Pediatric Dysphagia: Etiologies, Diagnosis, and Management [1 ed.] 9781597568647, 1597568643

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Pediatric Dysphagia

In summary, the overall aim of this comprehensive text is to provide all pediatric professionals involved in the care of dysphagic patients with a basic understanding of the complexity of this disorder, the anatomic, neurologic, and physiologic components involved in this disorder, an overview of the diverse population of children who suffer with this disorder, and with a wide range of management approaches based on patient needs and capabilities. The authors also address clinical problem solving and decision making, inspiring readers to develop multidisciplinary models of care at their own institutions.

Pediatric Dysphagia Etiologies, Diagnosis, and Management

Etiologies, Diagnosis, and Management

Pediatric Dysphagia is divided into five parts. In Part I, readers are provided with an overview of the embryologic development of aerodigestive structures that relate to swallowing, an introduction to neural organization related to swallowing function and physiologic aspects of swallowing, a synopsis of oral motor development, a discussion of the various etiologic categories of feeding and swallowing disorders, and an overview of genetic disorders associated with feeding and swallowing issues. Part II covers the clinical and instrumental assessment of patients, including the interdisciplinary feeding team infrastructure and function, the roles of individual members of the feeding team, the specific diagnostic tests commonly used in the assessment of feeding and swallowing issues, the classification of neonatal intensive care units, and the assessment and management of feeding and swallowing issues encountered in the neonatal intensive care unit. Part III focuses on the management of pediatric dysphagia, covering a wide range of treatment strategies and interventions for children with various categories of feeding disorders. Part IV includes an introduction to the concept of evidence-based practice and the application of evidence-based strategies in the management of dysphagia. Part V presents a brief overview of the role of ethics in healthcare and ethical considerations in the treatment of dysphagic children.

Willging Miller Cohen

Pediatric Dysphagia: Etiologies, Diagnosis, and Management is a comprehensive professional reference on the topic of pediatric feeding and swallowing disorders. Given that these disorders derive from abnormalities in the function and/or structure of the airway and digestive systems, multiple clinical specialists may be involved in the evaluation and management of affected children at any given point in time. Therefore, this text includes significant contributions from a wide range of experts in pediatric dysphagia, including members of the Interdisciplinary Feeding Team at Cincinnati Children’s Medical Center. These experts present an in-depth description of their roles in the diagnosis and management of dysphagic children, providing the reader with an understanding of why a multidisciplinary model of care is key to the optimization of outcomes.

Jay Paul Willging _ Claire Kane Miller _ Aliza P. Cohen

C

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www.pluralpublishing.com

J.P.W.

J.P.W.

Pediatric Dysphagia Etiologies, Diagnosis, and Management

Pediatric Dysphagia Etiologies, Diagnosis, and Management

Jay Paul Willging, MD Claire Kane Miller, PhD, MHA, CCC-SLP, BCS-S Aliza P. Cohen, MA

5521 Ruffin Road San Diego, CA 92123 e-mail: [email protected] Website: https://www.pluralpublishing.com

Copyright © 2020 by Plural Publishing, Inc. Typeset in 10/12 Garamond Book by Flanagan’s Publishing Services, Inc. Printed in the United States of America by Integrated Books International All rights, including that of translation, reserved. No part of this publication may be reproduced, stored in a retrieval system, or transmitted in any form or by any means, electronic, mechanical, recording, or otherwise, including photocopying, recording, taping, Web distribution, or information storage and retrieval systems without the prior written consent of the publisher. For permission to use material from this text, contact us by Telephone: (866) 758-7251 Fax: (888) 758-7255 e-mail: [email protected] Every attempt has been made to contact the copyright holders for material originally printed in another source. If any have been inadvertently overlooked, the publishers will gladly make the necessary arrangements at the first opportunity. Disclaimer: Please note that ancillary content (such as documents, audio, and video, etc.) may not be included as published in the original print version of this book. Library of Congress Cataloging-in-Publication Data: Names: Willging, Jay Paul, author. | Miller, Claire Kane, author. | Cohen, Aliza P., author. Title: Pediatric dysphagia : etiologies, diagnosis, and management / Jay Paul Willging, Claire Kane Miller, Aliza P. Cohen. Description: San Diego, CA : Plural Publishing, Inc., [2020] | Includes bibliographical references and index. Identifiers: LCCN 2019035306 | ISBN 9781597568647 (paperback) | ISBN 1597568643 (paperback) Subjects: MESH: Deglutition Disorders — etiology | Deglutition Disorders — diagnosis | Deglutition Disorders — therapy | Child Classification: LCC RC815.2 | NLM WI 258 | DDC 616.3/23 — dc23 LC record available at https://lccn.loc.gov/2019035306

Contents Foreword by Robin T. Cotton xi Preface xiii About the Editors xv Acknowledgments xvii Contributors xix

Part I.  Foundations Section 1.  Embryology

1 Embryologic Development of Aerodigestive Structures that

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Relate to Swallowing Claire Kane Miller, Aliza P. Cohen, and Jay Paul Willging

Section 2.  Neural Control of Swallowing

2 Neural Organization Related to Swallowing

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Claire Kane Miller, Lisa N. Kelchner, and Jay Paul Willging



3 Cranial Nerves Associated with Swallowing

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Claire Kane Miller, Lisa N. Kelchner, and Jay Paul Willging



4 Three Phases of Swallowing

49

Claire Kane Miller, Lisa N. Kelchner, and Jay Paul Willging



5 Respiration, Swallowing, and Protective Reflexes

53

Claire Kane Miller, Lisa N. Kelchner, and Jay Paul Willging

Section 3.  Oral Motor Development

6 Oral Motor Development

61

Claire Kane Miller, Aliza P. Cohen, and Jay Paul Willging

Section 4.  Etiologies

7 Syndromes, Sequences, and Associations

83

Claire Kane Miller, Aliza P. Cohen, and Jay Paul Willging



8 Neurologic Etiologies

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Claire Kane Miller, Aliza P. Cohen, and Jay Paul Willging

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vi Pediatric Dysphagia: Etiologies, Diagnosis, and Management



9 Structural Etiologies

105

Claire Kane Miller, Aliza P. Cohen, and Jay Paul Willging

10 Respiratory Conditions

119

Claire Kane Miller, Aliza P. Cohen, and Jay Paul Willging

11 Cardiac Conditions

123

Claire Kane Miller, Aliza P. Cohen, and Jay Paul Willging

12 Functional Disorders of the Esophagus

139

Claire Kane Miller, Aliza P. Cohen, and Jay Paul Willging

13 Functional Disorders of the Gastrointestinal Tract

143

Claire Kane Miller, Aliza P. Cohen, and Jay Paul Willging

14 Sensory Processing Disorders

147

Claire Kane Miller, Jennifer Maybee, Aliza P. Cohen, and Jay Paul Willging

15 Metabolic Disorders

151

Claire Kane Miller, Aliza P. Cohen, and Jay Paul Willging

16 Psychosocial and Behavioral Disorders

155

Claire Kane Miller, Lori Vincent, Aliza P. Cohen, and Jay Paul Willging

Section 5.  Genetics 17 Genetic Syndromes and Disorders and Their Associated Feeding Issues

161

Claire Kane Miller, Aliza P. Cohen, and Jay Paul Willging

Part II.  Clinical and Instrumental Assessment Section 6.  Interdisciplinary Feeding Team 18 Team Infrastructure and Function

199

Claire Kane Miller, Aliza P. Cohen, and Jay Paul Willging

19 Role of the Pediatric Otolaryngologist

203

Jay Paul Willging

20 Role of the Pulmonologist

213

Dan T. Benscoter

21 Role of the Pediatric Gastroenterologist

231

Vincent Mukkada, Aliza P. Cohen, and Jay Paul Willging

22 Role of the Registered Nurse

241

Candace J. Hochstrasser

23 Role of the Nurse Practitioner Candace J. Hochstrasser

243

Contents vii

24 Role of the Registered Dietitian

249

Amy E. Reed

25 Role of the Pediatric Speech-Language Pathologist

259

Claire Kane Miller

26 Role of the Occupational Therapist

265

Elizabeth J. Kirby

27 Role of the Social Worker

271

Sarah M. Weller

28 Case Study Reflecting Interdisciplinary Feeding Team Approach

281

Claire Kane Miller

Section 7.  Oral Motor Feeding Assessment 29 Clinical Oral Motor Feeding Assessment

289

Claire Kane Miller, Aliza P. Cohen, and Jay Paul Willging

Section 8.  Instrumental Assessment 30 The Videofluoroscopic Swallowing Study

329

Claire Kane Miller, Steven J. Kraus, Aliza P. Cohen, and Jay Paul Willging

31 Fiberoptic Evaluation of Swallowing

361

Claire Kane Miller, Aliza P. Cohen, and Jay Paul Willging

32 Adjunctive Diagnostic Testing in the Evaluation of Pediatric Dysphagia

397

Charles M. Myer IV, Claire Kane Miller, Aliza P. Cohen, and Jay Paul Willging

Section 9.  Assessment and Management of Feeding and Swallowing Issues in the Neonatal Intensive Care Unit

33 Classification of Neonatal Intensive Care Units

415

Claire Kane Miller, Alison S. Riley, Brenda K. Thompson, and Ann Clonan

34 Selective Conditions Frequently Seen in the Neonatal Intensive 421 Care Unit Claire Kane Miller, Alison S. Riley, Brenda K. Thompson, and Ann Clonan

35 The Neonate in the Neonatal Intensive Care Unit Environment

435

Claire Kane Miller, Alison S. Riley, Brenda K. Thompson, and Ann Clonan

36 Feeding Assessment of Neonates in the Neonatal Intensive Care Unit

441

Claire Kane Miller, Alison S. Riley, Brenda K. Thompson, and Ann Clonan

37 Therapeutic Interventions in the Neonatal Intensive Care Unit Claire Kane Miller, Alison S. Riley, Brenda K. Thompson, and Ann Clonan

449

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Pediatric Dysphagia: Etiologies, Diagnosis, and Management

Part III.  Management of Pediatric Dysphagia Section 10.  Overview of Treatment Strategies 38 Overview of Treatment Strategies

467

Claire Kane Miller, Aliza P. Cohen, and Jay Paul Willging

39 Management of Feeding Issues in Infants and Children with Craniofacial Anomalies

491

Claire Kane Miller, Aliza P. Cohen, and Jay Paul Willging

40 Management of Dysphagia in Children with Underlying Neurogenic Conditions

519

Claire Kane Miller, Aliza P. Cohen, and Jay Paul Willging

Section 11.  Sensory Processing Disorders 41 Sensory Processing Disorders and Regulatory Issues that Affect Feeding

553

Claire Kane Miller and Jennifer Maybee

42 Interventions for Sensory Processing Disorders

565

Claire Kane Miller and Jennifer Maybee

Section 12.  Behavioral Feeding Disorders and Intervention Strategies 43 Behavioral Feeding Disorders

581

Claire Kane Miller and Lori B. Vincent

44 Behavioral Assessment

587

Claire Kane Miller and Lori B. Vincent

45 Behavioral Feeding Interventions

593

Claire Kane Miller and Lori B. Vincent

Section 13.  Management of Gagging, Retching, and Tube Feeding Issues 46 Management of Gagging, Retching, and Tube Feeding Issues

617

Therese O’Flaherty, Aliza P. Cohen, and Jay Paul Willging

Part IV.  Evidence-Based Practice Section 14.  Evidence-Based Practice and Assessing Outcomes in Pediatric Dysphagia 47 Levels of Evidence Claire Kane Miller

633

Contents ix

48 Components of Evidence-Based Practice

637

Claire Kane Miller

49 Establishing Care Recommendations, Clinical Pathways, and Treatment Protocols

647

Claire Kane Miller

50 Integrating Functional Outcomes in the Dysphagia Treatment Plan

657

Claire Kane Miller

Part V.  Ethics in Pediatric Dysphagia Section 15.  Ethics in Pediatric Dysphagia 51 Ethics in Pediatric Dysphagia

665

Candace Ganz and Claire Kane Miller

Index 685

Foreword It is indeed an honor to write this foreword and to have personally been at the forefront of the conceptual and clinical change that transformed the model of care for children with airway and swallowing issues. The traditional fragmented approach became one in which all involved clinical specialists evaluated the patient and together developed an integrated management plan — an interdisciplinary team approach. The interdisciplinary feeding team at Cincinnati Children’s Hospital Medical Center exemplifies this holistic, cohesive model of care. The team began as a pilot project in 1987, with the mission of optimizing the wellbeing of children with complex feeding and swallowing issues. Since that time, we have become leaders of medical treatment offered in this format. Given the remarkable advancements in medical care that have been made over the past several decades, the number of children with complex syndromes and disorders pre-

senting to medical centers across the nation has dramatically increased. Many of these children experience difficulties with safe oral feeding and require input from clinicians with special expertise in pediatric dysphagia. Our interdisciplinary feeding team, along with other experts in various aspects of patient care, has written a comprehensive and unparalleled text designed to lay the foundation for an understanding of the embryologic, anatomic, neurogenic, cognitive, and behavioral components of dysphagia. They have also familiarized readers with the disorders and syndromes associated with dysphagia, the complexities of clinical decision making, the ethical issues often involved in patient care, and most important, the need to strive for evidence-based approaches to treatment. In sum, they have shared their philosophy for collaborative care, their respect for the knowledge and skills of multiple clinical disciplines, and a willingness to learn from others. Robin T. Cotton, MD, FRCS(C), FACS

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Preface Medical advancements in neonatal and pediatric care over the past several decades have led to the increased survival of infants and children with a wide spectrum of congenital conditions, syndromes, and sequences, many of which are associated with physiologic and anatomic abnormalities that result in feeding and swallowing disorders. Given the complexity of these patients, providing optimal care requires a multidisciplinary approach in which all involved health care professionals must not only assess the patient from the perspective of their own discipline, but must understand and appreciate the input and expertise of other team members. Our book reflects this model of care, including chapters written by members of the Interdisciplinary Feeding Team at Cincinnati Children’s Medical Center. We cover the roles played by our medical subspecialists in otolaryngology, pulmonology, and gastroenterology as well as the roles of the nurse, advanced nurse practitioner, dietitian, speech-language pathologist, occupational therapist, psychologist, and social worker. Our book is divided into five parts. In Part I, we provide readers with an overview of the embryologic development of aerodigestive structures that relate to swallowing, an introduction to key structures involved in the neural control of swallowing, a synopsis of oral motor development, a discussion of the various etiologic categories of

swallowing disorders, and an overview of genetic disorders associated with feeding and swallowing issues. Part II covers the clinical and instrumental assessment of patients, including the interdisciplinary feeding team approach, the specific diagnostic tests commonly used in assessing feeding issues, the classification of neonatal intensive care units, and the assessment and management of feeding and swallowing issues encountered in the neonatal intensive care unit. Part III focuses on the management of pediatric dysphagia, covering a wide range of treatment strategies and interventions for children with various categories of feeding disorders. In Part IV, we present an introduction to the concept of evidence-based medicine, an important component of decision-making in regard to treatment, and a topic that we have emphasized throughout the text. Part V presents a brief overview of the role of ethics in health care and in treating dysphagic children. It is our hope that the information in this text expands the knowledge of clinicians involved in the care of dysphagic patients, assists them in clinical problem solving and decision making, and inspires them to develop multidisciplinary models of care at their own institutions. This approach optimizes the outcomes of an extremely diverse population of complex patients, all of whom present with conditions and accompanying dysphagia. Jay Paul Willging Claire Kane Miller Aliza P. Cohen

xiii

About the Editors Jay Paul Willging, MD, is a Professor of Otolaryngology–Head and Neck Surgery at the University of Cincinnati College of Medicine. He completed his fellowship in pediatric otolaryngology at Cincinnati Children’s Hospital Medical Center (CCHMC) and has been a member of the Division of Pediatric Otolaryngology–Head and Neck Surgery at CCHMC since 1992. He is the Director of the Pediatric Otolaryngology Fellowship Training Program and also the Director of Clinical Operations for the Otolaryngology Division. He has served as the Director of the Interdisciplinary Feeding Team since 1999, and is also an active participant in numerous other multidisciplinary programs, including the Aerodigestive and Esophageal Center, the Craniofacial Anomaly Team, the Fiberoptic Endoscopic Evaluation of Swallowing Safety Clinic, and the Velopharyngeal Insufficiency Clinic. Dr. Willging has numerous peer-reviewed clinical and research publications and has been a longstanding contributor to textbooks on a wide range of otolaryngology topics, particularly feeding and swallowing disorders. Claire Kane Miller, PhD, MHA, CCC-SLP, BCS-S , is the Program Director of the

Aerodigestive Center/Interdisciplinary Feeding Team at Cincinnati Children’s Hospital Medical Center, and holds a clinical and research position in the Division of

Speech-Language Pathology at Cincinnati Children’s. She is a field service associate affiliate professor in the Department of Otolaryngology–Head and Neck Surgery at the University of Cincinnati College of Medicine and is also an assistant affiliate professor in the Department of Communication Sciences and Disorders at the University of Cincinnati. Her research and clinical interests are predominantly in pediatric dysphagia. Throughout her career, she has focused on instrumental swallowing assessment and the clinical management of infants and children with congenital and acquired airway anomalies. She has authored numerous publications and has presented both nationally and internationally on diverse aspects of pediatric dysphagia. Aliza P. Cohen, MA, is a medical and sci-

ence writer who joined the Division of Pediatric Otolaryngology–Head and Neck Surgery at Cincinnati Children's Hospital Medical Center (CCHMC) in 2006. She has worked collaboratively with faculty and fellows in pediatric surgery, pediatric neurology, pediatric pulmonary and sleep medicine, and pediatric otolaryngology. She has coauthored numerous articles and book chapters on a wide array of topics within these disciplines and has dedicated her efforts to mentoring fellows and faculty in the pursuit of excellence in writing.

xv

Acknowledgments We would like to express our gratitude to all of the professionals on the Interdisciplinary Feeding Team at Cincinnati Children’s Hospital Medical Center (CCHMC) who have taken the time to contribute to this text, drawing from both their clinical expertise and their years of experience in diagnosing and caring for a wide array of complex patients with feeding and swallowing issues. We would also like to extend a special thank you to other clinical specialists at our institution and elsewhere who have collaborated with us in this endeavor, as well

as to partners and colleagues at CCHMC who have provided guidance and support over the years. In addition, a wholehearted thank you to Joseph Alward for his invaluable assistance with all of the figures we have included in our text and to Joseph P. Willging for his artistic contributions. Lastly, each of us would like to thank our families for their enduring patience and unwavering support throughout this major project. Without this support, we would not have been able to bring our book to fruition. Jay Paul Willging Claire Kane Miller Aliza P. Cohen

xvii

Contributors Dan T. Benscoter, DO Division of Pulmonary Medicine, Cincinnati Children’s Hospital Medical Center Assistant Professor, University of Cincinnati College of Medicine Cincinnati, Ohio Chapter 20 Ann Clonan, MEd, CCC-SLP Division of Speech-Language Pathology, Cincinnati Children’s Hospital Medical Center Cincinnati, Ohio Chapters 33, 34, 35, 36, and 37 Aliza P. Cohen, MA Medical Writer, Division of Pediatric Otolaryngology–Head and Neck Surgery, Cincinnati Children's Hospital Medical Center Cincinnati, Ohio Chapters 1, 6, 7, 8, 9, 10, 11, 12, 13, 14, 15, 16, 17, 18, 21, 29, 30, 31, 32, 38, 39, 40, 46 Robin T. Cotton, MD, FRCS(C), FACS Director, Aerodigestive and Esophageal Center, Cincinnati Children’s Hospital Medical Center Professor, University of Cincinnati College of Medicine Cincinnati, Ohio Foreword Candace Ganz, EdD, CCC-SLP Director, Division of Speech-Language Pathology, Cincinnati Children’s Hospital Medical Center Affiliate Associate Professor, Department of Communication Sciences and Disorders, University of Cincinnati Cincinnati, Ohio Chapter 51 Candace J. Hochstrasser, MSN, APRN, FNP-BC, IBCLC Division of Gastroenterology, Hepatology, and Nutrition, Cincinnati Children’s Hospital Medical Center Cincinnati, Ohio Chapters 22 and 23 Lisa N. Kelchner, PhD, CCC-SLP, BCS-S Professor Emeritus, University of Cincinnati Department of Communication Sciences and Disorders Cincinnati, Ohio

xix



xx Pediatric Dysphagia: Etiologies, Diagnosis, and Management Chapters 2, 3, 4, and 5 Elizabeth J. Kirby, OTR/L Division of Occupational and Physical Therapy, Cincinnati Children’s Hospital Medical Center Cincinnati, Ohio Chapter 26 Steven J. Kraus, MD, MS Division Chief of Fluoroscopy, Department of Radiology and Medical Imaging, Cincinnati Children’s Hospital Medical Center Associate Professor of Radiology & Pediatrics Affiliated, University of Cincinnati College of Medicine Cincinnati, Ohio Chapter 30 Jennifer Maybee, OTR, MA, CCC-SLP Division of Speech-Language Pathology, Children’s Hospital Colorado Boulder, Colorado Chapters 41 and 42 Claire Kane Miller, PhD, MHA, CCC-SLP, BCS-S Division of Speech-Language Pathology, Cincinnati Children’s Hospital Medical Center Program Director, Aerodigestive and Esophageal Center/Interdisciplinary Feeding Team, Cincinnati Children’s Hospital Medical Center Cincinnati, Ohio Chapters 1, 2, 3, 4, 5. 6, 7, 8, 9, 10, 11, 12, 13, 14, 15, 16, 17, 18, 25, 28, 29, 30, 31, 32, 33, 34, 35, 36, 37, 38, 39, 40, 41, 42, 43, 44, 45, 47, 48, 49, 50, 51 Vincent Mukkada, MD Division of Gastroenterology, Hepatology, and Nutrition, Cincinnati Children’s Hospital Medical Center Associate Professor, University of Cincinnati College of Medicine Cincinnati, Ohio Chapter 21 Charles M. Myer IV, MD Division of Pediatric Otolaryngology–Head and Neck Surgery, Cincinnati Children’s Hospital Medical Center Assistant Professor, University of Cincinnati College of Medicine Cincinnati, Ohio Chapter 32 Therese O’Flaherty, MS, RD, LD, CSP Division of Nutrition Therapy, Cincinnati Children’s Hospital Medical Center Cincinnati, Ohio Chapter 46 Amy E. Reed, MS, RD, CSP, LD Northeast Cincinnati Pediatric Associates

Contributors xxi

Cincinnati, Ohio Chapter 24 Alison S. Riley, MA, CCC-SLP Division of Speech-Language Pathology Cincinnati Children’s Hospital Medical Center Cincinnati, Ohio Chapter 33, 34, 35, 36, and 37 Brenda K. Thompson, MA, CCC-SLP, BCS-S, CNT Division of Speech-Language Pathology, Cincinnati Children’s Hospital Medical Center Cincinnati, Ohio Chapter 33, 34, 35, 36, and 37 Lori B. Vincent, PhD, BCBA-D Division of Developmental and Behavioral Pediatrics, Cincinnati Children’s Hospital Medical Center Cincinnati, Ohio Chapters 43, 44, and 45 Sarah M. Weller, MSW, LISW-S Social Services, Cincinnati Children’s Hospital Medical Center Cincinnati, Ohio Chapter 27 Jay Paul Willging, MD Division of Pediatric Otolaryngology–Head and Neck Surgery, Cincinnati Children’s Hospital Medical Center Medical Director, Interdisciplinary Feeding Team, Cincinnati Children’s Hospital Medical Center Professor, University of Cincinnati College of Medicine Cincinnati, Ohio Chapters 1, 2, 3, 4, 5, 6, 7, 8, 9, 10, 11, 12, 13, 14, 15, 16, 17, 18, 19, 21, 29, 30, 31, 32, 38, 39, 40, 46

Part I

Foundations

Figure I. Branchial apparatus with the first arch defined. Source: Courtesy of Kathleen Sulik, PhD, Department of Cell Biology and Physiology, University of North Carolina at Chapel Hill.

Section

1

Embryology

1 Embryologic Development of Aerodigestive Structures that Relate to Swallowing Claire Kane Miller, Aliza P. Cohen, and Jay Paul Willging

Chapter Outline Overview Prenatal Development Neural Tube Development During the Embryonic Period Pharyngeal Arches The Pharyngeal Apparatus Pharyngeal Clefts Pharyngeal Pouches Congenital Anomalies of the Pharyngeal Pouches and Arches Arteries, Muscles, Bones, and Cartilages Arising from the Pharyngeal Arches Development of the Skull Development of the Face Congenital Malformations of the Facial Skeleton Development of the Palate Cleft Lip and Palate Lip Anomalies Development of the Tongue Congenital Malformations of the Tongue Lingual Thyroid Gland

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6 Pediatric Dysphagia: Etiologies, Diagnosis, and Management

Congenital Malformations of the Oral Cavity Development of the Gastrointestinal Tract Congenital Anomalies of the Gastrointestinal Tract Development of the Respiratory System Congenital Anomalies of the Respiratory System Questions Pertaining to Chapter

Overview Embryology is a branch of science that focuses on the formation, development, structure, and functional activities of embryos. The first 8 weeks of the embryonic period are critical, as it is during this period that major organs and systems begin to form.1 Interruptions or disturbances during this time frame are the catalyst for major congenital anomalies, many of which have a profoundly deleterious effect on the development of the aerodigestive tract, and ultimately adversely affect the normal feeding and swallowing process. The congenital lesions discussed in this chapter stem from abnormal occurrences during development, such as the lack of fusion between two structures, the lack of separation of two structures, the persistence of a structure that normally regresses, the trapping of one tissue within another, or the failure of a vital structure to form.

Prenatal Development The period of prenatal development is subdivided into (1) pre-embryonic development, which begins at fertilization and continues through cleavage (rapid cell division) and implantation of the fertilized egg to the wall of the uterus; (2) embryonic development, which extends from implantation to the end of the eighth developmental week; and (3) fetal development, which begins with the ninth developmental week

and continues until birth. After week 9 of gestation, the embryo is referred to as a fetus, as its basic form has been acquired. The fetal period is characterized by rapid body growth and differentiation of the tissues and organs that have been formed during the embryonic period. Box 1–1 The gestational period is divided into three trimesters, each of which lasts for three months. The first trimester is critical in that formation and development of the embryo (embryogenesis) takes place. Three cell types differentiate in early embryonic development as the embryo undergoes an invagination (formation) process. The process of gastrulation (formation of embryo layers) leads to the development of organs and tissues. The outer germ layer is referred to as ectoderm, which gives rise to the epidermis, oral cavity, inner ear, and eye lens. The middle germ layer is referred to as the mesoderm. Its derivatives include muscle (skeletal, cardiac, smooth), skeleton, the circulatory system, gonads, and the kidneys. The derivatives of the endoderm (inner germ layer) include the digestive and respiratory systems. Box 1–2 Invagination is a process of cellular migration. It is the initial step of gastrulation, which leads to a multilayered organism with three distinct germ cell layers — ectoderm, mesoderm, and endoderm.



1. Embryologic Development of Aerodigestive Structures

Neural Tube Development During the Embryonic Period Prenatal development begins with fertilization of the egg and the formation of a zygote (fertilized ovum), which contains the maternal and paternal chromosomes. The zygote is transported to the uterus by the ciliary action of the fallopian tube. By week  3 of gestation, the central nervous system (CNS) and the cardiovascular system begin to form. The origin of the CNS is the neural plate. This plate gives rise to the neural folds and the beginning of the formation of the neural tube, from which the brain and spinal cord form. As depicted in Figure 1–1, as the neural tube closes cranially (toward the cranium), the spinal cord and the major divisions of the brain develop. These divisions include the prosencephalon (forebrain), the mesencephalon (midbrain), and the rhombencephalon (hindbrain). By the end of week 3, further growth of the neural tube gives rise to the first stages of a recognizable face (frontal nasal process). By the end of week 4, the primary organization of the brain is identifiable. If the neural tube does not develop and close completely during the first 4 weeks of gestation, defects in the brain, spinal vertebrae, and/or spinal cord result. These defects are referred to as neural tube defects, and are the most common severe congenital anomalies of the CNS.2 Neural tube defects may be open to the surface (open neural tube defects) or closed, being covered with skin (closed neural tube defects). Open defects range from a complete opening of the neural tube on the surface of the skull and along the spine to only a localized opening. Open neural tube defects are considered to be the most severe.3 The two most common neural tube defects are anencephaly and spina bifida. In infants with anencephaly, there is normal formation of the spinal cord, but failure of neural tube closure for development of the brain. These infants lack a functional forebrain and cerebellum and typically sur-

Figure 1–1. This is a scanning electron micrograph of the embryo dorsal view, showing the neural tube closing, with open neuropores and the paired somites visible through the thin ectoderm. Features: surface ectoderm, neural tube, cranial (anterior) neuropore, caudal (posterior) neuropore, somites, heart, cut edge of amnion, 24 days, 13 somite pairs. Source: Courtesy of Kathleen Sulik, PhD, Department of Cell Biology and Physiology, University of North Carolina at Chapel Hill.

vive for only a few weeks. In infants with spina bifida, the spine does not grow normally over the spinal cord, causing exposure of the spinal cord and the meninges (Figure 1–2). In patients with meningocele malformations, spinal fluid and meninges (dura mater and arachnoid mater) protrude

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8 Pediatric Dysphagia: Etiologies, Diagnosis, and Management

Figure 1–2. In cases of spina bifida, the neural tube does not close by the end of the first month of pregnancy, leaving a small gap, the spina bifida defect, in the spinal cord. Source: Courtesy of the Midwest Fetal Care Center and Children’s Minnesota.

through an abnormal opening in the vertebral column (Figure 1–3). Myelomeningocele is the most severe form of spina bifida. It is characterized by exposure of the Box 1–3 The meninges are membranes that protect and cover the brain and spinal cord. They are composed of three protective layers: (1) a tough outer layer (dura mater), (2) a delicate middle layer (arachnoid mater), and (3) an inner layer firmly attached to the surface of the brain (pia mater).

fetal spinal cord and the neural elements through the opening in the spine, resulting in complete or partial paralysis of the body below the opening. Children with myelomeningocele are often unable to walk and may have bowel and bladder dysfunction. Closed neural tube defects (NTDs) may be located at either the brain or spinal levels, but are most often confined to the spine. These defects are referred to as spina bifida occulta. The most common presentations of an NTD are an abnormality along the spine such as a tuft of hair growing out of a dimple along the spine, a pigmented nevus (mole), a lumbosacral



1. Embryologic Development of Aerodigestive Structures

Figure 1–3. Types of spina bifida. Source: Courtesy of the Centers for Disease Control and Prevention, National Center on Birth Defects and Developmental Disabilities.

vascular anomaly (hemangioma, port-wine stain), a lipoma (skin doming caused by an underlying mass of fatty tissue), or a dimple in the lumbosacral region.4 Encephaloceles occur when brain tissue protrudes through gaps in the skull secondary to the lack of bone fusion. The portion of the brain that protrudes is covered by skin such that the protrusion is saclike in presentation. The protruding tissue may occur on any part of the skull where bone fusion did not occur (frontal, parietal, occipital, and sphenoidal regions), but most often affects the occipital region of the skull. The effects of an encephalocele vary between individuals, depending upon the size, location (anterior or posterior), and amount of brain tissue protruding from the skull. Large, posteriorly located encephaloceles are likely to be associated with microcephaly, and severely impact neurologic function and survival. Small encephaloceles located toward the front of the skull generally do not contain brain tissue and have a more favorable prognosis.2 A tethered spinal cord occurs as a result of either an open or closed neural tube defect. In this condition, the lower end of the spinal cord is attached to the

skin, which restricts movement and causes stretching of the cord. This restriction and stretching may result in neurologic damage, requiring surgical intervention to release the cord.

Pharyngeal Arches Human embryos have five pairs of pharyngeal arches (numbered in craniocaudal sequence) that give rise to the structures of the face, jaw, ear, and neck (Figure 1–4). These arches are also referred to as branchial arches. These arches surround the foregut (beginning of the digestive tract) of the embryo and are transiently present during days 20 to 35 of embryonic development. The arches are numbered 1, 2, 3, 4, and 6, as arch 5 either forms as a short-lived rudiment or does not form in humans (Figure 1–5).1 The development of the pharyngeal arches is regulated by HOX and other regulatory genes that control development of the embryo. Specific craniofacial defects may arise through the disruption of HOX gene expression as a result of a mutation or in response to a teratogen.1

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Pediatric Dysphagia: Etiologies, Diagnosis, and Management

Figure 1–4. The first (A), second (B), third (C), and fourth (D) arches are visible externally. The sixth arch does not form an external elevation. Source: Courtesy of Kathleen Sulik, PhD, Department of Cell Biology and Physiology, University of North Carolina at Chapel Hill.

The Pharyngeal Apparatus The pharyngeal apparatus consists of the paired pharyngeal arches, pharyngeal pouches, and pharyngeal clefts (grooves). The pouches and clefts separate the arches (Figure 1–6). The intraluminal surface of the pharyngeal apparatus is lined by endoderm. The pharyngeal clefts are located on the external surface of the embryo and are covered by ectoderm. Each pharyngeal arch has identical structures, including an internal pouch covered with endoderm, an external cleft covered with ectoderm, and a core of somatic mesoderm and neural crest mesenchyme

Figure 1–5. The pharyngeal arches numbered, and other structures identified. Source: Courtesy of Kathleen Sulik, PhD, Department of Cell Biology and Physiology, University of North Carolina at Chapel Hill.

between. The somatic mesoderm contributes the artery, vein, and muscle associated with a particular arch (Figure 1–7). The neural crest mesenchyme develops into bone, cartilage, and/or connective tissue in each arch. Each pharyngeal arch also has an associated cranial nerve with afferent and efferent branches that innervate the structures of the arch. The cranial nerve associated with each arch maintains innervation of the musculature associated with that arch (Table 1–1).

Pharyngeal Clefts Pharyngeal cleft 1 develops into the external auditory canal. The corresponding

Figure 1–6.  Pharyngeal arches (A), pouches (P), and clefts (C) are identified in this mouse, approximating human age 29 days. The ectoderm approximates the endoderm, separating cleft from pouch. The arch consists of mesoderm. Source: Courtesy of Kathleen Sulik, PhD, Department of Cell Biology and Physiology, University of North Carolina at Chapel Hill.

Figure 1–7. Structural components of the pharyngeal arch. Source: Courtesy of Loki austanfell. File licensed under Creative Commons https://commons.wikimedia.org/wiki/File:PharyngealArchHuman.jpg.

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Pediatric Dysphagia: Etiologies, Diagnosis, and Management

Table 1–1.  Pharyngeal Arch Derivatives Pharyngeal Arch

Skeletal Structures

Artery

Nerve

Muscles

1

Maxillary artery

Trigeminal (CN V)

Muscles of mastication; mylohyoid, anterior belly of the digastric muscle, tensor tympani, tensor veli palatini

Mandible, maxilla, malleus, incus, zygomatic and temporal bones

2

Stapedial

Facial (CN VII)

Muscles of facial expression, stapedius, stylohyoid, posterior belly of the digastric muscle

Stapes, styloid process, lesser cornu of the hyoid, upper part of the body of the hyoid bone

Common carotid

Glossopharyngeal (CN IX)

Stylopharyngeus

Internal carotid arteries

Hypoglossal (CN XII)

Aortic arch (left)

Vagus (CN X)

Cricothyroid

Right subclavian artery

Superior laryngeal nerve

Pharyngeal plexus

Pulmonary artery (partial left and right)

Vagus (CN X)

Intrinsic muscles of the larynx, striated muscle of the esophagus; pharyngeal plexus

Corticotympanic

3

4

6

Recurrent laryngeal nerve

Laryngeal cartilages: thyroid, cricoid, arytenoid, corniculate, and cuneiform cartilages Laryngeal cartilages: epiglottis, thyroid, cricoid, arytenoid, corniculate, and cuneiform cartilages

Source: Adapted from information in Larsen’s Human Embryology, Schoenwolf, Bleyl, Brauer, FrancisWest, 2015.1

pharyngeal pouch develops into the eustachian tube, and the membrane formed at the contact point between the invaginations of the pouch and the cleft develops into the tympanic membrane. Defects during the development of pharyngeal arch 1 may result in cysts or fistula tracts in the preauricular area or can extend into the neck. Pharyngeal clefts 2, 3, and 4 are engulfed

by the expansion of pharyngeal arch 2. The remnants of these structures may appear as cervical cysts or fistulae.1

Pharyngeal Pouches The pharyngeal pouches that form on the inside of the pharynx between the arches also give rise to structures. Pharyngeal



1. Embryologic Development of Aerodigestive Structures

pouch 1 develops into the eustachian tube and the majority of the middle ear cavity. Pharyngeal pouch 2 forms the crypts (infoldings) of the palatine tonsils, pharyngeal pouch 3 divides into superior and inferior portions that result in the thymus gland and the inferior parathyroid glands, and pharyngeal pouch 4 forms the superior parathyroid glands. Congenital Anomalies of the Pharyngeal Pouches and Arches.  Second pharyngeal

cleft and pouch anomalies are the most commonly seen.5 In that pharyngeal pouch 2 resides in the pharynx, developmental anomalies may present as masses in the oropharynx or as pharyngeal bands that cause obstruction of the upper aerodigestive tract. Fourth pharyngeal pouch anomalies may present as cysts or recurrent abscesses in the neck, generally on the left side. There is often a fistula opening in the left pyriform sinus. First pharyngeal pouch cysts that result from errors in embryogenesis may present in the lateral wall of the nasopharynx. Nasopharyngeal teratomas are solid masses of tissues derived from the embryonic ectoderm, mesoderm, and endoderm. Such teratomas may cause upper airway obstruction.

Arteries, Muscles, Bones, and Cartilages Arising from the Pharyngeal Arches Each of the pharyngeal arches is associated with specific arteries, muscles, and bones or cartilage (see Table 1–1). The maxillary and mandibular prominences of pharyngeal arch 1 develop into the maxilla and mandible. The derivatives of arch 1 include the maxillary artery, muscles of mastication, the mylohyoid muscle, the anterior belly of the digastric muscle, the tensor veli palatine muscle, and the tensor tympani muscle. The maxillary prominence of pharyngeal arch 1 gives rise to the maxilla, zygomatic bone, squamous temporal bone, palatine bone,

and the vomer. The mandibular prominence derivatives include the mandible, incus, and the malleus. Pharyngeal arch 2, also known as the hyoid arch, gives rise to the stapedial artery, muscles of facial expression, posterior belly of the digastric muscle, stylohyoid muscle, stapedius, the lesser horn of the hyoid and upper half of the body of the hyoid, the stapes, and the styloid process. Tissues from the first and second pharyngeal arches form the external ear. Pharyngeal arch 3 is associated with the common carotid artery and the proximal internal carotid artery. The stylopharyngeus muscle, as well as the greater horn of the hyoid and the lower half of the body of the hyoid emerge from pharyngeal arch 3. Derivatives of pharyngeal arch 4 include the proximal right subclavian arch of the aorta, the muscles of the soft palate (with the exception of the tensor veli palatine, which originates from arch 1), the muscles of the pharynx (with the exception of the stylopharyngeus, which originates from arch 3), the cricothyroid, and the cricopharyngeus. Pharyngeal arches 4 and 6 give rise to the thyroid cartilage, the cricoid cartilage, arytenoid cartilage, corniculate cartilage, and cuneiform cartilage. Lastly, pharyngeal arch 6 derivatives include the ductus arteriosus and proximal pulmonary arteries, the intrinsic laryngeal muscles (with the exception of the cricothyroid muscle, which originates from arch 4), the skeletal muscle of the esophagus, and the laryngeal cartilages in conjunction with pharyngeal arch 4.

Development of the Skull The bones of the skull are divided into two portions: the neurocranium (surrounds and protects the brain and sensory organs) and the viscerocranium (bones of the lower face and jaws). The bones of the infant skull are separated by fibrous connections called sutures, which meet at the fontanelles

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Pediatric Dysphagia: Etiologies, Diagnosis, and Management

(membranous areas) at the front and back of the skull (Figure 1–8). The changes in growth of a particular suture will affect the growth pattern of adjacent sutures.6 The metopic suture separates the frontal bones from each other, the coronal suture separates the two frontal bones from the paired parietal bones posteriorly, the sagittal suture separates the two parietal bones from each other, and the lambdoid suture

separates the occipital bone from the two parietal bones. The fontanelles allow for expansion of the cranium as the brain grows. The cranial sutures remain open in infancy and typically begin to fuse as the child approaches 2 years of age; however, complete ossification of the sutures does not occur until adulthood. The approximate time frames for suture closure are summarized in Table 1–2.

Figure 1–8. The cranial suture lines and bones of the skull. Source: Courtesy of Cincinnati Children’s Hospital Medical Center, Division of Pediatric Otolaryngology–Head and Neck Surgery. Table 1–2. Approximate Developmental Timeline for Suture Closure in Humans Suture Type

Closure Begins

Metopic

2 months

Sagittal

22 months, ossifies in adulthood

Coronal

24 months, ossifies in adulthood

Lambdoid

26 months, ossifies in adulthood

Source: Adapted from UpToDate, 2018.



1. Embryologic Development of Aerodigestive Structures

Premature fusion of the sutures (craniosynostosis) may occur due to environmental causes such as prenatal compression of the infant head, teratogens, metabolic disorders, gene mutations, or chromosomal abnormalities. In other cases, there is no identifiable causative agent. The premature closure of the sutures can adversely affect the normal growth of the brain and cause an abnormal skull shape secondary to the pressure of the growing brain against the skull. For example, if the sagittal suture fuses prematurely (synostosis), the head appears long, narrow, and “boat-shaped” (scaphocephaly) (Figure 1–9). If the coronal suture fuses pre-

maturely, the forehead appears flattened (anterior plagiocephaly) (Figure 1–10). If the lambdoid suture closes prematurely, flattening at the back of the skull occurs (posterior plagiocephaly). Lastly, if premature fusion of the metopic suture occurs, the head appears to be triangularly shaped (trigonocephaly) in combination with a narrow forehead with a midline bony ridge and closely positioned eyes. In individuals with double suture synostosis, more than one suture is prematurely fused. In those with bicoronal synostosis, the skull appears wider than normal (anterior brachycephaly). In bilambdoid

Figure 1–9. Sagittal craniosynostosis. Source: Courtesy of the Centers for Disease Control and Prevention, National Center on Birth Defects and Developmental Disabilities.

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Pediatric Dysphagia: Etiologies, Diagnosis, and Management

Figure 1–10. Unilateral coronal craniosynostosis. Source: Courtesy of the Centers for Disease Control and Prevention, National Center on Birth Defects and Developmental Disabilities.

synostosis, the skull is wider than normal (posterior brachycephaly), and in sagittal plus metopic synostosis, the head appears long and narrow (scaphocephaly). In complex multisuture synostosis (bicoronal, sagittal, metopic), the head appears short, wide, and/or pointed. Multisuture synostosis presents as a cloverleaf shaped skull. Craniosynostosis may occur in association with genetic syndromes such as Crouzon, Apert, Pfeiffer, Muenke, and Saethre-Chotzen (see Chapter 7). Chiari malformations are complex congenital structural abnormalities in the base of the skull that occur during development and that affect the structural relationships

between the cerebellum, brainstem, and the cranial base.7 The posterior fossa (cavity near the base of the skull), which encloses the cerebellum, is narrow and abnormally small in comparison to the size of the cerebellum. The relatively small posterior fossa causes the developing cerebellum and brainstem to be pushed inferiorly. The posterior portions of the cerebellum (cerebellar tonsils) protrude or herniate through the foramen magnum and potentially interfere with the normal circulation of cerebrospinal fluid (CSF) (Figure 1–11). The malformation may cause increased CSF pressure within the brain and produce hydrocephalus caused by the accumulation of excessive



1. Embryologic Development of Aerodigestive Structures

Figure 1–11. Chiari I malformation with herniation of the cerebellar tonsils below the foramen magnum. Source: Courtesy of Cincinnati Children’s Hospital Medical Center, Department of Radiology.

fluid in the brain. A fluid-filled cyst or cavity (syrinx) filled with CFS can also develop within the spinal cord (Figure 1–12). Box 1–4 Chiari malformations are named after Professor Hans Chiari, the pathologist who first classified these malformations into types in 1891. Later, Julius Arnold, a colleague of Professor Chiari, made additional contributions to the definition of Chiari II malformation, hence the name Arnold–Chiari malformation.8 Chiari I malformation is the least severe of the spectrum. It is characterized by >5 mm descent of the caudal tip of the cerebellar tonsils past the foramen magnum. Type II Chiari malformation is characterized by brainstem and fourth ventricle herniation and >5 mm descent of the caudal tip of the cerebellar tonsils past the foramen magnum, with spina bifida. Type II Chiari malformation is also often associated with myelomeningocele. Type III Chiari malformation is char-

Figure 1–12. Chiari malformation with an associated syrinx of the spinal cord. Source: Reprinted with permission of the American Syringomyelia and Chiari Alliance Project, Inc.

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Pediatric Dysphagia: Etiologies, Diagnosis, and Management

acterized by herniation of the cerebellum with or without the brainstem through a posterior encephalocele. Type IV Chiari malformation is characterized by cerebellar hypoplasia or aplasia, with normal posterior fossa and no hindbrain herniation.

Development of the Face The major development of the face is completed between the fourth and tenth embryonic weeks by the development and joining of five prominences: the frontonasal prominence, the two maxillary prominences, and the two mandibular prominences (Figure  1–13).9 Early in the fourth week, the forebrain enlarges and pushes the ectoderm anterior and laterally, creating the frontona-

Figure 1–13. Following closure of the anterior neuropore, the ectoderm that will line the nasal cavities (derived from the olfactory placodes [OP]) is located on the lateral aspects of the frontonasal prominence. Pharyngeal arches 1 and 2 are also seen. Source: Courtesy of Kathleen Sulik, PhD, Department of Cell Biology and Physiology, University of North Carolina at Chapel Hill.

sal process. Simultaneously, the two mandibular prominences and the two maxillary prominences from the first pharyngeal arch grow anteriorly and medially during week 4 of gestation. As these processes grow and fuse, they create the stomodeum (precursor of the mouth), which is separated from the gastrointestinal tract by the oropharyngeal membrane. Late in the fourth week, two nasal placodes (paired ectodermal nasal plates) develop on the frontonasal prominence (Figure 1–14). Late in week 5, the lateral and medial nasal processes appear, forming the nasal pits between them. During week  5, rupture of the oropharyngeal membrane occurs to form the broad appearing slitlike embryonic mouth. Early in week 6, the oronasal membrane forms and the median nasal processes begin to form the nasal sep-

Figure 1–14. In the fifth week of human gestation, the olfactory placodes line the nasal pits (NP). Medial (MNP) and lateral nasal prominences (LNP) form around the nasal pits. Pharyngeal arch I can be seen creating the lower jaw. Source: Courtesy of Kathleen Sulik, PhD, Department of Cell Biology and Physiology, University of North Carolina at Chapel Hill.



1. Embryologic Development of Aerodigestive Structures

tum and primary palate. Late in the sixth week, the lateral palatine processes and external ears develop. The lips and gums separate, the dental lamina appears, and the future inferior turbinates begin to form. Early in week 7, the philtrum and upper lip are formed and further development of the nasal septum occurs. By the end of the seventh week, the external ear is fully developed, the palatal shelves elevate and fuse to form the secondary palate, and fusion of the maxillary and mandibular processes occurs. The lateral nasal wall is well developed by the eighth week of gestation. Between weeks 9 and 10 of gestation, the nasal septum grows down from the roof of the nasal cavity to fuse with the upper surface of the primary and secondary palates along the midline, and ossification of the maxilla occurs. The nasal cavity is divided into a left and right nasal passage that open into the pharynx via the choanae (posterior portion of the nasal cavity). The mouth is reduced to its final width during the second month of gestation, as fusion of the lateral portions of the maxillary and mandibular swellings creates the cheeks. Macrostomia (a large mouth) occurs when too little fusion occurs, and microstomia (small mouth) occurs with too much fusion. The derivatives of the frontonasal, lateral nasal, medial nasal, maxillary, mandibular, and mesenchyme in the facial prominences are summarized in Table 1–3. Neural crest

cells give rise to the cartilage, bone, and ligaments in the facial and oral regions. By week 12, the ossification centers of all the facial bones are present.

Congenital Malformations of the Facial Skeleton Holoprosencephaly occurs when the embryonic forebrain (prosencephalon) does not divide into the right and left lobes of the cerebral hemispheres. This results in the reduction of the midventral parts of the CNS as well as the reduction of midfacial structures (skeletal and soft tissues). Affected infants may have facial deformities that affect the eyes, nose, and upper lip. For example, infants may present with a narrow forehead or hypotelorism (close-set eyes), or may lack a nose or philtrum. In extreme cases, only one eye may be present (cyclopia). There are three classifications of holoprosencephaly. These classifications include (1) alobar, characterized by severe facial features as a result of complete failure of brain division; (2) semilobar, in which the hemispheres have somewhat divided, resulting in a less severe form of the disorder; and (3) lobar, in which there is evidence of separate brain hemispheres; considered the least severe form of holoprosencephaly. In normal development, the intermaxillary process fuses with the lateral maxillary

Table 1–3. Derivatives of the Facial Prominences Frontonasal prominence

Forehead and the dorsum apex of the nose

Lateral nasal prominences

Sides (alae) of the nose

Medial nasal prominences

Nasal septum

Maxillary prominences

Upper cheek region, majority of upper lip

Mandibular prominences

Chin, lower lip, lower cheek regions

Mesenchyme in the facial prominences

Fleshy derivatives and bones

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Pediatric Dysphagia: Etiologies, Diagnosis, and Management

swellings to form the maxillary bones of the upper jaw. Disruption of the development of pharyngeal arches 1 and 2 leads to underdevelopment of the lower face and mandible, as seen in patients with Treacher Collins syndrome (mandibulofacial dysotosis). Disruption of pharyngeal arches 3 and 4 may result in DiGeorge syndrome (22q11.2 deletion syndrome), which is characterized by defects of the ear, palate, jaw, agenesis of the thyroid and thymus glands, and cardiovascular anomalies.

Development of the Palate Palatal development occurs during the embryonic and the early fetal periods (Figure 1–15). The primary palate is formed by the maxillary components of the first pharyngeal arch and the frontonasal prominence, and forms during the fifth to seventh week postconception. The primary palate includes the medial portion of the upper lip and the pre-

maxilla. The premaxilla is a wedge-shaped mass of tissue containing the anterior palate and the alveolar ridge. It contains the four central incisors and extends posteriorly to the incisive foramen (Figure 1–16). The incisive foramen is a small opening through which the nasopalatine nerve and the sphenopalatine artery pass to the oral mucosa of the hard palate. Embryologic fusion of the primary palate begins at the incisive foramen and process anteriorly, toward the lip along the incisive suture lines. During weeks 7 and 8 of gestation, the maxillary processes produce the palatal processes that initially grow vertically downward, parallel to the lateral surfaces of the tongue. By the eighth week, the two vertical shelves of bone lift and fuse in the midline; the fusion line is termed the median palatine suture or intermaxillary suture. The fused palatal processes form the secondary palate (Figure 1–17). The incisive foramen marks the central region where the primary and secondary palates meet. Growth and

Figure 1–15. The embryonic palate is complete by the end of week 12 of gestation. Source: Courtesy of Kathleen Sulik, PhD, Department of Cell Biology and Physiology, University of North Carolina at Chapel Hill.



1. Embryologic Development of Aerodigestive Structures

Figure 1–16. Newborn with a complete bilateral cleft lip and palate. The premaxilla is seen between the two cleft sites. Source: Reprinted with permission from Chandna P, Adlakha VK, Singh N. Feeding obturator appliance for an infant with cleft lip and palate. J Indian Soc Pedod Prev Dent. 2011;​ 29(1):71-73.

Figure 1–17. The secondary palatal shelves

lowering of the mandibular (primordium) is essential for the elevation of the palatal shelves and the lowering of the tongue.

palate or complete cleft of the lip, alveolar process, and the primary palate). Incomplete clefts, such as an incomplete cleft of the soft palate, occur when some degree of fusion has taken place. A submucous cleft palate occurs when oral mucosal membrane covers or “hides” the underlying cleft. Although the palate may appear normal, there may be changes in muscle function as a result of the abnormal development. During development, the mandibular (primordium) grows, which allows the tongue to lower relative to the palatal shelves. If the first pharyngeal arch does not develop appropriately, the mandibular (primordium) will not grow, the tongue will not be lowered, and a physical obstruction to the palatal shelf elevation will result. In this circumstance, a cleft of the secondary palate will occur in conjunction with micrognathia (small jaw), which results in glossoptosis (posterior displacement of the tongue). This circumstance is referred to as Pierre Robin sequence and is often associated with syndromes such as Treacher Collins and Stickler.

Cleft Lip and Palate Each site where merging or fusion of tissue occurs during the embryologic development of the face and palate is a potential site for a cleft. A cleft may be complete or incomplete. A complete cleft has bone, and all soft tissues are missing from the site. An incomplete cleft lacks bone and muscle, but has skin bridging the cleft site. There are different types and combinations of clefts (Figure 1–18). Classification based on embryologic development divides these anomalies into clefts of the primary palate (anterior to incisive foramen, including the lip and alveolus) and clefts of the secondary palate (posterior to the incisive foramen, including the soft palate alone or in combination with the hard palate). Complete clefts refer to the maximum degree of clefting (eg, complete cleft of the secondary

change their contours such that they initially approximate each other close to the midpoint, and fuse anteriorly and posteriorly from that point. Source: Courtesy of Kathleen Sulik, PhD, Department of Cell Biology and Physiology, University of North Carolina at Chapel Hill.

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Pediatric Dysphagia: Etiologies, Diagnosis, and Management

Figure 1–18. Types of clefts of the lip and palate: A. Unilateral left complete cleft of the lip and primary palate. B. Bilateral complete cleft of the lip and primary palate. C. Unilateral left complete cleft of the lip and palate. D. Bilateral complete cleft of the lip and palate. E. Cleft of the secondary palate. Source: Adapted from Luciano Abreu Brito, Joanna Goes Castro Meira, Gerson Shigeru Kobayashi, and Maria Rita Passos-Bueno, “Genetics and Management of the Patient with Orofacial Cleft,” Plastic Surgery International, vol. 2012, Article ID 782821, 11 pages, 2012. https://doi.org/10.1155/2012/782821

Lip Anomalies Joining of the medial nasal prominence with the lateral nasal prominence and maxillary prominence is necessary for normal development of the upper lip, which is complex in comparison to the development of the lower lip, and occurs later in embryogenesis.10 During the second and third months of gestation, the upper lip divides into the pars glabrosa and the pars villosa zones. The pars villosa is an inner zone similar to the mucosa of the oral cavity. The pars glabrosa is the outer smooth zone close to the skin. Hypertrophy of the pars villosa and the persistence of a horizontal sulcus between the pars glabrosa and the pars villosa give the characteristic appearance of a double lip.11 Other congenital anomalies of the lip include astomia, which is a rare condition in which complete union of the upper and lower lips occurs. The rudimentary oral aperture that is associated with severe forms

of holoprosencephaly, trisomy 18, and Hallermann–Streiff syndrome is termed microstomia. A transverse facial cleft, known as macrostomia, occurs in association with Angelman, Noonan, Beckwith–Wiedemann, Treacher Collins, and Williams syndromes.10 Congenital synechiae (adhesions) may occur between the hard palate and the floor of the mouth, tongue, or oropharynx. Synechiae may arise from the persistence of the buccopharyngeal membrane that separates the mouth from the pharynx in the embryo, and typically require surgical division.

Development of the Tongue The intrinsic and extrinsic musculature of the tongue is formed by the occipital somites, which are precursor populations of cells that differentiate into skeletal muscles, cartilage, tendons, vertebrae, and skin.



1. Embryologic Development of Aerodigestive Structures

The mucosa covering the anterior twothirds of the tongue arises from median and lateral tongue buds that originate from the floor of pharyngeal arch 1. The first pharyngeal arch forms the median tongue bud (tuberculum impar) and two lateral lingual swellings. As the two lingual swellings grow and expand, they overgrow the median tongue bud. Late in the fourth week of gestation, the second pharyngeal arch forms the copula and the third and fourth arches form the hypopharyngeal eminence. During the fifth and sixth weeks of gestation, the hypopharyngeal eminence continues to grow and the copula disappears. The hypopharyngeal eminence forms the mucosa of the posterior third of the tongue. The anterior two-thirds of the tongue fuses with the posterior one-third of the tongue in a V-shaped line of fusion referred to as the terminal sulcus. The foramen cecum is a “pit” in the center of the terminal sulcus that represents the origin of the thyroid gland before its migration to the neck. The nerves that supply pharyngeal arches 1 to 4 contribute to the complex innervation pattern of the tongue. The lingual nerve (branch of CN V3) supplies the sensory innervation to the anterior two-thirds of the tongue. The chorda tympani branch of CN VII transmits taste information from the anterior two-thirds of the tongue. The posterior two-thirds of the tongue is formed primarily from the third pharyngeal arch, and therefore both taste and sensory information are transmitted by CN IX (glossopharyngeal). A portion of the posterior tongue mucosa is formed by the fourth pharyngeal arch, and therefore sensations are transmitted via the superior laryngeal nerve (branch of CN X, vagus). The musculature of the tongue is innervated by CN XII (hypoglossal).

Congenital Malformations of the Tongue The most common malformations of the tongue are aglossia (complete absence of

the tongue), microglossia (small tongue), macroglossia (abnormally large tongue), and accessory tongue, which is also referred to as a cleft or bifid tongue.12

Lingual Thyroid Gland The thyroid gland derives from the fourth pouch and originates in the midline of the tongue base at the foramen cecum. The thyroid gland normally descends into the neck with development. Occasionally, however, it fails to descend, resulting in a lingual thyroid. A lingual thyroid mass presents as a mass in the tongue base that interferes with breathing and swallowing. Medications to suppress the thyroid gland will lead to a reduction of its size and improve both breathing and swallowing.

Congenital Malformations of the Oral Cavity Errors in the embryonic fusion of the anterior tongue, tongue base, and the primordial thyroid gland in the area of the foramen cecum may result in malformations of the oral cavity. Primitive foregut cysts may present in the floor of the mouth. A number of congenital tumors, including teratomas and epithelial choristomas (normal cells in an abnormal location), may arise in the oral cavity. Cysts and pseudocysts of the major and minor salivary glands are considered to be the most common soft tissue anomalies.

Development of the Gastrointestinal Tract The gastrointestinal tract arises during the process of gastrulation during the third week of gestation. The endodermal gut tube is created during the fourth week of gestation through a process of embryonic folding. This tube extends from the buccopharyngeal membrane cranially to the

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Pediatric Dysphagia: Etiologies, Diagnosis, and Management

cloacal membrane caudally. It consists of a cranial foregut (precursor of the pharynx, esophagus, stomach, liver, gall bladder, pancreas, and the cranial portion of the duodenum), midgut (origin of the caudal portion of the duodenum, the jejunum, ileum, ascending colon, and two-thirds of the transverse colon, and hindgut (precursor of the distal one-third of the transverse colon, the descending colon, the rectum, and the urogenital sinus). The primordium of the primitive stomach is visible by approximately week 4 of gestation. By week 5, the thoracic and abdominal portions of the foregut divide into the pharynx, esophagus, stomach, and proximal duodenum. Between gestational weeks 6 and 8, the epithelium of the gut tube becomes thickened and forms lumina that eventually open into the gut lumen. Subsequently, the villi (tiny finger-like structures that allow for absorption of nutrients in the lumen) are formed. The neuromuscular structures associated with the gastrointestinal tract are formed by neural crest cell migration into the rapidly growing alimentary tract. The neural crest cells differentiate into three separate layers of muscles that surround the gut mucosa and the neural network. The enteric nervous system controls and regulates motor function of the gut. The stomach is formed during gestational week 4 as the foregut begins to expand. During gestational weeks 7 and 8, the stomach undergoes a 90 degree rotation in a clockwise direction, causing the duodenum to acquire a C-shaped loop.

Congenital Anomalies of the Gastrointestinal Tract Congenital anomalies of the gastrointestinal tract include esophageal atresia, intestinal malrotation, atresia in the jejunoileal region, atresia in the duodenum, and diaphragmatic hernia. Esophageal atresia is the most com-

mon malformation of the esophagus. The etiology of this anomaly is considered to be failure of the esophageal endoderm to proliferate in synchrony with the elongation of the embryo.1 A failure in the formation of the tubular esophagus thus occurs. Errors in forming the tracheoesophageal septa and/ or recanalization lead to tracheoesophageal fistulae and/or esophageal atresia. The fetus is unable to swallow, which results in polyhydramnios (excessive amniotic fluid). This occurs because the amniotic fluid cannot pass into the intestines for return to the maternal circulation. Lateralization in the developing embryo refers to the positioning of organs during embryogenesis, resulting in a distinct leftright asymmetry. A number of abnormalities are related to errors of lateralization. In infants with situs inversus abdominis, the abdominal organs are located in the reverse of their normal position. If the midgut does not rotate normally as it retracts into the abdominal cavity, a malrotation of the midgut occurs, which causes intestinal obstruction that typically becomes evident shortly after birth. Intestinal malrotation also predisposes the infant to volvulus of the midgut, whereby the intestines bind and twist around the mesentery (tissues that provide blood and nerve supply to the intestine and attach the intestines to the wall of the abdomen). Volvulus interferes with the blood supply to the intestines and can result in necrosis (death) of the intestine. It is thus considered a surgical emergency. Congenital hypertropic pyloric stenosis occurs when there is overgrowth of the longitudinal muscle fibers of the pylorus, creating a marked thickening of the pyloric outlet region of the stomach. The resulting stenosis of the pyloric canal obstructs passage of food into the duodenum, and the newborn infant expels the contents of the stomach forcefully following a feeding (projectile vomiting). Omphalocele occurs when the midgut fails to retract into the abdominal cavity during development, and at birth,



1. Embryologic Development of Aerodigestive Structures

the coils of intestine are covered only with a transparent sac of amnion. An imperforate anus occurs when the anal membrane fails to break down prior to birth, necessitating surgical reconstruction.

Development of the Respiratory System The development of the trachea, larynx, lungs, esophagus, and stomach from the foregut region is interrelated. Therefore, defects in the development of one of these organs often causes abnormalities to develop in other anatomic regions of the gastrointestinal or respiratory systems.1 The development of the lungs begins on day 22 of gestation with the formation of the respiratory diverticulum (outpouching of the endodermal foregut). The respiratory diverticulum undergoes bifurcation between days 26 to 28, dividing into the right and left bronchial buds. These buds are the progenitors of the right and left bronchi and lungs. The proximal end of the respiratory diverticulum forms the trachea and the larynx. The larynx opens into the pharynx via the glottis, which is formed at the original point of the outpouching of the respiratory diverticulum. The laryngotracheal opening is initially a slit. As the hyobranchial eminences and arytenoid swellings develop, the opening takes on a T shape. The hypobranchial eminence gives rise to the epiglottis. The lumen becomes obliterated as the lumen of the larynx fills with mesenchyme during weeks 5 to 7. At week 9, recanalization of the lumen occurs to reestablish communication through the larynx to the trachea below, and forms an oval lumen. The trachea develops during the second month of gestation, extending from the larynx to the primary bronchi. The cricoid ring is the only complete ring that forms. The remaining tracheal rings are incomplete and described as C-shaped, with the gap in

cartilage located posteriorly. The trachea is composed of cartilage anteriorly and a soft muscular tracheal membrane posteriorly. During weeks 5 to 28, the primary bronchial buds undergo repeated rounds of branching to form the respiratory tree of the lungs. The first round of bronchial bud branching produces the three secondary bronchial buds on the right side of the embryo and two secondary bronchial buds on the left side. These secondary bronchial buds give rise to the lung lobes, with three buds in the right lung (upper, middle, lower) and two buds in the left lung (upper and lower). Further branching during week 6 of gestation produces the tertiary bronchial buds, which become the bronchopulmonary segments of the mature lung. By week 16, more branching occurs and the respiratory tree produces the terminal bronchioles, which further divide into the respiratory bronchioles. By week 28, the respiratory bronchioles sprout a final generation of stubby branches and a dense network of primitive alveoli is formed. Development of alveoli continues during lung maturation and is critical to the infant’s ability to breathe air and survive after birth. If the infant is born prematurely, the state of lung development is a primary determinant in survival.

Congenital Anomalies of the Respiratory System The total surface area for gas exchange in the lung depends on the number of alveoli. In the weeks prior to birth, specific alveolar cells begin to secrete surfactant, which facilitates inflation of the alveoli by decreasing surface tension of the fluid coating the air sacs. In the absence of surfactant, the alveoli collapse, which is the primary cause of respiratory distress syndrome in premature infants. Respiratory distress syndrome threatens infant survival and may cause immediate asphyxiation of

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the infant. Mechanical ventilation, which is often necessary to support respiration in the premature infant, may damage the delicate alveolar lining. Injury that leads to detachment of the layers of cells within the alveoli leads to hyaline membrane disease. Bronchopulmonary disease, also referred to as chronic lung disease, is characterized by lung inflammation and scarring, thus compromising the ability to adequately oxygenate the blood. Box 1–5 Hyaline membrane disease (HMD), also known as infant respiratory distress syndrome, is caused by the lack of surfactant in the lungs. HMD can be exacerbated by infection or trauma to the lungs. Dead cells and protein line the alveolar sacs, limiting gas exchange across the cell membranes. The majority of lung anomalies result from failure of the primitive lung bud to develop. The most severe congenital condition is the unilateral or bilateral absence of lung tissue (pulmonary agenesis). Conditions that restrict lung growth such as oligohydramnios (insufficient amniotic fluid secondary to premature rupture of membranes or fetal kidney abnormalities), abnormalities of the thoracic cage structure, and diaphragmatic hernia may cause pulmonary hypoplasia (reduced number of terminal air sacs). In infants with a congenital diaphragmatic hernia, development of the abdominal (viscera) may bulge into the pleural cavity, stunting the development of the lungs. Diaphragmatic hernias are surgically corrected at birth, and in some settings, can be corrected in utero following identification. Foregut duplications include bronchogenic cysts and esophageal cysts. These cysts arise from an abnormal budding in the foregut and lead to the development of

benign mediastinal masses that may cause problems secondary to infection or compression of other structures. Bronchogenic cysts are filled with air or fluid and may cause infection, hemorrhage, or in rare cases malignancy. Compression of the trachea or bronchi may cause symptoms including stridor, dyspnea, and cyanotic spells following birth. Esophageal cysts lead to abdominal symptoms. Foregut duplication cysts are generally not detected prenatally. Laryngeal clefts are caused by failure of the posterior cricoid lamina to fuse and may extend into the trachea if there is incomplete development of the tracheoesophageal septum, as described in the Benjamin and Inglis classification system for laryngeal clefts (Figure 1–19). Failure of the recanalization process leads to laryngeal atresia, laryngeal stenosis, or laryngeal webs, depending on the degree to which the airway lumen forms. Congenital tracheal anomalies include tracheal agenesis (complete absence of the trachea), tracheal atresia (incompletely formed trachea), tracheal webs, complete tracheal rings (encompassing a single ring, multiple rings, or the entire trachea), and congenital tracheomalacia. Tracheal atresia or total agenesis of the trachea is generally fatal at birth, unless there is a coexisting tracheoesophageal fistula for ventilation.13 In this situation, airflow is possible through the pharynx to the trachea through the fistula into the distal trachea and the lungs. A tracheal web presents as a thin layer of tissue that extends across the tracheal lumen. There is no associated deformity or abnormality of the underlying cartilaginous framework. The degree of respiratory symptoms correlates with the size of the available tracheal lumen. Treatment of tracheal obstruction includes rupturing the web by dilation, laser surgery, or open surgical approaches. Complete tracheal rings occur when there is congenital absence of the posterior membranous portion of the ring. Complete tracheal



1. Embryologic Development of Aerodigestive Structures

Figure 1–19. Benjamin and Inglis classification of laryngeal clefts. Source: Reprinted with permission from Benjamin B & Inglis A. Minor Congenital Laryngeal Clefts: Diagnosis and Classification. Annals of Otology, Rhinology & Laryngology. 1989;98(6).

rings are O-shaped ( compared to the normal C-shaped rings) and cause life-threatening narrowing of the airway. Primary tracheomalacia is defined as softening of the tracheal wall due to an abnormality of the cartilaginous rings and hypotonia of the myoelastic elements. Congenital tracheomalacia may occur in isolation or in combination with vascular abnormalities such as aortic arch abnormalities, innominate artery tracheal compression syndrome, and pulmonary artery slings. The most common types of vascular rings that may compress the airway and/ or the esophagus are due to developmental anomalies of the aorta and its branches. Fetal development of the aortic arch and

branches is shown in Figure 1–20. The persistence of vascular structures that normally regress, or the regression of structures that normally persist, results in congenital anomalies that can cause tracheal obstruction and abnormal arterial or venous circulation, all of which are potentially life-threatening and require surgical intervention.

Questions Pertaining to Chapter Questions pertaining to the information presented in this chapter are provided in Appendix 1–1.

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Figure 1–20. A vascular ring is a malformation of the aortic arch anatomy, where vessels partly or completely encircle the trachea and esophagus. A normal heart with a normal aortic arch is shown on the left. An example of a vascular ring, a double aortic arch, is shown on the right. Source: Used with permission of Mayo Foundation for Medical Education and Research, all rights reserved.

References

6. Babler WJ. Role of cranial sutures in normal and abnormal skull development. Neurosurg Clin N Am. 1991;2(3):539–549. 1. Schoenwolf GC BS, Brauer PR, Francis-West 7. Greenberg MS.Handbook of Neurosurgery. PH. Larsen’s Human Embryology. 5th ed. New York, NY: Thieme; 2006. Philadelphia, PA: Elsevier Churchill Living- 8. Koehler PJ. Chiari’s description of cerebellar stone; 2015. ectopy (1891). With a summary of Cleland’s 2. Stoll C, Dott B, Alembik Y, Roth MP. Associand Arnold’s contributions and some early ated malformations among infants with neuobservations on neural-tube defects. J Neural tube defects. Am J Med Genet A. 2011;​ rosurg. 1991;75(5):823–826. 155(3):565–568. 9. Som PM, Naidich TP. Illustrated review of 3. Harris LW, Oakes WJ. Open neural tube the embryology and development of the defects. In: Tindall GT, Cooper PR, Barfacial region, part 1: early face and lateral row DL, eds. The Practice of Neurosurgery. nasal cavities. AJNR Am J Neuroradiol. 2013;​ Baltimore, MD: Williams & Wilkins; 1996;​ 34(12):2233–2240. 2779–2789. 10. Jones KL. Smith’s Recognizable Patterns of 4. Drolet B. Birthmarks to worry about: cutaHuman Malformation. 6th ed. Philadelphia, neous markers of dysraphism. Dermatol PA: Elsevier Saunders; 2006. Clin. 1998;3:447–453. 11. Aggarwal T, Chawla K, Lamba AK, Faraz 5. Mandell DL. Head and neck anomalies reF, Tandon S. Congenital double lip: a rare lated to the branchial apparatus. Otolaryndeformity treated surgically. World J Plast gol Clin North Am. 2000;33(6):1309–1332. Surg. 2016;5(3):303–307.



1. Embryologic Development of Aerodigestive Structures

12. Emmanouil-Nikoloussi E, Kerameos-Foroglou C. Developmental malformations of human tongue and associated syndromes. Bulletin du Groupement International pour la Recherche Scientifique en Stomatologie & Odontologie. 1992;35(1-2):5–12.

13. Myer CM C, RT, Shott, SR. The Pediatric Airway: An Interdisciplinary Approach. Philadelphia, PA: J.B. Lippincott Company; 1995.

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Appendix 1–1

Questions Pertaining to Chapter 1 1. What distinguishes the embryonic stage from the fetal stage of development? a. All major systems form during the embryonic stage; the fetal stage consists primarily of rapid body growth and differentiation of the already formed tissues and organs b. The pharyngeal apparatus forms completely during the fetal stage of development; it does not emerge during the embryonic phase c. All organ systems develop during the embryonic stage d. The major event during the embryonic phase is primarily the development of the gastrointestinal tract 2. The pharyngeal arches are the embryologic basis of all the structures in the head and neck, and appear as: a. A series of three paired swellings that surround the embryonic midgut from days 16 to 40 b. A series of five paired swellings that surround the embryonic foregut from day 20 to day 35 c. A series of four paired swellings that remain visible throughout the embryonic phase and fetal development d. A series of six paired swellings that are visible for the first 4 weeks of the embryonic period

3. Chiari malformations are congenital structural defects in the posterior fossa that affect the: a. Parietal lobe of the brain b. Frontal lobe of the brain c. Cerebellum and brainstem d. Temporal lobe of the brain 4. The muscles of mastication are derived from: a. The fourth and sixth pharyngeal arches b. The second pharyngeal arch c. The first pharyngeal arch d. The third pharyngeal arch 5. The major development of the face is completed between the fourth and tenth embryonic weeks by the development and joining of: a. The frontonasal prominence, the two maxillary prominences, and the two mandibular prominences b. The two frontonasal prominences, one maxillary prominence, and one mandibular prominence c. The forebrain, nasal placodes, and the upper and lower lips d. The two frontonasal prominences and the nasal placodes

Section

2

Neural Control of Swallowing The normal swallow is generated through the actions of a neural network that comprises both volitional and reflexive components. The swallowing process depends upon sensory input and the generation of motor responses that propel the bolus through the upper aerodigestive tract and simultaneously protect the airway. Swallowing problems arise from defects in the

neural control centers responsible for safe swallowing or in the neural connections to the muscles responsible for swallowing. The chapters in this section lay the foundation for an understanding of the swallowing problems associated with congenital and acquired abnormalities in the central or peripheral nervous systems.

2 Neural Organization Related to Swallowing Claire Kane Miller, Lisa N. Kelchner, and Jay Paul Willging

CHAPTER OUTLINE Introduction Organization of the Brain Regions of the Brain The Brainstem and Control of Swallowing Sensory Neurons Motor Neurons Role of the Cerebral Cortex in Feeding and Swallowing

Introduction The normal feeding and swallowing process is the product of a highly complex neural network that is composed of both volitional and reflexive components. This integrated control center develops within the central nervous system (CNS) and is influenced by genetics, environmental factors, and experience with swallowing.1 Genetic mutations as well as environmental factors such as prenatal maternal drug exposure, maternal dietary deficiencies, viral illness contracted by the mother while pregnant, and alcohol and cigarette smoke exposure may inter-

fere with normal development of the CNS.2 Exposure to these adverse conditions early in development is likely to have significant negative consequences on the coordinated function of the CNS. The embryonic development of the CNS occurs early in gestation, with the full complement of neurons in the spinal cord and brain being present by week 25 of gestation. The cortex of the brain continues to develop well after birth. During the first year of life, dendritic processes develop on each cortical neuron to establish a highly integrated network. Abnormalities in the neural control of swallowing, in either the CNS or the peripheral nervous system

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(PNS) or both, result in dysphagia. The CNS is composed of the brain and spinal cord. The PNS is divided into the autonomic nervous system, peripheral motor, and sensory systems. The autonomic nervous system is further subdivided into the sympathetic and parasympathetic nervous system. The PNS includes the cranial, spinal, and peripheral nerves, which supply innervation to the viscera, glands, muscles, and skin. The PNS essentially connects the CNS with the rest of the body providing pathways for signal transmission. Box 2–1 A nerve cell is composed of a cell body, an axon that terminates on another cell body or muscle, and dendrites which receive input from other nerve cells. Understanding the neural control of feeding and swallowing and the problems associated with abnormalities in one or more areas regulating feeding is essential to the assessment of the care of patients with dysphagia and the development of a management strategy to treat or compensate for the problem.

Organization of the Brain The organization of the brain is modular. There are many neural connections within the modules that are organized around specific functions and in connection with modules of differing function. There is also a hierarchical organization of multiple neural modules within the body systems (eg, digestive, circulatory, lymphatic) to support complex functions. These related modules interconnect with each other more than with modules relating to disparate function (eg, visual system, auditory system, respiratory system). The cortical regions of the brain are responsible for what is termed “higher level function,” which comprises volitional tasks such as writing, speaking,

and bolus manipulation. In contrast, the subcortical regions of the brain and brainstem are associated with nonvolitional reflexive tasks such as motor signal refinement, breathing, and reflexive swallowing. Multiple regions of the brain interact during the performance of a task, modulating one another in a type of shifting of central control.3

Regions of the Brain The brain is organized into regions with specific functions. There are also welldefined structures that contain ascending or descending neural tracts and crossing cortical pathways (decussation) that account for the laterality of function. The brain is composed of four major anatomic regions: (1) the cerebrum (right and left cerebral hemispheres), (2) subcortical regions (basal ganglia and the limbic system), (3) the cerebellum, and (4) the brainstem. The cerebral cortex is the outer layer of the cerebrum. The cerebrum is divided into four distinct lobes, including the frontal lobe, the temporal lobe, the parietal lobe, and the occipital lobe. The insular lobe is located deep/inferior to the temporal and parietal lobes. These lobes are separated from each other by deep fissures. The lateral sulcus (Sylvian fissure) separates the frontal lobe from the temporal lobe. The central sulcus of Rolando separates the frontal lobes from the parietal lobes, posteriorly. The occipital lobe is demarcated from the temporal and parietal lobes by the parieto-occipital sulcus. Each lobe of the cerebrum has distinct functions. The frontal lobe is responsible for reasoning, planning, emotion, problem solving, some components of speech, and skilled motor movement. The parietal lobe is responsible for primary perception and sensory integration of touch, pressure, temperature, and pain. The temporal lobe is responsible for perception and recognition of auditory stimuli and memory. The occipital



2. Neural Organization Related to Swallowing

lobe is responsible for perception and integration of visual stimuli. The insular cortex is a portion of the cerebral cortex not visible on external inspection of the brain. Folded deep within the lateral sulcus, the insular cortex is thought to be important for the integration of key sensory information, particularly the gustatory pathway. It is also involved with consciousness and functions linked to emotion and the regulation of homeostasis. Box 2–2 Homeostasis refers to a stable physiologic state of the body’s internal environment. The primary motor cortex is one of the principal areas of the brain involved with motor function. It is located in the frontal lobe of the brain immediately anterior to the central sulcus, in an area called the precentral gyrus. The inferior lateral portion of this region is responsible for the execution of the motor signals that drive voluntary control of muscles involved in the sequential movements of the oral preparatory and oral phase of the feeding process. Anterior to the primary motor cortex is the premotor cortex, which is critical for motor movement planning, spatial guidance of movement, and sensory guidance of movement. Motor signals generated from the primary motor cortex descend via motor pathways into deeper portions of the brain. The upper motor neuron cell bodies originate within the primary motor cortex and their axons extend downward via the pyramidal tracts to the contralateral brainstem and spinal cord. The majority of these motor fibers cross the midline as they descend. A special collection of fibers within the pyramidal tracts contain motor fibers that ultimately connect to structures of the head and neck that are innervated by the cranial nerves. The corticobulbar tract of the pyramidal pathway connects the cerebral motor cortex to the regions of the brainstem responsible for carrying the motor function of the cra-

nial nerves. In general, injury to the motor cortex on one side will lead to a contralateral paralysis; however, the motor cortex responsible for the function of the pharynx and larynx has considerable bilateral representation. The result of this dual representation is that focal hemispheric damage does not necessarily result in contralateral laryngeal or pharyngeal weakness.4,5 The motor neurons from the pyramidal tracts pass through the basal ganglia and the cerebellum on their way to the brainstem. All motor signals involved in the execution of skilled motor movements are influenced and modified by both the ganglia and the cerebellum. The basal ganglia consist of both excitatory and inhibitory circuits to refine the motor signals, resulting in skilled movements. Without the refinement from the basal ganglia, extraneous movements (tics, resting tremors) or reduced movement (bradykinesia) would be evident in end organs such as the hands, legs, and larynx. The cerebellum is similarly responsible for the smooth coordination of voluntary movements. Cerebellar injury results in poor coordination of all skilled motor movements, including those that relate to the head and neck. Disruption in the speed and timing of movements, as well as restriction in the direction of movement, may occur. Limitations of the oral motor movements necessary for efficient feeding also may occur, and may interfere with the normal progression of skills. Cerebellar injuries may present with muscle tone abnormalities, including hypotonia, hypertonia, or fluctuating tone. The brainstem is considered the “core” of the swallowing system. Modulation of brainstem function occurs through innervation originating from higher cortical centers; however, the brainstem is able to generate impulses that initiate a swallow without supramedullary involvement.6,7 Although infants and adults with severe neurologic damage superior to the midbrain do swallow, the aspects of the oral phase of the swallow are likely to be severely impaired

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as evidence that a central pattern generator (CPG) is involved with human swallowing.8 While the cortex is not essential for the pharyngeal or esophageal phases of swallowing, it is required to facilitate coordination in the oral phase of swallowing. It is also essential for the development of oral motor/feeding skills necessary for the efficient and safe intake of liquids and ageappropriate solids.

The Brainstem and Control of Swallowing The brainstem has three primary subdivisions which include the midbrain (mesencephalon), the pons (metencephalon), and the medulla oblongata (myelencephalon) (Figure 2–1). The control centers for swal-

lowing, vocalization, respiration, and vasomotor control reside in the brainstem. These regions are referred to as central pattern generators (CPGs) — neuronal circuits that produce specific rhythmic motor patterns when activated. Examples of activities that are controlled by CPGs include swallowing, breathing, and vasomotor control.9,10 CPGs are present bilaterally in the brainstem, and many interconnections exist between CPGs that control the same function. This allows either side to initiate the bilateral neural motor patterns needed for coordinated function. When CPGs are stimulated, no peripheral feedback is required to complete the motor task. The integrity of the swallow is contingent upon the intact function of multiple cranial nerves that have their nuclei within the brainstem. These include the trigeminal (CN V), facial (CN VII), glossopharyngeal

Figure 2–1. Diagram showing the brainstem, which includes the medulla oblongata, the pons, and the midbrain. Source: Courtesy of Cancer Research UK/Wikimedia Commons. File licensed under Creative Commons https://commons.wikimedia.org/wiki/File:​ Diagram_showing_the_brain_stem_which_includes_the_medulla_ oblongata,_the_pons_and_the_midbrain_(2)_CRUK_294.svg.



2. Neural Organization Related to Swallowing

(CN IX), vagus (CN X), and hypoglossal (CN XII) nerves, and the two main groups of interneurons: the dorsal swallowing group and the ventral swallowing group.The dorsal swallowing group (DSG) is located in the nucleus tractus solitarius, which is found in the dorsomedial medulla and the reticular formation. The DSG contains generator neurons involved with the triggering, shaping, and timing of the swallowing pattern. The ventral swallowing group (VSG) is located in the ventrolateral medulla, which contains the “switching” neurons that distribute the neural activity to pools of neurons involved with swallowing activity (Figure 2–2). Box 2–3 The reticular formation is a primitive portion of the brain that receives impulses from and sends impulses to all parts of the CNS. It is found throughout the brainstem, with widely spaced neurons that form a continuous network of efferent and afferent pathways.

Sensory Neurons While input from the cerebral cortex is not needed for the pharyngeal and esophageal phases of swallowing, it is essential for the coordination of the oral phase of swallowing (see Chapter 4). Mechanoreceptors, nociceptors, chemoreceptors, special taste receptors, and thermoreceptors are located in the oral cavity, the tongue, and the pharynx. These receptors provide essential information to the brainstem regarding characteristics of the bolus. Afferent cranial nerve input from the oral cavity is integrated in the brainstem and is supplied by the maxillary branch of the trigeminal nerve (CN V2) and V3 for the lower mouth; the facial nerve (CN VII), which reflects the sensation of taste from the anterior two-thirds of the tongue; the glossopharyngeal nerve (CN IX), which reflects the sensation of

taste from the posterior third of the tongue and general sensory information from the tongue base, pharynx, vallecula, and part of the larynx; the vagus nerve (CN X), specifically the internal branch of the superior laryngeal nerve, which provides sensory information from the endolarynx. Sensory information from the oral cavity is integrated in the nucleus tractus solitarius and transmitted to the nucleus ambiguus. There are large motor nuclei in the ventrolateral aspect of the medullary reticular formation. Box 2–4 The endolarynx is a group of structures that surround the opening into the airway (epiglottis, aryepiglottic folds, false vocal folds, and true vocal folds). Sensory information primarily travels into the CNS via a “three order” neuron arrangement. Peripheral stimuli such as taste, temperature, and touch activate select receptor neurons that transmit the signals to corresponding pathways within the CNS. First order neurons extend from the endorgan sensory receptors (eg, receptors in the tongue and pharynx) to the cell bodies within the brainstem. Second order neurons cross to the contralateral side and travel up to the thalamus. Third order neurons transmit the sensory information from the thalamus to the corresponding regions of the primary sensory strip (postcentral gyrus) of the parietal cortex.

Motor Neurons Motor input from the cortex passes through the pyramidal tracts, which are composed of corticobulbar and corticospinal tracts. Although there is bilateral innervation to the motor nerves associated with swallowing, this bilateral representation varies. The motor nerves associated with swallowing are localized in the trigeminal (CN V), facial

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38 Neural control of the swallow.

Figure 2–2.



2. Neural Organization Related to Swallowing

(CN VII), glossopharyngeal (CN IX), vagus (CN X), and hypoglossal (CN XII) nerves. These nerves are not all involved equally during feeding and swallowing. For example, the motor nuclei of CN V and CN VII are active in the oral phase of swallowing, characterized by the oral motor patterns of reflexive jaw actions, chewing, licking, and sucking. The motor nucleus of CN XII controls the intrinsic and extrinsic muscles of the tongue. The nucleus ambiguus controls the muscles of the pharynx, larynx, and the esophagus through innervation of CN IX and CN X.

Role of the Cerebral Cortex in Feeding and Swallowing The oral phase of the swallow in infants is characterized by a reflexive repetitive suck–swallow sequence in the absence of voluntary contractions of muscles of mastication. This reflexive rhythmic suck–swallow process is mediated by the brainstem. The swallowing process transitions from a purely reflexive process to one modified by voluntary actions in conjunction with the increasing myelination of the nervous system. Box 2–5 Myelin is a fatty material that is deposited around a nerve. It acts as an insulator to allow nerve impulses to propagate faster along the nerve. The production of the myelin sheath is called myelination. This process begins during fetal development and rapidly increases during infancy and childhood. It begins in the spinal cord and proceeds rostrally. Within the cerebrum, myelin forms in the primary motor and sensory areas. In concert with this increasing neurologic maturation, the reflexive pattern of swallowing transitions to one influenced

by voluntary input. The underlying movements associated with swallowing, however, remain under the control of CPGs for swallowing that are located in the brainstem. Box 2–6 Functional magnetic resonance imaging (fMRI), transcervical magnetic stimulation, and electrophysiologic studies have provided evidence that neuronal activity associated with swallowing occurs in specific sites in the cortex: the lateral precentral gyrus, the lateral postcentral gyrus, and the right insula.* In general, one hemisphere is dominant in initiating swallowing, despite the fact that bilateral volitional swallowing activation usually occurs. Left-side dominance for swallowing is seen in 63% of patients.**  *Miller AJ. The neurobiology of swallowing and dysphagia. Devel Disabil Res Rev. 2008;14(2):​ 77–86. **Hamdy S. Role of cerebral cortex in the control of swallowing. GI Motility online. 2006. doi:10.1038/gimo8.

References 1. Martin RP, Dombrowski SC. Prenatal Exposures: Psychological and Educational Consequences for Children. Vol. 16. New York, NY: Springer Science and Business Media; 2008. 2. Rice D, Barone Jr S. Critical periods of vulnerability for the developing nervous system: evidence from humans and animal models. Environmental Health Perspectives. 2000;108(Suppl 3):511. 3. Humbert IA, German RZ. New directions for understanding neural control in swallowing: the potential and promise of motor learning. Dysphagia. 2013;28(1):1–10. 4. Ertekin C, Aydogdu I. Neurophysiology of swallowing. Clin Neurophysiol. 2003;​114(12):​ 2226–2244. 5. Hamdy S. Role of cerebral cortex in the control of swallowing. GI Motility online. 2006. 6. Lang IM. Brain stem control of the phases of swallowing. Dysphagia. 2009;24(3):333–348.

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7. Thexton AJ, Crompton AW, German RZ. Electromyographic activity during the reflex pharyngeal swallow in the pig: Doty and Bosma (1956) revisited. J Appl Physiol. 1985;. 2007;102(2):587–600. 8. Ertekin C, Aydogdu I. Neurophysiology of swallowing. Clin Neurophysiol. 2003;​114(12):​ 2226–2244.

9. Jean A. Brain stem control of swallowing: neuronal network and cellular mechanisms. Physiol Rev. 2001;81(2):929–969. 10. Miller, Arthur J. The Neuroscientific Principles of Swallowing and Dysphagia. San Diego, CA: Singular Publishing Group; 1999.

3 Cranial Nerves Associated with Swallowing Claire Kane Miller, Lisa N. Kelchner, and Jay Paul Willging

CHAPTER OUTLINE Cranial Nerves Associated with Swallowing Trigeminal Nerve Facial Nerve Glossopharyngeal Nerve Vagus Nerve Pharyngeal Branch of the Vagus Nerve Superior Laryngeal Branch of the Vagus Nerve Recurrent Laryngeal Branch of the Vagus Nerve Hypoglossal Nerve The Role of Sensation in Feeding and Swallowing Organization of the Swallowing Motor Pattern Oral Reflexes in the Infant

Cranial Nerves Associated with Swallowing As demonstrated in studies of mammals, including humans, the duration of the entire swallowing sequence ranges from 0.6 to 1.0 seconds.1,2 A thorough understanding of the role of the cranial nerves in each phase of the swallow is essential for the assessment and management of feed-

ing and swallowing dysfunction. As well, recognition of abnormalities in cranial nerve function and the potential effects of these abnormalities on the safety and efficiency of feeding and swallowing is crucial to the diagnostic process. The cranial nerves involved with feeding and swallowing include CN V, CN VII, CN IX, CN X, and CN XII (Figure 3–1). These nerves provide either motor or sensory function or both. A more in-depth description of the muscles

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Figure 3–1. Location of the cranial nerves on the ventral surface of the brain. CN I — olfactory; CN II — optic; CN III — oculomotor; CN IV — trochlear; CN V — trigeminal; CN VI — abducens; CN VII — facial; CN VIII — vestibulocochlear; CN IX — glossopharyngeal; CN X — vagus; CN XI — accessory; CN XII — hypoglossal. Source: Courtesy of Patrick J. Lynch, medical illustrator and derivative work: Beao *derivative work: Angelito7 (talk). File licensed under Creative Commons https://commons.wikimedia.org/wiki/ File:Brain_human_normal_inferior_view_with_labels_pt.svg.

associated with swallowing, the actions of these muscles, and their innervations are provided in Appendix 29–2.

Trigeminal Nerve The trigeminal nerve (CN V) has three main divisions: CN V1 (ophthalmic), CN V2 (maxillary), and CN V3 (mandibular). This nerve has both sensory and motor functions. The

ophthalmic and maxillary divisions are purely sensory, whereas the mandibular division supplies both sensory and motor function. Sensory awareness (tactile, proprioceptive, and nociceptive) of the face and mouth is provided by the trigeminal nerve. Motor function of the mandibular division of CN V controls the muscles of mastication as well as the tensor tympani and tensor veli palatini muscles of the soft palate and the mylohyoid and anterior belly of the digastric muscle.



3. Cranial Nerves Associated with Swallowing

Box 3–1 Muscles of mastication include the masseter, temporalis, medial pterygoid, and lateral pterygoid. The ophthalmic division of CN V passes through the cavernous sinus, enters the orbit, and then extends to provide sensation to the forehead and the upper part of the nose, upper eyelid, and cranial dura. The maxillary division of CN V also passes through the cavernous sinus. It then exits the skull through the foramen rotundum to innervate the upper lip and cheek, lower eyelid, anterior temple region, oral mucosa of the mouth lying above the tongue, nose, pharynx, maxillary teeth, upper alveolar ridge, maxillary palate, and cranial dura. The mandibular division of CN V exits the skull via the foramen ovale and provides sensory innervation to the lower lip and mandible, the posterior temple area, the lateral ear canal and tympanic membrane, the pinna, mandibular teeth, oral mucosa of the cheeks and floor of mouth, the anterior two-thirds of the tongue, the temporomandibular joint, and the cranial dura. The motor fibers innervate the muscles of the lower jaw for sucking and provide innervation to the palatal elevators associated with swallow initiation. A clinical correlate of this information is presented in Box 3–2. Box 3–2 Given that the motor function of the mandibular division of CN V has bilateral cortical representation, a large unilateral central injury (stroke) to one cerebral cortex is unlikely to cause an observable deficit in the muscles of mastication and the soft palate.

Facial Nerve The facial nerve (CN VII) provides motor innervation to the muscles of the face, which are referred to as the muscles of

facial expression. It also provides innervation to the stylohyoid, stapedius, and posterior belly of the digastric muscles as well as taste sensation to the anterior two-thirds of the tongue, general sensation to the external ear, and lacrimation (tear production). In addition, CN VII carries innervation to the submandibular and sublingual glands to increase salivation. The motor axons of the facial nerve originate in the facial motor nucleus in the caudal pons. The nerve tract loops around the nuclei of the abducens nerve (CN VI) before it leaves the brainstem at the cerebellar pontine angle. The facial nerve enters the internal auditory canal and courses through the temporal bone. It is totally encased in the boney facial canal and exits the skull through the stylomastoid foramen. The facial nerve innervates the ipsilateral muscles of the face. This nerve has five branches: temporal, zygomatic, buccal, marginal mandibular, and cervical. A clinical correlate of this information is presented in Box 3–4. Box 3–3 Ipsilateral refers to structures on the same side. In contrast, contralateral refers to structures on the opposite side. A traumatic injury to the left side of the brain will therefore manifest with weakness on the contralateral right side of the body. Box 3–4 The corticobulbar fibers from the motor strip to the lower motor neurons for the lower half of the face are mostly crossed, and those to the upper part of the face are bilaterally distributed. Damage to the corticobulbar fibers in one hemisphere usually results in motor deficits involving the lower quadrant of the contralateral face, yet the function of the upper face (forehead region) remains intact. However, a lesion of the lower motor neuron results in complete paralysis of one side of the face.

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CN VII supplies innervation to the lips, which facilitates lip closure and lip seal and prevents spillage during the oral preparatory and oral phase of the swallow. Lesions may result in drooling and problems with residual in the lateral sulci following swallows. Innervation to the buccinator muscle contributes to flattening of the cheeks and the ability to hold the bolus between the upper and lower teeth. The buccinator muscle provides a medially directed force that is opposed by a laterally directed force in the bolus from the tongue. Innervation to the stylohyoid and posterior belly of the digastric muscle contributes to the elevation and retraction of the hyoid during the swallow.

Glossopharyngeal Nerve The glossopharyngeal nerve (CN IX) is primarily a sensory nerve that mediates taste, salivation, and swallowing in concert with CN X and CN XII. The glossopharyngeal exits the brainstem via the jugular foramen in close proximity to CN X and CN XI. CN IX provides sensation to parts of the external ear, the external auditory meatus, the tympanic cavity, and the eustachian tube. It also provides sensory information from the oropharyngeal mucosal membranes, the mucosal membranes of the upper pharynx, the posterior third of the tongue, and the tonsils. CN IX also represents the afferent branch of the gag reflex. In addition, it provides motor innervation to the stylopharyngeus muscle, which elevates and pulls the larynx up toward the styloid process. The geniohyoid provides the strongest anterior pull to aid in opening the cricopharyngeus. The motor nucleus arises within the nucleus ambiguus. Clinical correlates of this information are presented in Boxes 3–5 and 3–6.

Vagus Nerve The vagus nerve (CN X) is a mixed sensory and motor nerve that exits the brainstem

Box 3–5 Lesions in the corticobulbar tract may result in contralateral hemianesthesia of the pharynx and involvement of the stylopharyngeus muscle, thus impacting the elevation of the pharynx and larynx during swallowing. Because of the bilateral innervation to the motor neurons associated with swallowing, the degree of deficit is variable. A lesion affecting CN IX can impair the gag reflex unilaterally. Lesions of the nucleus ambiguus (motor nuclei) or nucleus tractus solitarius result in ipsilateral hemianesthesia of the upper pharynx, tonsils, and posterior aspect of the tongue, as well as possible glossopharyngeal neuralgia.

Box 3–6 Impairment of glossopharyngeal nerve function results in decreased hyolaryngeal elevation. An isolated lesion of the glossopharyngeal nerve will not likely result in significant airway compromise, if other aspects of the swallow such as laryngeal closure and pharyngeal constrictor contract and sensation are intact. and skull along with the glossopharyngeal nerve and spinal accessory nerve via the jugular foramen. This nerve is the longest cranial nerve and is commonly referred to as the “wanderer” because of its length, multiple branches, and different pathways on the left and right sides of the body. As the vagus descends in the neck, it gives off a pharyngeal branch, a superior laryngeal branch (which has both internal and external branches), and a recurrent laryngeal branch. The main trunk then descends into the thorax to innervate viscera of the thorax and abdomen. On the left side, the recurrent laryngeal nerve (RLN) descends into the thorax and loops around the aorta before traveling back up to innervate the intrinsic muscles of the larynx. The right RLN loops under the subclavian artery and



3. Cranial Nerves Associated with Swallowing

then travels up to innervate the intrinsic muscles of the larynx.

Pharyngeal Branch of the Vagus Nerve The pharyngeal branch of the vagus nerve is sensory to the mucosa of the pharynx and special sensory to taste buds on the tip of the epiglottis and to a small area on the base of the tongue. This sensory information is projected to the nucleus tractus solitarius. The pharyngeal branch provides motor innervation to the levator veli palatini muscle, the muscularis uvulae, and the palatoglossus. This branch is an efferent branch of the gag reflex.

Superior Laryngeal Branch of the Vagus Nerve The superior laryngeal nerve (SLN) is divided into an internal branch and an external branch. The internal branch provides sensory input from the surface of the vocal folds, lateral pyriform channels, and epiglottis. The external branch provides motor input to the cricothyroid muscles of the larynx and is considered to be key to the swallow trigger.

Recurrent Laryngeal Branch of the Vagus Nerve The recurrent laryngeal branch of the vagus nerve provides motor input to the intrinsic muscles of the larynx, cricopharyngeus, pharyngoesophageal segment of the esophagus, and the inferior constrictor muscles. It also provides sensory input to the mucosa of the trachea. A clinical correlate of this information is presented in Box 3–7.

vides ipsilateral motor innervation to the intrinsic muscles of the tongue as well as to the styloglossus, hyoglossus, genioglossus, and geniohyoid muscles. The corticobulbar tracts bring voluntary cortical innervation from the contralateral hemisphere to the hypoglossal nuclei. A clinical correlate of this information is presented in Box 3–8. Box 3–7 Infants born with cardiac abnormalities such as patent ductus arteriosus, hypoplastic left heart syndrome, or other cardiac conditions that require surgical intervention, may be at risk for iatrogenic injury to the RLN, resulting in vocal fold paralysis. Similarly, infants born with esophageal atresia, tracheoesophageal fistula, or congenital diaphragmatic hernia and who undergo surgical procedures may be at risk for iatrogenic injury to the RLN, resulting in vocal fold paralysis. In both clinical scenarios, vocal fold paralysis may impact the ability to achieve and sustain airway protection during feeding.

Box 3–8 Central damage to the corticobulbar tracts involving the tongue results in weakness on the contralateral side, and the tongue deviates to the side of muscle weakness, which is opposite to the site of injury. In contrast, a lesion of the lower motor neuron causes the tongue to deviate toward the side of the injury. Oral motor dysfunction can be caused by central or peripheral damage involving the tongue, which results in impairment of the oral preparatory and oral transfer phases of the swallow.

Hypoglossal Nerve The hypoglossal nerve (CN XII) is a pure motor nerve with no sensory component. The motor nucleus (hypoglossal nucleus) lies within the medulla. This nerve exits the skull via the hypoglossal canal and pro-

The Role of Sensation in Feeding and Swallowing Sensory receptors in the tongue, soft palate, floor of mouth, and teeth are stimulated by

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the size, texture, temperature, and chemical composition of the food bolus. Sensory input from cranial nerves V, IX, and X stimulates various nuclei in the brainstem. These nuclei then modulate the pharyngeal response to the bolus in terms of the muscle recruitment needed in order to swallow a particular bolus. The resulting motor action that is triggered is the result of modulation by the CPG to create an output secondary to the sensory input received. As an example, chewing activity is triggered in response to tactile input representing a solid bolus type. The pharyngeal phase of the swallow is not triggered until sensory input is received, reflecting oral transport of the bolus posteriorly following completion of the oral preparatory phase of the swallow. The degree of muscle recruitment (reflecting the effort required to achieve a successful swallow) for the pharyngeal phase of the swallow is regulated by the size and consistency of the ingested bolus.

Organization of the Swallowing Motor Pattern The motor activity exhibited during the three phases of swallowing is unique to each phase. The oral preparatory phase of swallowing (also referred to as the oral phase) is characterized by a stereotypical sequence of electrical events that involve both inhibitory and excitatory pathways.1 Proper timing of muscle contraction and relaxation is essential to proper safe and efficient swallowing. The set of muscles that always participate in this fundamental motor pattern are defined as obligate muscles; these include the geniohyoid, palatopharyngeus, thyrohyoid, pharyngeal constrictors, muscles of the tongue, and muscles of the upper cervical esophagus. Rhythmic motion of the jaws associated with chewing and jaw opening rely on coordination of the muscles innervated by the trigeminal nerve. The muscles involved with these activities include the

mylohyoid, anterior belly of the digastric, and the medial and lateral pterygoids. The facial nerve is also involved with these same functions through innervation of the stylohyoid and posterior belly of the digastric muscles. The trigeminal motor nucleus and the facial motor nucleus receive both excitatory and inhibitory stimulation from the CPG responsible for these activities. The muscles that facilitate protrusion and retraction of the tongue during acts of sucking, chewing, and licking involve the intrinsic muscles of the tongue. Additionally, the genioglossus and the styloglossus muscles assist with these functions. The hypoglossal nerve carries impulses from the hypoglossal motor nucleus in the brainstem and receives modulation input from the swallowing CPG. To initiate the swallow, the “leading complex” (first set of muscles activated in a patterned response) begins with the contraction of the mylohyoid muscle, followed by a sequential pattern of contraction of the pharyngeal and laryngeal musculature. The motor innervation of the pharynx is predominantly through the motor component of CN IX (to the stylopharyngeus), the pharyngeal branches of CN X, and the pharyngeal plexus (made up of branches of CN IX, CN X, and a small branch of CN XI), which courses on the middle and inferior pharyngeal constrictors. The motor fibers in the pharyngeal plexus are carried by the vagus nerve and supply all of the muscles in the pharynx, with the

Box 3–9 The successful swallow requires the proper sequencing of muscle contraction in the oral cavity, the larynx, and the pharynx. This sequence of contractions propels the bolus, closes the vocal folds, and causes laryngeal elevation, epiglottic retroversion, and upper esophageal opening. Respiratory effort must stop at the time of the swallow.



3. Cranial Nerves Associated with Swallowing

exception of the stylopharyngeus (CN IX) and the tensor veli palatini (CN V). The RLN branch from CN X supplies all of the intrinsic muscles of the larynx except for the cricothyroid, which is supplied by the external laryngeal branch of the SLN from CN X.

Oral Reflexes in the Infant As discussed in Chapter 6, the infant exhibits automatic reflexive patterned responses to oral stimulation that reflect the sensory and motor functions of the cranial nerves. These include the rooting reflex, the suck– swallow reflex, phasic biting, the transverse tongue reflex, and the gag reflex. The rooting reflex is elicited by tactile stimulation to the corner of the mouth, which in turn causes the infant’s head to turn in the direction of the stimulus. The suck–swallow reflex is then initiated. Sucking in the newborn is reflexive and entirely mediated by the CPG in the brainstem. The phasic biting reflex is elicited by the application of pressure to the gums, causing the mouth to close on an object. It is responsible for early munching (vertical chewing pattern). The transverse tongue reflex is elicited by tactile stimulation of the lips or tongue, result-

ing in protrusion of the tongue or lateral tongue motion. The gag reflex is a stereotypic protective response to stimulation of the posterior tongue or posterior pharyngeal wall. The gag response is characterized by head, jaw, and tongue protrusion accompanied by pharyngeal contractions. This response is highly pronounced in the neonate and begins to diminish in intensity by 6 months of age. Primitive oral reflexes such as rooting and the early suck–swallow reflex support an infant’s survival, as they are predominantly protective. However, as the cerebral cortex matures and experience with food material is gained, there is a gradual transition of oral motor and swallowing function. This transition results in swallowing function that is under more volitional control. Persistence of primitive reflexes such as rooting and tongue protrusion may indicate abnormalities in cortical maturation.

References 1. Jean A. Brain stem control of swallowing: neuronal network and cellular mechanisms. Physiol Rev. 2001;81(2):929–969. 2. Ertekin C, Aydogdu I. Neurophysiology of swallowing. Clin Neurophysiol. 2003;​114(12):​ 2226–2244.

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4 Three Phases of Swallowing Claire Kane Miller, Lisa N. Kelchner, and Jay Paul Willging

CHAPTER OUTLINE Three Phases of Swallowing Oral Phase Pharyngeal Phase Esophageal Phase

Three Phases of Swallowing The act of swallowing (deglutition) enables food material or liquids to be carried from the mouth to the pharynx and esophagus, through which it then enters the stomach. Normal deglutition is a synchronized process that involves an intricate series of voluntary and involuntary neuromuscular contractions. This process is commonly divided into three distinct phases  —  the oral phase, the pharyngeal phase, and the esophageal phase. Given that each of these phases facilitates a specific essential function, a problem in one or more phases of the swallow constitutes dysphagia.

Oral Phase The oral preparatory and transfer phase of the swallow is under voluntary neural control and begins with the introduction of food material into the mouth. This phase is volitional and consists of a series of lip, tongue, and jaw movements that prepare the bolus for swallowing and propel it from the oral cavity to the pharynx. The duration of the oral phase is highly variable and depends not only on physical characteristics of the bolus such as taste, texture, and temperature, but also on external factors such as hunger, motivation, level of alertness, and the environment. This phase of the swallow requires complex sensory and motor integration.

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Box 4–1 Complex sensory input from taste, temperature, touch, and pressure mechanoreceptors travel via the trigeminal and facial nerves to the brainstem. It is here that information is integrated and stereotypic motor responses are generated. The initial phase of the swallow comprises two components. The first component is the oral preparatory phase whereby bolus manipulation occurs. This is followed by oral transfer, during which the tongue propels the bolus posteriorly toward the oropharynx for transfer. This sequence of events is accomplished by the actions of the suprahyoid muscles that facilitate the elevation of the tongue required for efficient bolus manipulation. Control of the bolus within the oral cavity is enhanced through the contraction of the orbicularis oris and buccinator muscles in the lips and cheeks, respectively. These muscles are essential for the containment of the bolus within the oral cavity prior to its transfer posteriorly, where the pharyngeal phase of swallowing will be initiated. In infants, the oral phase consists entirely of sucking, and the suck–swallow pattern must be coordinated with the cessation of respiration. This synchrony with respiration is under the control of the brainstem. There is steady maturation of control centers in the medulla, specifically regions of the nucleus ambiguus, nucleus tractus solitarius, and the hypoglossal nucleus. Rhythmic stability of the suck–swallow patterns follow a predictable maturational sequence.1,2 Feeding difficulties in infants are often the first sign of congenital or acquired injury or abnormalities to the central nervous system (CNS).

Pharyngeal Phase The pharyngeal phase of swallowing is reflexive and is triggered by the transfer of the bolus into the pharynx by the tongue with simultaneous hyolaryngeal elevation, epiglottic retroversion, and airway closure.

The intensity and duration of the muscle activity associated with the swallow is influenced by the consistency and size of the bolus.3 The main propulsive force acting on the bolus through the hypopharynx is generated by tongue-base retraction, with subsequent contraction of the pharyngeal musculature and shortening of the pharynx. Afferent (sensory) innervation of the pharyngeal phase of the swallow occurs via the trigeminal, facial, glossopharyngeal, and vagus nerves. Innervation of the larynx, pharynx, and epiglottis is provided by the internal branch of the superior laryngeal nerve of CN X. The recurrent laryngeal nerves of CN X provide afferent innervation to the larynx below the level of the vocal folds. Efferent (motor) innervation is provided by the trigeminal, facial, glossopharyngeal, vagus, and hypoglossal nerves, as well as the cervical nerve roots of C1 and C2. Efferent innervation to the larynx occurs via CN X, causing vocal fold and arytenoid joint motion. Coordination of swallowing and respiration is essential to minimize the risk of aspiration. Central pattern generators (CPGs) send inhibitory stimulation to the respiratory centers in the brainstem to create a respiratory pause associated with swallowing. This pause is referred to as swallowing apnea or respiratory cessation. Box 4–2 The spinal cord runs through the spinal canal of the vertebral column. There are 7 cervical vertebrae (C1–C7), 12 thoracic vertebrae (T1–T12), and 5 lumbar vertebrae (L1–L5). Box 4–3 Central pattern generators (CPGs) integrate the sensory information that defines the physical characteristics of the bolus and produces a motor pattern sufficient to create an effective swallow to clear the bolus from the hypopharynx. CPGs also inhibit respiration with transfer of the bolus into the hypopharynx.



4. Three Phases of Swallowing

Esophageal Phase The esophageal phase of the swallow is under both voluntary (somatic) and autonomic nervous system control.4 It is longer in duration than the oral and pharyngeal phases, lasting from 7 to 15 seconds. As the bolus is forced by tongue-base retraction into the pharynx, hyolaryngeal elevation pulls the upper esophageal sphincter (UES) open. In the resting state, the UES receives tonic neural innervation to maintain closure. Inhibition of this tonic stimuBox 4–4 The upper esophageal sphincter (UES) is the area of the upper digestive tract that forms a barrier between the esophagus and the pharynx, but that intermittently opens and closes to allow passage of contents during various physiologic events. The UES is composed of the cricopharyngeus muscle, which inserts onto the lateral aspect of the cricoid cartilage. When the cricopharyngeus is relaxed, there is a kidney bean–shaped lumen through the sphincter. When this muscle is contracted, the lumen is functionally obstructed.

lation occurs as the bolus moves into the upper esophageal segment. The esophageal phase of swallowing begins with relaxation of the UES. It involves the coordinated peristaltic waves of contraction to propel the bolus into the stomach. Both striated (voluntary) and smooth (involuntary) muscles are involved with esophageal propulsion.

References 1. Gewolb IH, Vice FL, Schweitzer-Kenney EL, Taciak VL, Bosma JF. Developmental patterns of rhythmic suck and swallow in preterm infants. Devel Med Child Neurol. 2001;43(1):22–27. 2. Gewolb IH, Bosma JF, Taciak VL, Vice FL. Abnormal developmental patterns of suck and swallow rhythms during feeding in preterm infants with bronchopulmonary dysplasia. Devel Med Child Neurol. 2001;​43(7):​ 454–459. 3. Ruark JL, McCullough GH, Peters RL, Moore CA. Bolus consistency and swallowing in children and adults. Dysphagia. 2002;17(1):​ 24–33. 4. Ertekin C, Aydogdu I. Neurophysiology of swallowing. Clin Neurophysiol. 2003;114(12):​ 2226–2244.

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5 Respiration, Swallowing, and Protective Reflexes Claire Kane Miller, Lisa N. Kelchner, and Jay Paul Willging

CHAPTER OUTLINE Relationship Between Swallowing and Respiration Airway Protective Reflexes Laryngeal Adductor Reflex Pharyngoglottal Closure Reflex Esophagoglottal Reflex Laryngospasm Maturation of the Cough Sudden Infant Death Syndrome Brief Resolved Unexplained Events

Relationship Between Swallowing and Respiration The temporal relationship between swallowing and respiration is complex and is defined in terms of the respiratory phases that occur before and after swallowing. Although neural pathways are not fully defined, it appears that common motor neurons for both respiration and swallowing are triggered by interneurons localized in the dorsal swallowing group (DSG) and the ventral swallowing group (VSG) regions

of the brainstem.1 Once oral transfer of the bolus occurs, multiple simultaneous and sequential events rapidly follow. Specifically, mechanical closure of the larynx occurs simultaneously with central inhibition of respiratory activity; this is referred to as swallowing apnea (SA). Under volitional swallowing conditions, multiple cortical sites are involved that influence breathing and swallowing coordination. Five respiratory phase categories have been described.These categories include (1) Inspiration–SA–Inspiration (II); (2) Inspiration–SA–Expiration (IE); (3) Expiration–SA–

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Expiration (EE); (4) Expiration–SA–Inspiration (EI); and (5) Prolonged respiratory pause.2 Maturation of swallowing and respiratory coordination occurs with age. In healthy infants, SA has been shown to occur in all of the above patterns. The typical pattern for breathing and swallowing in healthy adults is during expiration (EE).2–4 To ensure protection of the airway as the bolus passes through the pharynx and into the upper esophageal sphincter in both infants and adults, there is a respiratory pause during both nutritive and non-nutritive swallowing.5–7 This respiratory pause is mediated by the central pattern generator (CPG) in the brainstem. In adults, SA has been shown to begin prior to the initiation of the pharyngeal swallow and end with the re-initiation of respiration during laryngeal descent following the swallow.8 In infants, the coordination of the suck–swallow–breathe sequence undergoes a period of maturation, particularly during the first month of life. In both preterm and term infants, repeated swallows may occur without respiratory activity between swallows. Research has shown that this pattern dissipates with maturation and transitions to a more coordinated suck–swallow–breathe pattern. The duration of the apneic pause during the swallow varies, but is approximately 1 second for adults9 and less than 1 second for infants.10 Frequent or prolonged episodes of apnea associated with feeding may be representative of immaturity or may be a sign of central nervous system (CNS) abnormality. Historically, it was thought that sucking and swallowing occurred as isolated events, with each occurring independently  — ​ thereby allowing simultaneous breathing and swallowing. Because of the relatively high position of the larynx in the infant, this relationship was considered to protect the larynx from the flow of liquid from the oral cavity through the lateral channels around the larynx. Over the past several decades, however, extensive study of infant respiratory dynamics during feeding has led to the

current view that swallowing suppresses respiration and that simultaneous breathing and swallowing do not occur. Multiple studies of respiratory patterns during infant feeding show that the timing of swallowing within the ventilatory cycle varies and is subject to maturational changes and underlying medical conditions.10–12 As postnatal myelination occurs, voluntary feeding behaviors emerge.13 Sucking has been documented in the human fetus as early as 15 weeks’ gestation. In preterm infants, the coordinated suck–swallow– breathe sequence does not emerge until 34 weeks’ gestation. Typically, the rhythm of the suck-swallow sequence is paused when the respiratory requirements of the infant reach a certain threshold; however, there are situations in which sucking and swallowing activity continues despite respiratory needs.14 This places premature infants with immature neural system development and even full-term infants with underlying cardiac, respiratory, or other complex medical conditions are at increased risk for airway compromise during oral feeding. When oxygen saturation falls below a certain point or carbon dioxide levels rise above a given level, the central respiratory centers in the brain will trigger an inspiratory event. This occurs regardless of the presence of food or liquid in the hypopharynx, creating the possibility of aspiration.

Airway Protective Reflexes As discussed earlier in this section, the ingestion of liquids or solids elicits a complex sequence of neuromuscular events that comprises the act of swallowing. To prevent aspiration, closure of the airway during the swallow must occur. Coughing, choking, and apneic events may occur in response to stimulation of the airway. Mechanoreceptors and chemoreceptors that are present in the pharynx and larynx provide affer-



5. Respiration, Swallowing, and Protective Reflexes

ent sensory information to the brainstem regarding the presence and nature of material in those anatomic regions. Integration of this sensory information then elicits a reflexive protective response when necessary to protect the airway. Such reflexes include the laryngeal adductor reflex (LAR), the pharyngoglottal closure reflex, the esophagoglottal reflex (EGR), laryngospasm, and the cough.15–19 Sudden infant death syndrome (SIDS) and brief resolved unexplained events (BRUE) are discussed below in the context of these reflexes. Box 5–1 Mechanoreceptors are specialized neurosensory receptors that respond to mechanical stimuli. Chemoreceptors are specialized neurosensory receptors that respond to chemical stimuli.

Laryngeal Adductor Reflex The LAR is characterized by immediate glottic closure in response to mechanical or chemical stimulation of the laryngeal mucosa. The integrity of this response was formerly assessed by delivering a puff-of-air stimulus from an endoscope positioned 1 to 2 mm above the arytenoid mucosa during laryngopharyngeal sensory testing; however, the equipment required for this assessment is no longer available. Responses that occurred at >4 mm Hg (millimeters of mercury) were considered to be abnormal.20,21 Elevated sensory thresholds and impairment of the LAR have been found in numerous conditions associated with dysphagia.19

Pharyngoglottal Closure Reflex The pharyngoglottal closure reflex consists of brief closure of the vocal folds in response to sensory stimulation within the pharynx. The maturation of this reflex has

been followed in premature infants and has been shown to parallel other maturational changes seen in sensorimotor pharyngeal reflex development. The intensity of the stimulus needed to elicit this reflex (air, water, volume) decreases with maturation.22

Esophagoglottal Reflex The esophagoglottal reflex (EGR) is triggered when there is vigorous distention of the proximal esophagus such that the upper esophageal sphincter (UES) relaxes and permits refluxed gastric contents to pass into the hypopharynx.23,24 The afferent limb of this reflex is carried by the recurrent laryngeal nerve, whereas the efferent limb is carried by multiple cranial nerves. Once triggered, the EGR results in the anterior and superior movement of the larynx and closure of the vocal folds. The refluxed material is either expelled from the mouth or swallowed prior to the opening of the vocal folds. This reflex is present throughout life.18,25 Were it not present, aspiration of refluxed material would occur, leading to serious medical sequelae such as pneumonia.

Laryngospasm Laryngospasm is defined as glottic closure due to reflexive constriction of the laryngeal muscles in response to laryngeal stimulation.26 It typically occurs during the excitability phase (stage II) of general anesthesia and cannot develop in the awake state. Stimulation of the larynx during this time (stage II) by secretions, blood, or instrumentation will result in complete closure of the glottis and complete airway obstruction. Treatment of laryngospasm with the use of continuous positive airway pressure via a mask or with the administration of a paralyzing agent must be initiated in a timely manner. Failure to do so may lead to a life-threatening situation.

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Maturation of the Cough Although the previously described pharyngeal and laryngeal protective reflexes are present throughout life, the cough response is rarely present at birth. The predominant airway protective mechanisms during the neonatal period are apnea, swallowing, and laryngeal closure.27,28 Research on the emergence of the cough in the neonate has involved studies of laryngeal chemoreflexes (LCR) stimulated by fluids (saline or water) that come in contact with the mucosa of the larynx. Findings in animal studies suggest that maturation of LCR is consistent with an increase in coughing and a decrease in apneic and swallowing responses. Results of human studies suggest that coughing is infrequent in both preterm and term neonates. In term infants, a brief respiratory pause with one or two swallows has been found to be typical with the introduction of a bolus of water into the pharynx under test conditions. In contrast, a prolonged apneic response combined with bradycardia has been reported in preterm infants. As infants mature, rapid swallowing and apnea decrease, whereas the cough response and laryngeal constriction become more prominent in airway protection.27,28

Sudden Infant Death Syndrome Sudden infant death syndrome (SIDS) refers to the unexpected sudden death of a sleeping infant ranging in age from 1 to 6 months. Death from SIDS is unrelated to any identifiable disease or injury. Given the reported association between SIDS and gastroesophageal reflux (GER) in infants, the American Academy of Pediatrics has recommended that infants be positioned supine (on their back) during sleep, as this position reduces the risk of GER. Hypomyelination of the nervous system has also been implicated in this syndrome, as there is persistent immaturity of the neural control mechanisms for breathing and swallowing.29 If a reflux event does occur, the EGR

will close the larynx and induce a swallow to clear the material. Vocal fold opening will not occur until this clearing swallow occurs. Depending on the volume associated with the reflux event, multiple swallows may be required to clear the pharynx.

Brief Resolved Unexplained Events BRUE (brief resolved unexplained event), formerly referred to as an apparent lifethreatening event (ALTE), are defined as abrupt and unexplained occurrences of breathing abnormalities, often accompanied by choking, color change, and altered muscle tone. These events typically occur in children younger than 1 year of age. The subsequent evaluation to identify causes may involve clinical assessment of oral motor and feeding skills as well as instrumental studies of swallowing function. Although a definitive cause for BRUE is identified in only 50% of cases,30 possible causes include the following: gastrointestinal (GER and swallowing difficulty); neurologic (central or obstructive sleep apnea, neurologic variant laryngomalacia, seizures, intracranial bleeding, meningitis, CNS abnormalities, and brain tumor); respiratory (respiratory infections, pneumonia, and foreign body aspiration); metabolic (electrolyte disturbance, hypoglycemia, and metabolic disorders); cardiovascular (congenital heart disease, cardiomyopathy, arrhythmias); drugs; and non-accidental injury (factitious disorder imposed on another, formerly known as Munchausen syndrome by proxy). In some cases, infants presenting with BRUE die and may subsequently be classified as SIDS.

References 1. Jean A. Brain stem control of swallowing: neuronal network and cellular mechanisms. Physiol Rev. 2001;81(2):929–969. 2. Martin-Harris B, Brodsky MB, Price CC, Michel Y, Walters B. Temporal coordina-



5. Respiration, Swallowing, and Protective Reflexes

tion of pharyngeal and laryngeal dynamics with breathing during swallowing: single liquid swallows. J App Physiol. 2003;94(5):​ 1735–1743. 3. Martin B, Logemann J, Shaker R, Dodds W. Coordination between respiration and swallowing: respiratory phase relationships and temporal integration. J App Physiol. 1994;76(2):714–723. 4. Hiss SG, Treole K, Stuart A. Effects of age, gender, bolus volume, and trial on swallowing apnea duration and swallow/respiratory phase relationships of normal adults. Dysphagia. 2001;16(2):128–135. 5. Hiss SG, Strauss M, Treole K, Stuart A, Boutilier S. Swallowing apnea as a function of airway closure. Dysphagia. 2003;18(4):293–300. 6. Martin-Harris B, Brodsky MB, Michel Y, Ford CL, Walters B, Heffner J. Breathing and swallowing dynamics across the adult lifespan. Arch Otolaryngol Head Neck Surg. 2005;​ 131(9):762–770. 7. Stevenson RD, Allaire JH. The development of normal feeding and swallowing. Pediatr Clin North Am. 1991;38(6):1439–1453. 8. Palmer JB, Hiiemae KM. Eating and breathing: interactions between respiration and feeding on solid food. Dysphagia. 2003;​ 18(3):​169–178. 9. Treole K, Stuart A. Effects of age, gender, bolus volume, and trial on swallowing apnea duration and swallow/respiratory phase relationships of normal adults. Dysphagia. 2001;16(2),128–135. 10. Kelly BN, Huckabee ML, Jones RD, Frampton. Nutrtive and non-nutritive swallowing apnea duration in term infants: implications for neural control mechanisms. Respir Physiol Neurobiol. 2006;154(3):372–378. 11. Kelly BN, Huckabee M-L, Jones RD, Frampton CM. The early impact of feeding on infant breathing–swallowing coordination. Respir Physiol Neurobiol. 2007;156(2):147–153. 12. Lau C, Smith E, Schanler R. Coordination of suck‐swallow and swallow respiration in preterm infants. Acta Paediatr. 2003;92(6):​ 721–727. 13. Rogers B, Arvedson J. Assessment of infant oral sensorimotor and swallowing function. Ment Retard Devel Disabil Res Rev. 2005;​ 11(1):​74–82. 14. Goldfield EC, Richardson MJ, Lee KG, Margetts S. Coordination of sucking, swallowing, and breathing and oxygen saturation

during early infant breast-feeding and bottle-feeding. Pediatr Res. 2006;60(4):450–455. 15. Shaker R, Li Q, Ren J, et al. Coordination of deglutition and phases of respiration: effect of aging, tachypnea, bolus volume, and chronic obstructive pulmonary disease. Am J Physiol. 1992;263(5):G750–G755. 16. Shaker R, Ren J, Bardan E, et al. Pharyngoglottal closure reflex: characterization in healthy young, elderly and dysphagic patients with predeglutitive aspiration. Gerontology. 2003;49(1):12–20. 17. Jadcherla SR, Gupta A, Coley BD, Fernandez S, Shaker R. Esophago-glottal closure reflex in human infants: a novel reflex elicited with concurrent manometry and ultrasonography. Am J Gastroenterol. 2007;1 ​ 02(10):​ 2286–2293. 18. Jadcherla SR, Hogan WJ, Shaker R. Physiology and pathophysiology of glottic reflexes and pulmonary aspiration: from neonates to adults. Paper presented at: Seminars in Respiratory and Critical Care Medicine, 2010. 19. Broussard DL, Altschuler SM. Central integration of swallow and airway-protective reflexes. Am J Med. 2000;108 (Suppl 4a):​ 62S–67S. 20. Link DT, Willging JP, Cotton RT, Miller CK, Rudolph CD. Pediatric laryngopharyngeal sensory testing during flexible endoscopic evaluation of swallowing: feasible and correlative. Ann Otol Rhinol Laryngol. 2000;​ 109(10):​899–905. 21. Martin JH, Thomson JE, Aviv JE, et al. Laryngopharyngeal sensory discrimination testing and the laryngeal adductor reflex. Ann Otol Rhinol Laryngol. 1999;108(8):725–730. 22. Kahrilas PJ, Logemann JA. Volume accommodation during swallowing. Dysphagia. 1993;8(3):259–265. 23. Rudolph CD. Feeding disorders in infants and children. J Pediatr. 1994;125(6):S116–S124. 24. Shaker R, Hogan WJ. Reflex-mediated enhancement of airway protective mechanisms. Am J Med. 2000;108(4):8–14. 25. Jadcherla SR, Gupta A, Stoner E, Fernandez S, Shaker R. Pharyngeal swallowing: defining pharyngeal and upper esophageal sphincter relationships in human neonates. J Pediatr. 2007;151(6):597–603. 26. Hampson-Evans D, Morgan P, Farrar M. Pediatric laryngospasm. Pediatr Anesth. 2008;​18(4):303–307.

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27. Thach BT. Maturation and transformation of reflexes that protect the laryngeal airway from liquid aspiration from fetal to adult life. Am J Med. 2001;111(8):69–77. 28. Thach BT. Maturation of cough and other reflexes that protect the fetal and neonatal airway. Pulm Pharmacol Ther. 2007;​20(4):​ 365–370.

29. Reix P, St‐Hilaire M, Praud JP. Laryngeal sensitivity in the neonatal period: from bench to bedside. Pediatr Pulmonol. 2007;42(8):​ 674–682. 30. Ross-Russell R, Ravikumar K. Apparent lifethreatening episodes in children. Paediatrics and Child Health. 2007;17(5):188–192.

Section

3

Oral Motor Development

6 Oral Motor Development Claire Kane Miller, Aliza P. Cohen, and Jay Paul Willging

CHAPTER OUTLINE Introduction Oral, Pharyngeal, and Laryngeal Reflexes Adaptive Reflexes Rooting Suckling and Sucking Phasic Biting Transverse Tongue Reflex Protective Reflexes Cough Reflex Gag Reflex The Development of Oral Motor Feeding Skills The Emergence and Maturation of Sucking Behavior Non-nutritive and Nutritive Sucking Skills The Mechanics of Sucking Coordination of Respiration, Sucking, and Swallowing The Specifics of Breastfeeding Breastfeeding Issues Consulting a Lactation Specialist The Shift from Reflexive to Volitional Sucking (3 to 5 Months) The Development of Spoon-Feeding Skills (5 to 7 Months) The Development of Chewing Skills (7 Months to 2 Years) Jaw and Tongue Movements Involved in Chewing Lip Movements Involved in Chewing The Development of Biting Skills The Transition to Cup-Drinking

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Texture Progression Muscle Tone and Movement Function of the Oral Structures — Limiting Patterns Persistent Primitive Oral Reflexes Limitations in Jaw Movement Limitations in Tongue Movement Limitations in Lip and Cheek Movement The Role of Sensory Processing and Discrimination

Introduction Normal development of oral motor skills occurs in a predictable progression that reflects the simultaneous maturation of the central nervous system (CNS). Oral motor skills for feeding normally advance from early oral reflexive behaviors mediated by the brainstem to volitional oral movements. Suckling and sucking during bottle feeding and breastfeeding are gradually replaced by cup feeding, and the intake of pureed foods progresses to the intake of foods with increased viscosity and texture. Eventually, the development of active biting and mastication of a broad range of solids occurs. Self-feeding skills develop concurrently, as the infant progresses from total dependency on the feeder to independent finger-feeding and the use of utensils during the intake of both liquids and solids. This chapter describes the development of oral motor feeding skills and the factors that impact the normal progression of these skills.

Oral, Pharyngeal, and Laryngeal Reflexes Oral, pharyngeal, and laryngeal reflexes develop in utero and play a major role in early infant feeding by supporting the inter-

action of the muscles of the lips, cheeks, tongue, palate, and pharynx. These reflexes are categorized as either adaptive or protective, and their presence or absence yields important information regarding an infant’s neurologic maturity.1,2 Adaptive reflexes include rooting, suckling/sucking, phasic biting, and the transverse tongue reflex. The gag and cough are protective reflexes (Table 6–1). Box 6–1 Adaptive reflexes such as rooting and sucking assist the infant in seeking nutrition. Protective reflexes such as the cough and gag protect the airway from aspiration.

Adaptive Reflexes Rooting The rooting reflex aids the infant in locating the food source and is typically present by 32 weeks’ gestation.1,3 Rooting can be elicited by touching or stroking infants’ lips or cheeks. This tactile input elicits a head turn toward the stimulus and infants spontaneously open their mouth. If the rooting reflex is absent or diminished, this may signal either reduced sensory responsiveness or impaired neural integration, resulting in difficulty with the initiation of sucking.

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Touch to side lower gum ridge or lateral edge of tongue

Touch to posterior tongue or pharynx

Adaptive

Adaptive

Adaptive

Adaptive

Protective

Protective

Suckling

Sucking

Phasic biting

Transverse tongue

Gag

Cough

Foreign material that enters the upper airway; stimulation to the bronchial receptors by excessive secretions

Touch to gums

Tactile contact of nipple to tongue; tactile input to tongue

Tactile contact of nipple to tongue; tactile input to tongue

Touch or stroke to infant’s lips or cheeks

Adaptive

Rooting

Stimulus

Reflex Type

Reflex

Table 6–1. Oral, Pharyngeal, and Laryngeal Reflexes

Reflexive coughing

Sideways tongue movement toward stimulus

Infancy

26 to 27 weeks gestation

28 weeks gestation

28 weeks gestation

Rhythmical biterelease pattern of jaw opening and closing

Persists

~6 months

Persists

Diminishes

V VII IX XII

V VII IX XII

V VII XI XII

CN X

CN IX CN X

CN XII

CN V

CN CN CN CN

Persists

34 weeks gestation (can usually be seen on ultrasound at 15 to 18 weeks gestation)

CN CN CN CN

~6 months

18 weeks gestation

CN CN CN CN

Cranial Nerve Input

3 to 6 months

Disappearance

32 weeks gestation

Emergence

Up and down tongue movements during sucking

Backward and forward tongue motion; up and down jaw movements

Infant turns toward stimulation to find food source

Behavior

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Pediatric Dysphagia: Etiologies, Diagnosis, and Management

In contrast, excessive rooting may be indicative of hypersensitivity to tactile input or lack of inhibition to the stimulus, which may also interfere with sucking initiation.2 Rooting typically diminishes as the neurologic system matures and generally disappears by 6 months of age. A persistent rooting response to tactile stimulation may be a sign of neurologic immaturity or impairment.

Suckling and Sucking The term “suckling” is used by some authors to describe the earliest sucking pattern in infants. Suckling is described as a rhythmic forward-backward motion of the tongue in conjunction with a distinct opening and closing of the jaw with loose lip approximation on the nipple. Sucking is characterized by an updown movement of the tongue with smaller jaw excursions and firmer approximation of the lips on the nipple. Many infants up to 6 months of age use a combination of suckling and sucking patterns. In neonates, sucking is reflexive; however, by 4 to 6 months of age, there is a gradual transition to volitional control.4 The sucking reflex in early infancy is a patterned response involving integrated movements of the jaw, tongue, and lips. The reflexive component of sucking aids the infant in obtaining nourishment and is elicited by oral tactile input to the lips or tongue by a nipple, finger, or pacifier. The stimulus is typically drawn into the infant’s mouth and a rhythmic sucking action ensues. If the stimulus is removed during active sucking, infants will seek the stimulus by flexing their head. An absent or inconsistent reflexive sucking response may be indicative of a depressed neurologic status.

Phasic Biting The phasic (repetitive or alternating movement) bite reflex is stimulated by tactile input to the gums and is characterized by a

rhythmical bite–release pattern of jaw opening and closing. This reflex diminishes by 9 to 12 months of age. Persistence of this reflexive behavior takes the form of a tonic bite — a forceful biting pattern in which the child has difficulty releasing. A tonic bite significantly interferes with all aspects of feeding and indicates neurologic impairment.

Transverse Tongue Reflex The transverse tongue reflex is a sideways movement of the tongue toward a touch to one side of the lips or tongue. This reflex persists and is helpful in the development of lateral tongue movements required for bolus manipulation.

Protective Reflexes Cough Reflex The cough is a protective reflex to expel foreign material from the airway. It is triggered by material that enters the upper airway or by stimulation to the laryngeal, tracheal, or bronchial receptors. Protection from aspiration is mediated through the laryngeal adductor reflex (LAR), which is triggered by mechanical or chemical stimulation of the laryngeal mucosa.

Gag Reflex The gag reflex is stimulated by mechanical pressure to the receptors located on the posterior aspect of the tongue, soft palate, uvula, or pharyngeal wall. In newborns, the gag response may also be elicited by receptors on the mid-portion of the tongue. As infants mature, this reflex is elicited further back on the tongue. Although there is no direct relationship between the gag reflex and swallowing ability, an absent or diminished gag as well as a hyperactive gag may be indicative of a neurologic issue involving cranial nerves IX (glossopharyngeal) and X



6. Oral Motor Development

(vagus), which affect other aspects of the swallow. The gag reflex typically diminishes by 6 months of age.

The Development of Oral Motor Feeding Skills Feeding and swallowing in the neonatal period is an intricate process that requires infants to coordinate respiration with the rhythm of sucking and swallowing (Figure 6–1). Sucking behavior is reflexive and mediated by the brainstem, as are the neural mechanisms controlling the cessation of respiration that protect the airway from aspiration during swallowing. The transition to voluntary control of oral motor skills and the subsequent maturation of feeding

skills coincides with patterns of myelination in the brain.4 Thus, any abnormality in the infant feeding process may be a warning signal of compromised neurologic integrity.

The Emergence and Maturation of Sucking Behavior Sucking behavior has been documented in utero as early as 15 to 18 weeks’ gestation. Organization of a sucking burst–pause pattern emerges at approximately 32 weeks’ gestation.5 By 34 weeks, a stable rhythm during sucking generally becomes consistent. To support efficient sucking, alignment of the head, neck, and trunk is essential. A variety of positions may be used; for example, supine with slight elevation of the head, reclining at an angle of less than

Figure 6–1.  Lateral view of the upper aerodigestive tract, with surrounding structures.

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Pediatric Dysphagia: Etiologies, Diagnosis, and Management

45  degrees, or side-lying (Figure  6–2). In view of the postural tone in infants younger than 3 months of age, the goals of positioning include (1) keeping the infant in flexion, (2) maintaining orientation of the head and extremities around the midline and shoulders in a symmetric and forward position, (3) maintaining hip flexion at a 45- to 90degree angle, and (4) maintaining neutral anterior-posterior alignment of the head and neck.2,6

Non-Nutritive and Nutritive Sucking Skills Sucking may be nutritive or non-nutritive. Nutritive sucking refers to sucking that occurs in seeking nutritive input, whereas

Figure 6–2.  Infant in side-lying position. Source: Courtesy of Cincinnati Children’s Hospital Medical Center, Division of SpeechLanguage Pathology.

non-nutritive sucking refers to sucking that occurs without nutritive input (ie, with the use of a pacifier, oral motor toy, or fingers). The rate of non-nutritive sucking, which is 2 sucks per second, is generally faster than nutritive sucking and is associated with a series of brief pauses and bursts.5 However, the rate of swallowing with nonnutritive sucking is lower than that associated with nutritive sucking. The ability to demonstrate a non-nutritive sucking pattern does not necessarily ensure successful oral feeding; however, the ability to establish a non-nutritive sucking pattern is essential for beginning the transition to oral feeding.2

The Mechanics of Sucking In the neonate, the jaw provides a stable base for the movements of the tongue, lips, and cheeks. The sucking pads in the cheeks, which are composed of subcutaneous fat, passively provide positional stability to the tongue in order to support efficient sucking action. The lips work with the tongue to form an anterior seal around the nipple and help to stabilize the position of the nipple intraorally. The tongue forms a “central groove” that stabilizes the nipple and helps to direct the fluid posteriorly for swallowing. As the tongue compresses the nipple, positive pressure is created that expels liquid (Figure 6–3). The jaw and tongue drop down during sucking, generating negative intraoral pressure (suction) to pull fluid into the mouth. During sucking, the jaw moves downward in a rhythmic manner, enlarging the oral cavity; this facilitates the generation of suction. The palate and the tongue function together to maintain nipple position and compress the nipple. The ability to generate adequate negative pressure and suction is crucial to efficient liquid flow during infant feeding. Achieving and sustaining rhythmicity of sucking is the key component of normal infant sucking, combined with appropriate sucking strength, and coordinated movement of the



6. Oral Motor Development

Figure 6–3. A. The tongue compresses the nipple, and the positive pressure within the nipple expresses the liquid into the mouth. B. As the jaw and tongue descend during sucking, negative intraoral pressure is generated, and the suction force pulls fluid from the nipple into the mouth. Source: Courtesy of Joseph P. Willging.

oral structures. Disorganized, arrhythmic, and inefficient sucking behavior may occur with conditions such as prematurity, neuromotor disorders, chronic lung disease, and cardiorespiratory conditions. Box 6–2 The key components of normal infant sucking involve coordinated oral motor movements, appropriate sucking strength, and sustained rhythmicity.2 The development of efficient sucking occurs in stages, which are characterized by the presence or absence of the suction, the expression of breastmilk or formula while sucking, the frequency of sucking, and the rhythmicity of sucking.7 Mature sucking is characterized by rhythmic alternation of suction and expression. In contrast, immature sucking is marked by arrhythmic expression efforts coupled with lack of suction.7 The efficient flow of liquid to ensure an adequate volume of intake and nutrition requires the infant’s ability to generate adequate and rhythmic negative pressure and suction. Infants who are able to compress the nipple but who cannot generate suction will require some modification of the bottle

or nipple to aid liquid flow and intake during feeding. For example, infants with cleft palate have difficulty with liquid extraction because the open palate provides little surface area for the tongue to work against in order to compress the nipple. A reduction in both positive pressure (compression) and negative pressure (suction) results in impaired feeding ability, thus necessitating feeding modifications. Infants with neuromotor deficits and weak sucking efforts may also need special adaptations of the bottle or nipple system, such as changes in nipple type or flow rate to accommodate oral phase deficits.

Coordination of Respiration, Sucking, and Swallowing Safe and efficient nutritive sucking is an important indicator of normal development in early infancy that requires complex coordination between sucking, swallowing, and respiration. Intact brainstem pathways and cranial nerve function are essential. Investigations of the coordination of respiration and swallowing in normally developing infants during the first year of life show that respiration is suspended during swallowing — an event referred to as swallowing

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Pediatric Dysphagia: Etiologies, Diagnosis, and Management

apnea.8,9 For example, research conducted by Kelly et al8 documented swallowing apnea intervals of approximately (~) 0.672 seconds during nutritive swallowing and ~1.03 seconds during non-nutritive swallowing in a group of infants younger than 12 months of age. Preterm infants who are born prior to 34 weeks’ gestation have difficulty with coordination of sucking, swallowing, and respiration due to neurologic immaturity and the inability to coordinate the demands of ventilation and the respiratory effort of oral feeding.10,11 Studies of swallowing apnea duration as an indicator of feeding maturity show that the maturation is related to developmental age (postmenstrual age). Box 6–3 A post-menstrual age of 34 weeks is equivalent to a gestational age of 30 weeks plus a chronological age of 4 weeks. Clinical application: given that infants are not expected to have the neurologic maturity to support feeding until 34 weeks’ gestation, infants born at 30 weeks require an additional 4 weeks of chronological age before being expected to have the ability to feed. In the healthy infant, nutritive sucking is typified by burst–pause sucking patterns. These patterns are described as continuous, intermittent, or paused.12–15 A sucking burst is defined as a series of sucking events occurring with a typical frequency of 1 Hz followed by a pause of ~2 seconds prior to the next sucking burst.5 At the start of an oral feeding, infants engage in a continuous phase during which sucking is vigorous and continuous in relatively long sucking bursts. This phase is typically followed by an intermittent phase during which the sucking burst is shorter and the sucking is less vigorous, with longer pauses. The final paused phase consists of sporadic bursts of sucking that are less vigorous than the initial or intermittent phases.

The Specifics of Breastfeeding Breastfeeding and bottlefeeding involve distinctly different oral motor patterns.16–18 There are differences in the method of latching onto the breast as opposed to the nipple on a bottle, the sucking pressure required, the position and action of the tongue during sucking, the rate of sucking, and the pattern of milk flow. The rooting reflex is initiated by tactile stimulation of the nipple to the perioral area, which causes infants to turn their head toward the source of stimulation. The mother guides the infant to the breast to facilitate latching onto the breast to elicit the sucking reflex. A technique used to increase the depth of the baby’s latch is referred to as the “deep latch” technique. Box 6–4 The “deep latch” technique can be used to increase the depth of the baby’s latch. On the underside of the breast, the mother uses her fingers to compress the breast well back from the areola. She simultaneously uses her thumb for compression on the upper side of the breast, near the areola. The mother holds her baby with the opposite hand, placing her fingers on the side of the baby’s lower jaw. Holding the chin, she then directs the infant’s nose to the nipple, allowing the infant to latch with the lower jaw. She then guides the nipple into the baby’s mouth. During breastfeeding, the mother’s milk ejection, referred to as the “let-down” reflex, occurs during the first 1 to 3 minutes of sucking. The sucking rate within this period is relatively high in response to the high outflow of breastmilk. Infants who are unable to handle this increased flow rate will demonstrate disorganized swallowing patterns or a cough/choke response. Once this reflex subsides, the rate of nutritive sucking decreases to a rate similar to



that during bottlefeeding (one suck per second). Early studies by Ardran et al and Woolridge16,17 first described the mechanisms by which an infant removes milk from the breast. The nipple, with surrounding and underlying breast tissue, is elongated in the mouth by the suction created in the infant’s mouth. The nipple extends to the junction of the hard and soft palate. The lateral borders of the tongue cup around the nipple and form a central groove or trough to position it. Milk is expressed and propelled posteriorly by a rolling, peristaltic action of the tongue along the underside of the nipple. The negative suction pressure and positive compression pressure components work synchronously to maintain the position of the nipple and the flow of milk. The rates of non-nutritive and nutritive sucking vary during breastfeeding. Nonnutritive sucking occurs in short bursts at a rate of up to two sucks per second, generally prior to milk let-down or ejection. Nutritive sucking occurs at a slower rate, approximately one suck per second, in a continuous stream. As the feeding progresses, the sucking is characterized by a series of bursts with longer pauses in between. At the beginning of each sucking burst, the faster sucking rate may reoccur, presumably to restart the flow of milk from the breast.19 Breastfeeding Issues.  Inefficient, ineffec-

tive breastfeeding may occur as a result of behavioral, structural, or oral motor problems. If infants are compromised to the point at which their energy levels and endurance are poor, as is the case in infants with congenital heart conditions, feeding will be difficult. They must be in a physiologic state that supports the effort required for feeding. The inability to maintain appropriate feeding behavior and general alertness negatively impacts the ability to breastfeed. Structural problems may complicate the ability to breastfeed successfully. If oral opening is limited, the ability to accept the

6. Oral Motor Development

nipple may not be possible. Micrognathia may be associated with abnormal tongue positioning. A short lingual frenulum (ankyloglossia) may adversely affect tongue tip motion, whereas a thick upper lip frenulum may interfere with the ability to obtain a lip seal against the breast. In addition, immature oral motor skills negatively affect the ability to breastfeed. Excessive jaw motion during sucking negatively affects sucking efficiency. Inappropriate tongue tip elevation with mouth opening interferes with optimal placement of the nipple onto the body of the tongue. The lack of central grooving of the tongue makes it difficult to maintain the proper position of the nipple within the oral cavity. Tongue retraction prevents adequate contact between the nipple and the dorsum of the tongue for optimal suction and compression of the breast nipple. Consulting a Lactation Specialist. Com-

mon problems associated with breastfeeding that may arise during a clinical feeding assessment include problems with latching, breast pain, breast infection, inadequate milk supply, and failure of the let-down reflex. Given that some of these problems are outside the scope of practice for a speech-language pathologist (SLP), an International Board Certified Lactation Consultant with specialized training in the clinical management of breastfeeding is sometimes asked to provide consultation. The pediatric SLP may collaborate with the lactation consultant during the clinical feeding evaluation or be asked to consult on oral motor issues that may be contributing to difficulty with breastfeeding.

The Shift from Reflexive to Volitional Sucking (3 to 5 Months) By approximately 3 months of age, infant sucking transitions from a reflexive action to a volitional behavior. Although the sucking pads in the cheeks continue to pro-

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Pediatric Dysphagia: Etiologies, Diagnosis, and Management

vide positional stability for the tongue and nipple, they gradually disappear. When the infant reaches approximately 6 to 8 months of age, the muscles in the cheeks provide stability to support effective sucking. As the infant develops head, neck, and trunk control, positioning during feeding also changes. At 3 months, infants can generally be positioned in a reclining or sitting position ranging from a 45- to a 90-degree angle.

The Development of Spoon-Feeding Skills (5 to 7 Months) Breastmilk, formula, or both are the primary sources of nutrition during the first several months of life. Given the immaturity of the digestive system during the first 3 months of life, pureed foods are generally not presented to infants younger than 4 months of age. Depending on advice from the family pediatrician as well as parent and infant readiness, spoon-feeding may be introduced at 4 to 6 months of age. This period is referred to as “transitional feeding.” Readiness to transition to spoon-feeding is related to continued development of the CNS and well-defined anatomic changes. Anatomic changes with growth create increased space in the oral cavity that occurs with the downward and forward growth of the mandible. The absorption of the sucking pads in the cheeks creates additional intraoral space, facilitating bolus manipulation and transfer for swallowing. Between 6 and 24 months of age, the gradual eruption of deciduous teeth occurs, with eruption of all teeth typically by 2 years of age. Neural development is reflected in the inhibition of the previously described oral reflexive behaviors. Neural maturation together with musculoskeletal growth, motor learning, and peripheral afferent input from the oral cavity provided by the teeth enable the development of chewing skills.20

By 5 to 6 months, the infant can be placed in a supported sitting position at 90 degrees. The beginning stage of spoonfeeding is characterized by the use of the early suckling movement of the tongue in response to the tactile contact of the spoon to the lower lip. Typical foods offered at this stage include commercial baby foods or age-appropriate home-prepared foods blenderized to a thin pureed texture. Rather than using the upper lip to assist in removing the food from the spoon, infants typically use a suckling pattern of the tongue. Anterior loss of the food is caused by the forward-backward motion of the tongue and the lack of lip closure on the spoon. Gradually, visual recognition of the spoon develops, and the infant begins to exhibit anticipatory mouth opening when the spoon is seen. The tongue is held in a static position within the mouth in anticipation of the spoon, and the active front-back suckle tongue motion ceases. The stable tongue position facilitates placement of the spoon by the feeder onto the body of the tongue; this is a prerequisite for the development of upper lip motion to remove food from the spoon. Generally, by 6 months of age, infants begin to bring their upper lip down on the spoon. At 6 to 9 months, the upper lip moves both downward and inward to remove the food from the bowl of the spoon. The lower lip also becomes active in moving inward during presentation of the spoon. By approximately 12 to 15 months of age, children have learned to use the upper central incisors to clear food from the lower lip as it draws inward. By age 24 months, children display a mature pattern during spoon-feeding. They are able to achieve lip closure on the spoon, smooth anterior-posterior tongue movements to transfer food for swallowing, and active tongue movements to clean food from the upper and lower lips. The developmental sequence for spoon-feeding skills with semi-solid or pureed foods is presented in Table 6–2.



6. Oral Motor Development

Table 6–2. Developmental Sequence for Progression of Spoon-Feeding Skills Age Range

Skill

~3 to 4 months

Suckle response when presented with puree on spoon; anterior loss of bolus is typical

6 to 7 months

Visual recognition and anticipatory mouth opening; forward–backward tongue movements in response to purees; minimal anterior loss, as bolus is transferred for swallowing

8 to 9 months

Transition to up and down tongue motion; intermittent forward–backward tongue movements for bolus transfer

9 to 12 months

Lip closure with swallowing; tongue tip elevation with up–down tongue motion to transfer bolus for swallowing

12 to 18 months

Forward–backward movements of tongue are rare; tongue tip elevation during swallowing initiation is common; occasional tongue protrusion

18 to 24 months

Tongue tip elevation during bolus transfer for swallowing; no anterior loss of bolus; no tongue protrusion during bolus transfer

The Development of Chewing Skills (7 Months to 2 Years)

Jaw and Tongue Movements Involved in Chewing

The development of chewing skills depends on continued neural development and musculoskeletal growth, as well as sensory input (ie, exposure to chewable solids) and motor learning.20 Development of trunk and pelvic stability continues, and infants are able to be placed in a sitting position for presentation of solids. Several authors have described time periods that are critical for the acquisition of chewing skills.21,22 Children who are not exposed to the chewable solids during these sensitive time periods (6 to 7 months of age ) may have later difficulty learning to chew, subsequently developing an aversion to solids.21 Jaw, lip, and tongue movements involved in the acquisition of chewing skills are discussed below (Table 6–3).

A child’s initial chewing attempts are typically characterized by up and down jaw movements, referred to as vertical chewing. By ~9 months of age, vertical jaw motions are combined with diagonal jaw movements and the child begins to use lateral tongue movements for bolus manipulation prior to swallowing. Eruption of the deciduous teeth enables efficient biting and chewing to mechanically break down foods prior to transfer for swallowing. If food material is placed on the lateral tooth or gum surface, the tongue and jaw will move toward that side. Rotary (circular) jaw action emerges between 2 and 3 years of age. This action is characterized by a swinging motion of the jaw as the tongue carries the food to the op-

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Table 6–3. Development of Lip, Tongue, and Jaw Movements for Chewing Age Range

Lip, Tongue, and Jaw Motion in Response to Solids

5 to 6 months

Phasic biting predominates

6 to 9 months

Upper or lower lip may draw inward with presentation of food Cheek and lip tense with side placement of food to hold in place for chewing. Vertical jaw movements emerge during attempts at mastication. Intermittent phasic biting occurs Diagonal jaw movement occurs in response to food placed on the surface of the gum Lateral tongue movements begin to emerge

9 to 12 months

Upper and lower lips pull in with presentation of food to the lip Begin to see active lip motion in conjunction with jaw motion Lips make contact in the center or the side as the jaw moves up and down during chewing Upper lip may move forward and downward during chewing Vertical jaw movement occurs with intermittent diagonal jaw motion Tongue moves food from the center to the side of the mouth during chewing

12 to 15 months

Lips become active during chewing Upper incisors or gums are used to clear food from the lower lip There is occasional loss of food or saliva while chewing Diagonal rotary jaw movements increase

15 months to 24 months

Upper and lower lips are active during chewing Ability to chew with the lips closed develops Ability to control food intraorally without anterior loss when lips are open emerges Corner of lip and cheek draw inward to assist with control of food placement Jaw movements range between vertical, diagonal, and rotary Circular rotary chewing occurs when transferring food across the midline of the tongue from one side of the mouth to the other

24 months and beyond

Basic set of skills is in place for chewing; movements are refined as the child continues to develop strength and efficiency of chewing

posite side of the oral cavity. This circular swing motion is referred to as “circular rotary movement.” It occurs as the tongue moves food from one side of the mouth across the

midline to the opposite side. The rotary chewing pattern is typically used with firm or tougher foods that require extensive bolus manipulation prior to transfer for swallowing.



Lip Movements Involved in Chewing At approximately 6 months of age, infants pull in the upper and lower lip as food is presented. If food is presented at the side of the mouth, the infant typically displays an increased tension in the lips and cheeks to prevent it from falling into the lateral sulcus. The lips become more active with jaw motion, beginning to approximate as the jaw moves up and down during chewing. The upper lip may also move forward. Some anterior loss of food during chewing occurs. As infants approach 1 year of age, the incisors or gum surfaces are used to clear food off the lower lip and tension in the cheeks helps to control the position of the food in the mouth. By 18 months of age, children begin to demonstrate the ability to maintain lip closure while chewing, though they will often continue to chew with their lips open; this may result in some anterior loss of food. By 2 years of age, they typically use lip closure while chewing or can maintain food intraorally with tongue control if the lips are open during bolus manipulation. Strength and efficiency of chewing continues to emerge as the child develops.

The Development of Biting Skills Infants younger than 5 months of age actively mouth their toys and typically demonstrate the phasic bite and release pattern during oral play. However, when foods are introduced at this stage, the infant’s response is usually a sucking pattern. Some early phasic biting begins to occur in response to presentation of a soft, easily dissolvable solid, such as a soft cookie specifically made for toddlers. By 9 months of age, infants begin to develop the ability to hold an easily dissolvable toddler puff, cookie, or biscuit between their gums. Gradually, they display the ability to stabilize the jaw in a closed

6. Oral Motor Development

position as the feeder breaks off a small portion of the easily dissolvable item for chewing. By approximately 1 year of age, infants are able to demonstrate the ability to take a controlled sustained bite through a soft, easily dissolvable cookie or similar food item. At times, they may revert back to the phasic biting pattern, as strength and efficiency of the biting skill continues to emerge. Typically, by 18 to 21 months, toddlers show skill in biting through easy-tomanage solid items, though the jaw may be opened widely in anticipation. By 24 months of age, children are able to grade jaw opening to the appropriate size for the food being offered. The head may turn to the side to increase strength of the bite. Generally, by 36 months of age, biting skills are mature, with midline head positioning and an appropriate amount of jaw opening to accept the food. The developmental sequence for biting skills is summarized in Table 6–4.

The Transition to Cup Drinking Cups may be introduced to infants at 6 months of age. Infants generally respond to the initial presentations of the cup with an early suckle pattern, reverting back to earlier patterns of movement as is typical in normal development.6 As the feeder stabilizes the cup at the infant’s lips, the infant is able to establish a coordinated suck–swallow pattern to ingest the liquid. Wide jaw excursions are likely during intake of the liquid, resulting in significant anterior loss of the liquid during the initial attempts at cup drinking. Transition to more mature cup-drinking skills gradually occurs as infants approach 1 year of age. The suckle motion is replaced by a more mature sucking pattern during cup drinking. Jaw stabilization emerges, and infants are able to hold the jaw in a quiet open position when the cup is presented. They may use a bite on the edge of a cup for stability during the

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Table 6–4. Development of Biting Skills Age Range

Jaw Movement

~5 months

Phasic biting pattern

5 to 6 months

Sucking combined with phasic biting on easily dissolvable foods; no sustained bite through solids

6 to 9 months

Ability to hold easily dissolvable solid between gums or teeth; able to hold jaw in stationary position; uses intermittent phasic biting

9 to 12 months

Emergence of controlled, sustained bite on easily dissolvable solids, phasic biting on harder solids

12 to 18 months

Consistent use of controlled, sustained bite on easily dissolvable solids; develops sustained biting skill on harder solids

18 to 24 months

Develops ability to grade the opening of the jaw when biting foods of varying thickness; uses a controlled sustained bite on ageappropriate solid foods

24 to 36 months

Strength and efficiency of biting continue to emerge; mature biting skills generally develop by 36 months

learning stage. The ability to learn to stabilize the jaw in both the open and closed positions is a prerequisite for the development of efficient cup-drinking skills. Typically, by 24 months of age, children develop this internal jaw stabilization and master the use of a mature sucking pattern for efficient intake of liquid with a cup. The typical developmental sequence for attaining cupdrinking skills is summarized in Table 6–5.

Texture Progression As the oral reflexes become integrated with continued development of the CNS, oral motor skills for managing solids emerge. The typical progression from liquid and semi-solids to textures and solid foods is described in Table 6–6. As shown in this table, smooth solids such as infant cereal and pureed fruit or vegetables are generally introduced by spoon at 4 to 6 months of age, and a cup may also be presented for liquids. Thicker pureed foods with increased

texture are typically introduced at about 6 months, as postural control and oral motor skills continue to emerge. Easily dissolvable solids (eg, cookies for toddlers and biscuits) may also be given for sensory input and for practice in developing biting and chewing skills. Continued practice with the cup may take place at mealtime, with reliance on the bottle for intake of the appropriate volume of liquid. As lateral tongue movements emerge at approximately 7 to 9 months of age, mashed or ground table foods are initiated. By approximately 9 months, biting and chewing skills begin to emerge and easily dissolvable solids and chopped solids are appropriate. By 12 months of age, normally developing children are able to transition to the cup for fluid intake, though use of the bottle for comfort and for adequate fluid intake may continue. Transition to table foods is generally complete at this time, with intake of ground, mashed, and chopped foods with noticeable changes in texture such as lumps; however, food items must be prepared in appropriately sized pieces and the child must be able to easily break



6. Oral Motor Development

Table 6–5. Development of Cup-Drinking Skills Age Range

Oral Motor Action

4 to 6 months

Introduction of cup

6 to 8 months

Suckling pattern for liquid intake from cup; wide jaw excursions; liquid loss

8 to 12 months

Sucking pattern for liquid intake; up and down jaw excursions; tongue may protrude underneath cup to provide stability for sucking; liquid loss during intake

12 to 18 months

Sucking pattern for liquid intake; may bite down on cup to gain jaw stabilization; upper lip closes on edge of cup for seal while drinking; less jaw excursion while drinking

18 to 24 months

Use of a more mature up and down sucking pattern; cup is held between the lips; internal jaw stabilization is emerging

24 months

Use of a sucking pattern for liquid intake; may hold edge of cup with teeth; eventual development of internal jaw stabilization without biting on edge of cup

down these items with oral manipulation. Examples of food appropriate to each stage of development are outlined in Table 6–6.

Muscle Tone and Movement Safe and efficient feeding requires sufficient strength and finely tuned coordination of the oral motor musculature. Coordinated movements of the jaw, tongue, cheeks, and lips comprise multiple components, including muscle tension, direction of movement, timing, and force of contraction. The resultant pattern of movement varies according to the task being performed and depends on appropriate muscle tension to provide stability. Simultaneously, sufficient muscle relaxation must occur to allow a range of oral movements. Box 6–5 Resting muscle tone refers to the degree of contraction of a muscle while the individual is at rest.

Box 6–6 Muscle tension refers to the degree of muscle contraction. Hypotonia refers to a low degree of muscle tension that ranges from mild weakness to immobility of a muscle or joint. It can result from lack of innervation to a muscle due to injury to the peripheral nerve, damage to the cranial nerve or cranial nerve nucleus, or both. In contrast, hypertonia is characterized by a high degree of muscle tension, resulting in limitation of movement that ranges from a mild to an immobile muscle or joint. It results from damage to the brain or spinal cord and may be identified in a specific part of the body or throughout the body. If children have hypotonia and postural instability and attempt to compensate by tensing their muscles, a pattern referred to as “fixing” results. At times, fluctuating tone is present, which varies between hypotonia and hypertonia. Resting tone may be high, low, or normal; however, with intentional movement, the tone may shift to increased tension and subsequently

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Table 6–6. Texture Transition During Oral Motor Feeding Skill Development Age Range

Food Type

Examples

Oral Motor Skill

Birth to 4 months

Liquid

Breastmilk, formula

Suckling and sucking predominate

4 to 6 months

Smooth foods, purees, and blenderized foods

Rice cereal, fruit or vegetable purees, soft cookies, toddler biscuits or puffs

Anterior–posterior tongue movements

Phasic biting, practice with biting, precursors to developing biting and chewing skills

Easily dissolvable solids may be introduced with close monitoring by feeder 7 to 9 months

Increased texture of solids, fork-mashed soft solids

Regular applesauce, mashed potatoes

Efficient sucking, emergent skills for cup drinking

Easily dissolvable solids

Toddler cookies, soft biscuits

Emergence of tongue lateralization Vertical chewing motion in response to solids

9 to 12 months

Fork-mashed or slightly blended table foods Transition toward easy to manage solid foods

Casseroles, scrambled eggs, toast strips, pasta pieces, crunchy but dissolvable cookies, crackers

Increasing lateral tongue movements for mastication of foods Vertical chewing pattern with emergence of lateral tongue movements Transition to cup drinking Trend toward less formula intake as solid intake increases

12 to 18 months

19 to 24 months

24 months

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Easy to manage solid foods

Table foods requiring greater mastication

Wide range of textures

Crackers, breads, casseroles, soft fruit pieces, and tender meat such as flaked fish or chicken

Consistent tongue lateralization Emergence of mature rotary chewing pattern

Tender meats, steamed vegetables, and fruits

Chewing efficiency increases

All table foods with monitoring; avoid food known to have high choking risk for children younger than age 4 years, such as raw carrots, popcorn, hotdogs, round candies

Oral motor/feeding skills have emerged, with continuing refinement in skills

Cup drinking



alternate between varying degrees of high and low tone. This fluctuation may result in what appears to be constant extraneous writhing movements. Fluctuating tone may accompany conditions such as athetoid cerebral palsy. Oral motor hypotonia is often accompanied by exaggerated motion, which refers to movements beyond the normal range. For example, jaw opening may be exaggerated in a child with hypotonic muscles. Directions of movement include extension and flexion, retraction and protraction (also referred to as protrusion), elevation and depression, and lateral movement. Extension is characterized by straightening or opening, such as extending the tongue or opening the jaw; these are defined as extensor movements. Flexion is characterized by bending or closing, such as pulling the tongue back into the mouth or closing the jaw; these are defined as flexor movements. Retraction refers to a pulling back movement, such as retracting the tongue, jaw, or lips. Protraction and protrusion refer to pulling forward movements such as protrusion of the lips or the tongue. Elevation and depression refer to the upward and downward movements, respectively. Lateral movement refers to deflections of the tongue to the left or right. Combinations of these movements change the shape and position of the tongue to facilitate oral feeding. The speed or timing of movement is assessed by how rapidly it occurs within the context of other movements that are part of the overall movement pattern. For example, tongue lateralization during bolus manipulation involves movement of the tongue that quickly responds to changing the consistency of the bolus that is being chewed. Lastly, the term “thrust” describes sudden and rapid extensor movement such as a jaw or tongue thrust. Muscle tone may be increased or decreased on only one side of the body. This is described as asymmetrical distribution. In contrast, distribution of muscle tone that is equal on both sides of the body is defined as symmetrical.

6. Oral Motor Development

Function of the Oral Structures — ​Limiting Patterns Different degrees and ranges of impairment in oral motor skills for feeding are the result of abnormal muscle tone and movement patterns as well as the persistence of primitive oral and pharyngeal reflexes. Generally, the more the movement pattern interferes with the normal progression of feeding, the greater the impact on the child’s feeding ability.6

Persistent Primitive Oral Reflexes Normal neural development is associated with differentiation of cortical pathways and progressive myelination of the peripheral nervous system. These maturational developments result in the inhibition of primitive reflexes such as rooting, phasic biting, and tongue protrusion. When inhibition does not occur, these primitive reflexes are retained and interfere significantly with the progression of oral feeding. Excessive rooting, strong tongue protrusion, and tonic biting are exhibited with attempts at bottle feeding or spoon-feeding.

Limitations in Jaw Movements The jaw is the foundation upon which other oral motor actions are built. To work adequately, the cheeks, lips, and tongue require the proximal stability of the jaw. The child’s ability to stabilize the jaw provides the steady base that facilitates coordinated action of the lips and tongue. Difficulty with jaw control results in (1) reduced ability to volitionally open or close the mouth during eating and drinking, (2) difficulty with controlling movements for biting and chewing, and (3) poorly coordinated cheek, lip, and tongue movements. Infants with significant hypotonia have poor head, neck, and trunk stability. If the head is in hyperextension, jaw closure is

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difficult and an open-mouth posture results. This posture causes excessive up and down jaw motion with attempts at sucking. With growth, increased neck extension, shoulder retraction, and extension of the hips and pelvis are common and increase the difficulty in controlling jaw movements. Jaw thrusts, which are strong extensor patterns in the jaw, appear with presentation of spoon-feeding and bottle- or breastfeeding, significantly decreasing feeding efficiency. Infants and children with significant jaw instability often have a tonic bite reflex when presented with a spoon or cup, which significantly decreases the efficiency of oral feeding. Lastly, jaw clenching, which refers to involuntary tension with jaw closure, or jaw retraction, which refers to involuntary pulling backward of the jaw, limits opening of the mouth for acceptance of oral feeding.

Limitations in Tongue Movement Abnormalities in posture can affect muscle tone and mobility of the tongue. Retraction of the shoulder girdle (clavicle and scapula) with hyperextension of the head is accompanied by tongue retraction. In turn, tongue retraction precludes placement of the spoon onto the body of the tongue. In this setting, liquid or food is deposited into the anterior sulcus rather than onto the tongue, resulting in difficulty with bolus transfer. With abnormal increases in postural tone, more extensor posturing occurs. Tongue retraction may thus be exaggerated. By contrast, in children with low tone such as those with Down syndrome, tongue protrusion is common. In children with a tongue thrust, placement of the spoon or nipple onto the tongue is difficult, as the strong tongue thrust pattern causes forceful anterior loss of food and liquid from the mouth. Abnormalities of the facial nerve (CN VII) or glossopharyngeal nerve (CN IX) may be reflected in abnormal tongue configurations such as

tongue bunching (contraction) or flaccidity, resulting from paralysis or weakness.

Limitations in Lip and Cheek Movement Paralysis or low muscle tone in the cheeks and lips affects the efficiency of oral skills. If tone in the lips is weak, adequate lip closure to maintain saliva, food, and liquid in the mouth may not be achieved. If tone in the cheeks is weak, food may fall into the lateral sulcus rather than being actively manipulated and transferred by the tongue for swallowing. If muscle tone is increased, the lips and cheeks may be pulled into a retracted position, limiting the ability to suck efficiently and to remove food from a utensil.

The Role of Sensory Processing and Discrimination Sensory processing/discrimination refers to the way that the nervous system receives and processes messages from the senses. Information from the visual, auditory, proprioceptive, vestibular, tactile, olfactory, and gustatory senses is subsequently organized into appropriate motor and behavioral responses. A child’s responses or reactions during feeding may reflect difficulties with sensory processing and discrimination in varying degrees. Hypersensitivity, which is an overreaction, might occur in response to tactile input into the mouth during oral care or oral play, or following intake of a specific flavor or texture. Gagging, vomiting, or behavioral resistance to further presentations is likely to occur. The child’s diet may become highly restricted and selective, containing only foods that meet specific criteria in terms of visual appearance, shape, taste, texture, brand, and temperature.23 Hyposensitivity, an underreaction, may be reflected in a child’s seeming unawareness of food residue in the mouth, of flavor, or of the amount of food placed intraorally.



6. Oral Motor Development

References 1. Miller A. Oral and pharyngeal reflexes in the mammalian nervous system: their diverse range in complexity and the pivotal role of the tongue. Crit Rev Oral Biol Med. 2002;​ 13(5):409–425. 2. Wolf LS, Glass RP. Feeding and Swallowing Disorders in Infancy: Assessment and Management. 2nd ed. San Antonio, TX: The Psychological Corporation; 1992. 3. Sheppard JJ, Mysak ED. Ontogeny of infantile oral reflexes and emerging chewing. Child Devel.1984:831–843. 4. Rogers B, Arvedson J. Assessment of infant oral sensorimotor and swallowing function. Ment Retard Dev Disabil Res Rev. 2005;11(1):​ 74–82. 5. Wolff PH. The serial organization of sucking in the young infant. Pediatrics. 1968;42(6):​ 943–956. 6. Morris SE, Klein MD, Satter E. Pre-Feeding Skills: A Comprehensive Resource for Mealtime Development. 2nd ed. Austin, TX: ProEd; 2000. 7. Lau C. Development of infant oral feeding skills: what do we know? Am J Clin Nutr. 2016;​103(2):616S–621S. 8. Kelly BN, Huckabee ML, Jones RD, Frampton CM. Nutritive and non-nutritive swallowing apnea duration in term infants: implications for neural control mechanisms. Respir Physiol Neurobiol. 2006;154(3):372–378. 9. Wilson SL, Thach BT, Brouillette RT, AbuOsba YK. Coordination of breathing and swallowing in human infants. J Appl Physiol Respir Environ Exerc Physiol. 1981;50(4):​851–858. 10. Gewolb IH, Vice FL, Schweitzer-Kenney EL, Taciak VL, Bosma JF. Developmental patterns of rhythmic suck and swallow in preterm infants. Dev Med Child Neurol. 2001;​ 43(1):​22–27. 11. Miller MJ, Kiatchoosakun P. Relationship between respiratory control and feeding in the developing infant. Semin Neonatol. 2004;​9(3):221–227.

12. Mizuno K, Ueda A. The maturation and coordination of sucking, swallowing, and respiration in preterm infants. J Pediatr. 2003;​ 142(1):36–40. 13. Mathew OP. Science of bottle feeding. J Pediatr. 1991;119(4):511–519. 14. Koenig J, Davies A, Thach B. Coordination of breathing, sucking, and swallowing during bottle feedings in human infants. J Appl Physiol. 1990;69(5):1623–1629. 15. Selley WG, Ellis RE, Flack FC, Brooks WA. Coordination of sucking, swallowing and breathing in the newborn: its relationship to infant feeding and normal development. Br J Disord Commun. 1990;25(3):311–327. 16. Ardran GM, Kemp FH, Lind J. A cineradiographic study of breast feeding. Br J Radiol. 1958;31(363):156–162. 17. Woolridge MW. The ‘anatomy’ of infant sucking. Midwifery. 1986;2(4):164–171. Retrieved from http://www.ncbi.nlm.nih.gov/ pubmed/3643397 18. Moral A, Bolibar I, Seguranyes G, et al. Mechanics of sucking: comparison between bottle feeding and breastfeeding. BMC Pediatr. 2010;10:6. 19. Mizuno K, Ueda A. Changes in sucking performance from nonnutritive sucking to nutritive sucking during breast- and bottlefeeding. Pediatr Res. 2006;59(5):728–731. 20. Green JR, Moore CA, Ruark JL, Rodda PR, Morvée WT, Vanwitzenburg MJ. Development of chewing in children from 12 to 48 months: longitudinal study of EMG patterns. J Neurophysiol. 1997;77(5):2704–2716. 21. Illingworth RS, Lister J. The critical or sensitive period, with special reference to certain feeding problems in infants and children. J Pediatr. 1964;65:839–848. 22. Arvedson JC, Brodsky L. Pediatric Swallowing and Feeding: Assessment and Management. 2nd ed. Clifton Park, NY: Delmar Cengage Learning; 2002. 23. Zucker N, Copeland W, Franz L, et al. Psychological and psychosocial impairment in preschoolers with selective eating. Pediatrics. 2015;136(3):e582–e590.

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Section

4

Etiologies The normal developmental progression of feeding and swallowing skills requires the complex interaction of multiple body systems and age-related processes. Intact oral, pharyngeal, and esophageal structures, neurologic maturation, and precise neuromuscular coordination, are all essential. In some children, psychosocial factors may also have an impact. Dysfunction or impairment of even one of these components can have a significant effect on the development of safe and efficient oral feeding and swallowing. Thus, identifying the etiology of dysphagia prior to initiating treatment is essential. The chapters in this section reflect

a broad spectrum of etiologic categories, providing readers with brief descriptions of some of the conditions that fall within each of these categories. However, it is important to keep in mind that etiologic categorization is not always mutually exclusive. For example, an infant with a complex craniofacial anomaly may also have a neurologic diagnosis such as cerebral palsy, thus compounding difficulties in the feeding and swallowing process. Moreover, the underlying etiologies of pediatric dysphagia may progress or intensify as a result of medical complications, physiologic abnormalities, or environmental factors.

7 Syndromes, Sequences, and Associations Claire Kane Miller, Aliza P. Cohen, and Jay Paul Willging

CHAPTER OUTLINE Craniofacial Syndromes, Sequences, and Associations CHARGE Syndrome Apert Syndrome Crouzon Syndrome Treacher Collins Syndrome Craniofacial Microsomia 22q11.2 Deletion Syndrome Van der Woude Syndrome Stickler Syndrome Oromandibular Limb Hypoplasia Syndrome Pierre Robin Sequence Other Syndromes Moebius Syndrome Smith-Lemli-Opitz Syndrome Cornelia de Lange Syndrome Noonan Syndrome Coffin–Siris Syndrome Rett Syndrome Prader–Willi Syndrome Trisomy Trisomy 18 Trisomy 21 Williams Syndrome VACTERL Association

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Craniofacial Syndromes, Sequences, and Associations Children with craniofacial syndromes, sequences, or associations have a high likelihood of experiencing feeding and swallowing problems. The discussion below presents a succinct overview of many of these conditions. A more in-depth discussion of the craniofacial syndromes most commonly encountered in clinical practice and the management of feeding issues in children with these syndromes is presented in Chapter 39. Comprehensive descriptions of other syndromes, characteristics of dysphagia, and suggested dysphagia management strategies appear in Chapter 17. Box 7–1.  Syndromes Versus Sequences n Syndromes can often be traced to

a single genetic malformation (eg, trisomy 21), whereas sequences may have multiple disparate causes (eg, Pierre Robin sequence). n In syndromes, the causal relationship between a constellation of anomalies is often not understood. By contrast, in sequences, an entire cascade of events is often known. n In syndromes, there are often multiple defects resulting in multiple unrelated embryologic anomalies. In sequences, one primary defect causes a cascade of secondary anomalies.

CHARGE Syndrome Although features of this syndrome vary among affected individuals, the acronym CHARGE derives from features that are commonly seen: coloboma, heart defects, atresia choanae (choanal atresia), growth retardation, genital abnormalities, and ear

abnormalities. Although not part of the acronym, cranial nerve dysfunction is a common feature of CHARGE syndrome, affecting the motor and sensory components necessary for safe and efficient feeding and swallowing in both the oral and pharyngeal phases of the swallow. Most cases of CHARGE syndrome are attributed to a mutation in the CHD7 gene, though a small percentage of individuals with CHARGE do not have this mutation.1

Apert Syndrome Apert syndrome is a genetic disorder characterized by premature fusion of the cranial sutures (craniosynostosis) with associated syndactyly of the hands and feet (fusion of the fingers and/or toes). The skull is unable to grow normally, which results in characteristic facies that includes maxillary hypoplasia, giving the appearance of mandibular prognathism (protuberance of the mandible), proptosis (abnormal protrusion of the eyes), and hypertelorism (eyes that are set far apart). The nasopharynx and oropharynx are usually narrowed as a result of the severe maxillary retrusion and the palate is often high-arched, with crowded dentition. A cleft of the secondary palate and bifid uvula may also be present. The constellation of oral structural issues contribute to feeding dysfunction, which is further compounded by a narrow airway. Box 7–2 Children with either Apert syndrome or Crouzon syndrome have abnormal occlusion secondary to overgrowth of the lower jaw (prognathism) and underprojection of the maxillary teeth (retrusion).

Crouzon Syndrome Crouzon syndrome results from premature fusion of one or more of the coronal



7. Syndromes, Sequences, and Associations

sutures between the skull bones (craniosynostosis). Children present with midface hypoplasia, wide-set bulging eyes, stenotic posterior choanae, a narrowed nasopharyngeal airway, relative mandibular protuberance, crowded dentition, and maxillary retrusion leading to an anterior open bite. A cleft lip and palate may also be present. As with Apert syndrome, airway obstruction in infancy often necessitates a tracheotomy. Feeding difficulties occur secondary to abnormal craniofacial structures.

Treacher Collins Syndrome Treacher Collins syndrome occurs as the result of bilateral symmetric anomalies in the development of the first and second branchial arches, resulting in hypoplasia (underdevelopment) of the malar bones, maxilla, and mandible (Figure 7–1). These structural abnormalities interfere with the muscles of mastication and the temporomandibular joints.2 Feeding issues vary depending upon the infant’s non-nutritive oral skills. If a cleft palate is present, additional structural feeding problems occur.

Figure 7–1. Treacher Collins syndrome. Source: File licensed under Creative Commons, https://ru.wikipedia.org/wiki/%D0 %A4%D0%B0%D0%B9%D0%BB:Treacher_Collins_syndrome_(MedMedicine).jpg.

Craniofacial Microsomia The exact cause of craniofacial microsomia has not been determined, though several factors have been implicated, including chromosomal abnormalities and gene mutations that cause abnormalities during the development of the first and second pharyngeal arches. There may be differences in the size and shape of structures between the right and left sides of the face, ear abnormalities, and maxillary/mandibular hypoplasia. Facial involvement and mandibular hypoplasia contribute to oral feeding difficulties. Sucking mechanics are impaired due to restricted mandibular excursion, facial and masticatory muscle weakness, and abnormalities in the position and range of motion of the tongue.3,4

22q11.2 Deletion Syndrome The 22q11.2 deletion syndrome, also referred to as velocardiofacial syndrome, is a common microdeletion syndrome, resulting from a microdeletion on the long arm of chromosome 22. Features vary among individuals and include unique facial characteristics (elongated face, almond-shaped eyes, wide nose, small ears) as well as conotruncal cardiac anomalies, palatal dysfunction, immunodeficiency, and hypocalcemia (Figure 7–2).5 Velopharyngeal incompetence and/or hypotonia of the velopharyngeal musculature may result in nasal regurgitation during feeding.6 Underlying cardiac issues may affect endurance during feeding and affect the overall volume of oral intake. Box 7–3 Velopharyngeal incompetence refers to the inability of the velum to adequately separate the nasopharynx from the oral cavity during activities such as swallowing or speaking.

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appearance and that affects the connective tissue of the body’s joints and organs.9 It is estimated to occur in 1 in 7,500 newborns, and several different genes have been identified that may cause a form of this syndrome. Presentation among affected infants and children varies significantly, as individuals may have only a few or all features associated with the syndrome. Although the classic presentation is the same as that in children with Pierre Robin sequence (described later in this chapter), it is differentiated from this sequence by the presence of myopia, cataracts, retinal detachment, and the early onset of osteoFigure 7–2.  22q11.2 Deletion syndrome — ​ arthritis. Mid-face hypoplasia, high-arched velocardiofacial syndrome. Source: Courtesy palate, bifid uvula, and dental malocclusion of Cincinnati Children’s Hospital Medical Cen- may also be present. ter, Aerodigestive and Esophageal Center.

Van der Woude Syndrome Van der Woude syndrome (VWS) is the most common syndrome involving cleft lip and palate, and many infants born with this syndrome have both of these anomalies. Affected children generally also have depressions (pits) near the center of the lower lip, which may appear moist due to the presence of salivary and mucous glands in the pits.7 These pits may be blind-ended or may extend through the lip, having two openings (fistulae). VWS is inherited in an autosomal dominant pattern and genetic testing for mutations in the interferon regulatory factor 6 (IRF6) gene8 can be used to diagnose this condition. It is characterized by the association of congenital lower lip fistulae with either cleft lip, cleft palate, or both. Hypodontia (congenital absence of teeth) and dental malocclusion may also be present.7

Stickler Syndrome Stickler syndrome is a disorder that is characterized by a somewhat flattened facial

Oromandibular Limb Hypoplasia Syndrome Oromandibular limb hypoplasia syndrome represents a group of rare and overlapping syndromes that are characterized by variable congenital malformations of the tongue, palate, mandible, maxilla, and limbs. In each of these syndromes, potential abnormalities of the face, jaw, palate, and tongue affect the oral motor functions necessary for efficient feeding.

Pierre Robin Sequence Pierre Robin sequence (PRS) is related to genetic and non-genetic causes that affect normal development of the craniofacial structures. Underdevelopment of the mandible reduces the oropharyngeal area10 and causes posterior and superior displacement of the tongue. Airway obstruction is the primary cause of feeding issues, which typically involve pharyngeal collapse, blockage of the airway secondary to velum elongation, and base of tongue obstruction (glossoptosis secondary to retrognathia).



7. Syndromes, Sequences, and Associations

A subset of patients with PRS may exhibit “catch-up” mandibular growth by approximately 6 months of age.11

Other Syndromes As with children who have craniofacial syndromes, those with many other syndromes also experience feeding and swallowing problems. The discussion below pre­sents a succinct overview of some of these syndromes.

Moebius Syndrome Moebius syndrome is characterized by nonprogressive paralysis or weakness of multiple cranial nerves; however, cranial nerves (CN) VI (abducens) and CN VII (facial) are the most commonly involved. Involvement of CN VII may cause impaired lip closure, which results in drooling and poor sucking skills. Depending on the extent of brainstem involvement, coordination of the suck–swallow–breathe sequence can be affected during feeding. Additional abnormalities may include tongue malformations, micrognathia, and cleft palate. If CN VIII (vestibulocochlear) is affected, hearing loss is likely. There may also be underdevelopment of the pinna (external ear), which is referred to as microtia.

Smith-Lemli-Opitz Syndrome Smith-Lemli-Opitz syndrome (also referred to as SLOS) is an inherited disorder caused by a mutation in the 7-dehydrocholesterol reductase (DHCR7) gene. This mutation results in an impairment in the body’s ability to make cholesterol. Given that cholesterol is essential for normal fetal development and plays a critical role in the production of hormones and digestive acids, this deficiency disrupts growth and

development. SLOS is characterized by distinctive facial features, microcephaly, hypotonia, and intellectual disabilities.12 Many children with SLOS also have features of autism and behavioral issues.13 Low orofacial tone, high-arched palate, cleft palate, and tongue abnormalities often result in impaired oral sensorimotor skills and swallowing dysfunction.

Cornelia de Lange Syndrome The features of Cornelia de Lange syndrome (CdLS) vary from mild to severe, and include distinctive craniofacial features, microcephaly, autistic behaviors, developmental delay, skeletal abnormalities of the arms and hands, hirsutism (excessive hair growth), gastrointestinal issues, genital abnormalities, myopia, and hearing loss. Although mutations in the nipped B cohesin loading factor (NIPBL) gene have been identified in approximately half of all individuals with CdLS,14 this condition can result from mutations in five different genes. Feeding difficulties associated with CdLSin infants include sucking difficulty and poor suck– swallow–breathe coordination.15 Sensory processing issues may also be present, and affect the feeding skills of these patients.

Noonan Syndrome Infants and children with Noonan syndrome present with unusual facial features, heart defects, short stature, and skeletal malformations. A high-arched palate, poor teeth alignment, and micrognathia (a small lower jaw) may also be present. The most common cardiac defect is pulmonary valve stenosis, though some individuals may have hypertrophic cardiomyopathy (enlarged heart muscle). Feeding problems in infants with Noonan syndrome primarily stem from sucking weakness, which may affect nutritional intake and overall growth.16

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Pediatric Dysphagia: Etiologies, Diagnosis, and Management

Coffin–Siris Syndrome Coffin–Siris syndrome is a condition caused by a mutation in any of several genes. This results in distinctive facial features, including a wide mouth, thick upper and lower lips, a wide nose, and a flat nasal bridge, as well as microcephaly, intellectual disability, motor delays, central hypotonia, and fifth digit nail/toe hypoplasia oraplasia.17 Congenital anomalies are present in multiple systems, including the gastrointestinal, genitourinary, cardiac, and central nervous system. Feeding difficulty frequently occurs in infancy secondary to orofacial issues and underlying hypotonia.

Rett Syndrome Rett syndrome is a rare progressive neurodevelopmental disorder caused by a mutation in the MECP2 gene, which is responsible for making a protein (MeCP2) that is critical for brain function. This syndrome occurs almost exclusively in females after 6 to 18 months of normal development. It is characterized by developmental regression, most significantly in communication skills, and in the control of voluntary movements.18 Distinctive uncontrolled repetitive hand movements such as squeezing, clapping, tapping, or rubbing emerge. Autistic-like behaviors, respiratory issues, growth retardation, unusual eye movements, agitation and irritability, and seizures also may occur; however, symptoms, disease progression, and disease severity are widely variable. Difficulty with chewing and swallowing occur as a result of muscle wasting; oral intake and swallowing safety may therefore be compromised.

Prader–Willi Syndrome Prader–Willi syndrome (PWS) is a genetic disorder resulting from an abnormality in

a particular region of chromosome 15. It is recognized as the most common genetic cause of life-threatening childhood obesity. Infants with PWS have severe hypotonia and feeding difficulties. They are usually unable to breastfeed and frequently require tube feeding. Acquisition of motor and language milestones is delayed. In later infancy and early childhood (3 to 8 years of age), feeding difficulties resolve. This phase of PWS is followed by excessive food intake and the onset of obesity. Cognitive impairment, obsessive compulsive behavior, and behavioral issues are also common.

Trisomy Trisomy is a condition in which an extra copy of a chromosome is present in cell nuclei, causing developmental abnormalities. This can occur with any chromosome and most often results in a miscarriage. The most common types of trisomy that survive to birth include trisomy 8 (Warkany syndrome), trisomy 9, trisomy 13 (Patau syndrome), trisomy 18 (Edwards syndrome), trisomy 21 (Down syndrome), and trisomy 22. Of these conditions, trisomy 18 and trisomy 21 are the most common.19 Box 7–4 Normally, there are two copies of each chromosome. In patients with trisomy, however, there are three copies of a particular chromosome in each cell.

Trisomy 18 Trisomy 18, also known as Edwards syndrome, is a condition that occurs when individuals have three copies of chromosome 18 in each cell. The syndrome pattern includes intrauterine growth retardation, low birth weight, heart defects, microcephaly, micrognathia, and severe intellectual disabilities. Feeding issues occur consistently as a result of the craniofacial features, and infants



7. Syndromes, Sequences, and Associations

often require enteral nutrition.19 Only 5% to 10% of affected children live beyond the first year of life, with the major causes of death being central apnea, cardiac failure secondary to cardiac malformations, respiratory insufficiency due to hypoventilation, aspiration, and upper airway obstruction.19

Trisomy 21 Trisomy 21, also known as Down syndrome, is a condition that occurs when an individual has an extra copy of chromosome 21. It is estimated to affect 1 in every 700 newborns in the United States, making it the most common chromosomal condition. There are three cellular processes that result in three distinct types of trisomy 21: nondisjunction, translocation, and mosaicism. Regardless of the type of trisomy 21, extra copies of the genes on chromosome 21 disrupt normal development and result in variable features of affected children. These features include hypotonia, microcephaly, flattened facies, upward slanting eyes, small ears, short stature, a single deep crease across the center of the palm (simian crease), a relatively small oral cavity, and tongue protrusion. Conditions that commonly occur in these children include chronic otitis media, upper respiratory infections, hearing loss, obstructive sleep apnea, heart defects (atrial septal defect or ventricular septal defect), and varying degrees of intellectual impairment. Other less common conditions include thyroid disease, anemia, leukemia in infancy or early childhood, Hirschsprung disease, laryngeal cleft, esophageal atresia, and duodenal atresia. Feeding and swallowing issues may occur secondary to oral motor dysfunction (weak sucking skills), oral hypersensitivity, decreased feeding endurance secondary to underlying cardiac disease or hypotonia, suck–swallow coordination, and pharyngeal phase dysphagia, including inadequate hypopharyngeal clearance following swallows and compromised airway protection associated with swallowing.20,21

Box 7–5 During the production of the egg or sperm, a single copy of each chromosome is packaged. In children with nondisjunction trisomy 21, both copies of chromosome 21 are placed into a single egg or sperm. During fertilization, an egg with two copies of chromosome 21 fuses with a sperm carrying a single copy of chromosome 21; the fertilized egg replicates and every cell has three copies of this chromosome. This cellular process accounts for 95% of cases of trisomy 21.

Box 7–6 During the development of egg and sperm, part of chromosome 21 may attach to chromosome 14. This leads to an egg or sperm with a complete copy of chromosome 21 and a partial additional copy of chromosome 21. This cellular process accounts for approximately 4% of cases of Down syndrome.

Box 7–7 Mosaicism occurs early in development as a random event during cell division, whereby an extra copy of chromosome 21 occurs only in some cells. This results in a mixture of two types of cells, some containing the usual 46 chromosomes and some containing 47 chromosomes. The cells with 47 chromosomes contain an extra chromosome 21. This cellular process accounts for only 1% of all cases of trisomy 21.

Williams Syndrome Williams syndrome is a disorder that is caused by the deletion of genetic material from a specific region of chromosome 7; the deleted region includes 26 to 28 genes. This

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Pediatric Dysphagia: Etiologies, Diagnosis, and Management

syndrome affects many parts of the body and is characterized by mild to moderate intellectual disability or learning problems, unique bahavioral characteristics (overfriendliness, generalized anxiety, attention deficit disorder), distinctive facial features, cardiovascular disease (supravalvar aortic stenosis and peripheral pulmonary artery stenosis), and global developmental delays. Feeding issues may be secondary to underlying cardiac defects and related endurance issues during feeding.22 Feeding problems may also occur secondary to hypotonia, and include sucking difficulty, inefficient oral motor patterns, limited volume of oral intake, drooling, and delayed acquisition of chewing skills. Infants with Williams syndrome have also been reported to have an increased frequency of infant colic, constipation, and gastroesophageal reflux, all of which may compound early feeding difficulties.23,24

VACTERL Association VACTERL association is a disorder that affects numerous body systems. The VACTERL acronym represents the characteristic features of the association, which include vertebral defects, anal atresia, cardiac defects, tracheoesophageal fistula, renal anomalies, and limb abnormalities. Individuals who are diagnosed with VACTERL association typically have at least three of these characteristics and may also have additional abnormalities that are not among the characteristic features. In some patients, features are subtle, and the diagnosis may not be made until later in childhood or during adulthood. The specific genetic and environmental causes of VACTERL are as yet unclear; however, it is thought that it may have different causes in different children. In some cases, it is likely caused by the interaction of multiple genetic and environmental factors. If a tracheoesophageal fistula or esophageal atresia is present, abnormalities in esophageal motility persist following surgical repair and may lead to continued

feeding difficulties. Underlying cardiac anomalies may cause fatigue during feedings and affect overall endurance for feeding during infancy. Constipation may occur after repair of anal anomalies; this may affect appetite and motivation for eating. Box 7–8 An association is defined as a combination of anomalies that occur together more frequently than by chance alone, but which are not known to have a common cause. For example, VACTERL association involves vertebral anomalies, anal atresia, cardiac defects, tracheoesophageal fistula, renal anomalies, and limb abnormalities.

References 1. Bergman JE, Janssen N, Hoefsloot LH, Jongmans MC, Hofstra RM, van Ravenswaaij-Arts C. CHD7 mutations and CHARGE syndrome: the clinical implications of an expanding phenotype. J Med Genet. 2011:jmg. 2010​.08​7106. 2. Posnick JC, Tiwana PS, Costello BJ. Treacher Collins syndrome: comprehensive evaluation and treatment. Oral Maxillofac Surg Clin North Am. 2004;16(4):503–523. 3. Caron CJ, Pluijmers BI, Joosten KF, et al. Feeding difficulties in craniofacial microsomia: a systematic review. Int J Oral and Maxillofac Surg. 2015;44(6):732–737. 4. Heike CL, Hing AV, Aspinall CA, et al. Clinical care in craniofacial microsomia: a review of current management recommendations and opportunities to advance research. Am J Med Genet C Semin Med Genet. 2013;​ 163C(4):271–282. 5. McDonald-McGinn DM, Emanuel BS, Zackai EH. 22q11.2 deletion syndrome. In: Pagon RA, Adam MP, Ardinger HH, et al, eds. GeneReviews®. Seattle, WA: University of Washington; 2013. 6. Rommel N, Davidson G, Cain T, Hebbard G, Omari T. Videomanometric evaluation of pharyngo-oesophageal dysmotility in children with velocardiofacial syndrome. J Pediatr Gastroenterol Nutr. 2008;46(1):87–91.



7. Syndromes, Sequences, and Associations

7. Lam AK, David DJ, Townsend GC, Anderson PJ. Vander Woude syndrome: dentofacial features and implications for clinical practice. Aust Dent J. 1010;55(1):51–58. 8. Shprintzen RJ, Goldberg RB, Sidoti EJ. The penetrance and variable expression of the Van der Woude syndrome: implications for genetic counseling. Cleft Palate J. 1980;17(1):​52–57. 9. Kummer AW. Cleft Palate and Craniofacial Anomalies: Effects on Speech and Resonance. 3rd ed. Clifton Park, NY: Delmar Cengage Learning; 2014. 10. Rathe M, Rayyan M, Schoenaers J, et al. Pierre Robin sequence: management of respiratory and feeding complications during the first year of life in a tertiary referral centre. Int J Pediatr Otorhinolaryngol. 2015;​79(8):​ 1206–1212. 11. Sidman JD, Sampson D, Templeton B. Distraction osteogenesis of the mandible for airway obstruction in children. Laryngoscope. 2001;111(7):1137–1146. 12. Kelley RI, Hennekam RC. The Smith-LemliOpitz syndrome. J Med Genet. 2000;37(5):​ 321–335. 13. Freeman KA, Eagle R, Merkens LS, et al. Challenging behavior in Smith-Lemli-Opitz syndrome: initial test of biobehavioral influences. Cogn Behav Neurol. 2013;26(1):23–29. 14. Musio A, Selicorni A, Focarelli ML, et al. X-linked Cornelia de Lange syndrome owing to SMC1L1 mutations. Nat Genet. 2006;​38(5):​ 528–530. 15. Cates M, Billmire DF, Bull MJ, Grosfeld JL. Gastroesophageal dysfunction in Cornelia

de Lange syndrome. J Pediatr Surg. 1989;​ 24(3):248–250. 16. Sharland M, Burch M, McKenna WM, Paton MA. A clinical study of Noonan syndrome. Arch Dis Child. 1992;67(2):178–183. 17. Vergano SS, Deardorff MA. Clinical features, diagnostic criteria, and management of Coffin-Siris syndrome. Am J Med Genet C Semin Med Genet. 2014;166C(3):252–256. 18. Neul JL, Kaufmann WE, Glaze DG, et al. Rett syndrome: revised diagnostic criteria and nomenclature. Ann Neurol. 2010;68(6):​ 944–950. 19. Cereda A, Carey JC. The trisomy 18 syndrome. Orphanet J Rare Dis. 2012;7:81. 20. Frazier JB, Friedman B. Swallow function in children with Down syndrome: a retrospective study. Dev Med Child Neurol. 1996;​ 38(8):695–703. 21. Jackson A, Maybee J, Moran MK, WolterWarmerdam K, Hickey F. Clinical characteristics of dysphagia in children with Down syndrome. Dysphagia. 2016;31(5):663–671. 22. Cooper-Brown L, Copeland S, Dailey S, et al. Feeding and swallowing dysfunction in genetic syndromes. Dev Disabil Res Rev. 2008;​14(2):147–157. 23. Morris CA, Demsey SA, Leonard CO, Dilts C, Blackburn BL. Natural history of Williams syndrome: physical characteristics. J Pediatr. 1988;113(2):318–326. 24. Cunniff C, Frias JL, Kaye CI, Moeschler J, Panny SR, Trotter TL. Health care supervision for children with Williams syndrome. Pediatrics. 2001;107(5):1192–1204.

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8 Neurologic Etiologies Claire Kane Miller, Aliza P. Cohen, and Jay Paul Willging

CHAPTER OUTLINE Neurologic Etiologies Central Nervous System Etiologies Conditions Associated with Prematurity Intrauterine Growth Restriction Periventricular Leukomalacia Hypoxic Ischemic Encephalopathy Anoxic Encephalopathy Cerebral Palsy Chiari Malformations Brain Tumors Leukodystrophies Pediatric Cerebrovascular Accidents Abnormalities of the Corpus Callosum Myopathies Muscular Dystrophy Congenital Myopathies Peripheral Nerve Diseases Lower Motor Neuron Diseases Spinal Muscular Atrophy Botulism

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Neurologic Etiologies Central Nervous System Etiologies Conditions Associated with Prematurity Infants born prior to 37 weeks gestation are considered to be premature. Although medical and technologic advancements over the past several decades have resulted in significantly increased survival rates among these infants, they remain at risk for developing a broad array of complications and disorders.1 Morbidity is inversely related to gestational age (GA); however, there is no GA that that does not carry the risk of infants developing complications.1,2 While the cause of preterm birth cannot always be determined, risk factors that may trigger early labor include genetic abnormalities of the fetus, maternal conditions such as uterine abnormalities, diabetes, high blood pressure, poor nutrition, smoking, alcohol use, environmental exposures such as particulate air pollution,3,4 and early induction of labor. Box 8–1 Premature birth is the number one cause of death in newborns and the second leading cause of death in children younger than 5 years of age.

Box 8–2 The subcategories of preterm birth based on GA include extremely preterm (1750 cP *Viscosity is the measurement of a fluid’s internal resistance to flow. It is measured in units of centi­ poise (cP). Source: Adapted from National Dysphagia Diet Task Force, American Dietetic Association. National Dysphagia Diet: Standardization for Optimal Care. Chicago, IL: American Dietetic Association, 2012.

Box 30–5.  Will Mixing Rice Cereal with Breast Milk Provide a Reproducible Consistency? There are concerns that mixing rice cereal with breast milk does not provide a consistently thickened liquid, as the amylase in breast milk breaks down the cereal, thus decreasing the viscosity of the mixture. Therefore, prompt use is recommended.

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Table 30–3. Viscosity Levels of Common Liquids and Purees Using National Dysphagia Diet Descriptors Oral Product Name

Viscosity (cP)

Type of Liquid

1400 cP

Honey-like

Boost®

30 cP

Thin liquid

Boost® Plus

50 cP

Thin liquid

Cream, 50% fat

55 cP

Nectar-like

Ensure Enlive®

1–50 cP

Thin liquid

Ensure®

1–50 cP

Thin liquid

Ensure Plus®

1–50 cP

Thin liquid

Ensure® Pudding

>1751 cP

Spoon-thick

Glucerna® Shake

1–50 cP

Thin liquid

10,000 cP

Spoon-like

3 cP

Thin liquid

15,000 cP

Spoon-like

Peanut butter

250,000 cP

Spoon-like

Resource® 2.0

70 cP

Nectar-like

Boost Breeze®

6 cP

Thin liquid

180 cP

Nectar-like

1 cP

Thin liquid

Baby food, puree

Honey Milk Sour cream

Tomato juice Water

Source: Adapted from the American Dietetic Association, Approximate Viscosity Levels of Common Liquids and Pureed Foods, 2002.

Seating and Positioning Options Specialized seats are available for pediatric patients undergoing VFSS. Adjustments vary among manufacturers; however, these seats are designed to accommodate children of varying ages and allow for changes in positioning and support. For infants and toddlers, a radiolucent seat such as a Tumble Form™ may be placed within the available space of the videofluoroscopy equipment. Alternatively, it may be secured on the lower

end of the videofluoroscopy table when the table is in the vertical position. Regardless of the seating system, infants and children must be positioned as closely to their usual feeding position as possible and secured gently in the seat with Velcro® straps or a soft, cloth seatbelt. It is essential that they are positioned securely and maintain a relatively static position, thereby ensuring safety and minimizing movement during the study. If patients are not securely positioned and are able to freely move about, the radiologist will have difficulty in main-



30. The Videofluoroscopic Swallowing Study

taining an adequate view with the fluoroscopic equipment. Once the procedure is started, adjustments in body position and the height of the seat may be necessary to improve visualization and also to determine their effect on swallowing function. Table 30–4. Varibar® Thickness Categories for Liquids Thin: