Alex Wandeler, Sue Hamilton, and Sarah Brown.

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PART 9

Contributions to Rabies Management

Overview The chapters in Part 9 bring the book to a close. Since rabies ignores borders and much of Canada’s rabies experience is linked to rabies incidence in the United States, Chapter 38 examines rabies in the United States and discusses the international cooperation that has helped both countries design their rabies management methods and organization. The f­ inal chapter (Chapter 39) describes Canada’s contributions to rabies management, discusses the future of rabies management in Canada, and assesses the e­ xtent to which Canadian contributions have been or can be applied elsewhere.

38 The Role of the US Department of Agriculture (USDA), Wildlife Services in Wildlife Rabies Management Dennis Slate1 and Richard Chipman2 1

2

Science Advisor, National Rabies Management Program, USDA, APHIS, Wildlife Services (Retired), Concord, New Hampshire, United States Rabies Management Coordinator, National Rabies Management Program, USDA, APHIS, Wildlife Services Concord, New Hampshire, United States

Introduction The US Department of Agriculture (USDA) has a long history in rabies prevention and control, including the regulatory oversight for animal vaccines used in rabies control (Animal and Plant Health Inspection Service [APHIS], Veterinary Services, Center for Veterinary Biologics), research, and prevention and control programs (US Department of Agriculture, 1994). Wildlife Services (which had been known as Animal Damage Control until 1 August 1997) also has a long history of involvement in wildlife rabies prevention and control despite program changes in administration between USDA and the US Department of Interior (USDI) (Hawthorne, 2004). Throughout most of that history, which began in 1885, the program had an active role in wildlife rabies prevention and control, especially since 1931, when the program’s primary statutory authority (46 Stat. 1468; 7 USC 426–426b) charged Wildlife Services (WS) with the responsibility of conducting campaigns to suppress rabies to protect domestic animals. Consequently, from its early beginnings until 1939, when WS was transferred from USDA to USDI and became a foundation program for the US Fish and Wildlife Service, and after 1986, when the US Congress transferred the program back to USDA within APHIS (Hawthorne, 2004), WS was responsible for wildlife rabies control in USDA. The focus of this chapter is on the WS role in wildlife rabies prevention and control, particularly over the past 15 years in which WS has assumed a primary role for coordination of oral rabies vaccination (ORV). This chapter will also emphasize raccoon (Procyon lotor) rabies control given

that much of the WS coordination efforts have been directed toward several eastern states committed to the common goal of preventing the spread of raccoon rabies and exploring strategies to begin elimination of this rabies virus variant. While WS has a central federal role in wildlife rabies prevention and control in the United States, accomplishments are a reflection of collaboration, cooperation, and coordination among multiple state health, agriculture, and wildlife agencies; Centers for Disease Control and Prevention (CDC) and other federal agencies; universities; counterparts in Canada and Mexico; the private sector; and others.

Background Rabies prevention and control generates a broad bureaucratic and technical interface in the United States. This interface is shaped by the breadth of the rabies impact on humans, domestic animals, and wildlife. State agencies responsible for public health, animal health, and wildlife management have technical and regulatory roles, as well as public trust niches to responsibly fill in rabies outreach, surveillance, diagnostics, and control. The primary federal entities that collaborate with state partners in rabies education, surveillance, diagnostics, prevention, control, and research are the US Department of Health and Human Services (HHS), CDC, and USDA, APHIS, WS. Universities, practising veterinarians, private sector vaccine producers, organizations such as the Global Alliance for Rabies Control, and others also fill important roles in rabies education, surveillance, vaccine production, and

Contributions to Rabies Management

research. Effective rabies control programs are dependent on collaboration and cooperation among the diverse disciplines represented in agencies and other entities that form this broad interactive interface (Slate et al., 2009).

Collaborating Centre and Reference Laboratory, as well as a World Organisation for Animal Health (OIE) Rabies Reference Laboratory. Suppression of rabies is specifically identified in USDA, APHIS, WS primary authority, the Animal Damage Control Act of 2 March 1931 (46 Stat. 1468; 7 USC 426–426b), as amended, and that authority was expanded to include zoonotic diseases in the Act of December 1987 (101 Stat. 1329– 331, 7 USC 426c) (US Department of Agriculture, 1994). Accordingly, WS has a long history in rabies management, which remains a core program function today. The early involvement of WS was manifested through reduction of rabies reservoir populations as a part of predator control programs to protect livestock, particularly in the western United States. When fox rabies spread to the United States from Canada in the mid-1950s to early 1960s (Tabel et al., 1974; Blancou et al., 1991), tallow baits containing strychnine began to be distributed in large numbers by WS and cooperators in several eastern states in an attempt to control fox rabies (Lewis, 1968). Beginning in the 1970s, WS National Wildlife Research Center (NWRC; formerly the Denver Wildlife Research Center) with funding from the US Agency for International Development developed vampire bat rabies control methods for the topical application of anticoagulants on mist-netted bats (Linhart et al., 1972) and delivery of anticoagulants to feeding vampires through systemic injections in cattle (Thompson et al., 1972). With renewed interest in ORV in the United States in the late 1980s, NWRC conducted bait preference studies for the delivery of oral vaccines (Linhart et  al., 1994). Throughout its history WS has provided technical assistance on ­wildlife rabies issues. Bat exclusion methods and reduction of carnivore attractants near residences represent examples of advice provided to citizens to reduce the risk of exposure to rabies. The Vermont Rabies Hotline (Chipman et al., 1993) represents an active example of technical assistance that was specifically designed to provide timely, accurate one-on-one advice and referrals to concerned citizens as fox rabies spread into Vermont from Canada in 1991 (Brown & Szakacs, 1997) and in anticipation of raccoon rabies entering the state from the south. After two decades, this cooperative state-federal Rabies Hotline continues to provide valuable public service for Vermont citizens who coexist with raccoon and bat rabies (Hall et al., 2011). A commitment to research on the recombinant Vacciniarabies glycoprotein vaccine (V-RG, currently licensed as RABORAL V-RG, Merial Ltd., Athens, GA) at the Wistar Institute in the 1980s (Rupprecht et  al., 1986) provided the necessary foundation to proceed with field safety

Historical Perspective Rabies has changed dramatically in the United States over the past century. Before 1960 and before dog rabies was brought under control, the majority of reported rabies cases were in domestic animals (Held et  al., 1967). After 1960 wildlife (carnivores and bats) emerged as more visible reservoirs for rabies, increasing most dramatically from the late 1970s through the late 1990s as a result of the expanding mid-Atlantic raccoon rabies epizootic (Krebs et al., 1995; Krebs et al., 2002). For more than the past two decades, greater than 90% of reported animal cases occurred in wildlife (predominantly carnivore and bat reservoir species), with raccoons accounting for about one-third or more of annually reported cases since the late 1970s (Blanton et  al., 2010). Human deaths from rabies acquired in the United States had declined from more than 100 in the early 1900s to two or three a year by the 1990s (Centers for Disease Control & Prevention, 2011). The decrease in cases of human rabies is largely a function of successful dog rabies control, public health outreach and education, and timely access to effective ­post-exposure prophylaxis (Held et  al., 1967; Rupprecht et  al., 2006). Technological advances (Baer et al., 1971) have led to the development and use of effective oral vaccines and delivery systems to achieve control in specific wild carnivores at the landscape scale (MacInnes et al., 2001; Fearneyhough et al., 1998; Blancou, 2008; Rosatte et al., 2009a; Wandeler, 2008; Slate et al., 2009). The primary federal responsibility for rabies was transferred from USDA to HHS, CDC (formerly the Communicable Disease Center) in 1960 (Hanlon et  al., 1999) as a function of successful dog rabies control that has resulted in substantial decreases in rabid domestic animals since the early 1950s. Although dog rabies control had been achieved, this shift in responsibilities reflected the continuing need for science-based public health emphasis on prevention of rabies in humans. Because rabies is a nationally reportable disease, CDC assumed the responsibility for collating and reporting annual rabies trends within the United States and its territories. CDC also developed and maintains a strong rabies outreach, research, and technical capacity, and serves as a World Health Organization

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and efficacy trials on Parramore Island, Virginia, in 1990 (Hanlon et al., 1998); near Williamsport, Pennsylvania, in 1991 (Hanlon & Rupprecht, 1998); and Cape May, New Jersey, from 1992 to 1993 (Roscoe et al., 1998). The success of field trials and the continued rapid spread of raccoon rabies in the eastern United States spawned a series of independent ORV projects under experimental permit in the mid-1990s targeting raccoon rabies in the eastern United States (Bigler, 1997; Robbins et al., 1998; Smith et al., 1999; Olson et  al., 2000) and targeting canine rabies that had spilled over into coyotes (Canis latrans) in south Texas from sources in Mexico and a unique variant of grey fox (Urocyon cinereoargenteus) rabies in west Texas (Fearneyhough et al., 1998). The initial raccoon rabies ORV programs were generally limited in scope and designed to address specific questions relating to baiting issues and seroconversion in the target population, but served as critical building blocks that led to the expansion of ORV to the broader landscape level in the United States.

research in tandem with its trained personnel and infrastructure located within states, has a program focus on wildlife management, and has a close working relationship between program operations and research. In 1998 Congress appropriated funds for WS to cooperate with specific states (initially TX, OH, and VT) that had initiated ORV programs. Along with its first federal rabies funding, WS recognized that success in planning, implementing, and coordinating wildlife rabies management nationally would require inter-jurisdictional collaboration among diverse disciplines and authorities. To that end, a National Rabies Management Team was established in early 1999 and remains in place to facilitate coordination of ORV programs across state boundaries targeting specific rabies reservoir species. The National Rabies Management Team is a forum for exchange of rabies management ideas, concepts and information. It also established a framework for an expanding and diverse coalition of state and federal agency experts, as well as university and other expertise that helped marshal public support for strategic use of ORV to prevent raccoon rabies in the eastern United States, canine rabies in coyotes in south Texas, and a unique variant of rabies in grey foxes in west-central Texas from gaining a broader geographic footprint in the United States. From 2000 to 2003, the WS funding base increased substantially, allowing for expansion of ORV to states of strategic value along the Appalachian Ridge (PA, WV, VA, TN, GA, and AL) to prevent raccoon rabies from spreading to the west (Figure 38.1). Portions of western North Carolina were added beginning in 2005, except for the highest elevations of the Appalachian Mountains that support low raccoon abundance and, therefore, represent lower risk of spread. The National Rabies Management Team is composed of nine smaller working groups focused on surveillance, vaccine-baits-biomarkers, rabies management strategies, research prioritization, economics, environmental compliance, and other key topics. The full team or representatives from this team have met annually to provide input on a range of national wildlife rabies management issues since 1999 (Slate et  al., 2008). This collaborative, science-based approach to wildlife rabies management embodies the One Health Initiative (2019), a global strategy recognizing that human and animal health, including wildlife, are inextricably linked. This collaborative approach served as the model for the North American Rabies Management Plan (NARMP; US Department of Agriculture, 2008a), a continental framework for rabies prevention and control collectively developed by

Roles The WS primary roles in rabies management include (1) collaboration initiatives, (2) coordination of integrated rabies management, (3) enhanced surveillance and monitoring, and (4) research. WS currently purchases most of the ORV baits used in the United States and is the lead for field coordination of bait distribution in most states. The ORV program in Texas, which predated WS involvement at the national level in 1997, is the primary exception. Texas Department of State Health Services (TDSHS) is the lead for ORV within the state and continues to purchase baits that are distributed to prevent re-emergence of canine rabies in coyotes within Texas and towards the elimination of a unique variant of rabies in grey foxes (Sidwa et al., 2005). WS is a primary cooperator in Texas and provides baits to complement those acquired by TDSHS, as well as personnel to conduct enhanced rabies surveillance, baiting, and post-ORV sampling to evaluate bait uptake and rabies virus neutralizing antibody (RVNA) sero-prevalence.

Collaboration Initiatives WS was well suited to coordinate wildlife rabies control programs among states when an oral rabies vaccine became available for use in the United States. WS has a history of involvement in rabies management, does

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Figure 38.1: Use of ORV vaccine by state and year to prevent spread of raccoon rabies. NY: WS began collaboration in ORV in 1998. MA: WS began collaboration in ORV in 2001. VA: WS began collaboration in ORV in western Virginia in 2002; in 2000 and 2002, an independent ORV project was conducted in Fairfax County, Virginia. FL and MD: WS began collaboration in ORV in 2003. NJ: WS began collaboration in ORV in 2004. AZ: in 2005–2006, WS collaborated in ORV in skunks in Flagstaff, Arizona; in 2006, an ORV bait handout model was field-tested in feral/free-ranging dogs on Indigenous lands in northeast, Arizona; from 2009 to 2011, ORV was conducted targeting grey foxes in the area surrounding Flagstaff. NM: in 2010 to 2011, WS collaborated in ORV that was extended from west Texas into southeastern New Mexico to buffer against spread of this unique grey fox rabies virus variant into New Mexico. Source: Wildlife Services.

representatives from Canada, Mexico, the United States, and the Navajo Nation. In October 2008 the signing of NARMP by the participating nations formerly extended collaboration in rabies management to the North American continent, with a focus in international border areas. The NARMP identified four areas of emphasis for exchange of information and coordination among nations: communications, surveillance, control, and research. The formalization of this plan has spawned international collaborative initiatives to enhance rabies management. Notable examples include international border studies comparing post-ORV RVNA sero-prevalence from areas baited with ONRAB in Canada and RABORAL V-RG in the United States

(Fehlner-Gardiner et al., 2012; Mainguy et al., 2013), and closer coordination between border states and ­provinces involved in raccoon rabies control. Completion of recent studies evaluating the GnRH immunocontraceptive GonaCon in captive dogs on the Navajo Nation and in Mexico should serve as a link to future studies to determine the potential for integrating GonaCon into parenteral vaccination campaigns to control dog rabies (Bender et al., 2009; Vargas-Pino et al., 2013). Canine rabies spillover from domestic dog sources and viral perpetuation in coyotes (Fearneyhough et al., 1998) highlight rabies transmission impacts along an active dog-wildlife interface and point towards the need for improved dog population management, which potentially may be better achieved

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Role of the USDA in Rabies Management

through the effective integration of immunocontraception into specific rabies management strategies.

resulted in a decreasing trend in ORV baits distributed since 2006. The aftermath of the 2008 economic downturn also contributed to this trend, as some states that formerly purchased ORV baits no longer had the resources to do so. The most notable impact occurred in Ohio, where the Ohio Department of Health purchased most of the baits for use within the state from 1997 to 2008. WS has had to make adjustments in baiting to cover this shortfall because of the strategic importance of ORV in Ohio in preventing the westerly spread of raccoon rabies. The Ontario Ministry of Natural Resources (now the Ontario Ministry of Natural Resources and Forestry (OMNRF)) in Canada, provided substantial resources from 1996 to 2007 for ORV in New York within a 50-kilometre area of the Ontario border (i.e., St Lawrence River Valley and Niagara Frontier). The Ministère de la Santé et des Services sociaux du Québec also provided resources for the

Coordination of Integrated Rabies Management WS typically has committed more than 50% to 60% (~$10 million) of its annual rabies budget for the acquisition of baits, air services, and fuel to establish strategic ORV zones to prevent the spread of raccoon rabies (Plate 29), and to purchase baits to complement those bought by TDSHS for canine and grey fox rabies control. WS peak bait purchases occurred in 2005–2006 at 9.5 million and 9 million baits (increased purchases included access to additional contingency funds for rabies emergencies) as reflected in the trend for baits distributed from 1992 to 2013 (Figure 38.2). Level WS rabies budgets from 2006 to 2013, exacerbated by increasing bait and fuel prices, have

Figure 38.2: ORV bait distribution history in the United States, 1992–2013. Source: Wildlife Services.

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Contributions to Rabies Management

acquisition of ORV baits to be applied in northern Vermont along the Quebec border (Plate 29). The Canadian Food Inspection Agency (CFIA) provided resources in 2003 to initiate ORV in Maine to complement contingency actions in New Brunswick to eliminate raccoon rabies. These ORV programs in the northeastern United States were coordinated by Cornell University, with resources for baits also provided by WS and by New York state and specific counties in the state for use within their respective boundaries. WS was also a primary cooperator with Cornell University and northeastern US states that participated in bait distribution, surveillance, and monitoring activities. Raccoon rabies spread into southern Ontario in 1999 and western New Brunswick in 2000 (see Chapters 10 and 12). The incursion of raccoon rabies into southern Quebec in 2006 led to a shift of Quebec resources formerly used for Vermont to prevent raccoon rabies from spreading north from the United States to control and eliminate raccoon rabies within the province (Canac-Marquis et al., 2007). Through swift implementation of integrated contingency actions in Ontario (Rosatte et  al., 2001; Rosatte et  al., 2009b), New Brunswick (Badcock & Goltz, 2005), and Quebec (Cana-Marquis et al., 2007) – the invasions of raccoon rabies were stopped in Ontario by 2006, in Quebec by 2009, and in New Brunswick by 2002. In 2015 raccoon rabies r­ e-entered Quebec and Ontario. Quebec had a single case. The incursion in Ontario was contained but it is ongoing. New Brunswick had an invasion in 2014 that was controlled by 2017 (see Chapters 10, 11, and 12). After ONRAB (Artemis Technologies, Guelph, Ontario, Canada) became available for field use, it was incorporated into control and elimination strategies with ORV programs beginning in 2006 in Ontario and 2007 in Quebec. New Brunswick also distributed ONRAB in a field trial in 2008 in areas where raccoon rabies had previously been detected and used it again in 2015 to combat the ongoing epizootic. As funds that had been applied in the United States from Canadian provincial and federal sources diminished, WS transitioned to replace Cornell as the lead for coordinating ORV along the Canadian border beginning in 2005–2006. WS adjusted its national priorities to ensure the annual purchase of baits to maintain ORV zones along the New York, Vermont, New Hampshire, and Maine borders with Canada. Despite the challenges associated with diverse reservoirs and rabies virus variants in the United States and its territories (Blanton et al., 2009), there have been notable rabies control and elimination achievements through the application of ORV. The recent elimination of an arctic fox (Vulpes lagopus) variant in red foxes (Vulpes vulpes) from southern

Ontario, Canada, provides an example where successful ORV (Rosatte et al., 2009a) has had a direct benefit in the neighbouring northeastern United States, where this variant has not been reported since 2000 (Krebs et al., 2005). This example also provides a baseline for what may be gained through effective international collaboration as outlined in the NARMP (US Department of Agriculture 2008a). The elimination of a canine rabies variant from Texas and the United States (Blanton et  al., 2007) that originated from sources in Mexico (Velasco-Villa et al., 2008) and became established in the coyote populations in south Texas (Clarke et al., 1994; Fearneyhough et al., 1998; Sidwa et al., 2005) represents another success story. These achievements are the result of phased strategies to compartmentalize and eliminate (Tinline & MacInnes, 2004; MacInnes et al., 2001) or prevent spread to new areas (Slate et al., 2009), followed by campaigns toward elimination (Sidwa et al., 2005). The extensive geographic area occupied by specific rabies variants (Blanton et al., 2010) and the costs of vaccine-baits and delivery (Shwiff et  al., 2008) generally require application of phased ORV strategies to control and eliminate variants from sizable areas in North America. There are other noteworthy rabies management accomplishments in grey foxes (Sidwa et al., 2005) and raccoons (Slate et  al., 2009) in the United States. From May 2009 there had been no cases of a unique variant of rabies in grey foxes in west Texas until a case was reported in a cow in Concho County in 2013. Elimination of this variant from the United States will depend on recent contingency action baiting in 2013 and 2014, enhanced rabies surveillance in Texas and south of the US border, as well as effective management plans to prevent or quickly respond to potential re-emergence in Texas. Coordination of ORV along the leading edge of the distribution of raccoon rabies has prevented its broader geographic spread in the United States (Slate et al., 2009). This accomplishment has not been achieved without contingency actions that often integrate trap-vaccinate-release (TVR) with adaptive ORV baiting (e.g., high bait densities, multiple baitings per year, or the targeting of special areas representing higher risk for spread) strategies (Slate et al., 2009). The results of timely responses to incursions of raccoon variant of the rabies virus into southern Ontario, western New Brunswick, and southern Quebec from the United States underscore the value of preparedness to address emergencies (Rosatte et  al., 2009b; Badcock & Goltz, 2005; Canac-Marquis et al., 2007) that have arisen in spite of attempts in United States to prevent spread with ORV. However, contingency actions with TVR and population

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Role of the USDA in Rabies Management

reduction are labour intensive and expensive in comparison to ORV alone (Rosatte et al., 2001) and are not feasible to sustain over large tracts of land for extended time. Such events underscore the need to better understand the relationship among several factors critical to sound rabies management, such as raccoon population dynamics, the impact of raccoon variant virus spillover into skunks (Mephitis mephitis) (Guerra et  al., 2003), the effectiveness of the oral vaccine bait (Rosatte et  al., 2011), strategies (MacInnes et  al., 2001; Rosatte et  al., 2009a), the value of natural barriers (Root et  al., 2009), translocation (Chipman et  al., 2008), and surveillance (Slate & Rupprecht, 2012). Understanding the dynamics of rabies virus host shifts from bat sources to carnivores (Badrane  & Tordo, 2001) as have recently occurred in Flagstaff, AZ (Leslie et  al., 2006), is relevant both evolutionarily and from a real-time management perspective to prevent emergence of new terrestrial rabies virus variants (Kuzmin et al., 2012). ORV intervention has been in place around Flagstaff since 2009. The ORV goals are to prevent rabies virus host shifts to grey foxes from radiating outward from the Flagstaff focus and becoming established. Lack of seroconversion from ORV in wild skunks in the Flagstaff area (US Department of Agriculture, 2007; US Department of Agriculture, 2008b), as well as in skunks in captivity that were orally fed baits containing RABORAL V-RG (Grosenbaugh et  al., 2007), has required periodic ­integration of TVR to try to suppress rabies spread by skunks (Rupprecht & Slate, 2012). In 2011 WS along with state and federal cooperating agencies, conducted an ONRAB safety and immunogenicity field trial in southern West Virginia (Slate et al., 2014). This represented the first oral rabies vaccine bait field trial in the United States since the Cape May, New Jersey, trial with V-RG in 1992–1994 (Roscoe et al., 1998). If successful, this trial could signal the beginning of a new chapter in ORV in the United States through broader use of a vaccine bait that has performed well against raccoon rabies in Canada (Rosatte et al., 2009a). High bait density with ONRAB also holds promise in controlling rabies in skunks as indicated by the results of narrow flight-line spacing (250 metres) (Rosatte et  al., 2011). This strategy may prove effective in addressing residual foci of an Arctic variant of the rabies virus in skunks that have persisted in southwestern Ontario following successful ORV in red foxes through strategic campaigns with Evelyn-Rokitnicki-Abelseth (ERA) vaccine (Rosatte et  al., 2009a). In the United States, ONRAB similarly offers renewed hope for a vaccine bait that will help address raccoon rabies spillover and perpetuation in skunks.

Enhanced Rabies Surveillance and Monitoring In 2005 WS began to intensify enhanced rabies surveillance near ORV zones and undertake other rabies management activities to complement public health surveillance information to improve rabies management decisions. The presence or absence of specific variants of rabies virus represents the ultimate measure of program success or the need for management intervention. WS also conducts pre and postORV sampling of teeth for the presence of biomarker by age (Johnston et  al., 1987), and sera to evaluate vaccineinduced RVNA sero-prevalence. These represent important indices of program performance, as the likelihood of ORV success is tied in large measure to achieving adequate levels of population immunity (Thulke & Eisinger, 2008). Other activities include population density indexing for target species to guide ORV decisions, such as the potential need to increase bait densities or conduct other activities, such as TVR, to bolster the effects of ORV (Slate et al., 2009). Public health surveillance is typically based on human or domestic animal exposure events brought to the attention of public health officials (Blanton et al., 2007) and as such may have limited real-time value in delineating changes in rabies distribution by virus variant or “hot” rabies foci. Enhanced surveillance is designed to increase the geographic scope and intensity of sampling through the collection of specific high-value samples beyond those normally tested to protect public health. Consequently, enhanced surveillance information provides greater confidence in the spatial-temporal distribution of specific rabies variants for real-time decisions. Moreover, enhanced rabies surveillance takes on an even greater value in program decision making when applied along the leading edge of a unique rabies virus variant where ORV zones have been established, such as the western and northern distribution for raccoon rabies (Plate 29). The sampling protocol for enhanced rabies surveillance includes strange acting animals where no human or domestic animal exposure has been reported, road kills, animals found dead in addition to road kills, animals with injuries or lesions indicative of highly aggressive behaviour, and euthanized animals from focal trapping at sites where rabid animals were recently confirmed. Animals (e.g., terrestrial rabies reservoir species) captured by nuisance wildlife control operators may also be included as enhanced rabies samples, particularly in high-risk areas when they may help delineate rabies distribution where control is contemplated. As such, the increased number of suspect rabid animal samples from enhanced surveillance creates a burden on

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Contributions to Rabies Management

some state rabies laboratories for timely diagnosis. Access to a direct immunohistochemical test (dRIT) developed at CDC (Lembo et al., 2006) has mitigated this sample burden while facilitating timely analysis under an agreed upon protocol among WS, CDC, and participating states. All rabies positive samples are antigenically and genetically typed to rabies virus variant by CDC. From 2005 to 2013, WS submitted 77,174 enhanced rabies surveillance samples; 63,315 were tested through dRIT, resulting in 1172 confirmed rabid animals that would not likely have been available for rabies management decisions through public health surveillance alone (Table 38.1). The value of biomarkers in assessing bait uptake and as a correlate of seroconversion as a result of ORV is well ­ documented (Johnston et al., 1987; Sidwa et al., 2005). In the United States, biomarkers have been most useful in association with coyote and grey fox ORV in Texas, where canine teeth were available from dead coyotes and grey foxes to help assess program effectiveness (Sidwa et  al., 2005). Almost all post-ORV raccoon sampling is through live trapping, where the animal is anaesthetized and released after the collection of biological information and samples. Consequently, extraction of a canine tooth is not an option; therefore, a less intrusive sample of a first or second premolar is collected to determine specific age and if the biomarker is present. Given the lower deposition rates in premolars (Rosatte et al., 2008; Algeo et al., 2013), the biomarker information is of lower value as a correlate of population bait uptake, but in specific instances has proven useful in clarifying RVNA sero-prevalence results for individual animals. WS also continues to collect blood serum to determine raccoon serologic response to ORV. WS assists TDSHS with similar sample collections. RVNA levels (IU ≥ 0.05)1 annually have tended to average about 30% in raccoons (Slate et al., 2009), but are variable among states with some infrequently exceeding 50% (e.g., Alabama, Georgia, Maine, Tennessee, and Virginia). States with higher raccoon RVNA sero-prevalence often indicate samples collected from areas that tend to support lower raccoon abundance. A more comprehensive analysis of several years of population level antibody results is underway that may provide additional insight into dynamics and need for baiting strategy adjustments. While raccoon rabies has not spread appreciably to the west, the need for contingency actions involving TVR and special ORV baiting underscores the need to consider rabies management strategy refinements, such as targeted baiting and pursue field trials that could lead to access to more

Table 38.1  Enhanced rabies surveillance from 2005 to 2013 to support ORV in the United States.

Year

Enhanced surveillance samples

dRIT Tested

Rabid by dRIT

Percent rabid by dRIT

2005 2006 2007 2008 2009 2010 2011 2012 2013  Total

3,788 6,930 9,959 10,999 12,256 9,231 9,492 7,783 6,736 77,174

2,848 6,072 8,136 8,790 10,534 7,294 7,574 6,605 5,462 63,315

59 109 157 142 160 145 141 117 142 1,172

2.1% 1.8% 1.9% 1.6% 1.5% 2.0% 1.9% 1.8% 2.6% 1.9%

Source: compiled from Wildlife Services data.

effective vaccines baits. Post-ORV RVNA ­sero-prevalence in coyotes and grey foxes has generally been above 50% and not infrequently exceeds 70% (Sidwa et  al., 2005), levels at which elimination is achievable based on a contemporaneous assessment of models (Thulke & Eisinger, 2008). Elimination of canine rabies in coyotes through the integration of ORV into conventional dog rabies prevention and control in south Texas provides empirical evidence to validate model predictions. The United States was declared canine rabies free in 2007, but the risk of re-emergence from Mexico persists (Velasco-Villa et al., 2008). Raccoon abundance is also a focus of WS monitoring activities. Raccoon population densities are known to vary considerably over landscapes, ranging from nearly absent to high densities (Riley et  al., 1998; Rosatte et  al., 2010). Often, higher raccoon densities have been reported along urban/suburban-rural interface habitats where anthropogenic food subsidies are common (Hoffman & Gottschang, 1977; Prange et al., 2004) and in association with agriculture such as corn production areas (Beasley et  al., 2007a; Beasley, 2007b). In addition, throughout the predominantly forested Appalachian Mountain chain, the raccoon and raccoon hunting are imbedded in the local culture. Past raccoon population density indexing has been conducted largely based on three course-grained macro-habitat types: urban/suburban, agriculture, and forest. WS has used a conservative approach to index raccoon densities, which is based on unique captures from 50 live traps for 10 consecutive nights where traps were dispersed and frequently moved over 3 km2 sampling areas. WS indexed raccoon density 320 times in 18 states from 1997 to early 2011 (Figure 38.3). Some raccoon indexing has occurred on the same area for multiple years. Index values to date ranged from 0 to 53 raccoons, resulting in

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Role of the USDA in Rabies Management

Figure 38.3: Raccoon population density indexing for macro-habitat types. Source: Wildlife Services.

four coarse-grained density index groupings (0–5, 5.1–15, 15.1–25, and >25.1). Higher raccoon density indices were associated with sites that had greater urban-suburban interface components. Rural forest and agriculture complexes (US Geological Survey, 2014) were sampled most frequently, with indices that most commonly fell in the 5.1 to 15 raccoons/km2 range. Similar densities have been reported from rural habitats in southern Ontario (Rosatte et al., 2010). In spite of its limitations, this approach provided basic target species population information for ORV planning and evaluation, and may be of value in modelling given the volume of spatially-temporally data collected under a consistent protocol. WS continues to explore means

to improve upon this method or find practical alternatives (Beasely et al., 2012).

Research Formal research sponsored or conducted directly by WS is aligned with rabies management goals (US Department of Agriculture, 2008a) and priorities through an established process used by NWRC, Fort Collins, Colorado, and the National Rabies Management Team’s, Research Prioritization Working Group. Most of the formal rabies research in WS is conducted in-house by NWRC scientists within the Rabies Research Project at laboratories and

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Contributions to Rabies Management

captive animal facilities at the NWRC headquarters and at strategic field locations (McLean et  al., 2005). Studies are often conducted in collaboration with WS rabies operations, federal and state agency experts, universities, the private sector (e.g., vaccine companies), or other entities. Economic studies are conducted by economists at NWRC to address a variety of pertinent questions, including b ­ enefits-costs associated with a range of rabies management scenarios (Shwiff et al., 2007; Shwiff et al., 2008; Shwiff et  al., 2009; Shwiff et  al., 2011; Sterner & Smith, 2006; Sterner et  al., 2008; Sterner et  al., 2009). Given the need for a more advanced understanding of the complexities associated with effective wildlife rabies management, research to date has been conducted on a broad array of topics, such as target species movement patterns in relation to landscape or habitat features and rabies spread dynamics, and rabies management (Arjo et al., 2005; Arjo et al., 2008; Atwood et  al., 2011; Berentsen et  al., 2008; Puskas et  al., 2010; Ramey et  al., 2010); landscape genetics of rabies reservoir species (DeYoung et  al., 2009; Johnson et al., 2009; Root et al., 2009); biomarkers (Johnston et al., 2005; Johnston et al., 2006; Fry & Dunbar, 2007; Fry et al., 2010; Algeo et  al., 2013); bait acceptance and enhancements (Jojola et  al., 2004; Robinson et  al., 2004; Jojola et al., 2007); relationship between baiting and target species densities (Blackwell et al., 2004; Ramey et al., 2008; Sattler et  al., 2009); vaccine-induced seroconversion (Knowlton et al., 2001; Root et al., 2008); and rabies and immunocontraceptive vaccines and enhancements (Massei et al., 2010; Bender et al., 2009; Vargas-Pino et al., 2013). Since fall (2011), a significant portion of the field and captive research by NWRC scientists and operations has focused on the evaluation of safety and immunogenicity of ONRAB to help determine the merits of expanded use of this oral rabies vaccine within the United States. Risk modelling for rabies spread and enhancing economic analyses through state-of-the-science modelling represent other key areas of research emphasis. Longer term focus will include bait and rabies management strategy enhancements to more effectively increase vaccineinduced sero-prevalence. Priorities at the continental level under the NARMP include research on the immunocontraceptive vaccine GonaCon (Vargas-Pino et al., 2013) and future research and steps to undertake (e.g., dog fertility studies over several breeding cycles) to determine if this vaccine may be integrated into mass dog rabies vaccination campaigns in Mexico to help achieve canine rabies elimination. Comparative vaccine and rabies management strategy studies continue to

represent important initiatives along the Canada–US border (Fehlner-Gardiner et al., 2012; Mainguy et al., 2013).

Challenges and Future There have been many accomplishments during the period in which WS has been engaged as the federal lead in coordination of ORV in the United States. Perhaps the most important of these was the formation of a strong and diverse coalition dedicated to the common purpose of ensuring effective rabies management. Access to an oral rabies vaccine bait served as both a binding catalyst for the coalition and a tool to attack rapidly spreading wildlife rabies epizootics in the eastern United States and in Texas. Raccoon rabies has not spread appreciably, from 2009 there had been no cases of a unique rabies variant of rabies in grey foxes in Texas until a single case was reported in a cow June 2013, and canine rabies has once again been eliminated from the United States. None of these was possible without ORV, supported by a strong coalition that provided guidance and helped marshal support for programs adequate to meet the challenges exerted by wildlife rabies. While there has been progress toward control and elimination of specific wildlife rabies variants from defined areas in the United States and enhanced collaboration and coordination in rabies research, surveillance and management among North American nations, many technical, biological, economic and other challenges remain. For example, understanding rabies dynamics in skunks, irrespective of source of virus, and managing rabies in skunks presents a strong challenge. Will ONRAB, under practical rabies management strategies, live up to its promise as an effective oral vaccine to address rabies in skunks? Application of state-of-the-science economic modelling to add sophistication in understanding the benefits and costs of rabies management in wildlife is underway at WS, NWRC. Earlier benefit cost studies used to plan ORV in the United States (Kemere et al., 2002) indicated that ORV to prevent the spread of raccoon rabies was worth the undertaking, although ORV is not expected to impact the annual death of one to two humans in the United States from wildlife, which have occurred primarily from bats sources (De Serres et al., 2008). Recent modelling undertaken at the macroeconomic scale using REMI PI+ model (Regional Economic Models, Inc., Amherst, MA) projected a $1.1 billion economic impact in the absence of ORV intervention as r­ accoon rabies gained a much larger geographic footprint in the United States over a 22-year

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Role of the USDA in Rabies Management

horizon (Anderson et  al., 2014). The question remains, however, will the favourable output from new economic analysis, acknowledgment of substantial rabies control accomplishments to date, and a dedicated coalition of

rabies expertise provide a compelling case to continue to rally public support to sustain wildlife rabies management through ever-changing political and economic times to meet rabies prevention and control goals?

Note 1 ≥ 0.05 is used as the threshold index for RVNA activity, while IU ≥ 0.5 represents the point at which full neutralization of rabies virus occurs in the presence of RVNA.

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Vectorborne and Zoonotic Diseases, 9(6), 583–588. https://doi.org/10.1089/vbz.2008.0110 Rosatte R., Donovan, D., Allan, M., Howes, L., Silver, A., Bennett, K., ... Radford, B. (2001). Emergency response to raccoon rabies ­introduction into Ontario. Journal of Wildlife Diseases, 37(2), 265–279. https://doi.org/10.7589/0090-3558-37.2.265 Rosatte, R. C., Allan, M., Bachman, P., Sobey, K., Donovan, D., Davies, J. C., ... Schumacher, C. (2008). Prevalence of tetracycline and rabies virus antibody in raccoons, skunks, and foxes following aerial distribution of V-RG baits to control raccoon rabies in Ontario, Canada. Journal of Wildlife Diseases, 44(4), 946–964. https://doi.org/10.7589/0090-3558-44.4.946 Rosatte, R. C., Donovan, D., Davies, J. C., Allan, M., Bachmann, P., Stevenson, B., ... Lawson, K. (2009a). Aerial distribution of ONRAB baits as a tactic to control rabies in raccoons and striped skunks in Ontario, Canada. 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Journal of Wildlife Diseases, 47(2), 459–465. https://doi.org/10.7589/0090-3558-47.2.459 Roscoe, D. E., Holste, W. C., Sorhage, F. E., Campbell, C., Neizgoda, M., Buchannan, R., ... Rupprecht, C. E. (1998). Efficacy of an oral vaccinia-rabies glycoprotein recombinant vaccine in controlling epidemic raccoon rabies in New Jersey. Journal of Wildlife Diseases, 34(4), 752–763. https://doi.org/ 10.7589/0090-3558-34.4.752

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Role of the USDA in Rabies Management Rupprecht, C. E., Wiktor, T. J., Johnston, D. H., Hamir, A. N., Dietzschold, B., Wunner, W. H., ... Koprowski, H. (1986). Oral ­immunization and protection of raccoons (Procyon lotor) with a vaccinia-rabies glycoprotein recombinant virus vaccine. Proceedings of the National Academy of Science, 83(20), 7947–7950. https://doi.org/10.1073/pnas.83.20.7947 Rupprecht, C. E., Willoughby, R., & Slate, D. (2006). Current and future trends in the prevention, treatment and control of rabies. ­Expert Review of Anti-infective Therapy, 4(6), 1021–1038. https://doi.org/10.1586/14787210.4.6.1021 Rupprecht, C. E., & Slate, D. (2012). Rabies prevention and control: Advances and challenges. In R. G. Dietzgen & I. V. Kuzmin C ­ aister (Eds.), Rhabdoviruses: Molecular taxonomy, evolution, genomics, ecology, host-vector interactions, cytopathology and control (pp. 215–252). Norfolk, England: Academic Press. Sattler, A. C., Krogwold, R. A., Wittum, T. E., Rupprecht, C. E., Algeo, T. P., Slate, D., ... Slemons, R. S. (2009). Influence of oral rabies vaccine bait density on rabies sero-prevalence in wild raccoons. Vaccine, 27(51), 7187–7193. https://doi.org/10.1016/j.vaccine .2009.09.035 Shwiff, S. A., Sterner, R. T., Jay, M. T., Parikh, S., Bellomy, A., Meltzer, M. I., ... Slate, D. (2007). Direct and indirect costs of rabies exposure: A retrospective study in southern California (1998–2002). Journal of Wildlife Diseases, 43(2), 251–257. https://doi.org/10.7589 /0090-3558-43.2.251 Shwiff, S. A., Kirkpatrick, K. N., & Sterner, R. T. (2008). Economic evaluation of an oral rabies vaccination program for control of a ­domestic dog-coyote rabies epizootic: 1995–2006. Journal of the American Veterinary Medical Association, 233(11), 1736–1741. https://doi.org/10.2460/javma.233.11.1736 Shwiff, S. A., Sterner, R. T., Hale, R., Jay, M. T., Sun, B., & Slate, D. (2009). Benefit cost scenarios of potential oral rabies vaccination for skunks in California. Journal of Wildlife Diseases, 45(1), 227–233. https://doi.org/10.7589/0090-3558-45.1.227 Shwiff, S. A., Nunan, C. P., Kirkpatrick, K. N., & Shwiff, S. S. (2011). A retrospective economic analysis of the Ontario red fox oral ­rabies vaccination programme. Zoonoses and Public Health, 58(3), 169–177. https://doi.org/10.1111/j.1863-2378.2010.01335.x Sidwa, T. J., Wilson, P. J., Moore, G. M., Oertli, E. H., Hicks, B., Rohde, R. E., & Johnston, D. H. (2005). Evaluation of oral rabies ­vaccination programs for control of rabies epizootics in coyotes and gray foxes: 1995–2003. Journal of the American Veterinary ­Medical Association, 227(5), 785–792. https://doi.org/10.2460/javma.2005.227.785 Slate D., & Rupprecht, C. (2012). Rabies management in wild meso-carnivores. In E. Miller & M. Fowler (Eds.), Zoo and wild a­ nimal medicine current therapy (pp. 366–375). St. Louis, MO: Elsevier. Retrieved from https://www.ncbi.nlm.nih.gov/pmc/articles /PMC6082093/ Slate, D., Rupprecht, C. E., Donovan, D., Badcock, J., Messier, A., Chipman, R., ... Nelson, K. (2008). Attaining raccoon rabies ­management goals: history and challenges. In B. A. Dodet, R. Fooks, T. Müller, & N. Tordo (Eds.), Developments in Biologicals (­Basel): Vol. 131. Towards the elimination of rabies in Eurasia (pp. 439–447). Berlin, Germany: Karger Publishers. Retrieved from https://www.researchgate.net/publication/51409019_Attaining_raccoon_rabies_management_goals_History_and_challenges Slate, D., Algeo, T. P., Nelson, K. M., Chipman, R. B., Donovan, D., Blanton, J., ... Rupprecht, C. E. (2009). Oral rabies vaccination in North America: opportunities, complexities, and challenges. PLoS Neglected Tropical Diseases, 3(12), e549. https://doi.org/10.1371 /journal.pntd.0000549 Slate, D. R., Chipman, B., Algeo, T. P., Mills, S. A., Nelson, K., Croson, C. K., ... Rupprecht, C. E. (2014). Safety and immunogenicity of Ontario rabies vaccine bait (ONRAB) in the first United States field trial in raccoons (Procyon lotor). Journal Wildlife Disease, 50(3), 582–295. https://doi.org/10.7589/2013-08-207 Smith, K. A., Krogwold, R., Smith, F., Hale, R., Collart, M., & Craig, C. (1999). The Ohio ORV program. In Proceedings of the 10th ­annual rabies in the Americas (p. 91). San Diego, CA: California Association of Public Health Directors. Sterner, R. T., & Smith, G. C. (2006). Modeling wildlife rabies: Transmission, economics, and conservation. Biological Conservation, 131(2), 163–179. https://doi.org/10.1016/j.biocon.2006.05.004 Sterner, R. T., Sun, B., Bourassa, J. B., Hale, R. L., Swiff, S., Jay, M., & Slate, D. (2008). Skunk rabies in California (1992–2003) – Implications for oral rabies vaccination. Journal of Wildlife Diseases, 44(4), 1008–1013. https://doi.org/10.7589/0090-3558-44.4.1008 Sterner, R. T., Meltzer, M. I., Shwiff, S. A., & D. Slate. (2009). Tactics and economics of wildlife oral rabies vaccination, Canada and the United States. Emerging Infectious Diseases, 15(8), 1176–1184. https://doi.org/10.3201/eid1508.081061 Tabel, H., Corner, A. H., Webster, W. A., & Casey, G. A. (1974). History and epizootiology of rabies in Canada. Canadian Veterinary Journal, 15, 217–281. Retrieved from https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1696688/ Thompson, R. D., Mitchell, G. C., & Burns, R. J. (1972). Vampire bat control by systemic treatment of livestock with an anticoagulant. Science, 177(4051), 806–808. https://doi.org/10.1126/science.177.4051.806 Thulke H.-H., & Eisinger, D. (2008). The strength of 70%: revision of a standard threshold of rabies control. In B. A. Dodet, R. Fooks, T. Müller, & N. Tordo (Eds.), Developments in Biologicals (Basel): Vol. 131. Towards the elimination of rabies in Eurasia (pp. 291–298). Berlin, Germany: Karger Publishers. Tinline, R. R., & MacInnes, C. D. (2004). Ecogeographic patterns of rabies in southern Ontario based on time series analysis. Journal of Wildlife Diseases, 40(2), 212–221. https://doi.org/10.7589/0090-3558-40.2.212

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Contributions to Rabies Management US Department of Agriculture. (1994). Animal damage control final environmental impact statement. Washington, DC: Animal and Health Inspection Service. US Department of Agriculture. (2007). Cooperative rabies management program national report: 2007. Retrieved from http://www.aphis .usda.gov/wildlife_damage/oral_rabies/downloads/NationalReport_2007.pdf US Department of Agriculture. (2008a). North American rabies management plan. Retrieved from http://www.aphis.usda.gov/wildlife _damage/oral_rabies/downloads/Final%20NARMP%209-30-2008%20(ENGLISH).pdf US Department of Agriculture. (2008b). Cooperative rabies management program national report: 2007. http://www.aphis.usda.gov /wildlife_damage/oral_rabies/downloads/NationalReport_2008.pdf US Geological Survey. (2014). Landsat. http://landsat.usgs.gov Vargas-Pino, F., Gutiérrez-Cedillo, V., Canales-Vargas, E. J., Gress-Ortega, L. R., Miller, L. A., Rupprecht, C., ... Slate, D. (2013). ­Concomitant administration of GonaCon and rabies vaccine in female dogs (Canis familiaris) in Mexico. Vaccine, 31(40), 4442–4447. https://doi.org/10.1016/j.vaccine.2013.06.061 Velasco-Villa, A., Reeder, S. A., Orciari, L. A., Yager, P. A., Franka, R., Blanton, J., ..., Rupprecht, C. E. (2008). Enzootic rabies e­ limination from dogs and reemergence in wild terrestrial carnivores, United States. Emerging Infectious Diseases, 14(12), 1849–1854. https://doi .org/10.3201/eid1412.080876 Wandeler, A. I. (2008). The rabies situation in Western Europe. In B. A. Dodet, R. Fooks, T. Müller, & N. Tordo (Eds.), Developments in Biologicals (Basel): Vol. 131. Towards the elimination of rabies in Eurasia (pp. 19–25). Berlin, Germany: Karger Publishers.

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39 Assessing Canada’s Contributions to Rabies Management and Control Rowland R. Tinline1 and David J. Gregory2 1

Professor Emeritus, Geography, Queen’s University, Kingston, Ontario, Canada 2 Canadian Food Inspection Agency (Retired), Ottawa, Ontario, Canada

Introduction This book has dealt with the history and science of rabies in Canada through two centuries. Readers were led through a series of events in history detailing the emergence of rabies as a disease in humans, domestic animals, and wildlife; early elements of control of the disease; production of vaccines to treat and control rabies in humans, domestic animals, and wildlife; a gradual introduction of new diagnostics for the disease that positioned Canada to become a world leader in the understanding of the disease and the characterization of its virus; the implementation of a consistent data reporting system under the guidance of one federal regulatory body that provided the tools for successful control of the disease; recognition as a world leader in the control of rabies in wildlife through vaccination; and, with the exception of bats, dramatic reductions in rabies cases in southern Canada in humans, domestic animals, and wildlife over the past 30 years. Canada’s management and control of rabies, outlined in this book, is a success story in several ways: (1) very low numbers of human deaths from rabies; (2) elimination of rabies in domestic animals and control of rabies in terrestrial wildlife populations; (3) relatively low cost methods for control; (4) world leader in human and animal vaccine development; (5) development of innovative delivery systems for vaccinating terrestrial wildlife; (6) a growing understanding of the rabies virus and its interactions with animal populations through research and genetic analysis; and (7) an example of international cooperation in disease control. These achievements, however, have not been

without concerns – concerns that need to be addressed to maintain Canada’s success. This chapter reviews and assesses how well Canada has dealt with rabies and how that experience can foster continued success.

Success Preservation of Human Life From the outset, Canada’s rabies system focused on the preservation of human life and, in this regard, has been very successful. From 1905, when rabies became a reportable disease, to the 2018 there were only been 31 human deaths from rabies in Canada and a majority of those deaths (20) were due to contact with dogs (see Chapter 3b). Furthermore, 18 (90%) of those deaths associated with dogs occurred before mass vaccination of domestic animals began in the late 1950s and 1960s. Between 1970 and 2018 there were eight human deaths from rabies, and six of those deaths were linked to bats. The other two deaths were linked to contact with rabid dogs outside the country (Dominican Republic). Bites from rabid cats and rabid skunks have resulted in the deaths of four people (4/31 = 13%). As several chapters have noted, trends in incidence and control efforts in Canada are interrelated with those of our southern neighbour. Human deaths in the United States from rabies, for example, have also declined from more than 100 annually in the early 1900s to one or two by the 1990s (Centers for Disease Control and Prevention, 2011). By comparison with the situation in Canada and the United States, it is estimated

Contributions to Rabies Management

that rabies, primarily associated with contact with rabid dogs, is responsible for more than 59,000 deaths worldwide per year, with most of those occurring in Africa and Asia (­Centers for Disease Control and Prevention, 2019).

in rabies management are high. In reality, rabies management and control in Canada has been accomplished at a relatively low cost. Although costs of rabies surveillance, prevention, and control have been very difficult to obtain, Chapter 34 examines available data and concludes that the annual cost of rabies management in Canada is about 57 cents per person. Even if those estimates increase to one dollar per year per person, the cost seems very reasonable. Furthermore, the recent control programs have led to a continuing drop in rabies submissions and positive diagnoses. For instance, the submission of specimens to the federal Ottawa Laboratory Fallowfield (OLF) dropped seven-fold between 1989 and 2014 after the implementation of the rabies control program in Ontario in 1989 (see Chapter 10).

Control and Elimination of Rabies in Domestic and Wildlife Populations Before 1950 rabies incidence in domestic animals in Canada was low, sporadic, and primarily associated with dogs (see Chapter 2). Incidence was successfully controlled with quarantine measures. After the invasions of wildlife rabies in the 1950s, incidence in domestic and wildlife rabies increased, and then dramatically declined as aggressive control programs were introduced in various provinces. Since 1989 wildlife vaccine control programs in southern Ontario and Quebec have almost eliminated rabies (arctic fox strain) in foxes, skunks, and raccoons (see Chapters 10 and 11). Eradication programs based on population reduction, domestic animal vaccination, and oral vaccination of wildlife in mainland Newfoundland have controlled incursions of fox rabies from Labrador (see Chapter 13). Vaccine barriers (aerial baiting and trap-vaccinate-release) and point infection control (population reduction) programs have pushed the raccoon strain invasions from the United States back across the southern borders of Ontario, Quebec, and New Brunswick (see Chapters 10, 11, and 12) with the exception of the ongoing invasion of the raccoon rabies strain near Hamilton, Ontario, beginning in December 2015 (see Chapter 10). To date that invasion appears to be contained, but elimination will probably take another two years. This outbreak is unique as it was very probably the result of a long-distance transport (over 500 kilometres) of an infected animal (see Chapter 10). Population reduction, quarantine, and vaccination of domestic animals prevented the southward invasion of the arctic fox strain in coyotes in Alberta in the early 1950s. In 1971 rabies in skunks (skunk strain) appeared in southeastern Alberta along the border with Montana and Saskatchewan. A border population reduction zone targeting skunks was implemented in three counties of southern Alberta, and a five-kilometre radial depopulation zone was established around the location of any rabid skunk. Alberta has been free of skunk rabies since 1994 (see Chapter 7).

Vaccine Development: Human and Animal The Canadian story of rabies vaccine development for ­humans and animals, which spans one hundred years, has a number of firsts, including the recent development of a vaccine (ONRAB, see Chapter 17c) that has higher ­levels of sero-conversion in the field than all other available ­vaccines for the terrestrial mammals associated with rabies in North America (fox, raccoon, skunk). From 1913 into the 1950s, Connaught Laboratories (see Chapter 15) took a pioneering and leadership role in the post-exposure treatment of human rabies incidents by (1) bringing production of the Pasteur vaccine to Canada, and (2) developing a modified Semple vaccine. This first development allowed for human treatment closer to home (previously patients had to travel to New York), and the second, which used inactivated rabies virus and had fewer side effects, allowed physicians to administer treatment rather than requiring patients to go to a central laboratory (see Chapter 15a). In the 1950s research in the United States resulted in a duck embryo based vaccine that, while comparable to the Semple vaccine in efficacy, had fewer side effects and could be used in pre- and post-exposure situations. It was licensed in Canada in 1965, supplied by Eli Lilly Company, and widely used in Canada until 1980 (see Chapter 15a). Connaught remained an important contributor in the development of animal vaccines and, in 1933, produced a modified Semple vaccine for livestock in Trinidad, West Indies. Responding to pressure from the upsurge of wildlife rabies in the late 1940s and the 1950s, Connaught began supplying the federal Department of Agriculture with the Flury chick embryo type live vaccine developed

Low Cost Reports in the press citing the cost of air drops or noting the trauma of a human contact with rabies have left the public with the impression that the overall costs involved

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in the United States. In 1953 Connaught also supplied private veterinarians after the federal Department of Agriculture allowed them to immunize dogs against rabies (see Chapter 15b). Connaught’s major innovations in the development of animal vaccines began with the work of Dr Fenje that lead to the development of a unique virus strain called EvelynRokitnicki-Abelseth (ERA) first available in 1964 (see Chapter 15b). In an attenuated form, it was highly antigenic, suitable for livestock, pets, and wildlife, especially foxes, and it soon became recognized internationally as the best available vaccine for wildlife immunization. In 1968 the Ontario Inter-Ministerial Committee on Rabies (later called the Rabies Advisory Committee or RAC) awarded a grant to Connaught Laboratories to produce a vaccine that was safe and effective orally in foxes and to devise a means of delivering it to the foxes. By the end of the study in 1973, the scientists overseeing this project (Dr J. D. Black and Dr Kenneth F. Lawson) showed that an ERA vaccine contained within an oral bait (see Chapter 17b) produced an immunizing response in foxes. Although this development was promising, the RAC was reluctant to distribute baits containing live virus vaccine such as ERA in the field. Several frustrating years were spent working with inactivated rabies virus only to demonstrate that, although those vaccines produced an immunizing response injected intramuscularly, they were not effective orally. Concurrently, the research team at Connaught showed, in 1982, that a sponge bait with tallow containing commercial ERA (see Chapter 17b) produced a neutralizing rabies antibody in foxes. In 1984 the decision was made to use the attenuated ERA virus, but several challenges had to be addressed first: (1) increasing the titre of the vaccine, (2) improving the bait’s robustness since the sponge bait’s coating was prone to cracking and allowing bacteria to contaminate the vaccine; and (3) devising an appropriate container for the vaccine that allowed automated production and was suitable for air-dropped distribution (see Chapter 19). The result, by 1987, was a higher titre ERA vaccine packaged in the Ontario blister pack, which, over the years, was modified to be smaller and lighter and culminated in the ultralite bait weighing four grams (see Chapters 10, 17, and 19). As Figure 39.1 shows, the ERA vaccine bait was the mainstay of Canada’s control efforts against fox rabies in the 1990s. Although the initial control programs were successful, especially against fox rabies, it was determined that the ERA vaccine was not as efficacious in skunks or

raccoons. As described in Chapter 17a), another promising line of research was the development of a vaccine based on a recombinant of the G rabies gene and adenovirus. The rabies G protein was isolated and “patented” by the Wistar Institute in Philadelphia in 1978 and subsequently licensed for use in Canada. First attempts by Connaught at inserting this gene into Escherichia coli were unsuccessful as were attempts by Dr Campbell at the University of Toronto to insert the gene into canine adenovirus (see Chapter 17a). Dr Campbell took the problem to Drs Prevec and Graham at McMaster University. They inserted the rabies G protein into human adenovirus type 5, which, when administered to mice, produced high rabies antibody titres. Several alterations to this adenovirus construct produced, by 1993, a construct termed HAdRG1.3, which became the master seed of choice and, after years of development and testing, was transferred to Artemis (see Chapter 17c) in 1999. The task was to find a means to produce it commercially and to incorporate it within an oral bait. The result, now known as ONRAB, was very successful in controlling rabies in raccoons and works well in skunks and foxes. It was first used in the field in 2006 in Ontario (Figure 39.1) and subsequently in the campaigns against raccoon rabies in Quebec and New Brunswick. Given the high rate of post baiting rabies-positive antibodies in raccoons (74%) reported by Fehlner-Gardiner et al. (2012), it is reasonable to attribute success of those programs to the effective use of ONRAB. As well, use of ONRAB was effective in controlling the small foci of rabies in skunks in southwestern Ontario that persisted after fox rabies was controlled in that area (Rosatte et  al., 2011) Since 2010 ONRAB has been used exclusively in Canada (Figure 39.1). It is currently undergoing field testing in the United States to allow for its use for rabies control in raccoons and skunks. Between 1999 and 2006, rabies control efforts in Canada had also used RABORAL vaccinia-rabies glycoprotein (V-RG) a recombinant vaccine developed in the United States for use with raccoons. The United States had used this vaccine in its rabies control program since 1995. There was no spillover into other species, and it was believed to be more effective in skunks and raccoons than ERA. Although test results in Ontario in 1998 showed poor results for foxes, 2.8 million baits were used for the control of raccoon rabies in southeastern Ontario starting in 1999, and that program was successful. Field tests comparing V-RG and ONRAB showed the latter as superior in terms of producing rabies-positive antibodies in raccoons (74% versus 30%).

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Figure 39.1: Oral vaccines used in the baits in the oral rabies vaccination (ORV) programs in Canada between 1985 and 2014. The ORV campaign began in 1989 in Ontario, but small test drops were made in that province beginning in 1985. Source: created from OMNRF data.

and 19, is uniquely Canadian. It began with the efforts of a small number of people associated with Connaught who subsequently moved to Langford Laboratories. It was taken to full-scale development and production in 1997 with the transfer and incorporation to Artemis Technologies Inc, co-owned by Andrew Beresford, who had been the viral vaccines production manager at Langford, and Alex Beath, who owned the company that had helped maintain and develop the bait production machinery at Langford. Artemis Technologies is now owned solely by Alex Beath and the story of the company is told in Chapter 17c.

Technologies for the Control of Wildlife Rabies BAITS AND BAIT PRODUCTION

Wildlife rabies control by oral vaccination would not have been possible without a bait that could be mass produced. As previously noted, Canada pioneered the development of the blister pack, culminating in the ultralite bait, a PVC blister coated with an attractant and weighing only four grams yet containing enough vaccine to orally immunize an animal that bit through the blister pack and let the vaccine liquid fill its oral cavity. Over time, bait development has included (1) downsizing the first operational blister pack weighing about 17 grams to maximize payload in the aircraft and to ensure it was suitable for the smaller mouths of skunks, as well as foxes and raccoons; (2) redesigning various industrial packaging machines to allow millions of baits to be produced in several months; (3) deciding on an attractant, sugar-vanilla, that would be attractive to foxes, skunks, and raccoons; (4) designing enrobing technology to ensure that the attractant could not be separated from the blister so that the animal would be encouraged to chew and puncture the blister pack; (5) increasing the titre of the vaccine to improve its effectiveness in small doses; (6) ensuring that the titre would remain high in warm field conditions; and (7) designing a bait that could be handled easily by field staff and the bait distribution machinery in the aircraft. The story of these developments, told in Chapters 10, 17c,

DEVELOPMENT OF TECHNOLOGY FOR AIR-DROPPED BAITS

The development of vaccines and baits has gone hand in hand with the development of technology for delivering those baits by air quickly, accurately, and relatively inexpensively. Indeed, the current cost of air-drop technology (flight time, aircraft cost, air and ground crew, and flight planning) is approximately 10% of the cost of an aerial campaign. Vaccine and bait costs account for the remaining 90%. Early flight technology consisted of a two-seater Cessna aircraft flying about 700 feet above the ground parallel to forest edges. A technician in the rear seat threw baits through a metal chute, guided by the beat of a metronome whose frequency was set to achieve a target bait spacing on the ground given the aircraft’s cruising speed.

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Today, all flights are planned on digital maps and uploaded to a computer (bait controller) on board the aircraft (see Chapter 19) or to a smartphone when helicopters are used for smaller drops in suburban/urban areas. This equipment provides in-flight instruction to the pilot using GPS to ensure the planned flight lines are followed. In the Twin Otter aircraft, the bait controller controls the speed of an attached conveyor belt that directs baits to a chute so that the planned target density is achieved given the ground speed of the aircraft (calculated from GPS coordinates) and the planned flight-line spacing. In the helicopter the navigator does this by adjusting the number of baits used per flight-line. The bait controller on the aircraft also stores the on/off information and a continuous log of the location of dropped baits for feedback and future planning. Under good flying conditions, a Twin Otter can manage about four to five flights per day distributing some 80,000 to 120,000 baits per day and covering upwards of 4000 km2. This technology was exported to the United States as part of the cooperative program in North America and was first used in Texas and New York in 1995. Between 1995 and 2007, when Air Services in Ontario stopped providing aircraft for the US control programs, Twin Otters dropped almost 49 million baits in the US from Maine to Ohio and south along the west side of the Appalachians to Tennessee and to Texas (see Chapter 19). Over 30 million baits were dropped in Canada from 1975 (the first test drops) to 2017. As Chapter 19 describes, the development of this technology rests with the pioneering efforts of individuals in Ontario Ministry of Natural Resources (OMNR), the GIS Lab at Queen’s University, and a series of small Canadian companies that designed, built, and perfected the onboard bait machinery.

International Cooperation Canada has played a significant role in working internationally to develop and transfer knowledge of rabies control technology and methods. Since rabies knows no borders, Canada has actively participated in international forums to foster dissemination of knowledge and technical know-how between countries. A good example is the annual Rabies in the Americas conference (RITA) started in 1990 by key researchers in the United States and Canada to transfer knowledge throughout North and South America, which has evolved into a major event that rotates annually between countries in the Americas. Currently it draws delegates from more than 20 countries from five continents and attracts a variety of health care professionals, program administrators and research scientists from wildlife biology, virology, veterinary medicine, epidemiology, and ecology. Canada has hosted the conference six times since 1991. Another example is the Centre of Expertise for Rabies within the Canadian Food Inspection Agency (CFIA) at OLF, where researchers have been responsible for several significant improvements in rabies testing, virus typing and the next-generation sequencing (NGS) technologies (see Chapter 24d). Those NGS studies play a major role in understanding the evolution of the rabies virus and the ecology of the species involved. This group has maintained official designations from the World Health Organization (as a collaborating centre) and the World Organisation for Animal Health (as a reference centre), which gives it credibility at the international level. The group’s scientists are often consulted by investigators from other countries; they have hosted and trained many researchers from around the world in methods of rabies virus detection and characterization and serological techniques; and they have participated in a number of international initiatives and research projects, which played a significant role in educating personnel from developing countries in methods for rabies detection and control. Finally, the tripartite agreement, the North American Rabies Management Plan (NARMP), between government agencies in Canada, the United States, and Mexico in 2008 illustrates the growing recognition of the need for international cooperation. Recognizing existing cooperative ­initiatives between the member countries especially along the borders, the function of the plan is to further cooperation to ensure that various control initiatives are coordinated and strategies are devised to ensure that rabies management goals within each country are better realized.

Understanding the Rabies Virus Canadian scientists have played a leading role in understanding three major features of the rabies virus and its association with its animal vectors. These include (1) making the association of specific strains of the rabies virus with species (see Chapters 23, 29, and 30); (2) realizing that, in addition to being linked with specific species, virus strains were spatially distributed (see Chapters 10, 29, and 30) and correlated with physiographic patterns; and (3) that viruses have evolved during the last 75 years or more (see Chapters 23, 29, and 37). These findings have informed the development of control programs and led to the development of vaccines and baits appropriate to specific species (see Chapters 15, 17, and 19).

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that favourable topographic features assisted the rapid elimination of rabies in countries like Switzerland. Their data also demonstrated that the smaller the area to be controlled, the faster elimination was achieved. Of the 10 countries reporting, only France and Germany were similar in size to southern Ontario and the majority of the others were comparable to southeastern Ontario (about 30,000 km2). Further, the landscape of many of the countries with smaller control areas (Austria, the Czech Republic, Italy, Slovakia and Switzerland) was dissected or bounded by natural barriers. It is also worthwhile to note that the larger countries of Eastern Europe with significant areas of flat terrain (Poland, Ukraine) have yet to eliminate rabies. Note, too, that neither Canada nor the United States has tried to eliminate endemic skunk rabies in the vast and relatively flat western prairies, although Alberta has demonstrated it is possible to maintain a barrier to prevent rabies in skunks from moving north into the province (see Chapter 7).

Reasons for Success Over the past one hundred years, as noted above, Canada has shown that it is possible to manage rabies outbreaks and significantly reduce human deaths. Comparing the success of wildlife rabies control in Canada with that in the United States and the European Union, Canada has an excellent record in terms of eliminating rabies from wildlife terrestrial species over large areas and in four species. The reasons for this success include the technical developments cited above but also several other important factors: (1) geography, (2) administrative structure, (3) agency cooperation, (4) opportune timing, (5) policy change, (6) habitat change, (7) the availability of funding, and (8) pioneering researchers who have led the research, policy development, and control efforts.

Geography Canada’s major success in terms of wildlife controls lies in the control of rabies from the arctic fox strain in foxes and skunks in southern Ontario, Quebec, the Atlantic provinces, and in the recent campaigns to contain and prevent encroachments of the raccoon rabies strain along the border with the United States from southeastern Ontario, Quebec, and New Brunswick. The control of the arctic fox strain of rabies in southern Ontario was feasible because the Great Lakes and the St Lawrence and Ottawa Rivers acted as barriers to limit intrusions from neighbouring areas (see Chapter 30). The physiography of the area also created internal barriers that limited spread between regions. This meant that control efforts could be concentrated on a region and moved between neighbouring regions as rabies was controlled (see Chapter 10). In Quebec fox rabies was confined primarily to the St Lawrence Lowlands, a region that, without the influx of rabies from Ontario or the north, was probably too small to sustain fox rabies (see Chapter 11). In New Brunswick the presence of river barriers and the barrier effect of the Appalachians between New Brunswick, Quebec, and Maine narrowed the invasion fronts for both fox and raccoon virus strains and limited habitat. Control efforts, therefore, were concentrated in small at-risk areas and were quickly effective. Success in New Brunswick protected the other Maritime provinces (see Chapter 12). In the eastern United States, on the other hand, the north-south alignment of the ridge and valley structure of the Appalachians guided the northward march of raccoon rabies. Freuling et al. (2013) examined the success of ORV campaigns in Europe against fox rabies. Ten of the 19 European countries they studied had eliminated rabies. They noted

Administrative Structure Canada’s rabies control efforts have had two major advantages over those of Europe and the United States. First, until recently, Canada has had one agency, currently known as CFIA, responsible for laboratory and field investigations and sampling and collection activities. For almost 100 years only two to three major federal laboratories have been responsible for diagnosis and, this in turn, has ensured standardized procedures for submitting and testing samples. The highly consistent approach to these tasks has resulted in reliable country-wide data that have been shown to be adequate for most surveillance purposes (see Chapter 2, Part 3, and Chapter 21). Further, the same agency has been responsible for supporting control efforts across the country and helping to coordinate them. The recent European study cited above (Freuling et  al., 2013) noted that problem of having multinational jurisdictions is both the lack of comparable data for research and the increased difficulty in coordinating control activities, especially in border areas. Data in the United States are also highly variable in quality given that data collection and testing is primarily a state or even a county responsibility. Second, with the exception of the Maritime provinces, Canadian provinces are very large and rival the size of the entire rabies control area in Europe. Again this has produced consistent approaches to rabies control over large areas and minimized problems along shared borders. The major concern with size has been in the sparsely populated northern regions, where rabies incidents tend to be

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recorded in or near a few isolated settlements, leaving large tracts for which there is little or no information.

Opportune Timing/Policy Change In many respects the success of the Canadian rabies control programs was a combination of circumstances and developments that came together at the right time and place. For instance, before the 1950s Canada used quarantine methods to curtail outbreaks of rabies, most of which could be traced to dogs. The massive invasion of arctic fox rabies into southern Canada in the 1950s pressured the federal government to alter policy and allow vaccination of domestic animals by private veterinarians (see Chapter 15). Fortuitously, Connaught Laboratories had been working on animal vaccines before this and was able to accommodate the demand. The result was the apparent elimination of “dog” rabies in southern Canada but this was rapidly supplanted by the new invasion of an arctic fox strain of rabies. Far sighted individuals in Canada, the United States, and Europe had come to understand that the only answer to the growing threat of endemic rabies in wildlife was to develop a means to vaccinate terrestrial animals in the wild. Population reduction programs in foxes had failed as the populations quickly rebounded, creating a younger susceptible population that encouraged dispersal and, of course, further spread (see Chapter 26a). Fortunately, many elements were in place that made it possible to develop and implement wildlife vaccination. The magnitude of the wildlife outbreaks in eastern Canada in the 1960s, coupled with the death of four-year-old Donna Featherstone (Chapter 3b, case 34), commanded public attention and pushed governments to provide the necessary funds to develop better vaccines and baits. Advances in virology, a rapidly growing knowledge of the rabies virus molecular structure, and the development of analysis techniques such as polymerase chain reaction (PCR) and improved sequencing technologies were great complements to vaccine development. Concurrent and independent developments in navigation such as Loran-C and GPS, the growth of Geographical Information Systems, accessible and lowcost computing, and programmable logic controllers made the development of aerial baiting systems possible. Equally fortuitous was the cooperation between Ontario and the federal government to bring together scientists from industry, the universities and government agencies. The mix helped ensure that thinking went beyond the traditional boundaries of disciplines and agency structures. A final element in the mix was that wildlife rabies was a growing problem in Canada, the United States, and Europe. Hence, awareness was widespread and enriched the pool of ideas and people working on wildlife control.

Agency Cooperation As noted above, having one central agency dealing with a few large administrative units has helped foster cooperation among the agencies responsible for rabies control in Canada (see Chapter 31). The best example of that cooperation is probably the Rabies Advisory Committee in Ontario, set up to oversee and direct research and development of the successful control program in Ontario that eliminated terrestrial rabies in southern Ontario and kept raccoon rabies out of the province. Wildlife rabies research in Ontario began in the 1960s within the agency currently known as the Ontario Ministry of Natural Resources and Forestry (OMNRF). Although researchers in Canada, the United States, and Europe had discussed the prospect of wildlife rabies control, two scientists in OMNRF, David Johnston and his manager, Charles MacInnes, recognized that the budgetary commitment to develop a rabies control program went well beyond their existing department. MacInnes took the problem to the then deputy minister of OMNRF, Doug Roseborough, who, in turn, discussed this with senior ministry colleagues. The result was a proposal to set up an Inter-Ministerial Committee to look into wildlife rabies control. The mandate of this committee was soon widened and its membership expanded to include members from universities, industry (Connaught at the time), other government agencies, and representatives of what was then Agriculture Canada; it was re-constituted as the RAC. As Chapters 10 and 17 note, RAC, together with the Rabies Research Unit in OMNRF, became the guiding force in the development of the control programs in Ontario and subsequent programs in Quebec, New Brunswick, and some American states. It is worth recalling the words of one of the original members of RAC, Duncan Sinclair, a veterinarian and then dean of Arts and Science at Queen’s University: “If this effort succeeds it will be an excellent example of co-operation at a level seldom seen in Canada” (D. Sinclair, personal communication, October 1980). The multi-agency, multidisciplinary approach adopted by RAC and the multi-agency, multinational cooperation discussed above foreshadows the One Health Initiative currently advocated as a worldwide strategy for expanding cooperation and communication in all aspects of health care for humans, animals, and the environment. This concept argues that the synergism created by this approach will greatly advance knowledge and improve conditions for all species.

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whose ideas have been mentioned throughout the chapters of this book. These innovative persons and their ideas made possible the organizational, scientific, and technological changes that allowed the developments documented throughout this book. We have strived to ensure most of those persons have been identified as authors or have been cited in the discussions, references, and acknowledgments.

Changes in Habitat Although skunk rabies still remains endemic in the prairie provinces of Saskatchewan and Manitoba, incidence levels are low and they have had no desire to try ORV control methods. Chapter 8 argues, for instance, that major changes in the way agriculture is currently practised in western Canada (i.e., consolidation of farms and increasing field size) have reduced the hedge rows and farm buildings that are a habitat for skunks. As well, better buildings with concrete footings and steel roofs have helped eliminate denning sites. The result is a lower population of skunks with correspondingly lower rabies incidence. As a cautionary note, changes in habitat may well have contributed to the invasion of fox rabies in the 1950s. In Ontario, for example, the modernization and mechanization of a­ griculture after the Second World War led to the abandonment of marginal land. This in turn created ideal habitat for small mammals – a combination of open land and r­ eturning scrub brush. Dennis Voigt (personal communication), a biologist with OMNR, has argued that this led to high fox populations in southern Ontario, which made possible the rapid spread of fox rabies across the province. Rutty (see Chapter 15) argues that the northern development during and after the Second World War, particularly by the m ­ ilitary, increased opportunities for contact between a growing working dog population and wild animals infected with rabies. It is possible that increased contact promoted the expansion of rabies in arctic foxes and led to its southward expansion in the late 1940s and early 1950s.

Concerns By the end of 2013, rabies control and management in Canada appeared to have reached what Andrew Grove, the co-founder of Intel Corporation, called “a strategic inflection point” (Grove, 1996, pp. 31–32). Such a point changes the way we think and act, inevitably, for good or bad. On the good side, the demonstrated success of rabies control for terrestrial rabies in southern Ontario and Quebec and stopping the northern advance of raccoon rabies into eastern Canada suggested that Canada had the appropriate technology and administrative structures to continue and expand rabies control within Canada and along its borders. On the downside, there were several underlying concerns. First, success often leads to budget reduction, which, in the long run, affects an organization’s ability to respond to new threats. In Ontario, for example, rabies funding had begun to decline, staff with rabies expertise had retired or were about to retire, hiring was on hold, staff with rabies expertise were being reassigned to other projects, and research budgets were limited. In Quebec the Scientific Committee was struggling with the provincial government for funding to continue the efforts to reduce the risk of raccoon rabies entering from the bordering US states (see Chapter 11). Then, in April 2014 CFIA announced that it was withdrawing from its field activities of investigating rabies reports and collecting specimens across Canada, unless associated with human contact, and would provide only laboratory services and the resulting diagnoses. The collection and follow-up investigation would be carried out by provincial and territorial health agencies. In other words, the comprehensive centralized collection and diagnostic system that we have cited as being a major factor in Canada’s success in rabies management has been broken up. Provinces and territories have been left to design their own collection protocols, determine what samples to submit for testing (based on a risk assessment of human contact), and transport specimens to the CFIA diagnostic labs as necessary. CFIA would only be concerned with specimens that had proven animal rabies contact with humans. All other

Funding The crisis of the large number of outbreaks in various provinces in the latter half of the previous century placed tremendous pressure on government agencies to do something. Extensive press coverage increased this pressure. Press coverage of events, such as the death of Donna Featherstone in Ontario that we’ve discussed, provided ongoing pressure to eliminate the rabies threat and helped convince the Ontario cabinet to provide ongoing funding for rabies research that was overseen by RAC.

Pioneering Persons and Their Accomplishments Over the years, many Canadians have been involved in rabies management and control, and many could rightfully be termed pioneers. Canada’s success in rabies management and control owes a lot to these pioneering individuals,

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specimens would be tested outside CFIA laboratories, but positively tested samples with human contact were required to be submitted to CFIA for confirmation (see Chapters 24c and 29). Our colleagues in the United States who deal with a decentralized state system of laboratories, collection, and diagnosis have decried that system (C. D. MacInnes, personal communication, 2015). Furthermore, CFIA’s withdrawal from a central role left a potentially large hole in the cooperative structure that had been part of Canada’s past success. The withdrawal also placed an additional burden on Canada’s five veterinary colleges to provide students with the appropriate regulatory information. Where there had been one set of regulations there were now additional regulations in each of Canada’s 13 provinces and territories. In sum, at a peak in success, the unwitting strategic direction that seemed to be unfolding was cost cutting, limiting research, and shuffling responsibility onto other agencies. In December 2015 the outbreak of the raccoon strain rabies around Hamilton, Ontario, prompted a major test of Ontario’s readiness to respond. As Chapter 10 documents, that response was impressive. Within a couple of days of the confirmation of the first case, field crews were putting out baits, agencies newly responsible for carrying out CFIA’s previous collection mandate had met to reinforce contingency plans for cooperation, and wildlife surveillance based on direct rapid immunohistochemical test (dRIT) testing was underway. As the large size of the epizootic became apparent, the provincial government allocated $4 million to combat the outbreak, new hiring was done, and as the epizootic progressed into 2016, several new research projects were initiated. It was fortuitous that the Ontario outbreak occurred when institutional memory was fresh and the system was still ready to respond quickly. The outbreak has, however, emphasized some long-term concerns, reinforcing Grove’s “strategic inflection point” observation discussed previously. First, the triggering event was the long-distance transport of a rabid raccoon, an event likely to be repeated in the future. Second, it was clear that the epizootic was well underway by the time the first case was diagnosed. Third, as Chapter 10 has discussed, seroconversion rates measured in the field during this outbreak have been low. At the time of writing, it was not known if the level of vaccination protection in wildlife vectors (raccoons and skunks) was correspondingly low, and, if so, why this is happening. If the vaccination levels are low, the outbreak will be prolonged and more expensive to control. New research initiatives in Ontario are exploring a range of possibilities that could explain this situation and how, if required, to overcome it.

In sum, the Ontario outbreak is a timely reminder that real threats remain and that complacency in surveillance or limitations in research will make future success difficult. It is clear that rabies persists in the Arctic (see Chapter 26a) and continues to make occasional thrusts south as demonstrated in Labrador (see Chapter 13). Raccoon rabies continues to push north against the borders of eastern Canada, and skunk rabies persists in the prairies albeit at low levels. Coupled with the ongoing evolution of the virus, climate change, and changing land use patterns there is little doubt that the risk of terrestrial rabies recurring in southern Canada remains high. A further unknown is what is happening in bat populations and how that might influence rabies in terrestrial populations. For instance, white-nose syndrome is substantially reducing populations of some bat species known to be rabies reservoirs, but climate change could encourage other species, whose range is currently restricted to the United States, to venture further north, and they could bring new rabies strains with them.

Future Directions Despite the concerns noted above, recent aspects of research and program efficiency will, with continued attention, ensure that Canada maintains the ability to diagnose and control rabies in the coming years. Consider, for example, the use of the dRIT, discussed in Chapter 24c. This test provides a relatively low-cost, user-friendly, and rapid means of detecting rabies in a specimen without the necessity of sending specimens to a central testing laboratory for the traditional “gold standard” fluorescent antibody test (FAT). To date, positive test results using dRIT have been confirmed with FAT in terrestrial mammals and, as such, dRIT has become an effective screening tool for early detection of rabies in areas not likely to have submissions via the typical passive surveillance channels. Several provinces, however, have reported variable success using this test with bats, leading to false positives or indeterminate results. Quebec’s extensive experience and research using dRIT, however, seems to have resolved these problems and allowed the test to be a mainstay of that province’s surveillance efforts. On the other hand, the increasing use of dRIT at the provincial level, coupled with the federal government’s retreat from the collection process, leaves open the question of a country-wide and reliable system of rabies reporting and the collection of enough specimens at the central level to detect changes in viral strains and their persistence. Thus

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it remains imperative that some form of agreement develop between the provinces and territories and the federal government to ensure the maintenance of testing standards and the collection of enough samples for further research. Although the overall cost of rabies control has been low and the burden has been shared by government (see Chapter 34), the cost of ORAVAX aerial baiting campaigns in response to a future outbreak may appear to be high, given the relatively high cost of baits (over $1 per bait) and the large number of baits required on the ground. The possibilities are to reduce the cost of the baits or reduce the number being used. As well, baits may be stored at low temperature (−30°C) for longer periods before use. Decreasing bait cost will require a larger market, presumably in the United States. Although the United States has made increasing use of ONRAB, its extensive use will require licensing in the United States (see Chapters 38 and 17c). The other possibilities are to lower bait densities in control areas or be far more selective about where baits are dropped. Chapters 10 and 19 discuss the issue of lower bait density but, aside from acknowledging that the required bait density varies inversely with size of activity range of various species (fox, raccoon, skunk) and directly with the spatial distribution of various competitors for baits, there is no definitive bait density for raccoons and skunks that reaches the target species while minimizing surplus baits. For foxes in Ontario and Quebec, at least, the effective value seems to be 20 baits per km2. For other species, various campaigns have used densities of 75 to 300 baits per km2. A promising approach is to design the baiting campaign with land use patterns and landscape structure in mind. Chapters 10 and 11 describe some efforts to accommodate land use patterns in baiting campaigns. Recent simulation efforts by Rees and colleagues discussed in Chapters 10, 11, and 24 have demonstrated that landscape patterns affect the spread and control of rabies. They argue, therefore, that landscape structure should be included in planning an aerial baiting campaign. While this approach may or may not reduce the number of baits used in the short run, it will ensure a higher chance of success over the long term and, therefore, lower overall cost. Linked to developing more efficient testing and control is the question of why rabies persists in some circumstances and not in others. Chapters 10, 11, and 26a examine how the size of the infected area and meta-population structure of fox populations associated with physiographic barriers have affected the persistence of fox rabies in southern Ontario, Quebec, and the Maritimes. Chapters 26b and

27 discuss mechanisms for the spread and long-term persistence of rabies in the Arctic. Clearly, rabies in the Arctic acts as a reservoir for infection in canids and the potential for future invasions of the virus from the Arctic is large. Couple this potential with changing environments, changing climate, and relatively rapid changes in the virus (see Chapters 29 and 30), and there is greater need for ongoing surveillance and research on rabies in the Arctic. Recent advances in nucleotide sequence analysis of the rabies virus genome have significantly increased our knowledge of the genetic diversity of the rabies virus and related lyssaviruses (see Chapter 29). The potential for these tools to reveal the evolution of rabies viruses in conjunction with vector species and to provide tracking tools for better understanding of the spread of rabies is immense. Susan Nadin-Davis, the author of Chapter 29, points out that, “The relative ease with which RNA viruses can mutate and potentially adapt to new environments means that rabies virus epizootics around the world are never static but are continually changing over time.” She goes on to point out that changes could produce at least four possible scenarios for rabies in Canada’s future: (1) the expansion of rabies into new areas, (2) new virushost associations, (3) new variants of rabies virus, and (4)  changing interactions between species as a result of climate change and, therefore, new patterns of rabies. Clearly Canada needs to emphasize the development of the ­techniques and associated research to examine the genetic heterogeneity of the rabies virus, both in relation to patterns of rabies in Canada and, hopefully, to reveal novel strategies to cope with future change. In sum, we suggest that the best direction for Canada is (1) to ensure that rabies remains a reportable disease and ensure that the reporting of the disease and collections of specimens remain standardized between provinces and territories; (2) to continue assessing and developing tools for diagnosis and surveillance; (3) to maintain a strong capability for rabies control in terms of maintaining a supply of vaccine and baits and the personnel and equipment necessary to deliver them; (4) to promote bait development and production to reduce costs and to maintain production capability for the future; (5) to encourage research on rabies persistence and spread; (6) to refine current vaccination strategies to improve their effectiveness and efficiency; (7) to continue development of genetic sequencing technology and its application in understanding the evolution and spread of rabies in wildlife populations; and (8) to continue providing educational material on rabies and its control. Furthermore, Canada’s

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cooperation with other countries, particularly the United States (see Chapter 38), will foster development and innovation, help maintain our capacity to control rabies, and, most important, help prevent future invasions of raccoon and skunk rabies. If Canada can maintain these directions, it will be ready for the next rabies challenge and, as it has for the past century, continue to contribute to the global understanding of this disease.

• Two rabid bats were diagnosed in Dufferin County, ­Ontario. The first, on 30 July 2019, resulted in three people being treated as a result of possible bat contact (“3 People Treated,” 2019). The second, on 14 August, bit a woman in her home and resulted in her treatment. The bat was identified as a big brown bat (“Second Guelph Bat,” 2019). • Lindsay Kines (2019), from the Times Colonist, reported on a further two rabid bats found in September at Saanich on Vancouver Island near two elementary schools. One was a yuma bat (Myotis yumamensis) and the other a hoary bat (Lasiurus cinereus) (Erin Fraser, personal communication, 20 September 2019).

Recent Developments While this book was going to press in 2019, several incidents emphasized that, despite Canada’s successes in reducing or eliminating rabies in some domestic and terrestrial wildlife species, rabies in bats is a continuing problem, the threat of spread from the Arctic and the United States into terrestrial populations remains, and the distribution and ecology of the species involved wildlife rabies is changing. Several cases in bats received widespread media coverage across Canada.

It is noteworthy that big brown bats were involved in the incidents in Ontario and New Brunswick. The distribution of this species is changing. Dr James Goltz, manager of Veterinary Laboratory Services, New Brunswick Provincial Veterinary Laboratory, noted that “populations of big brown bats in New Brunswick are increasing … and this species has a tendency to take up residence in human dwellings and other buildings. Big brown bats were formerly rare in New Brunswick but now account for most of the submissions of bats for rabies testing and most of the rabid bats in the province” (personal communication, October 2019). The combination of increasing numbers and overwintering inside buildings increases the chance of human contact with big brown bats. However, populations of communal bats such as the little brown bat, the tricoloured bat, and the northern long-eared bat hibernate in caves have, over the past decade, been drastically reduced by white-nose syndrome, a fungal disease of bats. Hence, these species have much less interaction with people. Rabies does not respect borders. After years of steady decline in rabies incidence in Ontario, raccoon rabies was diagnosed in the Hamilton area of Ontario in December 2015. Subsequent viral testing demonstrated that this outbreak was most likely linked to a vehicular translocation case from southeastern New York State, over 500 kilometres distant (see Chapter 10). Currently, New Brunswick remains on alert as raccoon rabies is enzootic in Aroostook and Washington (Maine Center for Disease Control and Prevention, 2019), the two counties in the state of Maine that border New Brunswick. In late July 2019 a rabid skunk infected with the raccoon variant of rabies was found in St Stephen, New Brunswick, adjacent to the US border. Although control efforts have contained the outbreak in Ontario and reduced incidence, viral typing has demonstrated spillover into skunks and links to bats. As of September 2019, 12 cases of rabies in skunks had been

• In May 2019 a 21-year-old man was bitten by a bat while visiting Tofino, British Columbia (“B.C. Man Dies,” 2019). He did not seek medical advice or treatment. Six weeks later he was admitted to hospital in Victoria and then transferred to St Paul’s Hospital in Vancouver, where he died. Investigation later confirmed that the r­abies was a virus variant associated with the silver-haired bat (­Lasionycteris noctivagans) (S. Nadin-Davis, personal communication, 29 August 2019). This was the ninth human death from rabies in Canada since 1970. Seven of those nine deaths were linked to indigenous bats (see Chapter 27). The two other deaths were linked to dog bites acquired in the Dominican Republic. Since 2000, when virus typing became available, three of the four bat cases were related to a virus variant associated with silver-haired bats. The fourth was related to a virus variant associated with the little brown bat. • On the night of 15 July 2019 in New Brunswick, a child was bitten on his finger in his bedroom as one of the three family cats was chasing the bat around the bedroom (“Four-Year-Old Boy Bitten,” 2019). Subsequent testing at CFIA confirmed the bat was rabid (C. FehlnerGardiner, personal communication, 3 October 2019). Post-exposure prophylaxis was carried out immediately. The bat was a big brown bat.

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reported in Ontario, 11 with raccoon variant virus and the other with a variant associated with big brown bats (BBCAN1). During 2018 there were 22 positive skunks in the province, 5 with fox variant virus, 1 with BBCAN1, and 15 with raccoon-type virus (C. Fehlner-Gardiner, personal communication, 1 October 2019). In 1963, Kenneth Wells, Veterinary Director General for Canada, commented that “we can never hope to stamp out rabies in wildlife” (quoted in Schmidt, 1963). Those prophetic words are a reminder that eradication remains

a dream. Hence, protecting humans from rabies requires ongoing active and passive surveillance, continuing efforts to control rabies in wildlife (for example, during 2019, a total of 1,664,192 ONRAB vaccine baits were distributed in Canada: New Brunswick (341,700), southern Quebec (157,500) and southern Ontario (1,164,992)), research to understand rabies ecology in terrestrial wildlife and bats, rapid respond to outbreaks, and public education via all forms of media to appreciate the inherent dangers of this deadly disease.

References B.C. man dies of rabies after coming into contact with bat. (2019, July 15). CBC News. Retrieved from https://www.cbc.ca/news/canada/ british-columbia/bat-rabies-vancouver-1.5212965 Centers for Disease Control and Prevention. (2019). Take a bite out of rabies! Retrieved from https://www.cdc.gov/features/rabies /index.html Four-year-old boy bitten by rabid bat in Hartland, N.B. (2019, July 20). CBC News. Retrieved from https://www.cbc.ca/news/canada/ new-brunswick/rabies-bat-new-brunswick-1.5219239 Fehlner-Gardiner, C., Rudd, C., Donovan, D., Slate, D., Kempf, L., & Badcock, J. (2012). Comparing ONRABR and RABORAL V-RGR and New Brunswick, Canada and Maine, USA. Journal of Wildlife Diseases, 48(1), 157–167. https://doi.org/10.7589/0090-3558 -48.1.157 Freuling, C. M., Hampson, K., Selhorst, T., Schroder, R., Meslin, F. X., Mettenleiter, T. C., & Muller, T. (2013). The elimination of fox ­rabies from Europe: determinants of success and lessons for the future. Philosophical Transactions of the Royal Society of London, ­Series B, Biological Sciences, 368(1623), 20120142. https://doi.org/10.1098/rstb.2012.0142 Grove, A. (1996). Only the paranoid survive. New York, NY: Doubleday. Kines, L. (2019, September 19). Another bat with rabies found near a Greater Victoria elementary school. Times Colonist. Retrieved from https://www.timescolonist.com/news/local/another-bat-with-rabies-found-near-a-greater-victoria-elementary-school -1.23952290 Maine Center for Disease Control and Prevention. (2019). Maine animal rabies, 2019. Retrieved from https://www.maine.gov/dhhs/ mecdc/public-health-systems/health-and-environmental-testing/rabies/rabies2019.htm Rosatte, R. C., Donovan, D., Davies, J. C., Brown, L., Allan, M., von Zuben, ... Fehlner-Gardiner, C. (2011). High-density baiting with ONRAB® rabies vaccine baits to control arctic-variant rabies in striped skunks in Ontario, Canada. Journal of Wildlife Diseases, 47(2), 459–465. https://doi.org/10.7589/0090-3558-47.2.459 Schmidt, J. (1963, March 12). What they’re saying [Editorial]. Calgary Herald, p. 9. Second Guelph bat tests positive for rabies, says Wellington-Dufferin-Guelph Public Health. (2019, August 14). CBC News. Retrieved from https://www.cbc.ca/news/canada/kitchener-waterloo/fourth-rabid-bat-wellington-dufferin-guelph-1.5246419 3 people treated for rabies exposure in Dufferin County. (2019, July 30). CBC News. Retrieved from https://www.cbc.ca/news/canada/ kitchener-waterloo/3-people-treated-for-rabies-exposure-in-dufferin-county-1.5230441

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