Disorders of the Vestibular System: Diagnosis and Management 3031405234, 9783031405235

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Disorders of the Vestibular System Diagnosis and Management Benjamin T. Crane Lawrence Lustig Christopher de Souza Editors

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Disorders of the Vestibular System

Benjamin T. Crane  •  Lawrence Lustig Christopher de Souza Editors

Disorders of the Vestibular System Diagnosis and Management

Editors Benjamin T. Crane Department of Otolaryngology University of Rochester Rochester, NY, USA

Lawrence Lustig Department of Otolaryngology Columbia University New York, NY, USA

Christopher de Souza Department of Otolaryngology Lilavati Hospital Mumbai, Maharashtra, India

ISBN 978-3-031-40523-5    ISBN 978-3-031-40524-2 (eBook) https://doi.org/10.1007/978-3-031-40524-2 © The Editor(s) (if applicable) and The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 This work is subject to copyright. All rights are solely and exclusively licensed by the Publisher, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilms or in any other physical way, and transmission or information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed. The use of general descriptive names, registered names, trademarks, service marks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. The publisher, the authors, and the editors are safe to assume that the advice and information in this book are believed to be true and accurate at the date of publication. Neither the publisher nor the authors or the editors give a warranty, expressed or implied, with respect to the material contained herein or for any errors or omissions that may have been made. The publisher remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. This Springer imprint is published by the registered company Springer Nature Switzerland AG The registered company address is: Gewerbestrasse 11, 6330 Cham, Switzerland

Contents

1

 The Anatomy of the Vestibular System��������������������������������������������������    1 Rafael da Costa Monsanto, Henrique Furlan Pauna, and Sebahattin Cureoglu

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 The Physiology of the Vestibular System ����������������������������������������������   13 Jorge Spratley, Pedro Marques, and Pedro Alexandre

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 Tests to Evaluate the Vestibular System������������������������������������������������   27 Alexander Chern and Lawrence Lustig

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Menière’s Disease ������������������������������������������������������������������������������������   63 Hitomi Sakano and Benjamin T. Crane

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Vestibular Neuritis ����������������������������������������������������������������������������������   91 T. Logan Lindemann and Pamela C. Roehm

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Third Mobile Window Syndromes ��������������������������������������������������������  103 Benjamin T. Crane and Lloyd B. Minor

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Benign Paroxysmal Positional Vertigo ��������������������������������������������������  121 Carol A. Foster

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Traumatic Causes of Vertigo ������������������������������������������������������������������  145 Christopher de Souza, Rosemarie de Souza, Aishan Patil, Adip Shetty, Vimal Someshwar, and Manish Srivastav

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Vestibular Ototoxicity������������������������������������������������������������������������������  167 Christopher de Souza, Rosemarie de Souza, and Aishan Patil

10 Balance  and Vestibular Disorders in Children and Adolescents ��������  179 Joshua Gurberg, Henri Traboulsi, and Jacob R. Brodsky 11 Vestibular Migraine ��������������������������������������������������������������������������������  201 Danielle M. Gillard and Jeffrey D. Sharon

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Contents

12 Persistent Postural-Perceptual Dizziness ����������������������������������������������  229 Jeffrey P. Staab 13 Psychological  Morbidity in Patients with Vestibular Disorders����������  247 Jeffrey P. Staab 14 Vestibular Rehabilitation: A Patient-­Centered Approach��������������������  263 Eric R. Anson and Yoav Gimmon 15 Vestibular Implants����������������������������������������������������������������������������������  301 E. Loos, N. Verhaert, E. Devocht, N. Guinand, A. Perez-Fornos, C. Desloovere, and R. van de Berg 16 Aging  and the Vestibular System������������������������������������������������������������  317 Adam Thompson-Harvey and Yuri Agrawal Index������������������������������������������������������������������������������������������������������������������  333

Contributors

Yuri  Agrawal  Division of Otology, Neurotology, and Skull Base Surgery, Department of Otolaryngology—Head and Neck Surgery, Johns Hopkins University School of Medicine, Baltimore, MD, USA Pedro Alexandre  Department of Otorhinolaryngology, S. João University Hospital Center, Porto, Portugal Department of Surgery and Physiology, Faculty of Medicine University of Porto, Porto, Portugal Eric  R.  Anson  Department of Otolaryngology, University of Rochester, Rochester, NY, USA Department of Neuroscience, University of Rochester, Rochester, NY, USA Department of Physical Therapy, Strong Memorial Hospital, Rochester, NY, USA Jacob  R.  Brodsky  Department of Otolaryngology and Communication Enhancement, Boston Children’s Hospital, Boston, MA, USA Alexander  Chern  Department of Otolaryngology—Head and Neck Surgery, NewYork-Presbyterian/Columbia University Irving Medical Center and Columbia University Vagelos College of Physicians and Surgeons, New York, NY, USA Benjamin  T.  Crane  Departments of Otolaryngology, Neuroscience, and Biomedical Engineering, University of Rochester, Rochester, NY, USA Sebahattin  Cureoglu  Department of Otolaryngology, Head and Neck Surgery, University of Minnesota, Minneapolis, MN, USA Rafael  da Costa  Monsanto  Otopathology Laboratory, Otolaryngology, Head and Neck Surgery, University Minneapolis, MN, USA

Department of of Minnesota,

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Contributors

C.  Desloovere  Department of Neurosciences, Research Group ExpORL, KU Leuven, University of Leuven, Leuven, Belgium Department of Otorhinolaryngology—Head and Neck Surgery, University Hospitals Leuven, Leuven, Belgium Christopher de Souza  Lilavati Hospital, Mumbai, India Holy Family Hospital, Mumbai, India Holy Spirit Hospital, Mumbai, India Faculty SUNY Brooklyn, Brooklyn, NY, USA LSUHSC, Shreveport, LA, USA Rosemarie  de Souza  Department of Internal Medicine, BYL Nair Hospital, Mumbai, India E.  Devocht  Department of ENT/Audiology, School for Mental Health and Neuroscience (MHENS), Maastricht University Medical Center, Maastricht, The Netherlands Carol  A.  Foster  Department of Otolaryngology—Head and Neck Surgery, University of Colorado School of Medicine, Aurora, CO, USA Danielle  M.  Gillard  Department of Otolaryngology/Head and Neck Surgery, University of California, San Francisco, CA, USA Yoav  Gimmon  Department of Physical Therapy, Faculty of Social Welfare & Health Studies, University of Haifa, Haifa, Israel Department of Otolaryngology—Head and Neck Surgery, Sheba Medical Center, Tel-Hashomer, Israel N.  Guinand  Division of Otorhinolaryngology and Head-and-Neck Surgery, Department of Clinical Neurosciences, Geneva University Hospitals, Geneva, Switzerland Joshua  Gurberg  Department of Otolaryngology—Head and Neck Surgery, Pediatric Surgery, Montreal Children’s Hospital, Montreal, QC, Canada T.  Logan  Lindemann  Lewis Katz School of Medicine at Temple University, Philadelphia, PA, USA E.  Loos  Department of Neurosciences, Research Group ExpORL, KU Leuven, University of Leuven, Leuven, Belgium Department of Otorhinolaryngology—Head and Neck Surgery, University Hospitals Leuven, Leuven, Belgium Department of ENT/Audiology, School for Mental Health and Neuroscience (MHENS), Maastricht University Medical Center, Maastricht, The Netherlands Lawrence  Lustig  Department of Otolaryngology—Head and Neck Surgery, NewYork-Presbyterian/Columbia University Irving Medical Center and Columbia University Vagelos College of Physicians and Surgeons, New York, NY, USA

Contributors

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Pedro  Marques  Department of Surgery and Physiology, Faculty of Medicine University of Porto, Porto, Portugal Section of Vestibular Disorders, Department of Otorhinolaryngology, S.  João University Hospital Center, Porto, Portugal Lloyd B. Minor  Department of Otolaryngology-Head and Neck Surgery, Stanford Medicine, Stanford, CA, USA Aishan Patil  Vascular Surgery, Borders General Hospital, Melrose, Scotland, UK Henrique  Furlan  Pauna  Departamento de Otorrinolaringologia, Hospital Universitário Cajuru, Pontifícia Universidade Católica do Paraná (PUC-PR), Curitiba, Paraná, Brazil A.  Perez-Fornos  Division of Otorhinolaryngology and Head-and-Neck Surgery, Department of Clinical Neurosciences, Geneva University Hospitals, Geneva, Switzerland Pamela  C.  Roehm  Division of Otolaryngology, St. Christopher’s Hospital for Children, Philadelphia, PA, USA Hitomi  Sakano  Department of Otolaryngology, University of Rochester, Rochester, NY, USA Jeffrey  D.  Sharon  Department of Otolaryngology/Head and Neck Surgery, University of California, San Francisco, CA, USA Adip Shetty  Rajawadi Hospital, Mumbai, India Vimal Someshwar  KD Ambani Hospital, Mumbai, India Jorge Spratley  Department of Otorhinolaryngology, S. João University Hospital Center, Porto, Portugal Department of Surgery and Physiology, Faculty of Medicine University of Porto, Porto, Portugal Center for Health Technology and Services Research (CINTESIS), Health Research Network (RISE-TL4), Porto, Portugal Manish Srivastav  KD Ambani Hospital, Mumbai, India Jeffrey  P.  Staab  Department of Psychiatry and Psychology, Mayo Clinic, Rochester, MN, USA Department of Otorhinolaryngology—Head and Neck Surgery, Mayo Clinic, Rochester, MN, USA Adam  Thompson-Harvey  Department of Otolaryngology and Communication Sciences, Medical College of Wisconsin, Milwaukee, WI, USA

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Contributors

Henri  Traboulsi  Division of Pediatric Otolaryngology, Department of Surgery, Texas Children’s Hospital, Baylor College of Medicine, The Woodlands, TX, USA R.  van de Berg  Department of ENT/Audiology, School for Mental Health and Neuroscience (MHENS), Maastricht University Medical Center, Maastricht, The Netherlands N. Verhaert  Department of Neurosciences, Research Group ExpORL, KU Leuven, University of Leuven, Leuven, Belgium Department of Otorhinolaryngology—Head and Neck Surgery, University Hospitals Leuven, Leuven, Belgium

Chapter 1

The Anatomy of the Vestibular System Rafael da Costa Monsanto, Henrique Furlan Pauna, and Sebahattin Cureoglu

Introduction The inner ear consists of bony and membranous structures. The bone forms around the membranous labyrinth during fetal development and reaches its final form and size around 16 weeks of gestational age. The membranous labyrinth is housed in a densely packed bone, considered to be the hardest bone in the human body, which is the otic capsule. Galen, in the second century AD, named the inner ear “the labyrinth,” considering the complexity of its anatomical structure [1]. In the nineteenth century, the function of the vestibular labyrinth was only found to be related to balance and not to hearing. Marie Jean-Pierre Flourens was the first author to report that the semicircular canals were part of the balance system rather than the auditory system [2]. In her experimental studies, she observed that the destruction of pigeons’ semicircular canals affected their postural equilibrium and their ability to fly while not significantly affecting their hearing. The bony vestibular labyrinth delineates the semicircular canals and the vestibule. Each of the three semicircular canals is perpendicular to the others (Fig. 1.1). Within these areas are fluid-filled compartments (endolymphatic and

R. da Costa Monsanto (*) · S. Cureoglu Otopathology Laboratory, Department of Otolaryngology, Head and Neck Surgery, University of Minnesota, Minneapolis, MN, USA e-mail: [email protected]; [email protected] H. F. Pauna Departamento de Otorrinolaringologia, Hospital Universitário Cajuru, Pontifícia Universidade Católica do Paraná (PUC-PR), Curitiba, Paraná, Brazil

© The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 B. T. Crane et al. (eds.), Disorders of the Vestibular System, https://doi.org/10.1007/978-3-031-40524-2_1

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R. da Costa Monsanto et al. Superior semicircular canal Utricle Lateral semicircular canal

Posterior

Saccule

Anterior

Crus communis Posterior semicircular canal

Endolymphatic sac

Posterior cranial fossa

Cochlea (basal turn)

Endolymphatic duct (within the vestibular aqueduct)

Cochlear aqueduct

Fig. 1.1  Bony and membranous anatomy of the vestibular labyrinth

perilymphatic), one of which has a potassium-rich fluid (endolymph) and the other a sodium-rich fluid (perilymph). There are several openings in the bony labyrinth, including the small foramina (through which bundles of the vestibular nerve enter the vestibule), the vestibular aqueduct (that houses the endolymphatic duct), and the oval window.

Balance System The vestibular system is divided into two main categories: the central system, which includes the brain, cerebellum, and brainstem, and the peripheral system, which includes the vestibular organs and their pathways to the brainstem. This system as a whole is responsible for maintaining balance, stability, and spatial orientation. The vestibular organs consist of the semicircular canals, the utricle, and the saccule (Fig. 1.2). The semicircular canals are largely responsible for detecting angular accelerations, while the utricle and the saccule detect linear accelerations (including gravity). The saccule is a flattened sac that lies on the medial wall of the vestibule (Figs. 1.2 and 1.3). It is directly attached to the wall of the utricle superiorly; however, no connection exists between these two structures. Its macula is in a vertical position. The

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Superior canal

Utricle

Posterior canal

Vestibule

Saccule

Fig. 1.2  Relative positions of the membranous structures of the vestibular portion of the human inner ear

saccule communicates with the cochlear duct (ductus reuniens; Fig.  1.1) and the endolymphatic sinus (saccular duct). The utricle is an oval-shaped tube that lies superior to the saccule on the medial wall of the vestibule (Figs. 1.2, 1.4, 1.5, and 1.6). The utricular duct arises from the inferior part through a cleft-shaped opening to enter the endolymphatic duct. At the cleft-shaped opening, there is a thickened portion that forms the utriculo-endolymphatic (Bast’s) valve, which is responsible

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Fig. 1.3  Two sections of human temporal bones showing the saccular macula. (a) The vertical disposition of the sensory epithelium is shown in light microscopy (4×, Hematoxylin and Eosin). (b) The saccular macula seen in differential contrast interference microscopy showing structural differences between vestibular hair cell types I (1) and II (2)

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b

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Fig. 1.4 A representative human temporal bone section showing important landmarks. (a) Panoram of the external, middle, and inner ears (1×; Hematoxylin and Eosin). (b) and (c) The crista ampullaris and macula of the utricle, which had been marked in (a) in squares. 1: External auditory canal; 2: Tympanic membrane; 3: Malleus; 4: Incus (short process); 5: Middle ear (epitympanum level); 6: Aditus ad antrum; 7: Facial nerve (tympanic portion); 8: Cochlea; 9: Utricle; 10: Lateral semicircular canal; and 11: Internal auditory canal

for controlling the endolymphatic volume (Fig. 1.6) [3, 4]. As opposed to the saccule, the macula of the utricle lies in the horizontal plane. Each inner ear has three semicircular canals that are perpendicular to each other (Figs. 1.1, 1.2, and 1.4). The arrangement of the canals allows them to detect head rotation in multiple directions. The head movements result in displacement of the endolymph inside the ducts, which plays an important role in the physiology of balance. When considering the semicircular canals from both ears, it can be observed that some canals are in the same plane (left superior and right posterior; left posterior and right superior; and left and right lateral canals) (Fig. 1.5). The angle arrangements of the semicircular canals allow them to reconstruct the three-dimensional

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Right posterior canal Left superior canal

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Left posterior canal Right superior canal

Left and right superior canal

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Fig. 1.5  Schematic figure showing the relative planes of the semicircular canals. These planes are important to provide to the central nervous system information on head rotation, as contralateral canals in the same plane provide antagonistic information to the central vestibular system

Fig. 1.6  A representative human temporal bone section of the crista ampullaris of the lateral semicircular canal showing vestibular hair cells as well as transitional and dark cells

angular forces acting on the head. The ducts of the semicircular canals communicate with the utricle via five openings, one of which is the common crus, which consists of the union of the non-ampullated ends of the superior and posterior canals. The sensory epithelium of the vestibule shares structural and functional similarities with the cochlea [5]. In the vestibular apparatus, the sensory epithelium can be found in the form of maculae (utricle and saccule) and cristae (ampulla of the semicircular canals). Each macula is divided by a central curved zone termed striola, where hair-bundle polarization reverses. The polarization is in the direction toward

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the striola in the utricle, and away from the striola in the saccule. In the cristae, the hair cell polarization is away from the utricle in the superior and posterior canals, and toward the utricle in the lateral canal. Similarly to the organ of Corti in the cochlea, the vestibular sensory epithelium contains two different types of hair cells (Figs. 1.3, 1.4, and 1.6). Type I vestibular cells are flask-shaped and have a large nucleus, while type II cells are cylindrical in shape. At birth, the cristae have a higher density of hair cells as compared with the saccule and utricle. Each vestibular hair cell has cilia emerging from its apical portion. The cilia of the vestibular cells are quite different from their cochlear pairs: in the cochlea, the kinocilium is rudimentary, and there is a much larger number of stereocilia. In vestibular hair cells, a single, well-developed kinocilium emerges from the basal body of the cell at the periphery of the bundle. The exact function of the kinocilia is unknown, but it seems to establish the direction of mechanical sensitivity. The stereocilia tend to be shorter in type I hair cells as compared to type II cells. A single kinocilium emerges from the basal body of the cell at the periphery of the bundle. Stereocilia movement toward the kinocilium results in an excitatory stimulus, while displacements away from the kinocilium result in an inhibitory stimulus. The cilia of the hair cells are embedded in a gelatinous substance, the otolithic membrane (saccule and utricle), and the cupulae (semicircular canals). Although the precise composition of these is unknown, it is known that they contain acid mucopolysaccharides. In the otolithic membrane of the saccule and utricle, there is an otoconial layer, which contains crystals composed of calcium carbonate and other ions. At the base of the crista ampullaris and utricular/saccular maculae, two different types of cells are identified: transitional cells and dark cells (Fig. 1.6). Dark cells are distinguished from the surrounding cells by their characteristics: (1) intimate contact with melanin granules and (2) nuclei positioned high and close to the endolymphatic space that is intensely stained by Hematoxylin and Eosin. Transitional cells are cuboid cells located in between the vestibular hair cells and the dark cell epithelium. These cells are cuboid, are not associated with melanin granules, and have large, round nuclei located at the center of the cell body. Although the exact role of these cells is still under debate, it seems that they have similar roles as the stria vascularis in the cochlea, with dark cells being related to the strial marginal cells and transitional cells to the intermediate strial cells. It was demonstrated that dark and transitional cells have ionic transport mechanisms that contribute to the maintenance of the high potassium levels in the endolymph and to endolymph production [6–9].

Endolymphatic Sac and Duct The endolymphatic sac lies within the layers of the dura mater of the posterior fossa, on the posterior surface of the petrous bone. It is connected to the endolymphatic system by the endolymphatic duct, which lies in a bony canal called the vestibular aqueduct (Figs. 1.1 and 1.7).

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Fig. 1.7  Histological anatomy of the human temporal bone (panoram). The squared area represents the utriculo-endolymphatic valve, which controls the outflux of endolymph from the saccule (9) to the endolymphatic duct and sinus (12). 1: External auditory canal and tympanic membrane; 2: Malleus; 3: Incus (long process); 4: Stapes (footplate, oval window); 5: Protympanum and opening of the Eustachian Tube; 6: Tensor tympani muscle; 7: Facial nerve; 8: Saccule; 9: Utricle; 10: Lateral semicircular canal; 11: Posterior semicircular canal; 12: Endolymphatic duct; 13: Cochlea; 14: Internal auditory canal

Histologically, the endolymphatic duct is lined by squamous and cuboidal cells. The endolymphatic sac has an uneven surface with folds and crypts, in which degenerated cells and otoconia can be found. Some authors divide the endolymphatic sac into three different parts. The proximal part lies within a bony niche; the intermediate part lies partly in a bony niche and partly between layers of the dura mater; its epithelial lining has tall cylindrical cells that are arranged in papillae and crypts. The distal part is embedded within layers of the dura mater; its epithelium is cuboidal. In the lumen of the endolymphatic sac, products of cellular and otoconial degeneration can be found interspersed with free-floating macrophages. The presence of these macrophages suggests that the sac is involved with the immune response [10]. Additionally, the sac seems to be involved in the regulation of endolymph through cytochemical mechanisms. It has been demonstrated that the endolymphatic sac expresses receptors for vasopressin and aquaporin 2 [11].

Innervation Two distinct nerves can be found in the internal auditory canal that relate to vestibular function. The superior vestibular nerve receives fibers from the cristae of the superior and lateral semicircular canals, from the macula of the utricle, and from the

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Fig. 1.8 (a) Representative human temporal bone section showing the facial (3) and superior vestibular (4) nerves within the internal auditory canal. The squared area in (a) is shown at a higher magnification in (b) showing Scarpa ganglion cells of the superior vestibular nerve within the internal auditory canal. 1: Internal auditory canal; 2: Cochlea; 3: Facial nerve (intrameatal and tympanic portions); 4: Superior vestibular nerve traveling from the internal auditory canal toward the utricle and crista ampullaris of the lateral canal; 5: Utricle; 6: Lateral semicircular canal; 7: Posterior semicircular canal; 8: Middle ear cleft

anterosuperior portion of the macula of the saccule. The inferior vestibular nerve receives fibers from the cristae of the posterior semicircular canal and most of the saccular macula. The vestibular afferent neurons have their cell bodies in Scarpa’s ganglion, which sends a peripheral axon toward the vestibular sense organs and a central axon to the vestibular nuclei in the brainstem (Fig. 1.8). At birth, humans have an average of 22,000 cells in Scarpa’s ganglion [12]. The axons of the vestibular afferents are myelinated and heterogeneous in caliber. Large fibers give rise to calyceal terminals that embrace the hair cells, while smaller fibers end in small bouton-type terminals [13]. Efferent vestibular system fibers were also identified in experimental studies. They are located ventromedial to the ventral portion of the lateral vestibular nucleus. The efferent neurons seem to be cholinergic and produce other neurotransmitters and neuromodulators. After emerging from the brainstem, vestibular efferent fibers travel along the cochlear efferent fibers in the vestibular nerve trunk as far as the saccular ganglion, at which point they diverge at almost right angles to each organ. The fibers then supply the maculae and cristae. When activated, these efferent fibers result in a complex mix of excitatory and inhibitory effects on the responses of vestibular afferents. In the central nervous system, the vestibular nerve fibers connect to the four vestibular nuclei on the floor of the IV ventricle. These nuclei contact the oculomotor centers (nuclei of the III, IV, and VI cranial nerves) through the medial longitudinal fasciculus and reach centers in the neck and along the spinal cord (vestibulospinal tracts).

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The main function of the vestibular system is to inform the central nervous system of the position and movements of the head and the body. This implies on correcting the eye movements to keep them in harmony with the body movements. The vestibular system is extensively controlled by the cerebellum, which sends fibers to all the vestibular nuclei. The maintenance of the body’s equilibrium depends fundamentally on three systems: the eyes, the proprioceptive receptors, and the vestibular organs. It is well known, clinically, that to maintain body balance, at least two of these systems must be normal. It is now known that there are tracts arising from the oculomotor centers and from areas of the brain that process proprioceptive information and that bring information to the vestibular nuclei. These nuclei, therefore, are the integrators of the body balance system [14–16].

Vascular Supply The arterial supply to the membranous labyrinth is comprised of branches that also supply the bony labyrinth and the middle ear cleft. However, only some of these branches penetrate the endosteal layer of the bony labyrinth to supply the membranous structures. The anterior inferior cerebellar artery gives rise to the labyrinthine artery and the subarcuate artery before taking a recurrent course to the cerebellum (Fig. 1.9). The labyrinthine artery divides into the common cochlear artery and the anterior vestibular artery. The common cochlear artery divides into the main cochlear and vestibulocochlear branches. The vestibulocochlear artery branches into the posterior vestibular artery and the cochlear ramus. Of these branches, the anterior vestibular

Anterior inferior cerebellar artery Labyrinthine artery

Basilar artery Anterior vestibular artery

Arteries of the canals

Common cochlear artery

Main cochlear artery

Posterior vestibular Cochlear ramus artery Vestibulocochlear artery artery

Fig. 1.9  Sketch showing the principal arteries of the inner ear

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Vestibulocochlear vein

Anterior vestibular vein

Vein of vestibular aqueduct

Veins of the canals Posterior spiral Anterior vein spiral Common modiolar vein vein

Vein of the round window Vein at cochlear aqueduct

Posterior vestibular vein

Fig. 1.10  Sketch showing the venous drainage system of the human labyrinth

artery supplies: (1) the macula of the utricle; (2) a small part of the macula of the saccule; (3) the cristae and membranous canals of the superior and lateral semicircular canals; and (4) the superior surfaces of the utricle and saccule. The posterior vestibular artery supplies the macula of the saccule, the crista, and the inferior surfaces of the utricle and saccule. Regarding venous drainage (Fig. 1.10), the anterior vestibular vein carries blood from the utricle and the ampullae of the superior and lateral canals. The posterior vestibular vein drains the saccule, ampulla of the posterior canal, and basal end of the cochlea. The semicircular canals are drained by vessels that pass toward their utricular ends to form the vein of the vestibular aqueduct, which accompanies the endolymphatic duct and drains into the lateral venous sinus.

References 1. Hawkins JE, Schacht J. Sketches of otohistory. Part 8: The emergence of vestibular science. Audiol Neurootol. 2005;10(4):185–90. https://doi.org/10.1159/000085076. 2. Yildirim FB, Sarikcioglu L. Marie Jean Pierre Flourens (1794–1867): an extraordinary scientist of his time. J Neurol Neurosurg Psychiatry. 2007;78(8):852. https://doi.org/10.1136/ jnnp.2007.118380. 3. Hofman R, Segenhout JM, Buytaert JAN, Dirckx JJJ, Wit HP.  Morphology and function of Bast’s valve: additional insight in its functioning using 3D-reconstruction. Eur Arch Otorhinolaryngol. 2008;265(2):153–7. https://doi.org/10.1007/s00405-­007-­0424-­8. 4. da Costa MR, Pauna HF, Kwon G, et al. A 3-dimensional analysis of the endolymph drainage system in Meniere’s disease. Laryngoscope. 2017;127(5):E170–5. https://doi.org/10.1002/ lary.26155.

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5. da Costa Monsanto R, Schachern P, Paparella MM, Cureoglu S, de Oliveira Penido N. Progression of changes in the sensorial elements of the cochlear and peripheral vestibular systems: the otitis media continuum. Hear Res. 2017;351:2–10. https://doi.org/10.1016/j. heares.2017.05.003. 6. Ciuman RR.  Stria vascularis and vestibular dark cells: characterisation of main structures responsible for inner-ear homeostasis, and their pathophysiological relations. J Laryngol Otol. 2009;123(2):151–62. https://doi.org/10.1017/S0022215108002624. 7. Mittal R, Aranke M, Debs LH, et al. Indispensable role of ion channels and transporters in the auditory system. J Cell Physiol. 2017;232(4):743–58. https://doi.org/10.1002/jcp.25631. 8. Nin F, Yoshida T, Sawamura S, et al. The unique electrical properties in an extracellular fluid of the mammalian cochlea; their functional roles, homeostatic processes, and pathological significance. Pflugers Arch. 2016;468(10):1637–49. https://doi.org/10.1007/s00424-­016-­1871-­0. 9. Zdebik AA, Wangemann P, Jentsch TJ.  Potassium ion movement in the inner ear: insights from genetic disease and mouse models. Physiology (Bethesda). 2009;24:307–16. https://doi. org/10.1152/physiol.00018.2009. 10. Kämpfe Nordström C, Danckwardt-Lillieström N, Laurell G, Liu W, Rask-Andersen H.  The human endolymphatic sac and inner ear immunity: macrophage interaction and molecular expression. Front Immunol. 2019;9. https://www.frontiersin.org/articles/10.3389/ fimmu.2018.03181. Accessed 19 Dec 2022. 11. Sawada S, Takeda T, Kitano H, Takeuchi S, Kakigi A, Azuma H.  Aquaporin-2 regulation by vasopressin in the rat inner ear. Neuroreport. 2002;13(9):1127–9. https://doi. org/10.1097/00001756-­200207020-­00011. 12. Velázquez-Villaseñor L, Merchant SN, Tsuji K, Glynn RJ, Wall C, Rauch SD. Temporal bone studies of the human peripheral vestibular system. Normative Scarpa’s ganglion cell data. Ann Otol Rhinol Laryngol Suppl. 2000;181:14–9. https://doi.org/10.1177/00034894001090s503. 13. Merchant SN, Nadol J.  Schuknecht’s pathology of the ear. People’s Medical Publishing House; 2010. 14. Agrawal Y, Ward BK, Minor LB. Vestibular dysfunction: prevalence, impact and need for targeted treatment. J Vestib Res. 2013;23(3):113–7. https://doi.org/10.3233/VES-­130498. 15. da Costa R, Monsanto KALP, Tomaz A, Abrahão Elias TG, Paparella MM, de Oliveira PN. Evaluation of vestibular symptoms and postural balance control in patients with chronic otitis media. J Vestib Res. 2020;30:35. Published online 15 Feb 2020. https://doi.org/10.3233/ VES-­200691. 16. Yasuda T, Nakagawa T, Inoue H, Iwamoto M, Inokuchi A.  The role of the labyrinth, proprioception and plantar mechanosensors in the maintenance of an upright posture. Eur Arch Otorhinolaryngol. 1999;256(1):S27–32. https://doi.org/10.1007/PL00014149.

Chapter 2

The Physiology of the Vestibular System Jorge Spratley, Pedro Marques, and Pedro Alexandre

Introduction Human evolution has advanced through a variety of steps, of which one of the most significant has been the progress to bipedal locomotion and a vertical posture. This upright position, which allows walking and improves access to environmental awareness and vigilance, has been reached through an extremely delicate adaptation of a series of systems, which include arch reflexes and neurogenic modulation and harmonization encompassing the vestibular, ocular, proprioceptive, and central nervous systems. In fact, body balance results from the multisensorial integration centered in the vestibular nuclei, which sends information to motor structures, including the cerebellum and spinal cord, which play an important role in postural dynamics and J. Spratley (*) Department of Otorhinolaryngology, S. João University Hospital Center, Porto, Portugal Department of Surgery and Physiology, Faculty of Medicine University of Porto, Porto, Portugal Center for Health Technology and Services Research (CINTESIS), Health Research Network (RISE-TL4), Porto, Portugal P. Marques Department of Surgery and Physiology, Faculty of Medicine University of Porto, Porto, Portugal Section of Vestibular Disorders, Department of Otorhinolaryngology, S. João University Hospital Center, Porto, Portugal P. Alexandre Department of Otorhinolaryngology, S. João University Hospital Center, Porto, Portugal Department of Surgery and Physiology, Faculty of Medicine University of Porto, Porto, Portugal © The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 B. T. Crane et al. (eds.), Disorders of the Vestibular System, https://doi.org/10.1007/978-3-031-40524-2_2

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Dynamic oculomotor control Vision Thalamocortical projections Vestibular Nuclei

Vestibular system

Dynamic postural control Proprioception

Spatial orientation

Fig. 2.1  Mechanisms involved in balance

oculomotor control. Also, ascending projections towards the cortex contribute to cognitive functions such as spatial orientation and memory [1–3] (Fig. 2.1).

Embryogenesis of the Inner Ear Phylogenetics The development of a vestibular organ dates back around 500 million years, with the development of the statocyst in species belonging to the coelenterates phylum, such as hydras or jellyfish [4]. In addition to the gravity detection mechanism, it is likely that the statocyst allowed the organism to respond to sound waves. Regarding the phylogenetic development of the labyrinth, the vestibular part developed first, while the cochlear organ appeared later [5]. The mammalian ear, in which the human ear is included, is divided into outer, middle, and inner ear. The ear components derive from neural crest cells and the three germ layers (ectoderm, mesoderm, and endoderm), and their embryologic development is associated with the first and second pharyngeal arches [6, 7]. The inner ear originates from the ectoderm and is the first part of the ear to develop.

Embryology Around the fourth week of gestation, a thickening of the ectoderm, the otic placode, appears. It soon starts to invaginate the surrounding mesoderm, creating the otic pit [5, 7]. Fusion of the otic pit edges originates in the otic vesicle, or otocyst, the

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precursor to the membranous labyrinth. Thus, the membranous labyrinth inner layer derives from the ectoderm, while the outer layer is of mesodermal origin [7, 8]. The otocyst has two distinct regions: a dorsal vestibular/utricular part, which will give rise to the utricle, semicircular canals (SCCs), and endolymphatic duct, and a ventral auditory/saccular part, from which the saccule and cochlear duct originate [7, 9]. The otic capsule formation begins with a process of chondrification of the mesenchyme around the otocyst that originates a cartilaginous otic capsule. Later, the cartilage is reabsorbed and replaced by bone [5, 7]. These structures will develop to form the well-known vestibular and cochlear organs and the corresponding sensory epithelium that comprises the cristae of the SCCs, the utricular and saccular maculae, and the organ of Corti. The development of the inner ear ends, and the labyrinth reaches its adult size and shape around the 20th to 22nd week of gestation [7].

Anatomy of the Bony and Membranous Labyrinth The inner ear, or labyrinth, is enclosed within the petrous part of the temporal bone and contains the vestibulocochlear sensory organs [8]. It is composed of a series of hollow channels and cavities in the temporal bone—the bony labyrinth—inside which are located channels bounded by a membranous wall—the membranous labyrinth. The membranous labyrinth is composed of individual structures that are continuous with each other: the three SCCs, the utricle, the saccule, the cochlear duct, and the endolymphatic duct and sac [5]. The space between the bony labyrinth and the external surface of the membranous labyrinth is filled with perilymphatic fluid, while the membranous labyrinth contains endolymph. Globally, the inner ear has a posterior part, corresponding to the SCCs: a middle part, the vestibule (both associated with the vestibular function); and an anterior part, the cochlea, dedicated to the auditory function. The SCCs are three bony tunnels with a corresponding membranous canal on the interior. According to their spatial orientation in the anatomical position, they are named the superior (or anterior), horizontal (or lateral), and posterior SCCs. Each one has two extremities, both opening to the vestibule. One of the extremities in each canal has a dilation corresponding to the ampulla, which contains the crista ampullaris, where lies the sensory epithelium of the SCCs. The non-ampullary ends of the posterior and superior canals join to form a common opening in the vestibule (crus commune). The vestibule is a cavity with an oval shape, inside which reside the otolith organs, the utricle and saccule [8]. Each one consists of a membranous chamber filled with endolymph and containing a macula composed of sensory epithelium [5]. The medial wall of the vestibule lodges the utricle in a superior recess and the saccule in an inferior recess [10]. A narrow utricular canal and saccular canal emerge from the respective chambers and join in a common tunnel, forming the endolymphatic duct [8]. The endolymphatic duct (a component of the membranous labyrinth) runs inside the corresponding structure in the bony otic capsule, the vestibular

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aqueduct. The endolymphatic duct end enlarges to form the endolymphatic sac that rests on the posterior surface of the petrous bone, enveloped in dura layers [11]. Anteriorly, the cochlea is a spiraled bony canal displayed in a conical shape, with 2½ to 2¾ turns around a central bony axis, the modiolus, in which the cochlear nerve and spiral ganglion are situated [12]. The membranous labyrinth part located inside the cochlea takes the name of the cochlear duct (scala media) and is filled with endolymph. A narrow canal, the ductus reuniens, connects the cochlear duct with the vestibule. Superior to the cochlear duct and separated from it by Reissner’s membrane, lies the vestibular duct (scala vestibuli). The tympanic duct (scala tympani) is situated inferior to the cochlear duct and separated from it by the basilar membrane. Both vestibular and tympanic ducts contain perilymph and join each other at the cochlear apex—the helicotrema. The vestibular duct extends from the vestibule to the helicotrema, and the tympanic duct begins at the round window on the medial wall of the tympanic cavity.

How Do These Structures Interact? In line with the previous section on anatomy, the current chapter will offer an integrated overview of the mechanisms, functions, and pathways of the vestibular system that, in brief, allow self-movement detection. The main targets of this accurate system are to: (1) to ensure gaze stabilization; (2) enable balanced locomotion and body position; (3) provide general orientation of the body with respect to gravity; and (4) readjust autonomic functions after body reorientation. As described, the posterior pars of the labyrinth is composed of the vestibule and SCCs. Inside the vestibule, two vesicles can be found: the saccule and utricle, which contain ciliated neuroepithelial cells aggregated in the macula and are covered with a gel topped with calcium carbonate otoconia (Fig. 2.2). Fig. 2.2 Spatial orientation of utricle’s and saccule’s macula

rior

supe Saccular macula

an

ter

striola

ior

Utricular macula l

latera

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In the upright position, the macula of the saccule stands vertically, and the macula of the utricle stands in the horizontal plane. These two structures, due to the specific weight and inertia of the otoconia, are essentially sensitive to forces of linear acceleration and gravity as a result of minute displacements of the otoconia. In contrast, the SCCs—superior, lateral, and posterior—are orthogonally disposed and have each one a terminal dilation or ampulla that lodges the ciliated neuroepithelial cells of the crista ampullaris, covered with a gelatinous cupula that stays inside the ampulla like a sail and moves forward or backward according to endolymph dynamics elicited by angular or rotational movements of the head (Fig. 2.3).

a

b

Fig. 2.3 (a) Crista ampullaris and (b) utricle (courtesy by Vilhena de Mendonça, MD Círculo Médico)

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The cupula, composed of mucopolysacharides produced by the support cells of the cristae, has the same density as the endolymph and therefore does not deflect with linear acceleration. However, rotational movements of the head, in any direction, at least stimulate the crista of one of the SCCs through the inertial movement of the endolymph that deflects the respective cupula. The movement of the endolymph inside the SCC is in the opposite direction from the head rotation. For instance, a head rotation to the right on the horizontal plane leads to a flow of endolymph towards the ampulla (ampullopetal), creating an excitatory stimulus to the crista of the right horizontal SCC and away from the ampulla (ampullofugal) on the left horizontal semicircular, leading to an inhibitory stimulus on this side. The function of the SCC complex was already postulated in 1892 by Ewald [13] –– Head and eye movements occur in the plane of the canal being stimulated and in the direction of the endolymph flow. –– In the horizontal canal, ampullopetal endolymph flow causes a greater response than ampullofugal flow. –– In the vertical canals, ampullofugal endolymph flow leads to a greater response than ampullopetal flow. Each ciliated cell, either the more bottle-shaped type I (Fig.  2.4) or the more cylindrical type II (Fig. 2.5), shows at their apex one big cilium, or kinocilium, and a bundle of 60–100 smaller cilia, or stereocilia [14] (Fig. 2.6), distributed in a “pipe-­ organ” fashion and all connected by proteic myosin bundles [15].

Fig. 2.4  Electron micrograph depicting two type I ciliated cells of the crista ampullaris of the lateral semicircular canal of the rat. Please note the flask-shaped form of the cell and the surrounding nervous calyx: (1) amyelinated calyx; (2) endpoint of the myelin sheet of the afferent nerve; (3) efferent synapsis; (4) type I cell nucleus; (5) Golgi apparatus; (6) cilia; (7) granules in support cell; (8) apical microvilli; and (9) nucleus of type II ciliated cell. (Courtesy of Jorge Spratley, MD, PhD)

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Fig. 2.5 Electron micrograph depicting a type II ciliated cell of the crista ampullaris of the lateral semicircular canal of the rat. Please note the cylindrical shape of the cell. (1) Nucleus and (2) Cilia. (Courtesy of Jorge Spratley, MD, PhD)

The movement of the stereocilia toward the kinocilium leads to a change in the permeability of the cell and its subsequent depolarization with the creation of a positive action potential (Fig. 2.7), which is transmitted to the nerve through the synapse at the cell base. The opposite movement—the stereocilia away from the kinocilium—in contrast, leads to the repolarization of the cell. These phenomena in the SCCs—depolarization on the right ear, repolarization on the left ear, and vice versa—occur simultaneously in a symmetrical fashion, leading to a precise perception of the central nervous system nuclei of the direction of the movement.

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a

b

Fig. 2.6 (a) Electron micrograph depicting the cilia in a transversal section. (1) Kinocilium showing the typical array of nine pairs of microtubules. (2) Steriocilium, composed by an amorphous matrix of actin. (Courtesy of Jorge Spratley, MD, PhD). (b) Electron micrograph depicting the cilia in a longitudinal section. (1) Kinocilium; (2) steriocilia; (3) cuticular plate; and (4) union complex. (Courtesy of Jorge Spratley, MD, PhD)

Rest

Towards the Kinocilium

Rest

Excitation

Vestibular nerve discharge velocity

Fig. 2.7  Signal transduction in the vestibular system

Away from the Kinocilium

Inhibition

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Vestibular–Ocular Reflex The vestibular–ocular reflex (VOR) is a response that permits the ocular fovea to remain on a target while the head moves. It actually allows the individual to recognize faces or read while moving, such as while walking or, even, after high-­frequency head movements. It essentially responds to head accelerations, which can reach up to several thousands of degrees per square second. When sustained velocity is reached, the acceleration is no longer detected, and the stimulation is suspended after a few seconds as the cupula repositions itself in its central position. This is possible because there is a response of the extrinsic muscles of the eye, when functioning properly, which leads the eye to move in the opposite direction of the head while keeping the same velocity and amplitude. If this system is not working properly and accurately, either due to a velocity or amplitude deficiency, the shift in gaze causes a retinal slip that is perceived as an image movement, designated by oscillopsia. The information needed for these compensatory eye movements makes use of inputs from: –– SCCs and the otholits (VOR) –– Retina (optokinetic reflex) –– Neck somatosensors (cervico-ocular reflex) These different loops provide convergent and redundant information (“functional overlapping”), a partial compensation for each other’s deficiencies (“functional substitution”), and preferred frequency ranges of action (“functional specialization”) [16]. The pathways involved are complex and encompass neuronal information transmitted from the vestibular system, with an increased weight in the SCCs, to the oculomotor muscles. A classical three-neuron vestibular reflex pathway originates in the vestibular end organs, where fine-tuned motion sensors generate and transmit signals to the first-order bipolar vestibular ganglion cells, whose axons transmit signals to the vestibular nuclei neurons, which are then spread in the brainstem. Second-order vestibular nuclei neurons participating in the reflex pathways signal third-order, cranial, and spinal motor neurons, which control gaze, posture, and balance. Altogether, there are three major vestibular reflex pathways that regulate eye movements and balance essentially without involving cortical structures [17, 18]. Predictably, as it is actually easier to understand, we will illustrate how information is essentially conducted on the plane of the horizontal SCC (Fig. 2.8) [19]. The same occurs in the other planes, but due to the stimulation of different oculomotor muscles, the ocular movements are more complex. Indeed, there are three types of rotationally induced eye movements to be considered: horizontal, vertical, and torsional. Each of the six pairs of oculomotor muscles has to be coordinated to produce the desired response. The vertical SCCs and the saccule are sensible for controlling vertical eye movements, whereas the horizontal canals and the utricle regulate

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LR

MR

Oculomotor Nucleus (III)

MR

IR IO SR MR ATD

Trochlear Nucleus (IV)

Abducens Nucleus (VI)

LR

MLF

S

SG

L Inhibitory neuron Excitatory neuron

M I

Vestibular Nuclei

Fig. 2.8  Direct pathways of the horizontal semicircular canal vestibular–ocular reflex (adapted from Baloh 2001 [20]). SC scarpa ganglion, S superior nucleus, L lateral nucleus, M medial nucleus, I inferior nucleus, MLF medial longitudinal fasciculus, ASD ascending tract of Deiters, IR inferior rectus, IO inferior oblique, SR superior rectus, MR medial rectus, LR lateral rectus

horizontal eye movements. Torsional eye movements are essentially controlled by the vertical SCCs as well as by the utricle (Table 2.1). The first afferent neuron synapsis is in the respective vestibular nuclei associated with a particular SCC (Table 2.1). In the specific case of the lateral SCC, this occurs in the lateral vestibular nuclei. Specifically, when the head turns (accelerates) to the right (clockwise), on the precise plane of the horizontal SCC (Fig. 2.9), an ampullopetal endolymphatic flow occurs on the right side and an ampuloffugal flow on the left. As acknowledged, this action originates a deflection of the cupula and the cilia in the crista ampullaris of the right SCC towards the kinocilium and, consequently, the opening of mechanosensory K+ and voltage-gated Ca2+ channels, initiating an influx of both these ions into the cell with a subsequent depolarization. The previously described spontaneous basal activity of these sensory organs at rest also allows a status of hyperpolarization and inhibition on the left side, as the exact opposite motion occurs as a

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Table 2.1  Vestibular organs and oculomotor Ipsilateral and contralateral activation Vestibular organ Anterior SCC

Vestibular nucleus Superior

Ipsilateral oculomotor muscle Superior rectus

Contralateral oculomotor muscle Superior obliquus

Lateral SCC

Medial

Medial rectus

Lateral rectus

Posterior SCC

Medial

Superior obliquus

Inferior rectus

Utricle

Lateral

Saccule

Lateral

Interstitial nucleus of Cajal and from there to the oculomotor and trochlear nuclei Vestibulospinal pathways

SCC semicircular canal Fig. 2.9 Horizontal vestibular-–ocular reflex neuronal’s drift overview

Ocular motion Upward and contradirectional torsional Conjugate deviation of the eyes to the opposite side Downward and contradirectional torsional

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consequence of the reverse orientation of the cilia in the crista ampullaris on this side. During physiological rotatory stimulation, it has been revealed that the change in frequency of action potentials is roughly proportional to the deviation of the cupula [21]. This asymmetric information reaches the vestibular nuclei in the brainstem, mainly in the medial vestibular nuclei, where different connections mediate the VOR from the SCC to the oculomotor muscles (Fig. 2.9). In the situation presented, the vestibular nuclei interpret the discharge rates’ difference between left and right SCCs as movement to the right and therefore trigger the oculomotor nuclei to drive the eyes to the left to maintain gaze. The eye response to a head rotation resides in a slow phase until the eye reaches the edge of the outer canthus and a fast phase as a reset to the initial position. This pattern repeats itself as long as the stimulus continues, and these two types of repeated movements, as a saw-tooth pattern, characterize the vestibular nystagmus variety. The direction of the nystagmus is denominated by the fast phase, as it is the easiest to perceive. These movements can also be identified and characterized by vestibular testing procedures such as conventional videonystagmography.

Vestibulo-spinal and Vestibulo-colic Reflexes While the extraocular muscles are responsible for the compensatory ocular response to movement, through the VOR, the extensor muscles of the neck, trunk, and limbs are accountable for the body response through the vestibulo-colic and vestibulo-­ spinal reflexes. These reflexes trigger automatic compensatory movement of the head/trunk in very much the same way as with the VOR, controlling and balancing the extensor and flexor muscle tonus. These operate in coordination to achieve an appropriate balance, either in static or dynamic conditions. Gravity, as detected by the otolith system, acts as an additional driving input. Furthermore, proprioceptive and visual information concur to provide the correct body position, as gravity is only detected in the head, regardless of the position of the trunk and lower body. Two functional categories of vestibulo-spinal reflexes can be distinguished: those acting on the limb muscles, which stabilize the position of the trunk in space, and those acting on the neck muscles (vestibulo-colic reflexes), which stabilize the position of the head in space [22]. The two most important vestibular descending pathways involve the lateral vestibulo-­ spinal tract (LVST) and the medial vestibulo-spinal tract (MVST). Reflexive control of head and neck muscles arises through the neurons in the MVST. These neurons comprise the rapid vestibulo-colic reflex, whose role is to stabilize the head in space and to participate in gaze control [23]. Yet, the MVST neurons receive input from both the vestibule and the cerebellum, as well as somatosensory information from the spinal cord. These neurons carry both excitatory and inhibitory signals to innervate neck flexor and extensor motor neurons in the spinal

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cord, which clinically may be detected by the cervical vestibular evoked myogenic potentials (cVEMP). Last but not least, the LVST receives input from the cerebellum, the vestibule, and the proprioceptive sensors of the spinal cord. These same LVST fibers project ipsilaterally to many levels of motor neurons in the spinal cord to ultimately provide coordination of different muscle groups for postural control [24].

References 1. Brandt T, Schautzer F, Hamilton DA, Bruning R, Markowitsch HJ, Kalla R, et al. Vestibular loss causes hippocampal atrophy and impaired spatial memory in humans. Brain. 2005;128(Pt 11):2732–41. 2. Lopez C.  The vestibular system: balancing more than just the body. Curr Opin Neurol. 2016;29(1):74–83. 3. Wiener-Vacher SR, Hamilton DA, Wiener SI. Vestibular activity and cognitive development in children: perspectives. Front Integr Neurosci. 2013;7:92. 4. Gray O. A brief survey of the phylogenesis of the labyrinth. J Laryngol Otol. 1955;69(3):151–79. 5. Engstrom H. Microscopic anatomy of the inner ear. Acta Otolaryngol. 1951;40(1–2):5–22. 6. Anthwal N, Thompson H. The development of the mammalian outer and middle ear. J Anat. 2016;228(2):217–32. 7. Moore KL, Persaud TVN. The developing human: clinically oriented embryology. 10th ed. Elseivier Ltd; 2016. 8. Baloh R, Kerber KA.  Clinical neurophysiology of the vestibular system. 4th ed. Oxford Univesity Press; 2011. 9. Morsli H, Choo D, Ryan A, Johnson R, Wu DK.  Development of the mouse inner ear and origin of its sensory organs. J Neurosci. 1998;18(9):3327–35. 10. Rouvière H, Delmas A.  Anatomía Humana: Descriptiva, Topográfica Y Funciona. 11th ed. Elsevier; 2005. 11. Corrales CE, Mudry A.  History of the endolymphatic sac: from anatomy to surgery. Otol Neurotol. 2017;38(1):152–6. 12. Biedron S, Westhofen M, Ilgner J. On the number of turns in human cochleae. Otol Neurotol. 2009;30(3):414–7. 13. Ewald JR.  Physiologische Untersuchungen ueber das Endorgan des Nervus octavus. Bergmann; 1892. 14. Spoendlin HH. Organization of the sensory hairs in the gravity receptors in utricule and saccule of the squirrel monkey. Z Zellforsch Mikrosk Anat. 1964;62(5):701–16. 15. Engstrom H, Bergstrom B, Ades HW. Macula utriculi and macula sacculi in the squirrel monkey. Acta Otolaryngol Suppl. 1972;301:75–1. 16. Brandt T. In: Brandt T, editor. Vertigo: it’s multisensory syndromes. 2nd ed. London: Springer-­ Verlag; 2003. 17. Wilson VJ, Maeda M. Connections between semicircular canals and neck motorneurons in the cat. J Neurophysiol. 1974;37(2):346–57. 18. Ito M, Nisimaru N, Yamamoto M. Pathways for the vestibulo-ocular reflex excitation arising from semicircular canals of rabbits. Exp Brain Res. 1976;24:257–71. 19. Baloh RW, Kerber K. Baloh and Honrubia’s clinical neurophysiology of the vestibular system. New York: Oxford University Press, Inc.; 2010. 20. Baloh RW, Honrubia V. Clinical neurophysiology of the vestibular system. 3rd ed. New York: Oxford University Press, Inc; 2001.

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21. Goldberg JM, Fernandez C. Physiology of peripheral neurons innervating semicircular canals of the squirrel monkey. 1. Resting discharge and response to constant angular accelerations. J Neurophysiol. 1971;34:635. 22. Wilson VJ, Jones GM. Mammalian vestibular physiology. New York: Plenum Press; 1979. 23. Peterson BW, Goldberg J, Bilotto G, Fuller JH. Cervicocollic reflex: its dynamic properties and interaction with vestibular reflexes. J Neurophysiol. 1985;54(1):90–109. 24. Shinoda Y, Sugiuchi Y, Futami T, Ando N, Kawasaki T. Input patterns and pathways from the six semicircular canals to motoneurons of neck muscles. I.  The multifidus muscle group. J Neurophysiol. 1994;72(6):2691–702.

Chapter 3

Tests to Evaluate the Vestibular System Alexander Chern and Lawrence Lustig

Introduction Maintaining balance involves a complex interplay of the vestibular system, visual system (eyes and related anatomy), and proprioceptive system. Indeed, the etiology of “dizziness” can often be multifactorial and a challenging diagnosis. The thorough evaluation of a dizzy patient should always begin with a thorough history and physical exam, which are often sufficient to obtain a reasonable diagnosis explaining the patient’s symptoms [1]. However, although the majority of vestibular disorders may be elucidated from a thorough history and physical exam, appropriate vestibular tests can help refine the diagnosis and inform management decisions in specific situations. This chapter will focus on clinical and vestibular laboratory tests for the evaluation of the dizzy patient.

Physical Exam and Bedside Vestibular Evaluation A bedside vestibular evaluation is an important adjunct to a thorough otolaryngologic examination. It is important to conduct a detailed neurotologic examination, including a cranial nerve examination, evaluation for nystagmus and oculomotor function, positional tests, and postural tests. A physical examination should include evaluation of spontaneous, gaze-evoked, and headshake nystagmus. Spontaneous and gaze-evoked nystagmus may help A. Chern · L. Lustig (*) Department of Otolaryngology—Head and Neck Surgery, NewYork-Presbyterian/Columbia University Irving Medical Center and Columbia University Vagelos College of Physicians and Surgeons, New York, NY, USA e-mail: [email protected] © The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 B. T. Crane et al. (eds.), Disorders of the Vestibular System, https://doi.org/10.1007/978-3-031-40524-2_3

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localize the lesion in a patient with a suspected vestibular disorder [2]. Peripheral vestibular nystagmus is often suppressed by visual fixation but may be seen during funduscopic examination in the dark. Frenzel goggles have 10× diopter lenses that prevent visual fixation and may also help accentuate nystagmus. Skew deviation and a head tilt may suggest a unilateral disturbance of the vestibulo-­ocular pathways. Shortly after the unilateral vestibular loss, patients perceive the vertical as being tilted 10–30° toward the lesioned side. Although this distortion usually diminishes over time, in some cases it may be present even after vestibular compensation has taken place [3]. Several bedside tests are useful for detecting unilateral vestibular defects. The head impulse test (HIT; also known as the head thrust test, as described by Halmagyi [4]) is a passive head movement test where the examiner suddenly turns the patient’s head rapidly to the right or left along a horizontal plane (yaw plane) while the patient maintains gaze on the examiner. If the vestibulo-ocular reflex (VOR) is normal, the eyes remain fixed on the target. Patients with vestibular hypofunction may generate a “catch-up” saccade (known as the head thrust sign) when the head is rapidly turned toward the side of the lesion—this is considered a positive HIT. The head shake test is an active movement test—the patient turns his or her head vigorously back and forth with eyes closed for about 30 s to “charge” the brainstem’s velocity storage mechanism. Upon stopping and opening the eyes, nystagmus usually beats away from the pathologic side; head-shaking nystagmus is typically absent in normal subjects. “Tapping the head” [5] or application of a 60 Hz vibration stimulus to the mastoid bone [6] may also evoke horizontal beating nystagmus beating away from the side of vestibular hypofunction. Dynamic visual acuity testing is useful for patients suspected of having bilateral vestibular loss [7]. These abnormalities usually correlate with oscillopsia, as gaze stabilization during high-velocity head movements is facilitated by the VOR, which produces compensatory eye movements to stabilize images on the retina. Peripheral vestibular lesions decrease the gain of the VOR and increase retinal image slip during head movements. Worsening visual acuity by at least three lines on a visual acuity chart (i.e., Snellen chart) during head impulses turning from side to side at 1 Hz or more is abnormal. Hyperventilation is known to accentuate downbeating nystagmus in patients with cerebellar lesions [8] and may induce nystagmus toward the side of the vestibular schwannomas [9]. Subjective visual horizontal (SVH) and subjective visual vertical (SVV) are valuable clinical tests to measure otolith function, particularly utricular function [10, 11]. The gravitational input from otoliths usually dominates the patient’s perception of verticality or horizontality. To assess SVH or SVV, the patient is asked to sit with his or her head fixed in an upright position while looking at an illuminated line (i.e., on a computer display or projector) in complex darkness. The patient is asked to adjust the line several times from starting positions at different angles to his SVV or SVH.  In acute peripheral vestibulopathy, there is usually a deviation of SVV or SVH by several degrees toward the affected side. Central compensation will facilitate the gradual improvement of the patient’s tilt perception.

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Positional (or static positional) tests are discussed in the electronystagmography (ENG) and videonystagmography (VNG) portions of this chapter. Positioning (or dynamic positional) tests are also useful. These include the Dix-Hallpike maneuver and the roll test. The Dix–Hallpike maneuver is done to assess for BPPV of the vertical (posterior or anterior) semicircular canals (SCCs). To perform this test, the patient sits upright on the examination table with the head rotated 45° from the sagittal plane to the side. The patient is quickly lowered by the clinician such that the patient’s head hangs off of the table. If rotational or torsional nystagmus is observed, then the patient has BPPV of the posterior SCC ipsilateral to the side the head is turned toward or the anterior SCC contralateral to the side the head is turned toward. This is repeated with the head turned 45° to the other side. The roll test is used to evaluate for BPPV of the horizontal SCCs. With the roll test, the patient is placed in the supine position with the head raised 30° by the clinician. The patient’s head is rotated to both sides for 30 s, watching for horizontal geotropic or apogeotropic nystagmus. The laterality of the lesion is determined by the intensity of the evoked horizontal nystagmus. If geotropic nystagmus is observed, the lesion side is the side on which head movement evokes more intense nystagmus. If ageotropic nystagmus occurs, the lesion side is the side on which head movement evokes less intense nystagmus. Of note, BPPV most commonly occurs in the posterior SCC. Frenzel goggles may be useful for monitoring nystagmus during positioning tests by suppressing fixation. Other bedside tests include postural control tests, such as the Romberg test, tandem gait test, Fukuda stepping test, and past-pointing test. With the Romberg test, the patient is asked to stand erect with feet together and eyes closed. Increased sway or a fall toward either side is considered a positive (abnormal) sign. The basis of the test stems from the thought that balance comes from the combination of proprioception, vestibular input, and vision. If two of these systems are working, the patient should be able to maintain a fair degree of balance. By removing visual input, two of the systems remain, and if there is a vestibular or sensory (i.e., proprioceptive) disorder, the patient is more unbalanced. The tandem gait test has the patient walk in a straight line with one foot placed immediately in front of the other, arms down by their sides, and closed eyes. Healthy individuals can take 10 steps without deviation, while patients with vestibular dysfunction fail this test. The Fukuda stepping test has the patient march in place with eyes closed. After 50–100 steps, the patient is asked to open his or her eyes. A rotation greater than 30° toward one side is considered abnormal. With the past-pointing test, the clinician is facing the patient. The clinician extends his or her arms and points straight ahead with index fingers 6 in. apart. The patient is asked to lift both arms overhead while pointing with both index fingers and then to bring down both arms and touch the clinician’s index fingers while keeping arms extended. This is repeated with the patient’s eyes closed. A deviation to one side is considered a positive or abnormal test. Although the sophistication of the clinical examination of the vestibular patient continues to evolve [12], the clinician may need to quantify vestibular function for validation, prognostication, and treatment planning. Moreover, a vestibular abnormality that is not evident by clinical evaluation may be diagnosed using quantitative

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vestibular testing [13]. Objective evaluations of vestibular function may be useful in facilitating diagnostic refinement and informing management strategies in specific clinical scenarios.

Indications for Vestibular Testing Vestibular tests are tests of function whose purpose is to establish if there are abnormalities in the vestibular portion of the inner ear. If no inner ear abnormality is found, dizziness may be due to central nervous system (CNS) disorders (e.g., migraine, cerebrovascular disease), systematic disorders (e.g., dehydration, peripheral neuropathies), vascular disorders (e.g., hypotension), or psychological problems (e.g., anxiety). Studies suggest that vestibular testing is more accurate than clinical assessment in identifying inner ear disorders [13]. Auditory pathway tests (i.e., audiometry, auditory brainstem response test, and electrocochleography) can also be ordered similarly and are frequently ordered in conjunction with vestibular testing. One analysis demonstrated that hearing evaluation followed by either posturography or ENG was cost-effective [14]. Vestibular tests are also useful in detecting central vestibular disorders. One study demonstrated that internuclear ophthalmoplegia (central eye movement disorder) is missed by 71% of physicians without quantitative oculomotor testing [15]. Vestibular tests can help determine if more expensive tests (e.g., magnetic resonance imaging) are needed—they are more accurate than clinical findings in predicting abnormalities in neurology [16]. Finally, they may be useful to document peripheral vestibular disorders such as benign paroxysmal positional vertigo (BPPV), vestibular neuronitis, and gentamycin ototoxicity.

ENG and VNG ENG or VNG is the first step in vestibular testing. The traditional ENG utilizes electric potentials to detect eye movements, while the newer VNG relies on video analysis of eye motion through infrared cameras. Both rely on the VOR and its ability to generate efficient eye movements to keep the environment steady during head movements. ENG and VNG are useful for detecting any abnormality along that pathway—the peripheral vestibular system or the nerves that connect it to the brain and the eye muscles. These tests have four components: (1) oculomotor tests, (2) positional tests, (3) positioning tests, and (4) caloric tests, which will be detailed below. Equipment Standard ENG equipment consists of the following components [17]: (1) an amplifier of corneoretinal potentials that occur following eye movements, (2) band-pass

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and notch filters for filtering out undesignated muscle activity around the eyes and electrical noise in the room, (3) a signal recorder, (4) a printer, (5) a linear array, and (6) water and air caloric stimulators. The most common techniques used to record eye movements are electrooculography (EOG) for ENG and videooculography (VOG) for VNG.  EOG is a simple, inexpensive test that measures the change in corneoretinal potential by measuring the direction and velocity of eye movements using electrodes typically placed above, below, and to the side of the eyes, along with a ground electrode in the forehead [18]. Infrared VOG is an alternative method of recording eye movements utilizing infrared cameras that measure the eye in the dark for VNG [19]. Torsional eye movements are not recorded with EOG but can be seen with infrared video recordings. VNG may be more accurate and consistent compared to the traditional ENG because it is less sensitive to artifacts (i.e., lid movement artifacts and electrical noise generated by muscle). Clinical Application VNG/ENG is helpful in diagnosing vestibular pathology—since each ear is stimulated separately, the laterality of the disease can be determined. Data from VNG/ ENG can support the diagnosis of pathologies like BBPV, vestibular neuritis, Meniere’s disease, labyrinthitis, and ototoxicity, as well as brainstem and cerebellar diseases affecting oculomotor control mechanisms. With vestibular schwannomas, it may be helpful to predict the nerve from which the tumor originates; caloric weakness may be associated with tumors originating from the superior vestibular nerve. VNG/ENG may also predict whether the patient will experience vertigo after vestibular schwannoma removal. However, sole reliance on VNG/ENG to identify lesions of the CNS is not appropriate—abnormal findings do not necessarily indicate a CNS lesion [20, 21]. See Table 3.1 for comparisons of components of the bedside vestibular examination with subtests of standard VNG/ENG.

Oculomotor Tests Oculomotor tests assess the accuracy, latency, and velocity of eye movements for a given stimulus. The oculomotor test battery includes saccade tests, smooth pursuit tests, optokinetic nystagmus (OKN) testing, gaze-evoked testing, and fixation suppression testing—all of which assess accuracy, latency, and velocity of eye movements for a given stimulus. Abnormalities in oculomotor testing suggest a central neurologic etiology, as these tested eye movements originate in the cerebellum [22]. Saccade Tests Saccades are rapid, ballistic eye movements that abruptly change the point of fixation to bring an object of interest from the periphery of the visual field into the center of the line of sight. Saccades are controlled by the occipitoparietal cortex,

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Table 3.1  Components of bedside vestibular examination and subtests of standard VNG/ENG VNG/ENG subtests Smooth pursuit tracking Optokinetic nystagmus Spontaneous nystagmus Saccade testing

Description of the test Eye movement tracking of a moving target Eye movement response to an optokinetic stimulus Observe for fixation stability and spontaneous nystagmus, if any Observe the velocity, accuracy, and latency of rapid eye movements from one target to another Observe for nystagmus and gaze holding during eccentric gaze

Gaze-evoked nystagmus Static positional Observe for nystagmus during or after head position testing nystagmus Dix–Hallpike Observe for nystagmus after rapid head positioning from the sitting or head maneuver hanging right or left position Bithermal caloric Warm and cool irrigation applied to each ear for comparison of vestibular testing responses Clinical tests of vestibular loss Head thrust sign Looking for a catch-up saccade with quick head turns toward the side of unilateral vestibular loss Head shaking Observe for nystagmus away from the side of unilateral vestibular loss after nystagmus head shaking Vibration-induced Observe for nystagmus away from the side of unilateral vestibular loss nystagmus when mastoid vibration is applied Subjective visual Patient directs bar or line to what he or she perceives to be straight vertical; vertical in acute otolith dysfunction, the bar or line deviates to the side of unilateral vestibular (otolith) loss Dynamic visual Look for three-line decrease in visual acuity during rapid head turning acuity indicative of bilateral peripheral vestibular loss ENG electronystagmography, VNG videonystagmography

frontal lobe, basal ganglia, superior colliculus, cerebellum, and brainstem. Saccades can be elicited by the appearance of a novel target subject’s visual field (reflexive saccade) or by the intention of the subject (volitional saccade). Test Administration and Parameters To test saccadic eye movement, the patient is asked to follow a randomly moving LED target with as much accuracy as possible. The flashes occur sequentially in two positions: at the center of the array and then 15–20° to the right and left from the center. The interval between flashes is usually a few seconds, and the test is then repeated vertically. Saccades are tested for accuracy, velocity, and latency. Latency (the difference in time between the presentation of a new target and the initiation of eye movement)

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is normal between 150 and 250 ms in random patterns and shorter than 75 ms when the pattern is predictable. Abnormalities include prolonged latency, shortened latency, and differences in latency between the right and left eyes; these are seen in neurodegenerative diseases. Peak velocity is the maximum velocity that the eyes reach during a saccadic movement. There is no upper limit to normal, as velocities have been measured as high as 700°/s, but they generally range from 283 to 581°/s for 20° of amplitude in normal subjects. Velocities slower than 400°/s for large-amplitude saccades and slower than 200°/s for small-amplitude saccades are considered abnormal. Abnormal saccadic velocities include fast saccades, slow saccades, or differences in velocity between the right and left eye. Fast saccades can be observed in calibration errors and eye muscle restrictions. Sedative drug use is the most common cause of abnormally slow saccades. Other causes include drowsiness, cerebellar disorders, basal ganglia disorders, and brainstem lesions. Velocity asymmetry between the left and right eye is seen in intranuclear ophthalmoplegia, eye muscle restrictions, ocular muscle palsies, and palsies of cranial nerves III, IV, and VI. Accuracy is established by comparing the eye position relative to a target position. A saccadic eye movement that goes farther than the target position is considered a hypermetric saccade (or overshoot dysmetria). This is considered abnormal if it is greater than 115–120% of the target value. A saccadic movement that is shorter than the target position is referred to as a hypometric saccade (or undershoot dysmetria). This is considered abnormal if it is less than 75–80% of the target value. Undershooting by 10% of the amplitude of the saccade may be seen in healthy individuals, while hypermetric saccades are rarely observed in normal individuals. Inaccurate saccades suggest a pathologic condition of the cerebellum, brainstem, or basal ganglia. See Figs. 3.1 and 3.2 for examples of saccade testing. Smooth Pursuit Tests (Sinusoidal Tracking) In contrast to saccades, smooth pursuit describes much slower tracking movements designed to keep a moving stimulus fixated on the fovea. The neural pathways involved are distributed in the cortical and subcortical areas of the brain, as well as the fovea. Test Administration and Parameters To assess smooth pursuit, the LED moves back and forth between points on a light bar at a constant frequency, usually between 0.2 and 0.8 Hz/s, and a velocity between 20°/s and 40°/s in a sinusoidal pattern. Smooth pursuit performance declines with higher velocities and increasing age. The primary parameters of pursuit testing include gain, phase, and trace morphology.

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Fig. 3.1  Normal saccades and tracking seen in both eyes

Fig. 3.2  Delayed latencies with leftward gaze deviation and reduced rightward and leftward velocity

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Gain is the peak-to-target velocity ratio. For a stimulus of 0.5 Hz with a sweeping amplitude of 40°, a gain greater than 0.8 is considered normal. Saccade movements are eliminated from the calculation of gain. A low gain is suggestive of a CNS disorder. Phase is the difference in time between eye movement and target movement. Under optimal conditions, healthy subjects can track a target with a phase of 0°. The level of attention and drugs affecting the CNS can destroy pursuit performance. A morphological assessment of the tracings is also performed. A morphologic abnormality is referred to as a staircase of saccades, where the trace demonstrates a step-like eye movement when the target is being followed. Pursuit traces can be impaired symmetrically or asymmetrically—the asymmetrically impaired pursuit is more indicative of a CNS lesion than symmetrically impaired pursuit. Peripheral vestibular lesions may also impair smooth pursuit contralateral to the pathological side when the patient’s eyes are moving against the slow phase of spontaneous nystagmus. See Figs. 3.3 and 3.4 comparing normal smooth pursuit and abnormal saccadic pursuit. Optokinetic Tracking When actively experiencing vertigo, a patient relies on vestibular system stimulation and OKN to facilitate steady focus on objects as they move in a circular pattern around him or her. As the patient’s vestibular system fatigues with stimulation, the optokinetic system is solely responsible for the stabilization of the visual field. ENG tests the optokinetic tracking of targets by passing a light rapidly in front of a patient

Fig. 3.3  Normal smooth pursuit

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Fig. 3.4  Abnormal saccadic pursuit; central vestibular abnormality seen in a patient with cerebellar degeneration

from one direction, then the other. Asymmetries are noted and are signs of CNS dysfunction. Various tests have been done that have shown high rates of false-­ positive results with this test. Patients with optokinetic abnormalities in VNG/ENG may not need further neurological workup. OKN is an involuntary oculomotor response to a moving target filling at least 90° of the visual field. An optokinetic stimulus is presented using a 360°-turning cloth drum with black and white stripes. The normal response to an optokinetic stimulator is a smooth eye movement that follows the stimulus direction, both clockwise and counterclockwise. OKN is produced by the cortical and brainstem structures that produce pursuit and aims to stabilize the visual field on the retina. Optokinetic after-nystagmus is a form of nystagmus produced by the brainstem after a 10-s, constant velocity optokinetic stimulus and lasts approximately 30 s. OKN abnormalities are seen in deep parietal-lobe lesions and may be used to identify subtle ocular motor abnormalities (e.g., incomplete internuclear ophthalmoplegia). See Figs. 3.5 and 3.6 for normal and symmetric optokinetic tracking compared to abnormal tracking. Gaze Test A gaze test is conducted by recording eye movements while the subject fixes his or her vision on the center of a target. The patient then fixes his or her gaze 30–40° to the right, left, above, and below the center of the field. The patient’s gaze and gaze recording are sustained for a minimum of 30 s. Patients with gaze nystagmus cannot maintain stable conjugate eye deviation away from the primary position; thus, their vision is refocused back to the center by resetting corrective saccades. Gaze testing may uncover peripheral or CNS lesions that are either vestibular or nonvestibular in etiology, as well as congenital or spontaneous nystagmus. During and after unilateral vestibular dysfunction, vestibular spontaneous nystagmus is seen and beats away from the pathologic side. Typically, it manifests as horizontal nystagmus in an ENG recording, but it is actually both horizontal and torsional in nature. The intensity of vestibular spontaneous nystagmus increases

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Fig. 3.5  Normal and symmetric optokinetic tracking. Right and left 20°/s

when the gaze is oriented toward the direction of the nystagmus. See Fig. 3.7 for an example of spontaneous nystagmus. Peripheral gaze-evoked nystagmus is typically unidirectional on a horizontal plane—both horizontal and torsional. When the gaze is directed toward the nystagmus direction, its intensity increases; gaze-evoked nystagmus of CNS origin may change direction with the patient’s gaze. Vertical gaze nystagmus is always indicative of a CNS pathology. Gaze nystagmus is categorized as symmetric, asymmetric, rebound, or disassociated. In symmetric gaze nystagmus, the eyes move with equal amplitude in both directions. Ingestion of drugs affecting the CNS, such as multiple sclerosis, myasthenia gravis, and cerebellar atrophy, may cause symmetric gaze nystagmus. Asymmetric gaze nystagmus suggests a cerebellar or brainstem lesion. Rebound nystagmus starts in lateral positions and reverses its direction to the primary position, even with no evidence of initial nystagmus in the primary position. It is also strongly indicative of cerebellar or brainstem lesions. Disassociated (disconjugate) nystagmus is the difference in eye movements during gaze testing, usually resulting from medial longitudinal fasciculus lesions. See Figs. 3.8 and 3.9 for examples of normal and abnormal gaze testing.

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Fig. 3.6  Abnormal optokinetic tracking (40°/s), poor morphology. No visible or repeatable nystagmus

Fig. 3.7  Left beating spontaneous nystagmus (1–2°/s)

Fixation Suppression Testing Spontaneous nystagmus is established by placing the patient with vision denied (i.e., eyes closed) in a completely darkened room without visual or positional stimuli. If spontaneous nystagmus is found, slow-phase velocity is recorded. The patient is then asked to fixate on the center of a visual target (i.e., the central gaze). The fixation-suppression index is then calculated by determining the ratio of the slow-­ phase velocity with fixation to the slow-phase velocity without fixation. This index should be 10-dB PTA worsening or >15% discrimination worsening In 1996, the Committee on Hearing and Equilibrium reaffirmed and clarified the guidelines, adding initial staging and reporting guidelines. Initial hearing level Stage 1 2 3 4

Four-tone average (dB) ≤25 26–40 41–70 >70

Functional Level Scale Regarding my current state of overall function, not just during attacks. 1. My dizziness has no effect on my activities at all. 2. When I am dizzy, I have to stop for a while, but it soon passes and I can resume my activities. I continue to work, drive, and engage in any activity I choose without restriction. I have not changed any plans or activities to accommodate my dizziness.

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3. When I am dizzy, I have to stop what I am doing for a while, but it does pass and I can resume activities. I continue to work, drive, and engage in most activities I choose, but I have had to change some plans and make some allowance for my dizziness. 4. I am able to work, drive, travel, and take care of a family or engage in most activities, but I must exert a great deal of effort to do so. I must constantly make adjustments in my activities and budget my energies. I am barely making it. 5. I am unable to work, drive, or take care of a family. I am unable to do most of the active things that I used to do. Even essential activities must be limited. I am disabled. 6. I have been disabled for 1 year or longer and/or I receive compensation because of my dizziness or balance problem.

History Incapacitating, spinning vertigo, usually in the horizontal axis, is the most distressing complaint of the affected patient [64]. As is typical of peripheral vestibular dysfunction, the symptoms are exacerbated with any head movement. There is often accompanying nausea, vomiting, diarrhea, and sweating. Between attacks, patients may be entirely asymptomatic or may describe periods of disequilibrium, lightheadedness, and tilt. Sudden unexplained falls without loss of consciousness or associated vertigo are occasionally described. Tumarkin [83] attributed these to acute utriculosaccular dysfunction, so-called otolithic crises of Tumarkin or drop attacks. It is thought that, as a consequence of an abrupt change in otolithic input, an erroneous vertical gravity reference occurs. This in turn generates an inappropriate postural adjustment via the vestibulospinal pathway, resulting in a sudden fall [84, 85]. Attacks are so sudden that injury can occur. The patient often describes being pushed or feeling the world moving. The spells are short lived with little vertigo associated. Drop attacks have been reported in 2–6% of persons with Menière’s disease. They tend to occur in clusters and then spontaneously remit. Lermoyez described an unusual clinical presentation in which tinnitus and hearing loss precede and worsen with the onset of vertigo. When the vertiginous episode occurs, the tinnitus and hearing loss dramatically resolve. The temporal bone studies of one individual with such attacks noted hydrops and membrane ruptures isolated to the basal turns of the cochlea and the saccule [86]. Acute Menière’s attacks are rarely observed by physicians [87]. Horizontal nystagmus is the cardinal finding, but the direction varies over the course of the attack so it is not useful in determining the involved ear [88].

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Hearing Loss and Tinnitus The sensorineural hearing loss in Menière’s disease is typically fluctuating and progressive. It often occurs coincident with the sensation of fullness or pressure in the ear. A pattern of low-frequency fluctuating loss and a coincident nonchanging, high-­ frequency loss is described, a “peaked” or “tent-like” audiogram. This peak classically occurs at 2 kHz. Over time, the hearing loss flattens and becomes less variable [77]. Only 1–2% of patients progress to profound deafness. Additional features include diplacusis, a difference in the perception of pitch between the ears (43.6%) and recruitment (56%) [64]. Tinnitus tends to be nonpulsatile and variously described as whistling or roaring. It may be continuous or intermittent. Tinnitus often begins, gets louder, or changes pitch as an attack approaches. Following the attack there is frequently a period of improvement.

Investigations Videonystagmography (VNG) Recording of eye movements after caloric and rotational stimulation are a commonly available and reliable method of assessing vestibular function. The caloric test can often localize the involved ear. A significant caloric response reduction is found in 48–73.5% of patients with Menière’s disease [89]. Complete absence caloric response is reported in 6–11% of patients. In most cases, the caloric asymmetry is only slight [90].

Head Thrust Testing The head thrust popularized by Halmagyi is a very sensitive test for unilateral vestibular dysfunction [91]. However, in Menière’s disease, the asymmetry is subtle and only present in 29% of Menière’s patients [92].

Electrocochleography The summating potential (SP), as recorded by electrocochleography in response to clicks or tone bursts, in Menière’s patients, is larger and more negative. This is thought to reflect the distention of the basilar membrane into the scala tympani, causing an increase in the normal asymmetry of its vibration. The most commonly

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used value is the ratio of amplitudes of the summating potential and the eighth cranial nerve action potential (AP), the SP/AP ratio. This is based on the observed variability in the amplitude of the summating potential considering variables such as recording technique and electrode placement. The SP/AP ratio has been used to reduce the intertest variability, resulting in a more linear response. The summating potential becomes relatively larger in hydrops; thus, the SP/AP ratio increases [93]. The ratios are elevated in 62% of patients with Menière’s and 21% of control subjects. ECoG sensitivity can range 66.7–85.7% and specificity range from 80% to 100% [25]. Elevated ratios can also be observed in other potential causes of endolymphatic hydrops and vertigo (i.e., spontaneous intracranial hypotension) [94]. The difficulty in obtaining reproducible recordings, the variability of the wave amplitudes noted with patient age, hearing loss and stage of disease, as well as the availability of reliable, less invasive diagnostic methods, have resulted in electrocochleography infrequently being used for this purpose [95, 96] although some still advocate for it [97].

Dehydrating Agents The assumption that an increase in endolymph volume, with its effect on labyrinthine membrane behavior, produces, in part, the hearing loss and vestibular deficit in Menière’s disease has led to the administration of dehydrating agents (e.g., urea, glycerol, and furosemide). The goal is to reduce the volume abnormalities in the inner ear and produce a measurable change in response. Improvement has been measured with audiometrics, reduction in summating potential negativity (as recorded with electrocochleography), or a change in the gain of the vestibulo-­ occular response to rotational stimulation. The reported sensitivity and specificity of the test varies widely. Klockhoff reports a 60% sensitivity in cases of known Menière’s disease [98]. Psychological factors are a significant factor, leading some to question the usefulness of the test [95, 99].

Vestibular Evoked Myopotentials (VEMP) VEMP are generated by playing loud clicks in the ear which move the stapes footplate and stimulate the saccule. This is the start of a disynaptic pathway that passes through the vestibular nuclei then to synapses which relax the sternocleidomastoid muscle. The saccule is the second most common site affected by hydrops which has caused VEMP to be investigated as a potential diagnostic tool. In the normal ear, the best response is near 500  Hz. Ears affected by Menière’s disease have elevated VEMP thresholds with flattened tuning [100]. The interaural amplitude difference in the response has been implicated as a staging tool for Menière’s disease [101]. The most reliable finding seems to be that cervical VEMP (cVEMP) has reduced amplitudes [102, 103]. Delayed or absent VEMPs are only seen in half of Menière’s

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patients compared to >90% of normal patients [104]. Although these tests show differences between populations, they currently have limited diagnostic value due to the large individual variation in individual responses [105].

Treatment Therapy is aimed at the reduction of its associated symptoms. The optimal curative treatment should stop vertigo, abolish tinnitus, and reverse hearing loss. Unfortunately, long-term hearing impairment does not seem amenable to treatment [82]. Currently, almost all proven therapy is directed at relieving vertigo which is usually the most distressing symptom. Evaluating treatments for vertigo in Menière’s disease patients has been made difficult by the natural history of the disease which improves spontaneously in 60–80% of cases and many treatments have a significant placebo effect [67, 106, 107]. This is further supported by the 71% improvement in symptoms by patients who refused surgery [80], and placebo-controlled studies of endolymphatic sac surgery [15, 108] and medical therapy [109]. The large variety of Menière’s disease treatments exist due to extreme clinical variability, and difficulty in assessing effectiveness.

Dietary Modification and Diuretics Salt restriction and diuresis may be a reasonable initial therapy for Menière’s disease [110, 111]. The goal of salt restriction and diuretics is to reduce endolymph volume by fluid removal and/or reduced production. Despite the popularity of these treatments neither salt restriction [112] nor diuretics [113–115] has had their efficacy confirmed by double-blind placebo controlled studies. Carbonic anhydrase inhibitors such as acetazolamide were recommended based on the localization of carbonic anhydrase in the dark cells and the stria vascularis. However, their use has not proved to be clinically more effective than other diuretics [116]. Despite the lack of hard evidence to their efficacy, the authors feel low salt diet and diuresis is an appropriate and effective treatment for Menière’s disease with a low risk of side effects. Decreased caffeine intake may also have some efficacy [117].

Vasodilators In the belief that Menière’s disease was the result of strial ischemia, vasodilating agents have been used. Betahistine, an oral preparation of histamine, is one such medication [118]. Betahistine has historically been a popular Menière’s treatment in Europe [119]. In the United States, the drug is available only through compounding

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pharmacies and was often not covered by insurance making it infrequently prescribed. A recent large multicenter European trial demonstrated it was no more effective than a placebo [120], which strongly suggests it is an ineffective treatment.

Symptomatic Treatment Antivertiginous medications, antiemetics, sedatives, antidepressants, and psychiatric treatment have been reported to be beneficial in reducing the severity of the vertigo and vegetative symptoms and in improving tolerance of Menière’s symptoms [121]. Although this strategy is commonly used, it is the authors’ experience that the results are often not satisfactory to the patient. Sedatives and antiemetics can help ease the symptoms during an active vertigo event.

Local Overpressure Therapy One approach to decrease hydrops is by pulsing pressure in the middle ear. As early as 30 years ago, overpressure in the middle ear was reported to decrease Menière’s symptoms during acute vertigo attacks [122]. The mechanism of vertigo reduction is unclear, and it may facilitate endolymph absorption [123]. Since 2000, the Meniett device has been approved for use by the United States Food and Drug Administration. The device is a handheld air pressure generator that the patient administers as needed. The pressure is delivered in complex pulses up to 20 cm of water which is delivered over a 5 min period. The device requires a ventilation tube to be placed in the tympanic membrane prior to starting therapy. A randomized controlled trial demonstrated that the Meniett device had a significant decrease in vertigo symptoms for the first 3 months of therapy but afterward was similar to placebo [124]. More recent studies suggested it might have a role, but only when combined with another therapy [125], and it is no more effective than a placebo on its own [126]. In any case, it is currently rarely used and a recently survey revealed more than twothirds of neurotologists never recommend it to patients [127]. It should also be noted that simple placement of a ventilation tube with no additional therapy has been reported in control vertigo symptoms in many patients with Menière’s disease [128, 129].

Transtympanic Therapy Transtympanic injection (also referred to as intratympanic injection) is commonly performed with either dexamethasone or gentamycin for control of vertigo symptoms. The term “chemical labyrinthectomy” is often applied to intratympanic gentamicin treatment, but it may not be an appropriate assessment of the effect of

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Fig. 4.4  Response to head thrusts that excited each of the six semicircular canals in a typical subject measured 49  days after a single intratympanic injection of gentamicin in the right ear. (Figure reproduced from Carey et al. 2002 [131])

gentamicin on the labyrinth in titrated therapy. Installation of aminoglycosides into the middle ear was described by Schuknecht in 1957 with streptomycin injection through a microcatheter placed through the tympanic membrane [21]. Control of vertigo was achieved in these patients, but severe hearing loss in the treated ear also occurred in most patients. Although streptomycin is still used in some clinics and has excellent control of vertigo symptoms [130], the risk of profound hearing loss has led most to focus on gentamicin and dexamethasone. Gentamicin has a vestibulotoxicity that is high relative to its cochleotoxicity; thus, it can be used to control vestibular symptoms while often sparing the hearing. The gentamicin can be administered through either a tympanostomy tube or directly injected through the tympanic membrane. Peripheral vestibular deficits are evident on head thrust testing after even a single dose of gentamicin (Fig. 4.4) [131]. The concentration of the medication used and frequency of injection vary by series. The risk of hearing loss varies greatly by series depending on the dose and frequency of treatment. Lange [132] reported elimination of vertigo in 90% of 92 patients, but the incidence of hearing loss and level of vestibular function were not specified. Beck and Schmidt [133] sought to determine if complete ablation of vestibular function, as measured with ice water caloric response, was needed for vertigo control. They found that it was not, and that this end point led to severe to profound hearing loss in 58% of patients. Wu and Minor [24] found complete control of vertigo in 90%

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with profound sensory neural hearing loss in only 3% of patients. Nedzelski et al. [134] found control of vertigo was achieved in 83% of patients with substantial control in the remaining subjects. There was a 10% incidence of profound hearing loss in the treated ear. The current trend is away from multiple doses of gentamicin and toward a single injection regimen with additional doses only if needed to control symptoms (“titration therapy”). The risk of hearing loss with gentamicin using many current protocols is similar to the natural history of Menière’s disease [24, 110, 135], and a recent meta-analysis found the risk of hearing loss to be clinically negligible [136]. Gentamicin was found to be superior to dexamethasone for vertigo control in a randomized controlled trial [137]. In cases when gentamicin is not effective, it is likely because the medication is not getting into the inner ear [138]. Intratympanic injection of dexamethasone is considered by many to be a reasonable procedure to offer when vertigo is intractable, but the patient still has some functional hearing. The mechanism for steroid effect on vertigo symptoms is not currently clear. There is some evidence that Menière’s has an autoimmune component, which the steroids may address. Several studies have reported a beneficial effect of intratympanic injection of dexamethasone in the control of vertigo from Menière’s disease [139–142]. The risk of hearing loss or other complication from the steroid injection appears to be minimal. A small randomized trial has shown complete resolution of vertigo symptoms was achieve in 82% of patients getting dexamethasone vs. 57% with saline injection [143]. Dexamethasone injections may need to be repeated every 3 months to maintain free of vertigo symptoms, although the optimal dosing frequency is variable and unknown. Concentrations used have varied from 2 to 24 mg/mL but 10 mg/mL is typical. Sustained release formations of dexamethasone for Menière’s treatment have been developed [144], but it remains to be shown if these will be more effective than ordinary dexamethasone.

Endolymphatic Sac Surgery Surgical decompression of the endolymph for Menière’s was first described by Portmann in 1926 [8]. During the more than three quarters of a century that this technique has been practiced, there have been numerous variations on the concept. Despite significant investigation into techniques to decompress the endolymph, the etiology of endolymphatic hydrops as part of the pathophysiology of Menière’s disease is still an active area of controversy and debate. Several theories have been proposed which include release of external compression on the sac, neovascularization of the perisaccular region, allowing passive diffusion of endolymph, and creation of an osmotic gradient out of the sac [145]. However, histologic evidence reveals that the hydrops is not relieved after shunt placement [17]. Several variations on endolymphatic sac surgery have been described. Simple decompression, wide decompression that includes the sigmoid sinus [146], cannulating the endolymphatic duct, endolymphatic drainage to the subarachnoid space, drainage to the mastoid, and removal of the extraosseous portion of the sac [147]

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have all been advocated. A variety of prostheses have also been proposed from simple silastic sheets, tubes, and one-way valves designed to allow flow selectively in either the mastoid or subarachnoid direction. Thomsen et al. conducted a double-blind, placebo controlled study revealed that a mastoidectomy alone has the same efficacy as an endolymphatic shunt in a group of 30 patients with 15 randomly selected for each operation [15]. The efficacy of the procedure remains controversial with other authors re-examining the Thomsen et al. data and claiming a significant result would have been found if a different criteria for success were employed [148] or if different statistical methods were used [16]. A later randomized prospective trial demonstrated that endolymphatic shunt surgery was no more effective than placing a ventilating tube in the tympanic membrane [149]. A recent systematic review found little evidence to support endolymphatic sac surgery [150].

Vestibular Nerve Section Several approaches to the vestibular nerve have been described. The earliest approach was the retrosigmoid, with the first large series by Walter Dandy in the 1930s [9]. The terms retrosigmoid and suboccipital are now used interchangeably. The middle fossa approach to the internal auditory canal and superior vestibular nerve was developed by William House [151] and later modified to include sectioning of the inferior vestibular nerve [152]. A retrolabyrinthine approach has also been described [153]. Vestibular nerve section has a complete vertigo control rate of about 85–95% with 80–90% of patients maintaining their preoperative hearing after the procedure [154–156]. The procedure can also be done via endoscope which may decrease morbidity [157]. It offers much greater vertigo control rates than endolymphatic shunt procedures, but is also a more invasive and technically challenging procedure. It has been reported to have poor long term hearing preservation and has a risk of complications including facial weakness and cerebrospinal fluid leak [158]. A recent survey found nerve sections are now performed very infrequently by neurotologists [127], perhaps due to the rising popularity of transtympanic therapies which are effective and less invasive.

Labyrinthectomy The most destructive procedure for treatment of Menière’s is labyrinthectomy due to the uniform destruction of hearing and vestibular function. Ideal candidates are those that have no functional hearing and have failed more conservative treatments such as gentamicin injection. Despite this morbidity, the procedure has a higher rate of vertigo control than vestibular neurectomy [158, 159] and thus should be favored

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in patients without hearing and has been reported in improve quality of life in 98% of patients [160]. The procedure is most commonly performed via a transmastoid exposure but can be done via a transcanal approach.

Vestibular Therapy Vestibular rehabilitation is primarily used for postoperative recovery of Menière’s patients who have undergone ablative procedures.

Chapter Summary Menière’s disease is characterized by episodic attacks of vertigo, hearing loss, tinnitus, and aural fullness. Much progress has been made since Prosper Menière’s first description of the disease as a condition attributed to the inner ear. There are now defined diagnostic criteria, histopathological as well as imaging evidence of endolymphatic hydrops, and tests that measure inner ear function with variable sensitivity and specificity. Treatments now include medications to improve the severity of symptoms and delay hearing loss, and there has been continued evolution of surgical treatments to alleviate vertigo. However, the exact cause of the development of Menière’s disease and endolymphatic hydrops remains elusive, and therefore, the cure for it is yet to be discovered.

Quizzes 1. Most patients with Menière’s disease have a family history of the condition (T/F). 2. Endolymphatic sac surgery has an efficacy that is well supported by clinical trials (T/F). 3. For the case study example where you suspect Menière’s disease, what kinds of objective testing could help support the diagnosis? 4. For the case study example, what are potential treatments you can offer given the recent increased frequency of attacks despite being on diuretic medication? Answers 1. False. Family history is only present in 10–20% of case. 2. False. Although randomized controlled trials were done, the efficacy was similar to sham surgery. 3. Caloric testing may yield asymmetry with weakness of the affected ear. Electrocochleography may yield abnormally elevated SP/AP ratios >0.5. Reduced amplitudes may be seen on cVEMP on the affected side. 4. Oral or intratympanic steroid injections may be offered. If despite this she continues to experience frequent, debilitating symptoms, ablative procedures such as intratympanic gentamycin or labyrinthectomy may be discussed. The type of ablative treatment may be swayed by the degree of existing hearing loss.

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97. Mammarella F, Zelli M, Varakliotis T, Eibenstein A, Pianura CM, Bellocchi G.  Is electrocochleography still helpful in early diagnosis of Meniere disease? J Audiol Otol. 2017;21(2):72–6. https://doi.org/10.7874/jao.2017.21.2.72. 98. Klockhoff I. Diagnosis of Meniere’s disease. Arch Otorhinolaryngol. 1976;212(4):309–14. 99. Thomsen J, Vesterhauge S. A critical evaluation of the glycerol test in Meniere’s disease. J Otolaryngol. 1979;8(2):145–50. 100. Rauch SD, Zhou G, Kujawa SG, Guinan JJ, Herrmann BS. Vestibular evoked myogenic potentials show altered tuning in patients with Meniere’s disease. Otol Neurotol. 2004;25(3):333–8. 101. Young YH, Huang TW, Cheng PW. Assessing the stage of Meniere’s disease using vestibular evoked myogenic potentials. Arch Otolaryngol Head Neck Surg. 2003;129(8):815–8. 102. Taylor RL, Wijewardene AA, Gibson WP, Black DA, Halmagyi GM, Welgampola MS.  The vestibular evoked-potential profile of Meniere’s disease. Clin Neurophysiol. 2011;122(6):1256–63. https://doi.org/10.1016/j.clinph.2010.11.009. 103. Zuniga MG, Janky KL, Schubert MC, Carey JP. Can vestibular-evoked myogenic potentials help differentiate Meniere disease from vestibular migraine? Otolaryngol Head Neck Surg. 2012;146(5):788–96. https://doi.org/10.1177/0194599811434073. 104. Agrawal Y, Minor LB.  Physiologic effects on the vestibular system in Meniere’s disease. Otolaryngol Clin N Am. 2010;43(5):985–93. https://doi.org/10.1016/j.otc.2010.05.002. 105. Maheu M, Alvarado-Umanzor JM, Delcenserie A, Champoux F.  The clinical utility of vestibular-evoked myogenic potentials in the diagnosis of Meniere’s disease. Front Neurol. 2017;8:415. https://doi.org/10.3389/fneur.2017.00415. 106. Hamill TA. Evaluating treatments for Meniere’s disease: controversies surrounding placebo control. J Am Acad Audiol. 2006;17(1):27–37. 107. Torok N. Old and new in Meniere disease. Laryngoscope. 1977;87(11):1870–7. 108. Bretlau P, Thomsen J, Tos M, Johnsen NJ. Placebo effect in surgery for Meniere’s disease: nine-year follow-up. Am J Otol. 1989;10(4):259–61. 109. Thomsen J, Bech P, Prytz S, Vendsborg P, Zilstorff K. Meniere’s disease: lithium treatment (demonstration of placebo effect in a doubleblind cross-over trial). Clin Otolaryngol Allied Sci. 1979;4(2):119–23. 110. Santos PM, Hall RA, Snyder JM, Hughes LF, Dobie RA.  Diuretic and diet effect on Meniere’s disease evaluated by the 1985 Committee on Hearing and Equilibrium guidelines. Otolaryngol Head Neck Surg. 1993;109(4):680–9. 111. Devaiah AK, Ator GA. Clinical indicators useful in predicting response to the medical management of Meniere’s disease. Laryngoscope. 2000;110(11):1861–5. 112. Horner KC, Aurousseau C, Erre JP, Cazals Y.  Long-term treatment with chlorthalidone reduces experimental hydrops but does not prevent the hearing loss. Acta Otolaryngol. 1989;108(3–4):175–83. 113. van Deelen GW, Huizing EH.  Use of a diuretic (Dyazide) in the treatment of Meniere’s disease. A double-blind cross-over placebo-controlled study. ORL J Otorhinolaryngol Relat Spec. 1986;48(5):287–92. 114. Thirlwall AS, Kundu S.  Diuretics for Meniere’s disease or syndrome. Cochrane Database Syst Rev. 2006;3:CD003599. 115. Stern Shavit S, Lalwani AK.  Are diuretics useful in the treatment of Meniere disease? Laryngoscope. 2019;129(10):2206–7. https://doi.org/10.1002/lary.28040. 116. Shinkawa H, Kimura RS. Effect of diuretics on endolymphatic hydrops. Acta Otolaryngol. 1986;101(1–2):43–52. 117. Sanchez-Sellero I, San-Roman-Rodriguez E, Santos-Perez S, Rossi-Izquierdo M, Soto-Varela A. Caffeine intake and Meniere’s disease: is there relationship? Nutr Neurosci. 2017;21:1–8. https://doi.org/10.1080/1028415X.2017.1327636. 118. Wilmot TJ, Menon GN. Betahistine in Meniere’s disease. J Laryngol Otol. 1976;90(9):833–40. 119. Harcourt J, Barraclough K, Bronstein AM. Meniere’s disease. BMJ. 2014;349:g6544. https:// doi.org/10.1136/bmj.g6544.

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120. Adrion C, Fischer CS, Wagner J, Gurkov R, Mansmann U, Strupp M, et  al. Efficacy and safety of betahistine treatment in patients with Meniere’s disease: primary results of a long term, multicentre, double blind, randomised, placebo controlled, dose defining trial (BEMED trial). BMJ. 2016;352:h6816. https://doi.org/10.1136/bmj.h6816. 121. Pyykko I, Magnusson M, Schalen L, Enbom H. Pharmacological treatment of vertigo. Acta Otolaryngol Suppl. 1988;455:77–81. 122. Ingelstedt S, Ivarsson A, Tjernstrom O. Immediate relief of symptoms during acute attacks of Meniere’s disease, using a pressure chamber. Acta Otolaryngol. 1976;82(5–6):368–78. 123. Sakikawa Y, Kimura RS.  Middle ear overpressure treatment of endolymphatic hydrops in Guinea pigs. ORL J Otorhinolaryngol Relat Spec. 1997;59(2):84–90. 124. Gates GA, Green JD Jr, Tucci DL, Telian SA. The effects of transtympanic micropressure treatment in people with unilateral Meniere’s disease. Arch Otolaryngol Head Neck Surg. 2004;130(6):718–25. 125. Zhang SL, Leng Y, Liu B, Shi H, Lu M, Kong WJ.  Meniett therapy for Meniere’s disease: an updated meta-analysis. Otol Neurotol. 2016;37(3):290–8. https://doi.org/10.1097/ MAO.0000000000000957. 126. Russo FY, Nguyen Y, De Seta D, Bouccara D, Sterkers O, Ferrary E, et al. Meniett device in Meniere disease: randomized, double-blind, placebo-controlled multicenter trial. Laryngoscope. 2017;127(2):470–5. https://doi.org/10.1002/lary.26197. 127. Clyde JW, Oberman BS, Isildak H. Current management practices in Meniere’s disease. Otol Neurotol. 2017;38(6):e159–67. https://doi.org/10.1097/MAO.0000000000001421. 128. Sugawara K, Kitamura K, Ishida T, Sejima T. Insertion of tympanic ventilation tubes as a treating modality for patients with Meniere’s disease: a short- and long-term follow-up study in seven cases. Auris Nasus Larynx. 2003;30(1):25–8. 129. Montandon P, Guillemin P, Hausler R. Prevention of vertigo in Meniere’s syndrome by means of transtympanic ventilation tubes. ORL J Otorhinolaryngol Relat Spec. 1988;50(6):377–81. 130. Shea PF, Richey PA, Wan JY, Stevens SR. Hearing results and quality of life after streptomycin/dexamethasone perfusion for Meniere’s disease. Laryngoscope. 2012;122(1):204–11. https://doi.org/10.1002/lary.22362. 131. Carey JP, Minor LB, Peng GC, Della Santina CC, Cremer PD, Haslwanter T.  Changes in the three-dimensional angular vestibulo-ocular reflex following intratympanic gentamicin for Meniere’s disease. J Assoc Res Otolaryngol. 2002;3(4):430–43. 132. Lange G.  Gentamicin and other ototoxic antibiotics for the transtympanic treatment of Meniere’s disease. Arch Otorhinolaryngol. 1989;246(5):269–70. 133. Beck C, Schmidt CL. 10 years of experience with intratympanally applied streptomycin (gentamycin) in the therapy of Morbus Meniere. Arch Otorhinolaryngol. 1978;221(2):149–52. 134. Nedzelski JM, Chiong CM, Fradet G, Schessel DA, Bryce GE, Pfleiderer AG. Intratympanic gentamicin instillation as treatment of unilateral Meniere’s disease: update of an ongoing study. Am J Otol. 1993;14(3):278–82. 135. Postema RJ, Kingma CM, Wit HP, Albers FW, Van Der Laan BF. Intratympanic gentamicin therapy for control of vertigo in unilateral Meniere’s disease: a prospective, double-blind, randomized, placebo-controlled trial. Acta Otolaryngol. 2008;1-5:876. 136. Huon LK, Fang TY, Wang PC.  Outcomes of intratympanic gentamicin injection to treat Meniere’s disease. Otol Neurotol. 2012;33(5):706–14. https://doi.org/10.1097/ MAO.0b013e318259b3b1. 137. Casani AP, Piaggi P, Cerchiai N, Seccia V, Franceschini SS, Dallan I. Intratympanic treatment of intractable unilateral Meniere disease: gentamicin or dexamethasone? A randomized controlled trial. Otolaryngol Head Neck Surg. 2012;146(3):430–7. https://doi. org/10.1177/0194599811429432. 138. Crane BT, Minor LB, Della Santina CC, Carey JP. Middle ear exploration in patients with Meniere’s disease who have failed outpatient intratympanic gentamicin therapy. Otol Neurotol. 2009;30(5):619–24. 139. Barrs DM, Keyser JS, Stallworth C, McElveen JT Jr. Intratympanic steroid injections for intractable Meniere’s disease. Laryngoscope. 2001;111(12):2100–4.

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140. Sennaroglu L, Dini FM, Sennaroglu G, Gursel B, Ozkan S. Transtympanic dexamethasone application in Meniere’s disease: an alternative treatment for intractable vertigo. J Laryngol Otol. 1999;113(3):217–21. 141. Boleas-Aguirre MS, Lin FR, Della Santina CC, Minor LB, Carey JP. Longitudinal results with intratympanic dexamethasone in the treatment of Meniere’s disease. Otol Neurotol. 2008;29(1):33–8. 142. Kyrodimos E, Aidonis I, Skalimis A, Sismanis A.  Use of Glasgow Benefit Inventory (GBI) in Meniere’s disease managed with intratympanic dexamethasone perfusion: quality of life assessment. Auris Nasus Larynx. 2011;38(2):172–7. https://doi.org/10.1016/j. anl.2010.07.009. 143. Garduno-Anaya MA, Couthino De Toledo H, Hinojosa-Gonzalez R, Pane-Pianese C, Rios-­ Castaneda LC. Dexamethasone inner ear perfusion by intratympanic injection in unilateral Meniere’s disease: a two-year prospective, placebo-controlled, double-blind, randomized trial. Otolaryngol Head Neck Surg. 2005;133(2):285–94. 144. Lambert PR, Nguyen S, Maxwell KS, Tucci DL, Lustig LR, Fletcher M, et al. A randomized, double-blind, placebo-controlled clinical study to assess safety and clinical activity of OTO-104 given as a single intratympanic injection in patients with unilateral Meniere’s disease. Otol Neurotol. 2012;33(7):1257–65. https://doi.org/10.1097/MAO.0b013e318263d35d. 145. Shah DK, Kartush JM. Endolymphatic sac surgery in Meniere’s disease. Otol Clin N Am. 1997;30:1061–74. 146. Otrowski VB, Kartush JM. Endolymphatic sac-vein decompression for intractable Meniere’s disease: long term treatment results. Otolaryngol Head Neck Surg. 2003;128:550–9. 147. Gibson WP. The effect of surgical removal of the extraosseous portion of the endolymphatic sac in patients suffering from Meniere’s disease. J Laryngol Otol. 1996;110:1008–11. 148. Pillsbury HC 3rd, Arenberg IK, Ferraro J, Ackley RS. Endolymphatic sac surgery. The Danish sham surgery study: an alternative analysis. Otolaryngol Clin N Am. 1983;16(1):123–7. 149. Thomsen J, Bonding P, Becker B, Stage J, Tos M. The non-specific effect of endolymphatic sac surgery in treatment of Meniere’s disease: a prospective, randomized controlled study comparing “classic” endolymphatic sac surgery with the insertion of a ventilating tube in the tympanic membrane. Acta Otolaryngol. 1998;118(6):769–73. 150. Lim MY, Zhang M, Yuen HW, Leong JL. Current evidence for endolymphatic sac surgery in the treatment of Meniere’s disease: a systematic review. Singap Med J. 2015;56(11):593–8. https://doi.org/10.11622/smedj.2015166. 151. House WF. Surgical exposure of the internal auditory canal and its contents through the middle cranial fossa. Laryngoscope. 1961;71:1363. 152. Glasscock ME. Vestibular nerve section. Arch Otolaryngol. 1973;97:112–4. 153. Silverstein H, Norrel H. Retrolabyrinthine surgery: a direct approach to the cerebrellopontine angle. Otolaryngol Head Neck Surg. 1980;88:462. 154. Silverstein H, Jackson LE.  Vestibular nerve section. Otolaryngol Clin N Am. 2002;35(3):655–73. 155. Colletti V, Carner M, Colletti L. Auditory results after vestibular nerve section and intratympanic gentamicin for Meniere’s disease. Otol Neurotol. 2007;28(2):145–51. 156. Thomsen J, Berner B, Tos M.  Vestibular neurectomy. Auris Nasus Larynx. 2000;27(4):297–301. 157. Cutler AR, Kaloostian SW, Ishiyama A, Frazee JG. Two-handed endoscopic-directed vestibular nerve sectioning: case series and review of the literature. J Neurosurg. 2012;117(3):507–13. https://doi.org/10.3171/2012.6.JNS111818. 158. Alarcon AV, Hidalgo LO, Arevalo RJ, Diaz MP. Labyrinthectomy and vestibular neurectomy for intractable vertiginous symptoms. Int Arch Otorhinolaryngol. 2017;21(2):184–90. https:// doi.org/10.1055/s-­0037-­1599242. 159. Kaylie DM, Jackson CG, Gardner EK. Surgical management of Meniere’s disease in the era of gentamicin. Otolaryngol Head Neck Surg. 2004;132:443–50. 160. Diaz RC, LaRouere MJ, Bojrab DI, Zappia JJ, Sargent EW, Shaia WT.  Quality-of-life assessment of Meniere’s disease patients after surgical labyrinthectomy. Otol Neurotol. 2007;28(1):74–86.

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Further Reading Baloh RW. Prosper Meniere and his disease. Arch Neurol. 2001;58(7):1151–6. Basura GJ, Adams ME, Monfared A, Schwartz SR, Antonelli PJ, Burkard R, et  al. Clinical practice guideline: Meniere’s disease executive summary. Otolaryngol Head Neck Surg. 2020;162(4):415–34. https://doi.org/10.1177/0194599820909439. Chung JW, Fayad J, Linthicum F, Ishiyama A, Merchant SN. Histopathology after endolymphatic sac surgery for Meniere’s syndrome. Otol Neurotol. 2011;32(4):660–4. https://doi.org/10.1097/ MAO.0b013e31821553ce.

Chapter 5

Vestibular Neuritis T. Logan Lindemann and Pamela C. Roehm

Introduction Vestibular neuritis, also referred to as vestibular neuronitis, labyrinthitis, and acute unilateral peripheral vestibulopathy (AUPVP) [1], is an acute vestibulopathy of the peripheral vestibular system. It is one of the most common causes of peripheral vertigo, following benign paroxysmal positional vertigo (BPPV) [2, 3]. Vestibular neuritis may follow a nonspecific viral illness, although symptoms may present several weeks following the initial illness. Patients complain of a rapid-onset vertigo that lasts for days and then resolves over the next few weeks. Residual dizziness and imbalance may continue for several months. While vestibular neuritis is benign and most often associated with complete resolution of symptoms, it can be very debilitating for patients during the acute phase.

T. L. Lindemann Lewis Katz School of Medicine at Temple University, Philadelphia, PA, USA e-mail: [email protected] P. C. Roehm (*) Division of Otolaryngology, St. Christopher’s Hospital for Children, Philadelphia, PA, USA © The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 B. T. Crane et al. (eds.), Disorders of the Vestibular System, https://doi.org/10.1007/978-3-031-40524-2_5

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Etiology Patients with vestibular neuritis typically experience acute peripheral vertigo in the absence of hearing loss, suggesting an isolated vestibular nerve dysfunction. This dysfunction is hypothesized to result from vestibular nerve inflammation. Postmortem histopathology, obtained after death from unrelated causes, revealed isolated demyelination of the vestibular nerve [4, 5]. Elevations in acute phase reactants, including plasma fibrinogen and C-reactive protein (CRP), and MRI enhancement of the vestibular nerve suggest that demyelination occurs as a result of local inflammation [5]. Several etiologies, including viral reactivation, autoimmune damage, and vascular occlusion, have been proposed to explain these observations [4]. However, it is unclear whether inflammation of the nerve is the cause of this disorder, and so the term acute unilateral peripheral vestibulopathy (AUPVP) has been proposed as a more unbiased descriptor of this syndrome of symptoms, signs and test results [6].

Viral Inflammation Vestibular neuritis is generally considered to develop secondary to viral or postviral inflammation. The disorder is frequently associated with a recent viral illness, epidemics, and is most often diagnosed in the spring and summer seasons [4, 7]. However, patients exhibit no overt signs of systemic infection, and despite suggestive serology, no causative virus has been isolated [4, 8]. Interestingly, vestibular neuritis shares several similarities with Bell’s palsy. Both present as an acute idiopathic cranial neuropathy that is suspected to be secondary to viral inflammation, and are commonly treated with corticosteroids [9]. Mounting evidence suggests that the reactivation of a neurotropic virus, specifically herpes simplex type 1 (HSV1), may be responsible for the development of both disorders [4]. A recent genome-wide association study linked vestibular neuritis to a particular mineralocorticoid and glucocorticoid receptor, which functions as a host factor for HSV1 replication [10]. HSV1 has been shown to establish latency not only in trigeminal ganglia, but also geniculate and vestibular ganglia [11, 12]. The virus was found to readily reactivate within rat vestibular ganglia due to a number of stimuli [13]. Latency of HSV1 has been further associated with an infiltration of CD8+ T cells into vestibular ganglia, supporting an inflammation-induced vestibular nerve dysfunction [12]. While latent herpesvirus infection is the etiology most supported by evidence, confirmation of an inciting viral illness is obtained in less than half of patients [14].

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Autoimmune Vestibular neuritis frequently presents after the resolution of an upper respiratory illness. The delayed onset of symptoms suggests that the disorder may occur as a result of local, postinfectious inflammation, rather than as a direct result of infection [4]. Acute autoimmune neuropathies, such as Guillain–Barre syndrome, are well-­ known, and result from immunologic recognition and destruction of peripheral nerve myelin following infection or vaccination. However, local neuropathies following nonspecific respiratory illnesses are not well-described. The autoimmune hypothesis is primarily supported by an elevated CD4/CD8 ratio accompanying inner ear pathologies of unknown origin, including vestibular neuritis [4, 15]. The CD4/CD8 ratio often increases in autoimmune disease (in contrast to viral infection). The increased ratio was shown to be caused by a relative decrease in T-suppressor (CD8) lymphocytes in patients with otoneurological disease [16]. It has been proposed that with relatively fewer T-suppressor lymphocytes, “forbidden” plasma cells become unsuppressed and produce autoantibodies against the vestibular nerve [4].

Vascular Occlusion Vestibular neuritis often appears to develop secondary to acute inflammation. It has been suggested that vestibular neuritis patients suffer from an inherent proinflammatory state, leading to labyrinthine ischemia [4]. Elevated levels of acute phase reactants and proinflammatory peripheral blood mononuclear cells (PBMCs) have been measured in patients with acute vestibular neuritis [17]. Activated PBMCs induce endovascular adhesion and platelet-monocyte aggregation, potentially creating an environment favorable for microvascular occlusion [4]. A similar environment has been observed in patients with cardiovascular risk factors [18, 19]. One retrospective cross-sectional study found a significantly increased prevalence of cardiovascular risk factors among hospitalized vestibular neuritis patients [20]. It is possible that cardiovascular disease may contribute to an endovascular inflammatory response, resulting in a compromised blood supply to the vestibular nerve. However, this mechanism does not directly explain vestibular nerve demyelination observed in histopathologic studies of this disorder.

Clinical Findings and Pathophysiology Clinical features (Table  5.1) are consistent with an acute vestibular syndrome (AVS), resulting from a unilateral disruption in afferent vestibular nerve signaling. Patients complain of rapid-onset vertigo, nausea and vomiting, and imbalance.

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Table 5.1  Clinical overview of vestibular neuritis History  •  Acute, prolonged vertigo, typically resolving in days to weeks  •  Classically following resolution of an upper respiratory illness

a

Examination  •  Imbalance  •  Spontaneous horizontal-torsional nystagmus, beating away from the affected side  •  Positive head impulse test  •  Focal neurologic deficits absent

Vestibular testing  •  Consistent with a unilateral peripheral vestibulopathy  •  Superior/ horizontal SCC dysfunction with relative sparing of the inferior SCC  •  Negative HINTS exam

Treatment  •  Symptomatic relief: antivestibular medications, anticholinergics, and antiemetics  •  Corticosteroids to decrease inflammation  •  Vestibular rehabilitation

b

Fig. 5.1  Comparison of MRIs of patients presenting with similar symptoms. (a) Typical appearance of nonspecific vestibular nerve enhancement (arrow) seen with vestibular neuritis in a patient with sudden onset of spinning vertigo (image courtesy of Barton Branstetter, MD). (b) MRI of the brain and internal auditory canals with gadolinium of a patient who presented with sudden onset of vertigo and hearing loss demonstrating a left acoustic neuroma (arrowhead)

Initial examination reveals spontaneous nystagmus, positive head impulse test (HIT), and gait instability [7]. Ipsilateral sensorineural hearing loss is rarely present, and in these cases, the disorder is termed “labyrinthitis” [7]. Other neurologic signs such as facial droop, asymmetric weakness or loss of sensation, and dysarthria are signs of central nervous system (CNS) pathology and should prompt immediate evaluation for cerebrovascular accident (CVA) and other central nervous system pathologies, including tumors [14] (see section “Differential Diagnosis”) (Fig. 5.1). Key clinical signs in the acute phase of this disorder include a spontaneous horizontal-­ torsional nystagmus that beats away from the affected side [21].

5  Vestibular Neuritis Fig. 5.2  Anatomy of the peripheral vestibular system. The superior vestibular nerve and its branches pass through more narrow and longer bony channels than the interior vestibular nerve, and so it is more susceptible to injury. Abbreviations: IVG inferior vestibular ganglion, SCC semicircular canal, SVG superior vestibular ganglion. (Modified with permission from Lee and Kaylie, 2013 [48])

95 cochlear nerve cochlea

IVG

spiral ganglion

SVG

cle

utri

cule

horizontal SCC

sac

posterior SCC

superior vestibular nerve

common crus

superior SCC

Nystagmus is independent of gaze direction and follows Alexander’s law [14, 22]. HIT and caloric testing reveal impairment of the semicircular canals, preferentially affecting the superior and horizontal canals [21, 23]. Head tilt, skew deviation, and ocular torsion measurements reveal an ipsiversive (directed toward the ipsilateral side) ocular tilt reaction (OTR), resulting in an ipsiversive subjective visual vertical (SVV) tilt [24]. Finally, the affected side will show decreased or absent responses to vestibular-evoked myogenic potentials (VEMPs) [24]. Vestibular testing most often reveals superior and horizontal semicircular canal dysfunction with a relative sparing of the posterior semicircular canal [25]. This observation is likely explained by the natural course of the vestibular nerve divisions within the bony skull base (Fig. 5.2). The superior division, which innervates the superior and horizontal semicircular canals, runs within a bony canal that is longer and more restrictive than those in which the inferior division and singular nerves travel [23]. The superior division may be more susceptible to entrapment within the canal during periods of vestibular nerve inflammation, resulting in the unique exam findings described previously [4, 21, 23]. There are no specific diagnostic tests for vestibular neuritis. Diagnosis is made via careful consideration of the patient’s history and physical exam findings discussed.

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Differential Diagnosis A cerebellar or brainstem stroke may mimic vestibular neuritis. Patients over the age of 50 years and those with cardiovascular disease are of particular concern for infarction [14, 26]. While central nystagmus signs, including horizontal gaze, direction changing nystagmus and vertical or purely torsional nystagmus, are specific for stroke, they are not reliable indicators [27]. The HINTS triad (normal horizontal Head Impulse test, direction-changing Nystagmus, and deviation on Test of Skew) was shown to be 100% sensitive and 96% specific for detecting stroke [28]. The HIT, used to evaluate semicircular canal (SCC) function, is conducted by rapidly turning the patient’s head in the plane of a SCC pair while the patient fixes their gaze on a stationary target. Patients with normal SCC function maintain gaze fixation on the target with smooth compensatory eye movements, while those with vestibular dysfunction generate corrective saccades back to the target after the head impulse [29]. Peripheral AVS is typically associated with a unidirectional nystagmus that becomes more intense when gazing in the direction of the fast phase. However, nystagmus that changes direction on eccentric gaze is a sign of central AVS [28]. Test of skew is performed by covering one eye for several seconds and then quickly uncovering to compare both eyes. Vertical skew, or vertical realignment of the eye once it is uncovered, is concerning for central pathology. Benign HINTS examination was shown to rule out stroke with 100% sensitivity, better than a negative MRI with diffusion weighted imaging (DWI) performed within the first 24–48 h after symptom onset [28]. A potential drawback to standard HINTS testing is that it relies on subjective observations made by the physician [29]. Video head impulse testing (vHIT), which measures each HINTS component, has been developed as an objective tool for accurate diagnosis of AVS [27]. During this test, the patient wears goggles with head velocity sensors and a mounted high-speed camera. This system can accurately calculate the vestibule-ocular response (VOR) gain, or eye velocity relative to head velocity, to measure the function of each SCC individually [29].

Treatment Management of vestibular neuritis typically begins with symptomatic vestibular suppressants (Table 5.2). These include antihistamines, anticholinergics, antiemetics, and in severe cases benzodiazepines, which help to control initial dizziness, nausea, and vomiting. The CNS works to compensate for the initial insult, however, by bringing the unbalanced vestibular signals into equilibrium over the following days [7]. Vestibular suppressants function as symptomatic therapies during the time that central compensation remains insufficient to quell acute symptoms. These medications should be used with caution, as vestibular suppression and sedation can prolong symptoms by inhibiting central compensatory mechanisms and should not

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Table 5.2  Common symptomatic treatments for acute vestibular neuritis Drug Antihistamines

Route

Dose interval

Dimenhydrinate

IV Oral

50 mg 50–100 mg every 4–6 h 10–50 mg 25–50 mg every 4–6 h 25–50 mg 6–12 h

Diphenhydramine IV Oral Meclizine Antiemetics

Oral

Metoclopramide

IV Oral IV Oral IV Oral IM or IV Oral

Ondansetron Prochlorperazine Promethazine

Parenteral forms preferred in the emergent setting. 10 mg 5–10 mg every 6 h 4–8 mg 4 mg every 8–12 h 2.5–10 mg 5–10 mg every 6 h 12.5–25 mg 12.5–25 mg every 4–6 h Use with caution due to risk of dependency.

Benzodiazepines Alprazolam Clonazepam Diazepam Lorazepam

Additional information Parenteral forms preferred in the emergent setting.

Oral Oral Oral Oral

0.5 mg every 8 h 0.25–0.5 mg 8–12 h 1 mg every 12 h 1–2 mg every 8 h

IV intravenous, IM intramuscular

be continued longer than 3 days [6]. Benzodiazepines should be reserved for symptomatic temporary initial treatment for severe vestibular neuritis, as they also carry a risk of dependency. Treatment with corticosteroids accelerates recovery of the peripheral vestibular system, possibly by decreasing inflammation, edema, and compression of the vestibular nerve secondary to viral reactivation [4]. Immune system suppression would also decrease autoimmune inflammation, supporting a potential autoimmune etiology [4]. Recommendations range from lower dosages up to 1 mg/kg prednisone for 10 days. Finally, vestibular exercises are recommended to enhance central compensatory mechanisms in patients recovering from vestibular neuritis. Vestibular therapy is typically designed to target the visual and optokinetic, vestibular, and somatosensory systems [30]. Exercises may include eye movements while following objects, head and body tilts and rotation, and balance exercises with eyes closed. Patients should develop an individualized rehabilitation program in collaboration with a

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vestibular therapist, in addition to home exercises. Initially, exercises should occur in short intervals to cause tolerable dizziness without triggering nausea and vomiting [31]. Exercise duration and repetitions can steadily be increased and adjusted as the patient’s symptoms improve.

Prognosis Patients typically experience acute dizziness over the span of days as the CNS gradually equilibrates mismatched peripheral vestibular signals. A prolonged interval of imbalance and dizziness typically follows the acute period, lasting for several weeks to months. Not all patients fully recover from vestibular neuritis. In fact, 30–50% of patients continue to suffer from varying dizziness and imbalance months to years after the initial episode [32–34]. Early initiation of vestibular rehabilitation is thought to accelerate recovery by enhancing central compensatory mechanisms. Vestibular exercises speed recovery of balance function and reduce perception of dizziness, thereby allowing patients to more quickly return to normal daily activities [30, 31]. Corticosteroids have similar early benefits, accelerating vestibular compensation [35]. Most evidence suggests that standard vestibular rehabilitation and corticosteroids yield similar outcomes for long-term recovery [36–38]. However, a recent study found that early vestibular rehabilitation, in addition to a 10-day prednisolone taper, significantly reduced perceived dizziness and improved daily function after 12 months when compared to 10 days of corticosteroids alone [31]. Long-term prognosis may also be explained by the patient’s visual and psychological predisposition. Visual dependence, or the degree of weighting visual input relative to vestibular input in evaluation of spatial orientation, plays a large role in long-term recovery. Patients in one study of 28 patients at least 6 months following vestibular neuritis who displayed the worst residual dizziness on Dizziness Handicap Inventory (DHI) (scores from 36 to 80) had higher visual dependence on Rod-and-­ Disk Testing than controls (6.35° v, 3.39°). There was no significant difference on Rod-and-Disk Testing between controls and patients who had minimal residual dizziness on DHI [39]. Other studies have found similar delays in recovery for patients with strong visual dependence after vestibular neuritis. Psychological conditions, including anxiety and depression, have also been associated with worse long-term outcomes following vestibular neuritis over a 10-month period and these poor outcomes can be further exacerbated by high levels of autonomic arousal (as measured by symptoms such as diaphoresis and palpitations) [32, 33]. In addition to standard therapy, patients with psychological factors associated with poor recovery may require pharmacotherapy and cognitive therapy to improve clinical outcomes following acute vestibular neuritis [32].

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Recurrence Risk Patients have a low risk of subsequent cases of vestibular neuritis. A study that followed 103 patients for an average of 10 years found only 2 patients (1.9%) developed a second case of vestibular neuritis [40]. Both patients developed subsequent vestibular neuritis in the contralateral ear and their symptoms were less severe during the second episode of this disorder [40].

Additional Sequelae Vestibular neuritis is one of the most common causes of secondary benign paroxysmal positional vertigo (BPPV) (15% of secondary BPPV) [41]. These secondary BPPV episodes affect the ipsilateral posterior semicircular canal to the initiating vestibular neuritis [42–45]. These findings suggest relative sparing of the inferior vestibular nerve division during vestibular neuritis, which innervates the posterior semicircular canal and is consistent with findings that the superior vestibular nerve branch is more susceptible to inflammatory damage due to vestibular neuritis [42]. Inflammatory damage to the macula and utricle may result in the displacement of otoliths, which collect in the dependent posterior semicircular canal, resulting in a pure posterior semicircular canal BPPV [42]. Additionally, the demyelinated superior vestibular nerve branch may be relatively unable to detect dislodged otoliths in the superior and horizontal SCCs. Finally, most patients experience acute anxiety following an episode of vestibular neuritis. Approximately 15% ultimately develop a somatoform or panic disorder [46]. Interestingly, severity of vertigo is not correlated with the development of the disorders. Rather, patients with poor psychosocial support networks are at higher risk of subsequently developing somatoform or panic disorders [47].

Summary Vestibular neuritis is a unilateral vestibulopathy due to inflammation of the vestibular nerve. Patients experience a rapid-onset, prolonged vertigo that resolves over days to weeks, with residual dizziness persisting until central compensation occurs. Initial examination may reveal a spontaneous nystagmus beating away from the affected side and positive HIT. Signs of central neurologic dysfunction should be absent. Vestibular suppressants may be useful during the first few days for symptomatic relief but may inhibit central compensatory mechanisms if use continues beyond this period. Treatment typically includes a combination of corticosteroids to reduce inflammation and early vestibular exercises to enhance central compensation.

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References 1. Strupp M, Mandala M, Lopez-Escamez JA. Peripheral vestibular disorders: an update. Curr Opin Neurol. 2019;32(1):165–73. https://doi.org/10.1097/WCO.0000000000000649. 2. Neuhauser HK.  The epidemiology of dizziness and vertigo. Handb Clin Neurol. 2016;137:67–82. https://doi.org/10.1016/B978-­0-­444-­63437-­5.00005-­4. 3. Muelleman T, Shew M, Subbarayan R, Shum A, Sykes K, Staecker H, et al. Epidemiology of dizzy patient population in a neurotology clinic and predictors of peripheral etiology. Otol Neurotol. 2017;38(6):870–5. https://doi.org/10.1097/MAO.0000000000001429. 4. Greco A, Macri GF, Gallo A, Fusconi M, De Virgilio A, Pagliuca G, et al. Is vestibular neuritis an immune related vestibular neuropathy inducing vertigo? J Immunol Res. 2014;2014:459048. https://doi.org/10.1155/2014/459048. 5. Bartual-Pastor J.  Vestibular neuritis: etiopathogenesis. Rev Laryngol Otol Rhinol (Bord). 2005;126(4):279–81. 6. Strupp M, Magnusson M. Acute unilateral vestibulopathy. Neurol Clin. 2015;33(3):669–85, x. https://doi.org/10.1016/j.ncl.2015.04.012. 7. Baloh RW. Clinical practice. Vestibular neuritis. N Engl J Med. 2003;348(11):1027–32. https:// doi.org/10.1056/NEJMcp021154. 8. Matsuo T.  Vestibular neuronitis—serum and CSF virus antibody titer. Auris Nasus Larynx. 1986;13(1):11–34. https://doi.org/10.1016/s0385-­8146(86)80020-­7. 9. Fishman JM. Corticosteroids effective in idiopathic facial nerve palsy (Bell’s palsy) but not necessarily in idiopathic acute vestibular dysfunction (vestibular neuritis). Laryngoscope. 2011;121(11):2494–5. https://doi.org/10.1002/lary.22327. 10. Rujescu D, Hartmann AM, Giegling I, Konte B, Herrling M, Himmelein S, et al. Genome-wide association study in vestibular neuritis: involvement of the host factor for HSV-1 replication. Front Neurol. 2018;9:591. https://doi.org/10.3389/fneur.2018.00591. 11. Arbusow V, Schulz P, Strupp M, Dieterich M, von Reinhardstoettner A, Rauch E, et  al. Distribution of herpes simplex virus type 1  in human geniculate and vestibular ganglia: implications for vestibular neuritis. Ann Neurol. 1999;46(3):416–9. https://doi.org/10.1002/ 1531-­8249(199909)46:33.0.co;2-­w. 12. Arbusow V, Derfuss T, Held K, Himmelein S, Strupp M, Gurkov R, et al. Latency of herpes simplex virus type-1 in human geniculate and vestibular ganglia is associated with infiltration of CD8+ T cells. J Med Virol. 2010;82(11):1917–20. https://doi.org/10.1002/jmv.21904. 13. Roehm PC, Camarena V, Nayak S, Gardner JB, Wilson A, Mohr I, et al. Cultured vestibular ganglion neurons demonstrate latent HSV1 reactivation. Laryngoscope. 2011;121(10):2268–75. https://doi.org/10.1002/lary.22035. 14. Hotson JR, Baloh RW.  Acute vestibular syndrome. N Engl J Med. 1998;339(10):680–5. https://doi.org/10.1056/NEJM199809033391007. 15. Bumm P, Schlimok G.  T-lymphocyte subpopulations and HLA-DR antigens in patients with Bell’s palsy, hearing loss, neuronitis vestibularis, and Meniere’s disease. Eur Arch Otorhinolaryngol. 1994:S447–8. https://doi.org/10.1007/978-­3-­642-­85090-­5_178. 16. Bumm P, Muller EC, Grimm-Muller U, Schlimok G. [T-lymphocyte subpopulation and HLA-DR antigens in hearing loss of vestibular neuropathy, Meniere’s diseases and Bell’s palsy]. Laryngorhinootologie. 1991;70(5):260–6. https://doi.org/10.1055/s-­2007-­998033. 17. Kassner SS, Schottler S, Bonaterra GA, Stern-Straeter J, Hormann K, Kinscherf R, et  al. Proinflammatory activation of peripheral blood mononuclear cells in patients with vestibular neuritis. Audiol Neurootol. 2011;16(4):242–7. https://doi.org/10.1159/000320839. 18. Bonaterra GA, Hildebrandt W, Bodens A, Sauer R, Dugi KA, Deigner HP, et  al. Increased cyclooxygenase-2 expression in peripheral blood mononuclear cells of smokers and hyperlipidemic subjects. Free Radic Biol Med. 2005;38(2):235–42. https://doi.org/10.1016/j. freeradbiomed.2004.10.021. 19. Bonaterra GA, Hildebrandt W, Bodens A, Sauer R, Dugi KA, Deigner HP, et  al. Increased gene expression of scavenger receptors and proinflammatory markers in peripheral blood

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mononuclear cells of hyperlipidemic males. J Mol Med (Berl). 2007;85(2):181–90. https:// doi.org/10.1007/s00109-­006-­0117-­6. 20. Oron Y, Shemesh S, Shushan S, Cinamon U, Goldfarb A, Dabby R, et  al. Cardiovascular risk factors among patients with vestibular neuritis. Ann Otol Rhinol Laryngol. 2017;126(8):597–601. https://doi.org/10.1177/0003489417718846. 21. Fetter M, Dichgans J. Vestibular neuritis spares the inferior division of the vestibular nerve. Brain. 1996;119(Pt 3):755–63. https://doi.org/10.1093/brain/119.3.755. 22. Silvoniemi P. Vestibular neuronitis. An otoneurological evaluation. Acta Otolaryngol Suppl. 1988;453:1–72. https://doi.org/10.3109/00016488809098974. 23. Gianoli G, Goebel J, Mowry S, Poomipannit P. Anatomic differences in the lateral vestibular nerve channels and their implications in vestibular neuritis. Otol Neurotol. 2005;26(3):489–94. https://doi.org/10.1097/01.mao.0000169787.99835.9f. 24. Jeong SH, Kim HJ, Kim JS. Vestibular neuritis. Semin Neurol. 2013;33(3):185–94. https://doi. org/10.1055/s-­0033-­1354598. 25. Aw ST, Fetter M, Cremer PD, Karlberg M, Halmagyi GM. Individual semicircular canal function in superior and inferior vestibular neuritis. Neurology. 2001;57(5):768–74. https://doi. org/10.1212/wnl.57.5.768. 26. Norrving B, Magnusson M, Holtas S. Isolated acute vertigo in the elderly; vestibular or vascular disease? Acta Neurol Scand. 1995;91(1):43–8. https://doi.org/10.1111/j.1600-­0404.1995. tb05841.x. 27. Kattah JC. Use of HINTS in the acute vestibular syndrome. An overview. Stroke Vasc Neurol. 2018;3(4):190–6. https://doi.org/10.1136/svn-­2018-­000160. 28. Kattah JC, Talkad AV, Wang DZ, Hsieh YH, Newman-Toker DE. HINTS to diagnose stroke in the acute vestibular syndrome: three-step bedside oculomotor examination more sensitive than early MRI diffusion-weighted imaging. Stroke. 2009;40(11):3504–10. https://doi. org/10.1161/STROKEAHA.109.551234. 29. Halmagyi GM, Chen L, MacDougall HG, Weber KP, McGarvie LA, Curthoys IS. The video head impulse test. Front Neurol. 2017;8:258. https://doi.org/10.3389/fneur.2017.00258. 30. Strupp M, Arbusow V, Maag KP, Gall C, Brandt T. Vestibular exercises improve central vestibulospinal compensation after vestibular neuritis. Neurology. 1998;51(3):838–44. https://doi. org/10.1212/wnl.51.3.838. 31. Tokle G, Morkved S, Brathen G, Goplen FK, Salvesen O, Arnesen H, et al. Efficacy of vestibular rehabilitation following acute vestibular neuritis: a randomized controlled trial. Otol Neurotol. 2020;41(1):78–85. https://doi.org/10.1097/MAO.0000000000002443. 32. Bronstein AM, Dieterich M.  Long-term clinical outcome in vestibular neuritis. Curr Opin Neurol. 2019;32(1):174–80. https://doi.org/10.1097/WCO.0000000000000652. 33. Cousins S, Kaski D, Cutfield N, Arshad Q, Ahmad H, Gresty MA, et  al. Predictors of clinical recovery from vestibular neuritis: a prospective study. Ann Clin Transl Neurol. 2017;4(5):340–6. https://doi.org/10.1002/acn3.386. 34. Adamec I, Krbot Skoric M, Ozretic D, Habek M. Predictors of development of chronic vestibular insufficiency after vestibular neuritis. J Neurol Sci. 2014;347(1–2):224–8. https://doi. org/10.1016/j.jns.2014.10.001. 35. Batuecas-Caletrio A, Yanez-Gonzalez R, Sanchez-Blanco C, Perez PB, Gonzalez-Sanchez E, Sanchez LA, et  al. Glucocorticoids improve acute dizziness symptoms following acute unilateral vestibulopathy. J Neurol. 2015;262(11):2578–82. https://doi.org/10.1007/ s00415-­015-­7918-­x. 36. Shupak A, Issa A, Golz A, Margalit K, Braverman I. Prednisone treatment for vestibular neuritis. Otol Neurotol. 2008;29(3):368–74. https://doi.org/10.1097/MAO.0b013e3181692804. 37. Goudakos JK, Markou KD, Psillas G, Vital V, Tsaligopoulos M. Corticosteroids and vestibular exercises in vestibular neuritis. Single-blind randomized clinical trial. JAMA Otolaryngol Head Neck Surg. 2014;140(5):434–40. https://doi.org/10.1001/jamaoto.2014.48.

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38. Ismail EI, Morgan AE, Abdel Rahman AM.  Corticosteroids versus vestibular rehabilitation in long-term outcomes in vestibular neuritis. J Vestib Res. 2018;28(5–6):417–24. https://doi. org/10.3233/VES-­180645. 39. Cousins S, Cutfield NJ, Kaski D, Palla A, Seemungal BM, Golding JF, et al. Visual dependency and dizziness after vestibular neuritis. PLoS One. 2014;9(9):e105426. https://doi.org/10.1371/ journal.pone.0105426. 40. Huppert D, Strupp M, Theil D, Glaser M, Brandt T. Low recurrence rate of vestibular neuritis: a long-term follow-up. Neurology. 2006;67(10):1870–1. https://doi.org/10.1212/01. wnl.0000244473.84246.76. 41. Baloh RW, Honrubia V, Jacobson K. Benign positional vertigo: clinical and oculographic features in 240 cases. Neurology. 1987;37(3):371–8. https://doi.org/10.1212/wnl.37.3.371. 42. Turk B, Akpinar M, Kaya KS, Korkut AY, Turgut S. Benign paroxysmal positional vertigo: comparison of idiopathic BPPV and BPPV secondary to vestibular neuritis. Ear Nose Throat J. 2019;100:145561319871234. https://doi.org/10.1177/0145561319871234. 43. Karlberg M, Halmagyi GM, Buttner U, Yavor RA.  Sudden unilateral hearing loss with simultaneous ipsilateral posterior semicircular canal benign paroxysmal positional v­ ertigo: a variant of vestibulo-cochlear neurolabyrinthitis? Arch Otolaryngol Head Neck Surg. 2000;126(8):1024–9. https://doi.org/10.1001/archotol.126.8.1024. 44. Mandala M, Santoro GP, Awrey J, Nuti D. Vestibular neuritis: recurrence and incidence of secondary benign paroxysmal positional vertigo. Acta Otolaryngol. 2010;130(5):565–7. https:// doi.org/10.3109/00016480903311278. 45. Balatsouras DG, Koukoutsis G, Ganelis P, Economou NC, Moukos A, Aspris A, et al. Benign paroxysmal positional vertigo secondary to vestibular neuritis. Eur Arch Otorhinolaryngol. 2014;271(5):919–24. https://doi.org/10.1007/s00405-­013-­2484-­2. 46. Godemann F, Schabowska A, Naetebusch B, Heinz A, Strohle A. The impact of cognitions on the development of panic and somatoform disorders: a prospective study in patients with vestibular neuritis. Psychol Med. 2006;36(1):99–108. https://doi.org/10.1017/S0033291705005921. 47. Godemann F, Schuller J, Uhlemann H, Budde A, Heinz A, Strohle A, et al. Psychodynamic vulnerability factors in the development of panic disorders—a prospective trial in patients after vestibular neuritis. Psychopathology. 2009;42(2):99–107. https://doi.org/10.1159/000203342. 48. Lee S, Kaylie DM.  Balance (anatomy: vestibular nerve). In: Kountakis SE, editor. Encyclopedia of otolaryngology, head and neck surgery. Berlin: Springer; 2013. https://doi. org/10.1007/978-­3-­642-­23499-­6_577.

Chapter 6

Third Mobile Window Syndromes Benjamin T. Crane and Lloyd B. Minor

Learning Objectives • The normal inner ear has openings at the round and oval window. Additional or third windows can be the source of symptoms including conductive hearing loss, dizziness, oscillopsia, autophony, and bone conducted hyperacusis. • Pathophysiology of third window syndromes. • Different types of third window syndromes have been described. • Symptoms that are suggestive of a third window syndrome, and other possible causes of these symptoms that should be considered in the differential diagnosis. • Appropriate work up, and limitations of testing. • Available treatment options including risks and potential benefits.

Introduction The normal inner ear has two mobile windows which are not surrounded by fixed bone. These are the oval window where the stapes interfaces with the inner ear and the round window. In a normal inner ear, any displacement of the stapes results in a pressure wave that travels through the cochlea to the round window. Third mobile window syndromes represent a pathological extra opening into the inner ear. The best known and most extensively studied of these superior canal dehiscence B. T. Crane (*) Departments of Otolaryngology, Neuroscience, and Biomedical Engineering, University of Rochester, Rochester, NY, USA L. B. Minor Department of Otolaryngology-Head and Neck Surgery, Stanford Medicine, Stanford, CA, USA e-mail: [email protected] © The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 B. T. Crane et al. (eds.), Disorders of the Vestibular System, https://doi.org/10.1007/978-3-031-40524-2_6

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syndrome (SCDS) [1] has well understood pathophysiology, and curative surgery therapy is now regularly performed throughout the world [2]. Of course it is also possible to have a pathologic opening in almost any other area of the inner ear including other semicircular canals [3, 4], or the cochlea such as near the facial nerve [5, 6]. The pathophysiology of these conditions is due to this “third mobile window” in addition to the oval and round windows [7]. With an abnormal opening in the labyrinth, pressure entering the labyrinth via the stapes at the oval window is partially shunted away from the round window to a new low impedance canal pathway in the canal. Bone conducted sound also now has a new route of entrance into the inner ear via the dehiscence. Posterior semicircular canal dehiscence is now recognized as a third mobile window syndrome [3, 8]. This condition usually also presents with pulsatile tinnitus, sound or pressure induced vertigo, and bone conduction hyperacusis symptoms. Other atypical symptoms which can mimic Meniere’s disease have been described [9, 10]. Dehiscence of the posterior canal can be associated with jugular bulb anomalies, fibrous dysplasia [11], congenital syndromes, cholesteatoma [12], and iatrogenic injury. In a recent review, the most common presenting symptoms were sound induced vertigo (38%), mixed hearing loss (36%), and tinnitus (34%) [3]. Thus, symptoms are often similar to SCDS, although like SCDS, it is believed that many patients may be asymptomatic and never present for evaluation. Transmastoid plugging of the posterior canal seems to be the most the most common treatment for this condition [8, 12, 13]. Lateral semicircular canal dehiscence usually occurs as a complication of chronic otitis media [14], cholesteatoma, and associated surgical treatment. Such fistulas are found in 2% of revision canal wall up mastoidectomy and 13% of revision canal wall down mastoidectomy [15]. Management of these fistulas is controversial some have advocated a complete removal of the cholesteatoma with repair of the bony defect [16], while others have advocated leave some cholesteatoma over the fistula and doing a canal wall down procedure [17]. Enlarged vestibular aqueduct syndrome (EVAS) is also recognized as a cause of third mobile window syndrome due to a larger than normal vestibular acting as a path for acoustic energy to be shunted away from the cochlea. The criteria used for diagnosis is typically the midpoint of the vestibular aqueduct being 1.5 mm or greater [18]. The finding is often bilateral and can be associated with other conditions such as Pendred syndrome and choanal atresia. Hearing loss is often the predominate feature and it is often conductive although a sensorneural hearing loss is also present in many cases. Perhaps because acoustic energy is not shunted through the semicircular canals, only rarely is vertigo a symptom of EVAS [19]. Surgical treatment associated with closing or reducing the size of the vestibular aqueduct has not been successful. Discussion will now focus on SCDS as this is the most common and most extensively studied third window syndrome, and because other third window syndromes often include similar symptoms. Patients with SCDS can present clinically with sound-induced vertigo and oscillopsia (bouncing of vision), and with decreased hearing thresholds for bone conducted sounds (i.e., conductive hyperacusis) while having increased thresholds for air conducted sounds. This can lead to difficulty

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hearing external air conducted sound but also causes heighted perception of bone conducted sound so patients can hear their pulse, eye movements, chewing or steps as well as experience autophony. The dizziness and vertigo symptoms are common and can be disabling. These symptoms include chronic disequilibrium as well as vertigo induced by loud sound or pressure changes [2, 20, 21].

Diagnostic Evaluation As with any complaint of dizziness, a good history is key. Patients with SCDS usually present with a primary complaint of either autophony or dizziness although they occasionally have isolated conductive hearing loss [22] that can mimic otosclerosis. Vertigo related to SCDS is usually brief and induced by loud sound or pressure changes. Sound-induced dizziness or oscillopsia is present in 90% of SCDS patients [21]. Pressure induced vestibular symptoms, often manifest with coughing or straining, are present in 73% of patients, with 67% exhibiting both pressure- and soundrelated symptoms [21]. Chronic disequilibrium may also be attributed to SCDS [23]. Auditory symptoms are common and may be present in 85% of SCDS cases [24]. Hyperacusis for bone-conducted sound [25, 26] is present in 52% [21]. Symptoms often include hearing one’s pulse or eye movements. Autophony or the patients hearing their own voice sounding disturbing to them is present in up to 60% of patients [21, 27]. Eye movements in the plane of the superior canal evoked by sound or pressure are the hallmark clinical finding of SCDS [28, 29]. The eyes should be examined under Frenzel or video goggles to eliminate visual fixation. Tones at levels up to 110 dB nHL should be delivered in one ear at a time. Sound-evoked eye movements were noted in 82% of SCDS patients [21]. Eye movements can also be induced with Valsalva maneuvers (75%) or pressure applied to the external auditory canal (45%). Depending on the type of stimulus and the direction of endolymph flow either excitation or inhibition of the superior canal may occur. Eye movements evoked by pressure or sound almost always occur in the superior canal plane. If eye movements are in another direction, the SCDS diagnosis should be questioned, and alternative diagnoses of posterior canal dehiscence [30] or horizontal canal fistula [31] considered. Sound-evoked rotation of the head in the superior canal plane occurred in 14% of patients. The audiogram is an important part of the SCDS evaluation, and a minority of patients have only auditory symptoms [21, 22, 32, 33]. Conductive hearing loss (CHL) is often largest at lower frequencies [22, 32, 34], and bone conduction thresholds can be negative (conductive hyperacusis). Because of the CHL and normal appearance of the ear, some patients with primarily auditory symptoms have been misdiagnosed as having  otosclerosis [33]. The key differences are (1) that conductive hyperacusis does not occur in otosclerosis, and (2) that the acoustic stapedial reflex, which is often normal in superior canal dehiscence, should be absent with otosclerosis.

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Vestibular-evoked myogenic potentials (VEMP) responses are enhanced in SCDS.  The cervical VEMP (cVEMP) is measured from the sternocleidomastoid muscles using averaged electromyography in response to multiple loud clicks or tone bursts delivered to the ear. The reflex is thought to be activated by sound transmitted through the stapes footplate to the saccule which is innervated by the inferior vestibular nerve [35]. Decreased cVEMP thresholds and large amplitude responses are indicative of SCDS. cVEMP thresholds for air-conducted 500 Hz tone bursts, for example, cVEMP thresholds were 80–95 dB SPL for 13 patients with SCDS (83.85 ± 1.40 dB SPL, mean ± SD), 20–30 dB lower than in normal control subjects (110.25 ± 1.28 dB SPL) [36]. It has been argued that cVEMP is better than 90% sensitive and specific for SCD [37] but sensitivity and specificity depend on the parameters used [38]. Ocular VEMP (oVEMP) similarly measures averaged electromyography in response to tone bursts delivered to the ear or sometimes forehead taps. The oVEMP reflex is thought to be activated by sound or vibration being transmitted via the utricle and superior vestibular nerve to the contralateral inferior oblique muscle [39, 40]. The amplitude of this excitatory potential is measured through surface recording electrodes placed beneath the eyes. Some prefer the evaluation oVEMP responses as they may be more easily tolerated and more sensitive and specific for detection of SCDS than the cVEMP [41–43]. The oVEMP responses can also be done more quickly as they do not require finding a threshold. As a result, oVEMP testing is becoming more widely available at academic centers. Despite its utility for diagnosis, these tests are poorly correlated with patient symptom severity [44]. The VEMP is not always measurable and is likely to be absent in those with previous middle ear surgery. Although the oVEMP measurements can circumvent this problem using forehead taps [42], this version of the test is less commonly available. The VEMP threshold may also be decreased in other conditions such as enlarged vestibular aqueduct syndrome [45]. Use of VEMP can also differentiate SCDS from middle ear causes of conductive hearing loss in which VEMP should be absent [46]. Imaging of the temporal bone using computed tomography (CT) must show the absence of bone over the superior canal (SC) for SCDS to be considered. If the SC appears covered by bone on CT the diagnosis of SCDS is excluded; however, the appearance of a dehiscence on CT does not rule out thin bone covering the SC below the resolution of the scanner. Thus, CT is a highly sensitive test for SCD but it is not specific [47] due to a high rate of false positives. In a review of temporal bone CT scans done in the general population, 9% of scans had apparent SCD with one observer calling as many as 12% [48]. Many are likely false positives caused by the limits of resolving thin bone, since the incidence of SCD in a survey of temporal bones was only 0.7% [49]. Images should be reconstructed in the plane of the superior canal as well as orthogonal to it so that any dehiscence can be definitively demonstrated. However, due to the high risk of false-positive findings and overestimation of dehiscence size [50], the diagnosis of SCD must never be based on a CT alone. Magnetic resonance imaging (MRI) may suggest SCD [51]. The best images are a T2-weighted protocols (e.g., Constructive Interference in Steady State, or CISS) and reconstructed in the plane of the superior canal. However, even these protocols

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Table 6.1  Proposed diagnostic criteria for superior semicircular canal dehiscence syndrome (SCDS) Diagnostic criteria for superior semicircular canal dehiscence syndrome  1. At least one of the following symptoms consistent with a third window lesion of the inner ear:    (a) Bone conduction hyperacusis    (b) Pulsatile tinnitus    (c) Acute sound-induced vertigo and/or oscillopsia    (d) Pressure-induced vertigo and/or oscillopsia  2. At least one of the following diagnostic tests indicating a third mobile window of the inner ear:    (a) Nystagmus characteristic of excitation or inhibition of the affected superior canal evoked by sound (Tullio phenomenon) or changes in middle ear pressure (Hennebert sign) or intracranial pressure    (b) Low-frequency negative bone conduction thresholds on pure tone audiometry    (c) Enhanced VEMP responses (low cervical VEMP thresholds or high ocular VEMP amplitudes)  3. High-resolution temporal bone CT imaging with multiplanar reconstructions demonstrating dehiscence of the superior canal  4. Not better accounted for by another vestibular disease or disorder

may have a high false-positive rate, and CT is probably the better study for most evaluations. However, MRI may be appropriate for evaluating the efficacy of previous canal plugging by assessing the fluid signal in the superior canal [52]. The diagnosis of SCDS should be based on CT imaging showing a dehiscence, symptoms consistent with a mobile third window, and at least one physiologic measure supporting the presence of a third mobile window. The proposed diagnostic criteria for diagnosis of SCDS [2] are shown in Table 6.1.

Differential Diagnosis Other common conditions can cause symptoms similar to SCDS making it important to consider a differential diagnosis. When conductive hearing loss is present in a setting without trauma and with a normal otoscopic exam, SCDS should be considered along with otosclerosis. Autophony raises the possibility of a patulous Eustachian tube, but SCDS can produce a similar sensation. Episodic vertigo evoked by intracranial or middle ear pressure changes could indicate a perilymphatic fistula, but SCDS should strongly be considered as an alternative diagnosis. We have seen several patients who have undergone previous surgical explorations for these presumed otological disorders, only later to be found to have SCDS. The conductive hearing loss with SCDS often appears similar to otosclerosis because both occur in adulthood with a normal otoscopic exam [33]. The audiograms differ in that patients with SCDS often have negative bone conduction thresholds, and if there is no previous history of middle ear surgery the acoustic reflex is often intact. Autophony is often the predominant symptom in patients with a patulous Eustachian tube (PET) [53], but it can also be the most disturbing symptom in

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SCDS [54]. One distinguishing feature is that patients with PET typically have autophony for their breath sounds (especially for nasal breathing), whereas patients with SCDS usually do not [53]. A history of vertigo and hyperacusis to bone conducted sound are atypical of a PET. The audiogram, VEMP, and CT will typically differentiate a PET from SCDS. Perilymph fistula and fenestrations of other semicircular canals are considered in the differential diagnosis of SCDS [4, 55, 56]. The diagnosis of perilymph fistula is most clear in the presence of recent stapes surgery, temporal bone fracture, or barotrauma injury. In these cases, acute vertigo is usually accompanied by a sensorineural hearing loss. A fistula in the horizontal canal can be acquired in cases of cholesteatoma or prior mastoidectomy [15]. Spontaneous perilymph fistula is a controversial diagnosis, which if considered at all should only be considered after all other possible causes are excluded [57]. The most common cause of spontaneous (nonpositional) vertigo is vestibular migraine [58–60]. The migraine incidence is 17.6% of females and 5.7% of males [61], and approximately 25% of these report associated vertigo [62]. Migraine is much more common than SCDS, and inevitably symptoms in some patients with radiographically apparent SCD with nonspecific symptoms may be better explained by migraine. Particularly challenging are those patients who have both SCDS and migraine [2, 63]. It may be difficult to determine if their sound sensitivity is due to one more than the other, for example. Their chronic disequilibrium may be related to migraine, or it may be due to the constant transmission of intracranial pressure pulsations through the dehiscence. The symptoms of SCDS could serve as triggers to exacerbate migraine in susceptible individuals. However, the neurotologist must also consider that failure to recognize and treat coexistent migraine can lead to disappointing results in SCDS surgery, as it can with other causes of vertigo. Optimization of migraine treatment is recommended prior to SCD surgery [2, 63].

Operative Decision Making The physician and patient must weigh the symptom severity against the risks and benefits of surgery. In the authors’ experience, only a third of patients with SCDS elect to have surgery, with the remaining patients choosing to live with their symptoms or making lifestyle changes to avoid situations that exacerbate symptoms. Control of comorbid vestibular migraine has in several cases allowed patients to avoid surgery. Most SCDS patients present to a neurotology clinic for dizziness or vertigo of variable severity. Some patients are disabled by their symptoms, and surgery is the only viable option for them to have an acceptable quality of life. Autophony, or the abnormal sound of one’s own voice, can be disabling. There is no medical treatment for autophony symptoms due to SCDS, as the sound transmission is via bone, not the Eustachian tube. Thus, for SCDS patients who are

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significantly disturbed by autophony, surgery is the only option for relief and has been shown to have a significant benefit [54, 64]. Conductive hearing loss is common in SCDS [22, 27, 65, 66], but it is often limited to low frequencies and one ear, so many patients do not have a significant disability from it. The risk of hearing loss progressing over time is also low [67, 68]. In most patients, the conductive hearing loss improves with surgery [65, 69]. However, plugging of SCD also carries a risk of hearing loss [70], which is greater in patients with prior ear surgery [65, 69]. Patients who have hearing loss as their primary symptom of SCDS should be encouraged to consider nonsurgical options such as a hearing aid. Pulsatile tinnitus and bone conduction hyperacusis can be disabling in some and the primary reason to seek treatment. In rare cases, nonsurgical options can ameliorate these symptoms for instance in cases were the SCDS occurs at the superior petrosal sinus, embolization [71], or stenting [72] of the superior petrosal sinus has improved symptoms. Although dizziness symptoms are often the motivation for surgery, imbalance symptoms may be worse during the immediate postoperative period. Symptoms improve as the patient adapts, and we typically prescribe vestibular rehabilitation. Benign paroxysmal positional vertigo (BPPV) has been reported in as many as 24% of cases [73] after plugging, and can be treated with repositioning maneuvers. Plugging of the superior canal will cause loss of function due to hydrodynamic insufficiency of the plugged canal [74, 75]. However, patients can adapt very well to this single-canal insufficiency, as low-frequency, low-acceleration head movements still generate useful inhibitory signals from the contralateral posterior canal.

Bilateral Dehiscence About a quarter of individuals with SCDS have the appearance of bilateral SCD on high-resolution CT scan [76]. Fortunately, one side is usually responsible for most symptoms. In some cases, symptoms and signs can be elicited from both ears. In such patients that do have bilateral SCDS, every effort should be made to identify the more symptomatic ear and operate on that side first. In most cases, symptoms will either resolve after operating on the more symptomatic side or abate to the point that contralateral surgery is not required. Only 11% of patients with bilateral SCDS opt to have bilateral surgery [76]. We recommend the second side only be considered for plugging surgery after sufficient time for adaptation in the partial loss of vertical semicircular canal function, typically after 6 or more months have passed since the operation. Plugging of both superior canals significantly impairs the ability to sense downward head rotation in the vertical plane, so these patients are at risk of developing vertical oscillopsia during ambulation [76]. Patients with bilateral SCDS had worse symptom control than those with unilateral disease if one or both sides were treated [64].

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Near Dehiscence Although controversial, it is recognized that symptoms of SCDS can occur even if very thin bone over remains over the superior canal [77]. In these cases, CT is often read as showing a dehiscence, and the patient can have other objective evidence of dehiscence including an air-bone gap on audiometry, increased oVEMP amplitude, and low cVEMP thresholds. Although these patients can benefit from surgery, caution is suggested as these patients have more residual symptoms and may have a higher rate of postoperative complications than patients with frank dehiscence [2] but they can, in some cases, benefit from surgery [78].

Operative Technique The middle cranial fossa approach was described first [1] and is the technique detailed in the following paragraphs. An alternative transmastoid approach has also  become popular. Advocates of the transmastoid approach have noted that it avoids a craniotomy, involves no temporal lobe retraction, and may lead to better stability of the canal plug. Moreover, most otolaryngologists are more familiar with mastoidectomy [79, 80]. The transmastoid approach was initially described in two patients in 2001, and although these patients were relieved of vertigo symptoms, one patient experienced significant sensorineural hearing loss after surgery [81]. More recently additional reports of transmastoid superior canal plugging have been published with both minimal morbidity and improvement in symptoms [2, 79, 80, 82–86]. The middle fossa approach has, in principle, some advantages. The transmastoid approach does not allow direct confirmation of the dehiscence, and transmastoid plugging of a superior canal that was later found to be intact has been described [79]. The transmastoid approach may not be possible in patients with a low hanging dura or extensive tegmen dehiscences [79]. In the transmastoid approach, openings in the canal need to be created and plugging material must be advanced beyond these openings to be successful. Thus, the plug is placed closer to the sensory epithelia of the ampulla and the utricle. This may be more traumatic to these structures, risking disturbance of their baseline firing rates. Furthermore, opening the superior canal distal to the dehiscence may place the plug into the common crus, causing loss of sensory function of the posterior canal as well [75]. The transmastoid approach also creates a new dehiscence which can make it difficult to know the source if the patient develops residual symptoms later. Finally, the transmastoid approach requires drilling, irrigation, and suctioning on the bony canal. Once the canal is opened, these manipulations could contaminate or remove perilymph from the canal and cause collapse of the membranous labyrinth or serous labyrinthitis. Round window plugging or reinforcement has been suggested as a treatment for SCDS [87, 88]. The procedure does not directly address the third window at the superior canal and some patients developed worse symptoms after this procedure

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[87]. A recent retrospective case review suggested that although some patients reported improvement in subjective symptoms such as autophony and vertigo, improvement in objective tests such as VEMP were rare and hearing was often diminished after the procedure [89]. Many of these patients require revision surgery via a transmastoid or middle fossa approach [90]. Due to the poor outcomes and because it does not directly address the known pathophysiology of the disease, round window plugging is not widely considered to be an appropriate treatment [89, 91]. The transmastoid approach may be preferable in cases where the patient cannot tolerate a middle fossa surgery, or the dehiscence cannot easily be accessed through the middle fossa—for instance when the dehiscence is at the superior petrosal sinus [92, 93]. Some patients who have been symptomatic after a middle fossa approach have had relief of symptoms with a revision surgery via a transmastoid approach [83]. It is difficult to directly compare outcomes associated with a transmastoid and middle fossa approach because of differences in relative indications between them. For middle fossa approach, the incision is made from the helical root around the helix to a location over the external auditory canal, and then superiorly. Temporalis fascia is harvested for later use in plugging the superior canal and for repair of any tegmen defects or cerebrospinal fluid leak that may occur. Afterward, the temporalis muscle is divided, and the area of the craniotomy exposed. The craniotomy should be centered over the superior canal, the external auditory canal is often a good landmark but image navigation can be used. The lower border of the craniotomy is placed just high enough to avoid the mastoid air cells. The width and height of the craniotomy should accommodate a middle fossa retractor, typically 3 cm wide by 4 cm high. The craniotomy is opened by drilling troughs around the borders using a 4-mm burr. The dura should remain intact, and the bone flap removed and preserved in saline. The dura is further elevated from the edges of the craniotomy to allow retraction. The sharp edges of the craniotomy are removed using small Kerrison rongeurs, and the bone chips created in this process can be used as plugs for the superior canal. The middle cranial fossa retractor is placed and used to gently elevate the dura off the middle fossa. Dura here can be thin, especially if tegmen dehiscences are also present, and large cotton balls soaked in saline are a minimally traumatic means for the dural elevation. A hemostatic agent such as dry microfibrillar collagen (Avitene®) or gelatin powder (Gelfoam®) mixed as a paste with thrombin is generously applied in advance of the cotton balls. The surgeon is careful to only suction on the cotton balls and not to directly suction the area of the dehiscence because of the risk that this poses for removing excessive perilymph or for tearing the membranous labyrinth, which could cause sensorineural hearing and vestibular loss. After identifying the superior canal dehiscence, attention is shifted toward plugging. Small pieces of previously harvested temporalis fascia are gently slid into the two open lumens of the bony superior canal. Several pieces are used to advance the plugs a few millimeters beyond the dehiscence. Care must be taken that one end is not thus left open because its fascia is displaced, which is common as fascia is pushed in the other side. To prevent this, once the fascia is in place, bone chips

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matching the diameter of the canal are firmly lodged so as to “cork” each end of the dehiscence. Other groups have used materials such as bone wax [94] or a mixture of fibrin glue and bone dust [79]. The surgeon must ensure a watertight seal is obtained to prevent pressure transmission through the third mobile window. Bone cement can also be used to resurface the area after plugging. Closure is achieved by anchoring the previously harvested bone flap in place. The temporalis muscle is reapproximated with absorbable sutures, and the skin is closed with staples and/or suture. A drain is not typically used, but a gentle pressure dressing is maintained for 2 days.

Postoperative Care A monitored bed with neurological checks in the immediate postoperative period is recommended due to the epidural hematoma risk. Postoperative patients are treated with intravenous steroids which can be quickly tapered. Patients frequently experience nausea during the initial hours after surgery. This is best controlled with intravenous promethazine (Phenergan). For the first 24–26 h, short acting narcotics can be administered by the patient-controlled analgesia (PCA) with proper neurological nursing assessments to ensure that any change in neurological status is not masked by excessive sedation. Routine postoperative analgesics are sufficient to control the pain thereafter. If the patient is experiencing intense pain or if there is any change in mental status, an epidural hematoma may be the cause and an immediate head CT should be considered. The typical hospitalization lasts a total of 2 or 3 days.

Long-Term Results Most patients are extremely satisfied with the surgery, with studies supporting improvements in overall quality of life [86, 95], autophony [54], and dizziness symptoms [96]. Relief of dizzy symptoms has been documented by measuring the dizziness handicap inventory (DHI) [97] which improved by 26 points. Patients with more severe dizziness (DHI ≥30) improving by an average of 39 points [96]. Nearly all patients would recommend the surgery to others [64]. For some patients, autophony or hyperacusis for internal sounds are the primary reason for undergoing SCDS surgery and this is the most reported presenting symptom after dizziness [27]. Autophony is on average 89% improved immediately after surgery [54] and similar improvement is maintained long term [64]. Some autophony symptoms may take time to resolve due to fluid collecting in the middle ear after surgery. The results for improving hearing with SCD surgery are gratifying if conductive hyperacusis is documented preoperatively. Dramatic results have been reported in some patients, [98] but are uncommon. The air-bone gap that is present prior to surgery typically closes within several months after surgery [69, 99] once any

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middle ear effusions or hemotympanum have resolved; however, patients can also experience hearing loss after SCD surgery. Two larger series found a mild (~10 db) high-frequency sensorineural hearing loss in 25% of cases [69, 99] and profound hearing loss has been reported in 2.5% of cases [100]. In patients with previous middle cranial fossa or stapes surgery, one series found the risk of hearing loss was high [65]. A recent review found audiometric outcomes varied significantly among studies and although transmastoid and middle fossa approaches seem to be safe, subjective hearing improvement was not significant [101]. However, our own experience is that air-bone gaps, if present prior to surgery, are reduced after surgical plugging of the affected canal, and that symptoms of conductive hyperacusis like autophony and pulsatile tinnitus are also ameliorated.

Summary The diagnosis of SCDS is based on patient history, physical exam including eye movements in response to sound or pressure, and other supporting studies including the audiogram, VEMPs, and CT imaging. The spectrum and severity of symptoms of SCDS vary significantly among individuals, and the potential benefit of surgery must be carefully compared to the risks and probability of success in each patient. A large fraction of patients with SCDS do not opt for surgery. Both middle fossa and transmastoid approaches are reasonable treatments for SCDS.  Patients generally experience an improvement in symptoms of  dizziness, autophony, and hyperacusis symptoms. Although there is often an improvement in hearing after surgery, this must be carefully weighed against the risk of hearing loss, which is significant in patients who have had previous middle fossa or stapes surgery. Quiz Questions 1. True/False: Superior canal dehiscence is usually congenital. 2. True/False: Horizontal canal dehiscence is occurs as a complication of cholesteatoma or mastoidectomy surgery. 3. True/False: Computed tomography (CT) is the gold standard for diagnosis of SCD, and if it is seen on CT, no further testing is required for diagnosis. 4. True/False: Vestibular migraine is much more common than third window symptoms and should be treated prior to considering treatment for SCDS. 5. True/False: When the threshold of cervical vestibular-evoked myopotentials is higher than 95 dB nHL, it suggests SCDS. 6. True/False: Ocular vestibular-evoked myopotentials have a larger than normal amplitude in patients with SCDS. 7. True/False: Transmastoid plugging of the superior canal is a good option for patients who are not candidates for a middle fossa approach. 8. True/False: Plugging the round window directly addresses the site of the dehiscence in third window syndromes.

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9. True/False: The majority of patients with SCDS opt to get surgical treatment. 10. True/False: Conductive hearing loss with an absent acoustic reflex and otherwise normal ear exam suggests SCDS. Quiz Answers 1. False. Congenital SCD is very uncommon. 2. True. The horizontal canal is the most frequent site of violation of the inner ear due to cholesteatoma and related surgery. 3. False. CT has a high positive rate with about 10% of scans showing dehiscence, while the true incidence is probably closer to 1%. 4. True. Vestibular migraine is much more common than SCDS and other third window syndromes. 5. False. Threshold of cVEMP above 95 dB nHL is normal. cVEMP thresholds in SCDS are typically lower than normal. The exact threshold may depend on the lab and technique but typically less than 75 dB. 6. True. Large oVEMP amplitudes suggest SCDS. 7. True. Most agree either the transmastoid or middle fossa approaches are reasonable. 8. False. The round window is part of normal inner ear physiology, a third window must occur at other site. Round window plugging is not considered to be standard of care. 9. False. In several series, about one in three patients opts to get surgery. Many patients with superior canal dehiscence probably never develop symptoms. 10. False: Conductive hearing loss with an absent acoustic reflex suggests otosclerosis. In SCDS, the acoustic reflex should be present.

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49. Carey JP, Minor LB, Nager GT.  Dehiscence or thinning of bone overlying the superior semicircular canal in a temporal bone survey. Arch Otolaryngol Head Neck Surg. 2000;126(2):137–47. 50. Tavassolie TS, Penninger RT, Zuniga MG, Minor LB, Carey JP. Multislice computed tomography in the diagnosis of superior canal dehiscence: how much error, and how to minimize it? Otol Neurotol. 2012;33(2):215–22. https://doi.org/10.1097/MAO.0b013e318241c23b. 51. Browaeys P, Larson TL, Wong ML, Patel U. Can MRI replace CT in evaluating semicircular canal dehiscence? AJNR Am J Neuroradiol. 2013;34(7):1421–7. https://doi.org/10.3174/ ajnr.A3459. 52. Sharon JD, Pross SE, Ward BK, Carey JP.  Revision surgery for Superior Canal dehiscence syndrome. Otol Neurotol. 2016;37(8):1096–103. https://doi.org/10.1097/ MAO.0000000000001113. 53. Poe DS.  Diagnosis and management of the patulous eustachian tube. Otol Neurotol. 2007;28(5):668–77. 54. Crane BT, Lin FR, Minor LB, Carey J. Improvement in autophony symptoms after superior canal dehiscence repair. Otol Neurotol. 2010;31:140–6. 55. Minor LB.  Labyrinthine fistulae: pathobiology and management. Curr Opin Otolaryngol Head Neck Surg. 2003;11(5):340–6. 56. Weinreich HM, Carey JP. Perilymphatic fistulas and superior semi-circular canal dehiscence syndrome. Adv Otorhinolaryngol. 2019;82:93–100. https://doi.org/10.1159/000490276. 57. Friedland DR, Wackym PA. A critical appraisal of spontaneous perilymphatic fistulas of the inner ear. Am J Otol. 1999;20(2):261–76; discussion 76–9. 58. Eggers SD.  Migraine-related vertigo: diagnosis and treatment. Curr Pain Headache Rep. 2007;11(3):217–26. 59. Dieterich M, Obermann M, Celebisoy N.  Vestibular migraine: the most frequent entity of episodic vertigo. J Neurol. 2016;263(Suppl 1):S82–9. https://doi.org/10.1007/ s00415-­015-­7905-­2. 60. Lempert T, Olesen J, Furman J, Waterston J, Seemungal B, Carey J, et  al. Vestibular migraine: diagnostic criteria. J Vestib Res. 2012;22(4):167–72. https://doi.org/10.3233/ VES-­2012-­0453. 61. Tepper SJ. A pivotal moment in 50 years of headache history: the first American migraine study. Headache. 2008;48(5):730–1. 62. Kayan A, Hood JD.  Neuro-otological manifestations of migraine. Brain. 1984;107(Pt 4):1123–42. 63. Jung DH, Lookabaugh SA, Owoc MS, McKenna MJ, Lee DJ. Dizziness is more prevalent than autophony among patients who have undergone repair of superior canal dehiscence. Otol Neurotol. 2015;36(1):126–32. https://doi.org/10.1097/MAO.0000000000000531. 64. Alkhafaji MS, Varma S, Pross SE, Sharon JD, Nellis JC, Santina CCD, et  al. Long-term patient-reported outcomes after surgery for superior canal dehiscence syndrome. Otol Neurotol. 2017;38(9):1319–26. https://doi.org/10.1097/MAO.0000000000001550. 65. Limb CJ, Carey JP, Srireddy S, Minor LB.  Auditory function in patients with surgically treated superior semicircular canal dehiscence. Otol Neurotol. 2006;27(7):969–80. 66. McEvoy TP, Mikulec AA, Armbrecht ES, Lowe ME.  Quantification of hearing loss associated with superior semi-circular canal dehiscence. Am J Otolaryngol. 2013;34(4):345–9. https://doi.org/10.1016/j.amjoto.2013.01.009. 67. Patel NS, Hunter JB, O’Connell BP, Bertrand NM, Wanna GB, Carlson ML. Risk of progressive hearing loss in untreated superior semicircular canal dehiscence. Laryngoscope. 2017;127(5):1181–6. https://doi.org/10.1002/lary.26322. 68. Lookabaugh S, Niesten ME, Owoc M, Kozin ED, Grolman W, Lee DJ.  Audiologic, cVEMP, and radiologic progression in superior canal dehiscence syndrome. Otol Neurotol. 2016;37(9):1393–8. https://doi.org/10.1097/MAO.0000000000001182. 69. Ward BK, Agrawal Y, Nguyen E, Della Santina CC, Limb CJ, Francis HW, et al. Hearing outcomes after surgical plugging of the superior semicircular canal by a middle cra-

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nial fossa approach. Otol Neurotol. 2012;33(8):1386–91. https://doi.org/10.1097/ MAO.0b013e318268d20d. 70. Gioacchini FM, Alicandri-Ciufelli M, Kaleci S, Scarpa A, Cassandro E, Re M. Outcomes and complications in superior semicircular canal dehiscence surgery: a systematic review. Laryngoscope. 2016;126(5):1218–24. https://doi.org/10.1002/lary.25662. 71. Aw GE, Parker GD, Halmagyi GM, Saxby AJ.  Pulsatile tinnitus in superior semicircular canal dehiscence cured by endovascular coil occlusion of the superior petrosal sinus. Otol Neurotol. 2020. Publish ahead of print. https://doi.org/10.1097/MAO.0000000000003012. 72. Ionescu EC, Coudert A, Reynard P, Truy E, Thai-Van H, Ltaief-Boudrigua A, et al. Stenting the superior petrosal sinus in a patient with symptomatic superior semicircular canal dehiscence. Front Neurol. 2018;9:689. https://doi.org/10.3389/fneur.2018.00689. 73. Barber SR, Cheng YS, Owoc M, Lin BM, Remenschneider AK, Kozin ED, et al. Benign paroxysmal positional vertigo commonly occurs following repair of superior canal dehiscence. Laryngoscope. 2016;126(9):2092–7. https://doi.org/10.1002/lary.25797. 74. Janky KL, Zuniga MG, Ward B, Carey JP, Schubert MC. Canal plane dynamic visual acuity in superior canal dehiscence. Otol Neurotol. 2014;35(5):844–9. https://doi.org/10.1097/ MAO.0000000000000336. 75. Carey JP, Migliaccio AA, Minor LB. Semicircular canal function before and after surgery for superior canal dehiscence. Otol Neurotol. 2007;28(3):356–64. 76. Agrawal Y, Minor LB, Schubert MC, Janky KL, Davalos-Bichara M, Carey JP. Second-side surgery in superior canal dehiscence syndrome. Otol Neurotol. 2012;33(1):72–7. https://doi. org/10.1097/MAO.0b013e31823c9182. 77. Ward BK, Wenzel A, Ritzl EK, Gutierrez-Hernandez S, Della Santina CC, Minor LB, et al. Near-dehiscence: clinical findings in patients with thin bone over the superior semicircular canal. Otol Neurotol. 2013;34(8):1421–8. https://doi.org/10.1097/MAO.0b013e318287efe6. 78. Baxter M, McCorkle C, Trevino Guajardo C, Zuniga MG, Carter AM, Della Santina CC, et al. Clinical and physiologic predictors and postoperative outcomes of near dehiscence syndrome. Otol Neurotol. 2019;40(2):204–12. https://doi.org/10.1097/MAO.0000000000002077. 79. Agrawal SK, Parnes LS. Transmastoid superior semicircular canal occlusion. Otol Neurotol. 2008;29(3):363–7. 80. Crovetto M, Areitio E, Elexpuru J, Aguayo F. Transmastoid approach for resurfacing of superior semicircular canal dehiscence. Auris Nasus Larynx. 2008;35(2):247–9. 81. Brantberg K, Bergenius J, Mendel L, Witt H, Tribukait A, Ygge J. Symptoms, findings and treatment in patients with dehiscence of the superior semicircular canal. Acta Otolaryngol. 2001;121(1):68–75. 82. Kirtane MV, Sharma A, Satwalekar D.  Transmastoid repair of superior semicircular canal dehiscence. J Laryngol Otol. 2008;1-3:356. 83. Powell HR, Khalil SS, Saeed SR. Outcomes of transmastoid surgery for superior semicircular canal dehiscence syndrome. Otol Neurotol. 2016;37(7):e228–33. https://doi.org/10.1097/ MAO.0000000000001103. 84. Creighton F Jr, Barber SR, Ward BK, Sharon JD, Carey JP. Underwater endoscopic repair of superior canal dehiscence. Otol Neurotol. 2020;41(4):560. https://doi.org/10.1097/ MAO.0000000000002277. 85. Zhang L, Creighton FX Jr, Ward BK, Bowditch S, Carey JP. A cohort study of hearing outcomes between middle fossa craniotomy and transmastoid approach for surgical repair of superior semicircular canal dehiscence syndrome. Otol Neurotol. 2018;39(10):e1160–e7. https://doi.org/10.1097/MAO.0000000000002040. 86. Allsopp T, Kim AH, Robbins AM, Page JC, Dornhoffer JL.  Quality of life outcomes after transmastoid plugging of superior semicircular canal dehiscence. Am J Otolaryngol. 2020;41(2):102287. https://doi.org/10.1016/j.amjoto.2019.102287. 87. Silverstein H, Kartush JM, Parnes LS, Poe DS, Babu SC, Levenson MJ, et al. Round window reinforcement for superior semicircular canal dehiscence: a retrospective multi-center case series. Am J Otolaryngol. 2014;35(3):286–93. https://doi.org/10.1016/j.amjoto.2014.02.016.

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88. Nikkar-Esfahani A, Whelan D, Banerjee A. Occlusion of the round window: a novel way to treat hyperacusis symptoms in superior semicircular canal dehiscence syndrome. J Laryngol Otol. 2013;127(7):705–7. https://doi.org/10.1017/S0022215113001096. 89. Succar EF, Manickam PV, Wing S, Walter J, Greene JS, Azeredo WJ. Round window plugging in the treatment of superior semicircular canal dehiscence. Laryngoscope. 2017;128:1445. https://doi.org/10.1002/lary.26899. 90. Chemtob RA, Noij KS, Qureshi AA, Klokker M, Nakajima HH, Lee DJ.  Superior canal dehiscence surgery outcomes following failed round window surgery. Otol Neurotol. 2019;40(4):535–42. https://doi.org/10.1097/MAO.0000000000002185. 91. Ahmed W, Rajagopal R, Lloyd G.  Systematic review of round window operations for the treatment of superior semicircular canal dehiscence. J Int Adv Otol. 2019;15(2):209–14. https://doi.org/10.5152/iao.2019.6550. 92. Schneiders SMD, Rainsbury JW, Hensen EF, Irving RM.  Superior petrosal sinus causing superior canal dehiscence syndrome. J Laryngol Otol. 2017;131(7):593–7. https://doi. org/10.1017/S0022215117001013. 93. McCall AA, McKenna MJ, Merchant SN, Curtin HD, Lee DJ.  Superior canal dehiscence syndrome associated with the superior petrosal sinus in pediatric and adult patients. Otol Neurotol. 2011;32(8):1312–9. https://doi.org/10.1097/MAO.0b013e31822e5b0a. 94. Cheng YS, Kozin ED, Remenschneider AK, Nakajima HH, Lee DJ. Characteristics of wax occlusion in the surgical repair of superior canal dehiscence in human temporal bone specimens. Otol Neurotol. 2016;37(1):83–8. https://doi.org/10.1097/MAO.0000000000000916. 95. Remenschneider AK, Owoc M, Kozin ED, McKenna MJ, Lee DJ, Jung DH.  Health utility improves after surgery for superior canal dehiscence syndrome. Otol Neurotol. 2015;36(10):1695–701. https://doi.org/10.1097/MAO.0000000000000886. 96. Crane BT, Minor LB, Carey JP. Superior canal dehiscence plugging reduces dizziness handicap. Laryngoscope. 2008;118(10):1809–13. 97. Jacobson GP, Newman CW.  The development of the dizziness handicap inventory. Arch Otolaryngol Head Neck Surg. 1990;116(4):424–7. 98. Wilkinson EP, Liu GC, Friedman RA.  Correction of progressive hearing loss in superior canal dehiscence syndrome. Laryngoscope. 2008;118(1):10–3. 99. Niesten ME, McKenna MJ, Herrmann BS, Grolman W, Lee DJ. Utility of cVEMPs in bilateral superior canal dehiscence syndrome. Laryngoscope. 2013;123(1):226–32. https://doi. org/10.1002/lary.23550. 100. Xie Y, Sharon JD, Pross SE, Abt NB, Varma S, Della Santina CC, et al. Surgical complications from superior canal dehiscence syndrome repair: two decades of experience. Otolaryngol Head Neck Surg. 2017;157(2):273–80. https://doi.org/10.1177/0194599817706491. 101. Ossen ME, Stokroos R, Kingma H, van Tongeren J, Van Rompaey V, Temel Y, et  al. Heterogeneity in reported outcome measures after surgery in superior canal dehiscence syndrome-a systematic literature review. Front Neurol. 2017;8:347. https://doi.org/10.3389/ fneur.2017.00347.

Further Reading Crane BT, Minor LB, Carey JP. Superior canal dehiscence plugging reduces dizziness handicap. Laryngoscope. 2008;118(10):1809–13. Mikulec AA, McKenna MJ, Ramsey MJ, Rosowski JJ, Herrmann BS, Rauch SD, et al. Superior semicircular canal dehiscence presenting as conductive hearing loss without vertigo. Otol Neurotol. 2004;25(2):121–9. Minor LB.  Clinical manifestations of superior semicircular canal dehiscence. Laryngoscope. 2005;115(10):1717–27.

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Minor LB, Solomon D, Zinreich JS, Zee DS.  Sound- and/or pressure-induced vertigo due to bone dehiscence of the superior semicircular canal. Arch Otolaryngol Head Neck Surg. 1998;124(3):249–58. Succar EF, Manickam PV, Wing S, Walter J, Greene JS, Azeredo WJ. Round window plugging in the treatment of superior semicircular canal dehiscence. Laryngoscope. 2017;128:1445. https:// doi.org/10.1002/lary.26899. Williamson RA, Vrabec JT, Coker NJ, Sandlin M. Coronal computed tomography prevalence of superior semicircular canal dehiscence. Otolaryngol Head Neck Surg. 2003;129(5):481–9.

Chapter 7

Benign Paroxysmal Positional Vertigo Carol A. Foster

Benign paroxysmal positional vertigo (BPPV) causes the illusion that the environment spins briefly but violently when making certain head movements. It is the most common cause of room-spinning vertigo. The disorder has a significant lifetime prevalence of 2.9%, so over 200 million people worldwide will experience this disorder. It is more prevalent in women and with age, affecting up to 10% of elderly people [1]. Fortunately, it is one of the best-understood peripheral vestibular disorders and is treatable with simple and highly efficacious maneuvers.

History Although BPPV must have occurred throughout human history, its clinical description awaited the detailed observations of the 1914 Nobel Prize winner and vestibular expert Dr. Robert Barany. His assistant, Dr. John Karlefors, brought him a female patient with positional vertigo, and in 1921, Barany published a paper describing her brief, mixed torsional and vertical nystagmus that varied with eye position and that was triggered by lying down with the head turned [2]. He also described a fatigue in the response, with a decline in the nystagmus when the positioning was repeated. He surmised incorrectly that the spells emanated from the otolith organs, and this continued to be accepted as the cause for decades. The correct mechanism for the nystagmus was not to be understood for nearly 60 years. Dr. Margaret Dix and her mentor, Dr. Charles S. Hallpike, published a method to elicit the nystagmus of BPPV and named the disorder “positional vertigo of the C. A. Foster (*) Department of Otolaryngology-Head and Neck Surgery, University of Colorado School of Medicine, Aurora, CO, USA e-mail: [email protected] © The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 B. T. Crane et al. (eds.), Disorders of the Vestibular System, https://doi.org/10.1007/978-3-031-40524-2_7

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benign paroxysmal type” in their 1952 paper [3]. Their method, now called the Dix–Hallpike maneuver, built on Barany’s description and head hanging maneuvers used by his Swedish protégé, Dr. Carl Nylen. Dix and Hallpike were the first to note a latency of several seconds between the positioning of the head and the onset of the nystagmus. A few years later in 1956, Drs. John Lindsay and Garth Hemenway at the University of Chicago studied patients with acute unilateral vestibular losses followed by positional vertigo, and noted that the utricle was not the source of positional vertigo spells following those losses, because their cases had a total loss of utricular function. They correctly surmised that the problem lay in the posterior semicircular canal or saccule, since these were the only structures undamaged in the ears they studied [4]. Dr. Harold Schuknecht, Chief of Otolaryngology at the Massachusetts Eye and Ear Infirmary, published a 1962 paper that identified the posterior semicircular canal as the site of the problem and provided a mechanism for the disorder [5]. He posited correctly that particles within the inner ear, probably otoconia, moved into the canal and affected the cupula. He proposed that cupulolithiasis, particles adherent to the cupula in the affected canal, cause the attacks. This is may be true for a small subset of patients with BPPV but did not explain the more typical attacks. In 1979, Drs. Stephen Hall, Ralph Ruby and Joseph McClure at Queens University and the University of Western Ontario provided the critical mechanistic breakthrough by reasoning that it was free-floating dense particles in the posterior semicircular canal, called canalithiasis, that stimulated cupular motion and set off spells (Fig.  7.1). They correctly agreed with Schuknecht that the particles were likely to be otoconia [6]. The fact that particles could be moved by gravity and were in an open-ended canal suggested the possibility that they could be removed without surgery. A year later, Dr. John Epley devised a clever maneuver to remove these particles from the posterior canal, and over time demonstrated its efficacy [7]. A series of other maneuvers have since been devised.

Fig. 7.1  Left labyrinth viewed from the medial side in the upright head position. Otoconia accumulate in the most dependent part of the ear, adjacent to the posterior canal ampulla. (With permission from Foster CA. Overcoming Positional Vertigo. Boulder, CO: Bull Publishing; 2019)

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Within a few years, Dr. Joseph McClure identified that canalithiasis could also cause symptoms when particles were in the horizontal semicircular canal [8] and it became clear that all three canals were vulnerable to the disorder, with BPPV of the posterior canal being the most common.

Relevant Anatomy BPPV results from an interaction of the semicircular canals with the adjoining utricle. The semicircular canals are narrow membranous rings encompassing about two thirds of a circle that originate from the sac containing the utricle and terminate at an ampullated end containing the crista and cupula. They are set roughly orthogonally, with the horizontal (lateral) canals and labyrinth tilted upward at about 30° from the horizontal plane. The anterior (superior) canal is thus set superiorly with respect to the horizontal canal, and the posterior (inferior) canal is set inferiorly. The nonampullated end of the two vertical canals are fused into a common crus that opens into the roof of the utricular sac, while the horizontal canal has an adjacent but separate entrance into the sac. Each ampulla contains a motion sensor and is a rounded, dilated extension of the canal attaching it to the utricular sac. The ampullae are open to the utricular sac on one side, and open to the canal on the other, but are divided in half by the crista/ cupular complex that prevents fluid or particle movement from the utricle across the ampulla into the canal (Fig. 7.2). However, endolymph can freely enter or exit the canal at the nonampullated end. The crista is set within the ampulla perpendicular to the canal. It is a saddle-­ shaped ridge nearly dividing the ampulla in half. The unattached edge of this ridge projects toward the center point of the circular plane of each canal. Hair cells located in the crista have long kinocilia that extend into the ampulla. They are contained in a transparent mass, the cupula, that stretches from the crista across the ampulla and is attached to the opposite wall [9]. This creates a fan-shaped structure that partitions the ampulla in half. The cupula consists of protein fibrils and glycosaminoglycans. These mucopolysaccharides are highly hydrophilic and distensible. The utricle can sense gravity and other forms of linear acceleration because it is topped by a membrane embedding relatively dense particles of calcium carbonate, the otoconia, that exert a downward force on the sensor. It is the movement of this mass of particles that bends the hair cell projections that extend into the membrane and allows the detection of linear acceleration. The particles are adherent to the membrane and are coated with a sticky proteinaceous substance that helps them adhere to each other. However, with aging, pieces of otolithic membrane and particle masses can detach from the utricle and move throughout the endolymph. Because they are denser than endolymph, gravity can move these relatively heavy particles into dependent parts of the inner ear.

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Fig. 7.2  Cross-section of the ampulla perpendicular to the crista and cupula, in the plane of the canal. The cilia from the hair cells extend into the cupula, which divides the canal side of the ampulla from the utricular side. Although flame-shaped in cross-section, if seen from the side, the cupula is a half-circular fan shape. (With permission from Foster CA.  Overcoming Positional Vertigo. Boulder, CO: Bull Publishing; 2019)

Physiology of BPPV During head rotation and acceleration in the plane of each canal, the relative inertia of endolymph causes it to move freely with respect to the skull in a complete circle through the canal and utricle and by this movement bows the cupula within the ampulla [9]. This moves the kinocilia and their linked stereocilia, resulting in hair cell depolarization. This in turns results in a nystagmus that is unique to that canal. Each semicircular canal responds to only two directions of fluid movement: toward or away from the cupula. The responses are asymmetric, reflecting asymmetries in hair cell responses. Ewald’s laws specify that fluid movement toward the ampulla and cupula (ampullopetal) is stimulatory for the horizontal canal, while movement away from the ampulla (ampullofugal) is inhibitory. The opposite is true for the vertical canals [10]. Each canal responds best to movements in the plane of the canal, and not at all to responses at 90° to the canal, with graded responses in between. Most natural head rotations thus stimulate more than one canal [11].

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BPPV results when otoconia that may contain portions of the gelatinous membrane [12] become detached from the utricle and enter a semicircular canal. The nonampullated ends of the semicircular canals open into the vestibule above the utricle, so particles are most easily displaced into the canal when the head is dependent. The otoconia can be easily moved by gravity. If only a few particles are dispersed in the canal, no detectable effect may be noticed. However, if a large clump of particles forms that can move as a piston in the canal, symptoms of dizziness arise (Fig. 7.3). The movement of the clump under the influence of gravity, even when there is no head rotation, can cause movement of the fluid in the canal, stimulating the hair cells via cupular movement. Unlike natural head movements, this can stimulate a single semicircular canal, giving rise to a unique set of findings for each canal. The direction of movement of the particles (ampullopetal vs. ampullofugal) influences the severity of nystagmus. For example, because ampullopetal movement in the horizontal canal is stimulatory, it causes a more intense vertigo than the same direction of fluid movement in a vertical canal. Because particles can potentially move in two directions in each canal (toward the ampulla or toward the utricle), most BPPV cases have a direction changing positional nystagmus when the head is rotated 180° in the plane of the affected canal. The posterior canal is most often affected by BPPV, comprising about 86% of all BPPV cases [13]. When a person lies supine with the head turned to one side, the posterior canal opening and the entire canal on that side lies below the utricle, Fig. 7.3  Just as a syringe moves fluid with the action of a piston, free-floating particles in the narrow semicircular canal move the cupula as they are displaced by gravity. (With permission from Foster CA. Overcoming Positional Vertigo. Boulder, CO: Bull Publishing; 2019)

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allowing reflux of particles under the influence of gravity. This canal is the most dependent part of the labyrinth in the upright head, so particles can easily accumulate in it. The horizontal canal is affected in about 11% of cases [13]. The position most likely to cause reflux into this canal is lying supine with the head turned to the side and dependent, such as during the Dix–Hallpike maneuver. Although infrequent, the vertigo with horizontal canal involvement tends to be the most severe and is more likely to be accompanied by vomiting. The anterior canal is the least affected canal, about 1% of cases. This canal is entirely above the utricle, allowing the half of the canal proximal to the utricular opening to drain when the head is upright and reducing the risk of particle accumulation. Velocity storage affects the responses to BPPV. Natural horizontal head rotations are larger and more prolonged than vertical head rotations and velocity storage is thus greatly enhanced for the horizontal canals compared to the vertical canals [14]. These differences tend to enhance the vertigo and nystagmus of H-BPPV compared to the anterior and posterior canal forms.

Clinical Presentation Because the posterior canal is the most frequently affected canal, all the classic BPPV descriptions are of this canal. Over the past few decades, a greater appreciation of the involvement of the anterior and horizontal canals has altered the understanding of presenting symptoms. The main mass of otoconia can either be located deep in the canal in or near the ampulla (ampullary arm), or near the canal exit (utricular arm of the horizontal canal, common crus of the fused vertical canals), resulting in two opposite directions of direction-changing positional nystagmus for each canal. Particles can be either free-floating or entrapped and this also alters the clinical syndrome. As noted, most BPPV patients have free-floating particles in the posterior semicircular canal (P-BPPV). The particles accumulate in the ampullary arm adjacent to the ampulla and crista, so reclining will cause the particles to fall away from the vertically oriented ampulla in this position. This ampullofugal motion is stimulatory to the posterior canal and the vertigo is intense. The onset of this type of BPPV is typically in bed, while lying down quickly or rolling over. After a brief lag, the patient will awaken seeing the room spin torsionally and violently. The spell lasts from a few seconds up to a minute in a crescendo–decrescendo fashion. After the vertigo subsides, if no further head movements are made, the vertigo abates. However, any vertical or rolling head movement while reclining will set off another nearly identical attack, although the length and violence of the spinning declines (fatigues) if spells are set off repeatedly over a few minutes. Sitting up immediately after an attack will reverse the nystagmus to a transient downbeating nystagmus. Additional common triggers include arising from bed, lying down abruptly, and

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tipping the head up or down. In the upright person most head rotations are horizontal, outside the plane of the affected posterior canal. This attenuates the vertigo, but there can be a low grade persistent disequilibrium throughout the day. Reaching up toward a high shelf, tipping the head up while washing hair in the shower, bending over toward the floor or other vertical head motions can set off brief spells of vertigo when upright. Nausea commonly accompanies the vertigo and vomiting sometimes occurs. Horizontal canal BPPV (H-BPPV) caused by free-floating particles is often more violent than the posterior canal variety and more likely to cause vomiting. Onset is usually while performing maneuvers for P-BPPV [15]. After a successful P-BPPV maneuver that has displaced particles back into the utricle, repeating the Dix– Hallpike maneuver places the horizontal canal immediately below the removed particles. They can then easily reflux into the utricular arm of the horizontal canal. Since this canal has its greatest response to ampullopetal fluid motion, reflux causes intense stimulation. The patient sees the room spin horizontally, exhibits considerable distress, and may vomit within as little as 30 s. Rotating the head while supine will set off additional spells with reversals in nystagmus direction. Nystagmus in H-BPPV is usually characterized as either geotropic (beating toward the floor), or apogeotropic (beating away from the floor/toward the ceiling). The nystagmus tends to last longer than P-BPPV, sometimes exceeding 1 min. The free-floating form of anterior canal BPPV (A-BPPV) is milder and much less common than the other two forms. Like the posterior canal, ampullofugal movements are stimulatory, but in the anterior canal, reflux causes ampullopetal movement of fluid and the vertigo is accordingly less severe. Like H-BPPV, it usually arises after treatment for P-BPPV. The anterior and posterior canals are fused at the common crus, so reflux into the crus must first occur followed by a horizontal head movement to allow particles to fall into the ampullary arm of the anterior canal. This can happen when assuming the face-down position, such as during the Semont maneuver. The superior orientation of the anterior canal in the head allows particles in or near the common crus to fall back out when the head is returned to upright, often ending the attack. All three canals can also show BPPV due to entrapped particles. This always affects the ampullary arm of the canal. Classically this has been ascribed to particles within the ampulla that adhere to the cupula (cupulolithiasis). Particles can be contained within the ampulla or may be blocked from free movement by an obstruction near the ampullary-canal junction, or possibly at an anatomic narrowing near the midpoint of the canal or at the common crus (canalith jam) [16–19]. Typically, this arises in patients undergoing maneuvers for pre-existing BPPV. It is heralded by a sudden very persistent vertigo that is milder in the vertical canal forms, and more violent for the horizontal canal form. This usually results in a very prolonged direction changing positional nystagmus when the head is rotated in the plane of the canal. Once it arises, maneuvers may seem to have no effect on the vertigo and the symptoms can last indefinitely in some. Cupulolithiasis—attachment of otoconia to the cupula—is believed to be the dominant cause of persistent direction-changing positional nystagmus. This belief

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is based on studies showing a basophilic deposit on the cupula, affecting up to 22% of cupulae in Moriarty’s postmortem anatomic studies [5, 20]. None of the patients in this series of 1031 temporal bones had BPPV symptoms, however. Otoconia were dissolved by the preparation method so were not proven to be the source of the deposits, and the frequency of deposits greatly exceeds the infrequent incidence of cupulolithiasis in the literature. If otoconia adhere to the cupula, one would expect more deposits to occur on the utricular side of the cupula (short arm cupulolithiasis), because the ampulla is widely open to the utricle and its otoconia on that side, but most reported cases appear to be consistent with lithiasis of the canal side of the cupula. Canalith jam can result in a prolonged blockage of the canal with a spontaneous nystagmus and canal paresis on caloric testing, or can be reversible [17, 19, 21]. It can result in an apogeotropic positional nystagmus, and thus can mimic cupulolithiasis [17]. Free-floating particles trapped in the ampullary arm by a narrowed area in the canal could alternately lodge in the narrowing to form a jam, then dislodge and move into the ampulla and directly impact the cupula. This type of reversible jamming results in an apogeotropic positional nystagmus and so may not be easily distinguished from cupulolithiasis.

Physical Examination The Dix–Hallpike maneuver has been successfully used for the detection of P-BPPV for many decades and is the standard of care. The head and body are rotated through nearly 180° at high acceleration in the plane of the posterior semicircular canal, causing any particles it contains to be dislodged. At the conclusion of this movement the head is hanging and turned to one side (Fig. 7.4). This allows any particles Fig. 7.4  The Dix–Hallpike maneuver, left ear. The head is rotated 45° to the left prior to reclining the patient to the head hanging position. (With permission from Foster CA. Overcoming Positional Vertigo. Boulder, CO: Bull Publishing; 2019)

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near the ampulla of the posterior canal to move ampullofugally (the stimulatory direction) by gravity, maximizing nystagmus. The head is also placed facing the examiner, so that any nystagmus that occurs can be easily seen. Some practitioners apply Fresnel lenses on the patient to reduce fixation and further enhance the nystagmus. Once placed in the head hanging position, there is a brief latency of a few to several seconds, followed by the onset of a torsional up beating nystagmus following a crescendo-decrescendo pattern that peaks and declines over 10–60 s [22]. The velocity of the nystagmus is very brisk. The upward most eye is easiest to view and is best used to analyze the nystagmus. The axis of rotation of this eye is located in the upper medial quadrant of the upward eye near the iris edge if the pupil is centered, resulting in a mixed torsional and upbeating nystagmus (Fig. 7.5(1)), but the position of the rotational axis in the upper quadrant of the globe does not change with pupil movement [23]. If the pupil of the upward eye is moved toward the rotational axis nearer the medial canthus, the nystagmus becomes more purely torsional, and as it is moved away from the rotational axis toward the lateral canthus, it transcribes a wider arc and thus the nystagmus becomes more vertical. During successful maneuvers, the torsional and upbeating nystagmus continues as particles are rotated ampullofugally and out of the canal. On repeated Dix–Hallpike, a torsional upbeating nystagmus will be seen if some particles remain in the canal. The appearance of a new, fine downbeating nystagmus on Dix–Hallpike after a successful maneuver indicates that removed particles are refluxing back into the posterior canal through the common crus. This can also occur if particles are not completely removed during a maneuver, allowing them to reflux back toward the ampulla when the patient sits up. Particles trapped within the ampulla will result in a persistent positional nystagmus that resembles classic torsional upbeating nystagmus when supine or in head hanging, but milder and prolonged greater than 1 min. When the patient is raised to the upright seated position and then bent forward with the face down, the nystagmus reverses to a fine downbeating nystagmus [24]. For H-BPPV, determining the affected ear is critical before a maneuver is applied. H-BPPV is often first noted while performing maneuvers for P-BPPV and is typically seen on Dix–Hallpike. The nystagmus is brisk, horizontal, and often frightening to the patient (Fig. 7.5(2)). During reflux, the beat direction will be toward the ground (geotropic) and toward the affected ear. The affected ear is the ear that has just undergone treatment for P-BPPV. If a patient arrives with a history suggesting pre-existing H-BPPV, it will be necessary to determine whether it is the geotropic or apogeotropic form, which will determine whether the particles are freely moving in the utricular arm (geotropic form) or are within the ampulla or moving in the ampullary arm of the canal where they are likely to become entrapped (apogeotropic form). H-BPPV nystagmus will reverse direction when the supine patient is rolled from one side to the other, and also if the upright head is centered and tipped downward and upward. Recording the direction of nystagmus in these positions can be used to determine which ear is involved (Table 7.1).

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Fig. 7.5  The nystagmus of BPPV. The axis of rotation for each semicircular canal is perpendicular to the plane of the canal. Projected forward onto the eye, this axis determines the nystagmus seen. The eye is in mid-position in this series. Dark lines indicate the movement of the pupil during fast phases. (1) The posterior canal axis is near the iris, allowing torsional upbeating movement to be seen. (2) The horizontal canal axis is near the bottom of the globe, so little torsion is seen. (3) The anterior canal axis is near the canthus and slightly tilted, so little torsion is seen, and the nystagmus is downbeating and oblique (With permission from Foster CA.  Overcoming Positional Vertigo. Boulder, CO: Bull Publishing; 2019)

Combining a half-Hallpike with Asprella’s single maneuver test technique [25] is usually sufficient to determine the side of involvement. The head of the table is raised to 30°, and the seated patient is rapidly reclined with the head centered. This movement places the horizontal canal in the vertical plane, maximizing particle

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Table 7.1  Determining the affected ear in H-BPPV A. Head roll

Geotropic

Apogeotropic

B. Supine head center (“Lean”)

Le beang

Right beang

Le beang

Right beang

C. “Bow”

Right beang

Le beang

Right beang

Le beang

D. Side with greatest nystagmus

Right

Le

Right

Le

E. Null point side

Right

Le

Le

Right

F. Canal Paresis side

Right

Le

Le

Right

Affected Ear

Right

Le

Le

Right

Gray shading = test method and affected ear. Circle the nystagmus direction or affected side for each test, and mark under the “Geotropic” column or “Apogeotropic” column based on results of the head roll test. The bottom box of the column with the most circled answers gives the affected ear (A) Head roll test: patient placed with right ear down, then left ear down (geotropic = nystagmus beats toward ground; apogeotropic  =  nystagmus beats toward ceiling). (B) Supine head center (Asprella method, Lean test): patient faces ceiling, note nystagmus direction. (C) Bow test: Patient bends forward facing floor, note nystagmus direction. (D) Side with greatest nystagmus: nystagmus velocity or intensity is increased with one ear down compared to the other ear down. (E) Null point side: Measure nystagmus while slowly rotating the head from right to left or vice versa. The null point is the point at which no nystagmus is seen or abruptly switches direction on VNG, usually about 20° to one side only. (F) Canal paresis side: side with a 25% or greater canal paresis. If there are no localizing findings on tests (D–F), the results of tests (A–C) are sufficient to determine the affected side

displacement. A horizontal nystagmus will be seen, and the direction should be noted. The head is then turned 90° to one side and any nystagmus direction and intensity noted, then turned to the opposite shoulder while noting nystagmus direction and intensity. It is important to note whether the nystagmus intensity is greater when one ear is down. A geotropic nystagmus beats toward the floor, while an apogeotropic nystagmus beats toward the ceiling. Similarly, patients can also be tested from the seated position using the bow-and-lean test by tipping the head to face the ceiling (“lean”), noting nystagmus direction, and then moving the head to face the floor (“bow”) and again noting the direction of the resulting nystagmus. A roll test

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must then be done from the supine position to determine whether it is apogeotropic or geotropic [26]. There are a few simple ways to determine the affected side once this information is obtained. The simplest and fastest localizing clue is nystagmus intensity, which is often more severe on one side. The nystagmus on the most intense side usually beats toward the affected ear. In a geotropic nystagmus with the greatest response with the right ear down, the nystagmus will beat toward the dependent right ear, which is the affected ear. If the nystagmus is greatest with the right ear down but is apogeotropic, it will beat upward toward the left ear, and the left ear is the affected ear. Unfortunately, the intensity of the nystagmus is not always clearly different between sides and additional localizing methods must then be used. The result of the initial head centered Asprella test can determine the side once the nystagmus has been characterized as geo- or apogeotropic. For geotropic BPPV, the nystagmus will beat away from the affected ear with the head centered. In the apogeotropic form, it will beat toward the affected ear. The direction of the nystagmus in the “lean” (face-up) portion of the bow-and-lean test gives the same outcome. If VNG monitoring is being used, a third method can determine the side of involvement. There will be a null point (cessation of the nystagmus) as the head is slowly rotated from right to left or vice versa [27]. The null point is usually found at about 20° toward the affected side in both geotropic and apogeotropic forms [28]. A null point that is centered or symmetric suggests that the problem maybe not be due to BPPV. If particles obstruct the canal or ampullary neck forming a canalith jam, a canal paresis on the affected side may be seen on caloric testing [29] and this provides additional localizing information. Rarely, a transient direction fixed nystagmus can be seen during maneuvers for apogeotropic H-BPPV. This unusual situation has been attributed to separate clumps of otoconia in both the ampullary and utricular limbs of the canal moving in opposite directions during head positioning [30, 31]. Unusual mixed forms of paroxysmal nystagmus (horizontal transitioning to vertical, for example) can indicate BPPV affecting more than one canal. Determining the affected ear and canal is less difficult with the vertical canals. When reflux into the common crus occurs during maneuvers, particles usually pass into the posterior canal, and the affected ear is the downward ear on Dix–Hallpike to the symptomatic side. Entrapment is indicated when the nystagmus is unusually persistent (greater than 1 min) and many repeated maneuvers over several sessions fail to result in improvement or resolution. The anterior canal is oriented superiorly, so it requires rotation to a face-down placement to cause reflux, and in this position, it is difficult for the operator to detect unless recording goggles are in use. Because free-floating particles in the utricular arm of the canal in A-BPPV can exit when the head is returned to the upright position, patients presenting with A-BPPV typically have the type caused by ampullary arm or trapped particles. Otoconia that pass more than halfway around the semicircular canal will fall toward the cupula instead of exiting when the patient returns to the upright position. This allows particles to directly impact the cupula, resulting in a continuous low-grade dizziness. The Deep Dix–Hallpike allows detection of this

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type [32]. The seated patient is placed in head hanging with the head centered. Any particles in or near the ampulla will be displaced in this position, resulting in a fine downbeating oblique nystagmus. The axis of ocular rotation will be in the lower quadrant of the eye very close to one canthus, so very little torsion will be seen with the pupil in mid-position (Fig. 7.5(3)). Particles in the right anterior canal will cause a nystagmus that beats obliquely downward and slightly toward the patient’s left, while the left anterior canal causes a nystagmus that beats obliquely downward and slightly toward the patient’s right [15].

Diagnostic Dilemmas Direction changing positional nystagmus occurs in a number of central and peripheral vestibular disorders other than BPPV. Disorders that alter the specific gravity of the endolymph or the cupula mimic cupulolithiasis but do not respond to maneuvers. The most common form is positional alcohol-induced nystagmus (PAN), which causes a geotropic nystagmus in its acute phase reflecting alcohol uptake into the cupula, resulting in a “light cupula.” This causes the cupulae in all six ampullae to float upward [33]. The reversal phase to an apogeotropic nystagmus indicates an elevation in alcohol levels in the endolymph with respect to the cupula. This results in a “heavy cupula” relative to endolymph that reverses the nystagmus direction as the cupulae sink downward in the direction of gravity. PAN is easily differentiated from BPPV by the acute history of alcohol intoxication and its disappearance over the course of several hours. Acute vestibulopathies can also result in light cupula [34]. A brisk spontaneous nystagmus beating away from the affected ear is often found in these cases. The positional and spontaneous nystagmus resolves over the course of several days, in contrast to cupulolithiasis which can persist for months. As in PAN, light cupula can result either from any process that lowers specific gravity in the cupula or that raises the specific gravity in endolymph [35]. Heavy cupula is at present thought to be primarily due to cupulolithiasis but can also occur if endolymph specific gravity is lowered or in canalith jam near the ampulla. Cupulolithiasis usually involves only one semicircular canal, so the presence of both horizontal and vertical direction changing positional nystagmus indicates a more widespread aural or central problem.

Management BPPV can be quickly relieved by removing the particles from the semicircular canals. Many maneuver variations have been devised to achieve this goal. It may require repeated maneuvers in a single session to completely clear all particles from

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the affected canal. All maneuvers rotate the head in the plane of the treated canal, but it is also necessary to rotate the entire body in order to achieve this. Most patients do not require medication to suppress the vertigo during maneuvers. For patients with intractable vomiting during maneuvers, meclizine, benzodiazepines, and antiemetics can make the patient more comfortable. These can also be given for motion-sensitive patients who wish to do maneuvers at home.

Maneuvers for the Posterior Canal For classic P-BPPV, the Epley maneuver is the most efficacious for clinic use with a success rate after repeated maneuvers exceeding 90% [21]. Most patients are cleared after 1–3 maneuvers. The diagnostic test, the Dix–Hallpike maneuver, is the first step in the maneuver and moves particles about halfway toward the exit. The patient is then rolled to the opposite shoulder. After pausing to allow further gravity-­ mediated movement of particles, the patient is moved to the sitting position during which the particles exit the canal (Fig. 7.6). The Epley maneuver has several advantages over other maneuvers for clinic use. First, by incorporating the diagnostic test as the first movement, the clinician can see the nystagmus and confirm the location of particles, while simultaneously and efficiently moving them toward the exit. Second, it is designed to move the particles continuously toward the canal exit using both gravity and fluid motion, while other maneuvers may slosh particles back and forth. Disadvantages are that after a successful maneuver, repeating the Dix–Hallpike can cause reflux of newly removed particles into the common crus or horizontal canal [15]. This can be mitigated by waiting 15 min between maneuvers. It also causes substantial vertigo and nausea because the particles are moving swiftly in the most stimulatory direction. This means that an assistant is usually required to help restrain the patient on the table and move them as needed. The Semont maneuver is also effective for P-BPPV, although there is less evidence supporting it than for the Epley maneuver [36]. The patient is seated on the exam table facing the examiner. A variation of the Dix–Hallpike is performed, with the patient moved onto one side instead of supine, ending with the head in typical Dix–Hallpike position, face up, chin elevated and rotated 45° toward the shoulder on the unaffected side. This allows identification of P-BPPV and begins movement of the particles toward the exit. The patient is then raised to the upright position maintaining the 45° rotation of the head toward the shoulder. Without pause, movement continues until the opposite shoulder is down on the table (Fig. 7.7). The head will then be turned facing the floor at a 45° angle. The patient is then raised to the upright seated position. The advantages of the Semont maneuver are that the sideways Dix–Hallpike variation is as effective as the supine maneuver incorporated into the Epley maneuver for diagnosis and initial movement of particles. It can also be done without an assistant because the patient remains facing the examiner on one side of the table,

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Fig. 7.6  Epley maneuver, right ear. The Dix–Hallpike is performed, followed by rotation of the head through 180°. The patient is then moved upright. (With permission from Foster CA. Overcoming Positional Vertigo. Boulder, CO: Bull Publishing; 2019)

while the Epley requires rotating the patient lengthwise to face the opposite side of the table. However, there are disadvantages. After the diagnostic Dix–Hallpike, the next steps of the Semont maneuver raise the head of the patient, which allows some particles to slosh back toward the ampulla rather than continuing toward the utricle as in the Epley maneuver. Having the head then placed face down increases the risk of reflux into the anterior canal. Like the Epley maneuver, it also carries a similar risk of reflux into the posterior or horizontal canals because it incorporates a form of the Dix–Hallpike maneuver. These and other maneuvers have been advocated for home use but carry a risk of canal conversion to H-BPPV because of the included Dix–Hallpike maneuver. The Dix–Hallpike maneuver is designed to maximize nystagmus so it is easily visible to

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Fig. 7.7  Semont maneuver, right ear. The seated patient is reclined with the head turned to the left at 45°, away from the tested right ear. After reclining with the right shoulder down (left side of figure) the head is in typical Dix–Hallpike position. Keeping the head turned 45° to the left, the patient is then raised back to the seated position and reclined on the left shoulder, head now facing downward at 45° to the floor (right side of figure). (With permission from Foster CA. Overcoming Positional Vertigo. Boulder, CO: Bull Publishing; 2019)

Fig. 7.8  Half somersault maneuver, left ear. Positions are held for 30 s or until the sensation of vertigo ceases. (1) The kneeling patient rocks the head and body back until facing the ceiling. (2) The head is placed upside down on the floor. (3) The head is rotated 45° to face the left elbow. (4) The head is quickly raised to back/shoulder level. The patient should view the left elbow to keep the head at 45° from the midline. (5) The head is kept turned left and is raised fully upright as the patient returns to the kneeling position. If the right ear is being treated, the head is turned toward the right elbow in steps (3)–(5). (With permission from Foster CA. Overcoming Positional Vertigo. Boulder, CO: Bull Publishing; 2019)

the clinical examiner, but at home an examiner is not present and maximizing nystagmus also maximizes the experience of vertigo and so is counterproductive. The half somersault maneuver was devised as a home exercise to reduce the risk of H-BPPV while still clearing particles [37] (Fig. 7.8). It does not include the Dix– Hallpike, reducing overall vertigo and the risk of canal conversion. In addition, an assistant is not required. The patient tips the head upward to move particles away from the ampulla, and then places the head upside down on the floor. Particles are drawn through the canal by gravity alone. The head is then rotated 45° to place the posterior canal in the sagittal plane. The head is then rotated upward in two stages until the head is upright. This rotates the particles out using fluid motion and gravity.

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While it avoids canal conversion and reduces vertigo, it may require more repetitions than the Epley maneuver (four on average) to completely clear the canal. If particles become entrapped in the posterior canal ampulla, a very persistent torsional, upbeating nystagmus is seen when supine or on Dix–Hallpike that reverses to a fine downbeating nystagmus when seated with the head facing down and to the affected side [24]. This may require many maneuvers to dislodge. Placing the patient in the Dix–Hallpike head position and vibrating the head can sometimes dislodge the particles, resulting in a burst of typical P-BPPV. An Epley maneuver can then be used to remove the particles from the canal.

Maneuvers for the Horizontal Canal When H-BPPV occurs during treatment of the posterior canal, the onset of horizontal nystagmus on Dix–Hallpike indicates that particles are refluxing by gravity into the horizontal canal. Returning the patient to upright as soon as horizontal nystagmus is identified stops further reflux. Any particles remaining in the horizontal canal can then be removed in a few simple steps. In the Gufoni maneuver, the supine patient is raised upright to face the examiner, then reclined on the opposite side with the shoulder down, head rotated slightly upward [38] (Fig. 7.9). The head is then rotated smoothly to face the table. Since this maneuver incorporates raising the patient to upright, it is the best maneuver to stop and correct reflux. Usually only one maneuver is required. It can be performed without an assistant. Patients with pre-existing, free-floating H-BPPV will usually present with geotropic H-BPPV.  Identifying the side of involvement is important as noted in the prior section. The Gufoni maneuver is highly effective for pre-existing H-BPPV. The log roll maneuver has been used for many years for H-BPPV [39]. The supine patient is rolled away from the affected ear, moving the particles with both gravity and fluid motion toward the vestibule. It is necessary to perform a 360°

Fig. 7.9  Gufoni maneuver, right ear. The patient is seated facing the operator. Positions are held for 30 s. (1) While upright, the head is turned 45° to the right. (2) Move the patient onto their left side. (3) Rotate the head left toward the table. (4) Return the patient to the upright position, keeping the head turned toward the left. (With permission from Foster CA. Overcoming Positional Vertigo. Boulder, CO: Bull Publishing; 2019)

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rotation of the body to complete the maneuver. This type of rotation is somewhat difficult to perform on a narrow exam table and requires an assistant. An exercise mat on the floor can be used for log roll treatment and a mat is also useful during any maneuver for morbidly obese patients who cannot be treated safely on an exam table. The Vannucchi–Asprella maneuver is a simple alternative to the log roll that reduces the need to rotate the entire body [40]. The patient is placed supine, and the head is next turned 90° away from the affected ear. The patient is then raised to the seated position. This is usually sufficient to remove particles from the horizontal canal. A disadvantage of maneuvers for free-floating particles in the horizontal canal is that performing maneuvers for the incorrect ear can lead to conversion to the much more serious ampullary arm or entrapped forms including cupulolithiasis and canalith jam. All maneuvers are designed to rotate the head away from the affected ear, moving the particles toward the utricle. If a patient is accidentally rotated toward the affected ear, particles are moved deeper toward the ampulla where they can lodge. Determining the affected ear can be confusing and lead to this mistake. Fortunately, most cases of H-BPPV occur during maneuvers, and the affected ear is always the ear with P-BPPV that is undergoing treatment. The Gufoni maneuver immediately stops reflux by raising the patient upright and the design of the maneuver ensures that the correct ear is being treated. The apogeotropic form of H-BPPV indicates that particles are in or very near the ampulla, where they can be entrapped (lodging within the ampulla or attached to the cupula, as in cupulolithiasis). Maneuvers have a lower success rate for this form of H-BPPV. Due to the enhanced sensitivity of the horizontal canal, nystagmus can be extremely severe, and vomiting may limit maneuvers. The affected side should first be determined. Horizontal head shaking on the upright patient can help dislodge particles from the ampulla, followed by the maneuvers above [41]. As in the posterior canal form, vibration can be used to move particles from the ampulla. The patient is placed supine with the head elevated 30° and turned 20–45° toward the affected ear. Vibration is then applied to the mastoid. Repeated quick horizontal head rotations while supine can also be used to dislodge particles. If the particles are recalcitrant to office maneuvers, patients can do these exercises at home. Once converted to the geotropic forms, indicating that the particles have move to the utricular arm, the maneuvers above resolve the problem.

Maneuvers for the Anterior Canal Because common crus reflux brought on by Dix–Hallpike reverses when the patient’s head is returned to upright, only the cases with entrapped particles in or near the ampulla are usually seen by a physician. An oblique and downbeating nystagmus on Dix–Hallpike indicates that particles are in the ampulla of the anterior canal. Because anterior canal particles are often entrapped, maneuvers are less effective than for the free-floating forms seen in the other canals. The Deep

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Dix–Hallpike is the simplest maneuver [32] (Fig. 7.10). The patient is placed supine with the neck hyperextended off the table so that the top of the head points toward the floor. If particles can exit the ampulla, they will move about halfway toward the canal exit in this position. The patient’s head is then raised in two steps, first to a semireclined position and then to a face-forward and down position, allowing particles to exit. In the Yacovino and Hain version, the head is centered so both anterior canals are treated simultaneously, although neither canal will be exactly in the plane of head rotation. In another version using head dependency, the head is turned away from the affected ear to place it in the plane of head rotation, and the patient is moved to a supine position and then the body is raised upright with the head and chin tipped downward [42]. Performing an Epley maneuver from the opposite (unaffected) side has also been used. Unfortunately, the success rate in resolving A-BPPV is lower than for other forms. This is likely to be due to entrapment of particles in the ampulla or at the common crus. Placing the patient in the deep Dix– Hallpike position and then applying vibration for several minutes can result in an abrupt release of particles from their entrapment, after which completing the maneuver resolves the BPPV. Patients can also do the deep Dix–Hallpike repeatedly as a home exercise.

Prognosis While most patients achieve a complete resolution of dizziness with maneuvers, the condition is recurrent. Home exercises should be taught to reduce the need for ongoing clinical care. People who are too frail to perform home exercises may require repeated clinic visits and should be taught how to avoid reflux. Lying flat on the back or inverting the head increases the risk of recurrence, and avoidance of these positions may allow these patients to reduce the frequency of spells [43].

Fig. 7.10  Deep Dix–Hallpike maneuver for both anterior canals. Each position should be held for 30–60 s. (1) The patient is moved to the head-hanging position with the head centered. (2) The patient’s head and torso are elevated until facing forward and upward. (3) The patient is moved forward to face the knees. (With permission from Foster CA.  Overcoming Positional Vertigo. Boulder, CO: Bull Publishing; 2019)

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Surgery Surgery should be reserved for frequently recurrent or entrapped forms that cannot be resolved or controlled with maneuvers. Canal-plugging is highly effective [44]. It can be used for all three canal forms [45, 46]. Relief from vertigo is immediate, but the procedure disables the canal, so there can be some residual dizziness as compensation to the loss occurs. Rarely, ablative procedures can be used if multiple canals are involved in one ear and attacks are very frequent.

Controversies The original description of Epley’s maneuver included slow rotation of the head along with continuous mastoid vibration to move the particles while causing minimal nystagmus. This was felt to be more comfortable for patients, who experienced little vertigo during treatment [7]. Later practitioners found that rotating the head quickly without vibration was equally effective, although the vertigo is more intense. The use of vibration during maneuvers became unpopular after a study showed both forms of treatment had similar 1 week and long term outcomes after three maneuvers [32], and a Cochrane review recommended against its use [47]. Otoconial masses are sticky and can become lodged during maneuvers. This is likely to occur when particles are entrapped in or near the ampulla, such as during apogeotropic H-BPPV and with cupulolithiasis or canalith jam. Vibration is likely to be helpful when this occurs [48]. During the Dix–Hallpike maneuver, some patients show no nystagmus until vibration is applied, which allows adherent particles to mobilize. No studies comparing Dix–Hallpike with and without vibration have yet been performed. Requiring patients to maintain an elevated head position or wear a soft collar as a head elevation reminder for a few days after maneuvers was advocated by early practitioners of maneuvers. Keeping the head elevated prevents an immediate recurrence in the first days after treatment. Many subsequent studies showed that future long-term recurrences were not affected by short-term head position restrictions [47]. Since there is a risk of particle reflux every time the head is placed in a dependent position, head positioning restrictions would need to be used continuously to prevent future recurrence. This is not needed for most patients who will have only occasional recurrences.

References 1. von Brevern M, Radtke A, Lezius F, Feldmann M, Ziese T, Lempert T, et al. Epidemiology of benign paroxysmal positional vertigo: a population based study. J Neurol Neurosurg Psychiatry. 2007;78(7):710–5.

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2. Barany R. Diagnose von krankheitserch-eingungen im mereiche de otolithenapparates. Acta Otolaryngol. 1921;2:434–7. 3. Dix MR, Hallpike CS. The pathology symptomatology and diagnosis of certain common disorders of the vestibular system. Proc R Soc Med. 1952;45(6):341–54. 4. Hemenway WG, Lindsay JR. Postural vertigo due to unilateral sudden partial loss of vestibular function. Ann Otol Rhinol Laryngol. 1956;65(3):692–706. 5. Schuknecht HF. Cupulolithiasis. Arch Otolaryngol. 1969;90(6):765–78. 6. Hall SF, Ruby RR, McClure JA. The mechanics of benign paroxysmal vertigo. J Otolaryngol. 1979;8(2):151–8. 7. Epley JM.  The canalith repositioning procedure: for treatment of benign paroxysmal positional vertigo. Otolaryngology Head Neck Surg. 1992;107(3):399–404. 8. McClure JA. Horizontal canal BPV. J Otolaryngol. 1985;14(1):30–5. 9. Hillman DE, McLaren JW.  Displacement configuration of semicircular canal cupulae. Neuroscience. 1979;4(12):1989–2000. 10. Ewald EJR.  Physiologische Untersuchungen über das Endorgan des Nervus octavus. Wiesbaden Bergmann; 1892. 324 p. 11. Cremer PD, Halmagyi GM, Aw ST, Curthoys IS, McGarvie LA, Todd MJ, et al. Semicircular canal plane head impulses detect absent function of individual semicircular canals. Brain. 1998;121(Pt 4):699–716. 12. Kao WT, Parnes LS, Chole RA.  Otoconia and otolithic membrane fragments within the posterior semicircular canal in benign paroxysmal positional vertigo. Laryngoscope. 2017;127(3):709–14. 13. Cakir BO, Ercan I, Cakir ZA, Civelek S, Sayin I, Turgut S. What is the true incidence of horizontal semicircular canal benign paroxysmal positional vertigo? Otolaryngol Head Neck Surg. 2006;134(3):451–4. 14. Shaikh AG, Palla A, Marti S, Olasagasti I, Optican LM, Zee DS, et al. Role of cerebellum in motion perception and vestibulo-ocular reflex-similarities and disparities. Cerebellum. 2013;12(1):97–107. 15. Foster C, Zaccaro K, Strong D. Canal conversion and re-entry: a risk of Dix-Hallpike during canalith repositioning procedures. Otol Neurotol. 2012;33:199–203. 16. Riga M, Korres S, Korres G, Danielides V. Apogeotropic variant of lateral semicircular canal benign paroxysmal positional vertigo: is there a correlation between clinical findings, underlying pathophysiologic mechanisms and the effectiveness of repositioning maneuvers? Otol Neurotol. 2013;34(6):1155–64. 17. Comacchio F, Poletto E, Mion M. Spontaneous canalith jam and apogeotropic horizontal canal benign paroxysmal positional vertigo: considerations on a particular case mimicking an acute vestibular deficit. Otol Neurotol. 2018;39(9):e843–8. 18. Schubert MC, Helminski J, Zee DS, Cristiano E, Giannone A, Tortoriello G, et al. Horizontal semicircular canal jam: two new cases and possible mechanisms. Laryngosc Invest Otolaryngol. 2020;5(1):163–7. 19. Bronstein AM, Kaski D, Cutfield N, Buckwell D, Banga R, Ray J, et al. Head-jolting nystagmus: occlusion of the horizontal semicircular canal induced by vigorous head shaking. JAMA Otolaryngol Head Neck Surg. 2015;141(8):757–60. 20. Moriarty B, Rutka J, Hawke M. The incidence and distribution of cupular deposits in the labyrinth. Laryngoscope. 1992;102(1):56–9. 21. Epley JM.  Human experience with canalith repositioning maneuvers. Ann N Y Acad Sci. 2001;942:179–91. 22. Young AS, Lechner C, Bradshaw AP, MacDougall HG, Black DA, Halmagyi GM, et  al. Capturing acute vertigo: a vestibular event monitor. Neurology. 2019;92(24):e2743–53. 23. Della Santina CC, Potyagaylo V, Migliaccio AA, Minor LB, Carey JP. Orientation of human semicircular canals measured by three-dimensional multiplanar CT reconstruction. J Assoc Res Otolaryngol. 2005;6(3):191–206.

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46. Uetsuka S, Kitahara T, Horii A, Imai T, Uno A, Okazaki S, et al. Transient low-tone air-bone gaps during convalescence immediately after canal plugging surgery for BPPV. Auris Nasus Larynx. 2012;39(4):356–60. 47. Hunt WT, Zimmermann EF, Hilton MP.  Modifications of the Epley (canalith repositioning) manoeuvre for posterior canal benign paroxysmal positional vertigo (BPPV). Cochrane Database Syst Rev. 2012;2012(4):CD008675. 48. Faralli M, Longari F, Ricci G, Marinetti D, Frenguelli A. Mastoid oscillation in the treatment of the apogeotropic variant of benign paroxysmal positional vertigo of the lateral semicircular canal. Mediterr J Otol. 2008;4:152–6.

Chapter 8

Traumatic Causes of Vertigo Christopher de Souza, Rosemarie de Souza, Aishan Patil, Adip Shetty, Vimal Someshwar, and Manish Srivastav

Perilymph Fistulae Christopher de Souza, Rosemarie de Souza, Aishan Patil and Adip Shetty Perilymphatic fistula (PLF) can be defined as an abnormal communication between the inner ear (the cochlear and the vestibule) and the middle ear cavity, mastoid, or intracranial cavity. Tests to currently diagnose PLFs have a significant limitations, lacking the sensitivity and specificity that is needed to provide an accurate and consistent diagnosis. Major improvements in radiological imaging modalities and emerging technologies including the use of biomarkers have recently shown immense promise to help diagnose PLF. PLFs cause cochlear and vestibular symptoms which can cause significant disability. PLFs can be divided into two groups. Those patients in whom a cause or an antecedent event can be identified and those in whom a possible cause cannot be identified.

C. de Souza (*) Lilavati Hospital, Mumbai, India R. de Souza Department of Internal Medicine, BYL Nair Hospital, Mumbai, India A. Patil Vascular Surgery, Borders General Hospital, Melrose, Scotland, UK A. Shetty Rajawadi Hospital, Mumbai, India V. Someshwar · M. Srivastav KD Ambani Hospital, Mumbai, India © The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 B. T. Crane et al. (eds.), Disorders of the Vestibular System, https://doi.org/10.1007/978-3-031-40524-2_8

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Surgical techniques for stapes surgery, especially the need for a reliable seal over the neo fenestra, have evolved considerably through the years. PLFs present as a complication in approximately in 1% of stapedotomy procedures. The incidence of PLF increases significantly in those individuals requiring revision stapedectomies. It is found that one third of patients undergoing revision stapedectomy will likely develop PLF.

Perilymphatic Fistula Post Stapedectomy A perilymph fistula is one of the common causes of sensorineural hearing loss following stapedectomy. It is thought that perilymph fistulae occur because of inadequate closure of the fenestra at the footplate, too long of a prosthesis, or possible increased perilymph pressure. The diagnosis and treatment of this condition is vital, because it has the potential to cause irreversible profound sensorineural hearing loss, as well as puts the patient at risk of developing meningitis. Newlands [1] reported on a patient who developed acute otitis media, labyrinthitis, and meningitis 16 months following stapedectomy. Poststapedectomy PLF carries an increased risk of labyrinthitis and meningitis. Should labyrinthitis occur with or without meningitis, fistula repair must be undertaken as soon as the infection has been treated [2]. Perilymph fistulae have been observed with all types of stapes surgeries and with all techniques. Even as early as 1961, Lewis [3] described a perilymphatic fistula, observing that the polyethylene strut used was responsible for perilymph leakage.

Signs and Symptoms of Perilymphatic Fistula The most common symptoms are 1. Fluctuating sensorineural hearing loss 2. Roaring tinnitus 3. Vertigo 4. Fullness in the ear While these symptoms are also associated with endolymphatic hydrops, the key to making a diagnosis of perilymphatic fistula is the proximity to stapedectomy surgery. If it occurs immediately following surgery, the diagnosis of perilymphatic surgery is obvious. This is termed as “primary” or “early” perilymphatic fistula. If instead symptoms occur long after stapedectomy, then establishing a diagnosis of perilymphatic fistula may not be as straightforward. This fistula is termed “delayed” or “secondary” perilymphatic fistula. (For criteria to diagnose PLF see Table 8.1).

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Table 8.1  Criteria to diagnose a definite PLF (a) Fluctuating or nonfluctuating hearing loss (b) Tinnitus (usually described as being “roaring”) (c) Vertigo (d) Aural fullness 1. (a) External trauma to the ear, blow to the head, exposure to an explosive blast.  Or  (b) Barotrauma caused by events like, e.g., nose-blowing, sneezing, skydiving, underwater diving, straining, or lifting of heavy weights. 2. Direct trauma to the inner ear caused by Q-tip injury, stapedotomy operation, temporal bone fracture  (a) Laboratory testing for a perilymph biomarker with high sensitivity and specificity.

Incidence Perilymph fistulae account for up to 9%–10% of stapedectomy failures [4–6]. However, other analyses have documented a far lower incidence. Feldman and Schuknecht [7] analyzed 154 revision stapedectomies and reported that perilymphatic fistulae were found in just five cases. The incidence of perilymphatic fistulae as a cause of failure in stapedectomy is approximately the same for both short term and long term follow up [6].

“Early” (Primary) Perilymph Fistula Stapedectomy by necessity involves the creation of a fistula for the insertion of the prosthesis. The primary perilymph fistula occurs when the fistula created at the time of surgery persists and fails to seal off the vestibule from the middle ear. This can occur immediately following surgery, and symptoms can persist for days and weeks following surgery.

Signs and Symptoms The typical symptoms consist of hearing loss, tinnitus, and vertigo. Since these symptoms are also typical of endolymphatic hydrops, a perilymphatic fistula can be confused with endolymphatic hydrops. The most common symptom in some series is vertigo, while in others the most common symptom is a drop or a fluctuation in hearing [8]. Harrison et  al. [9] reviewed 46 cases of poststapedectomy perilymphatic fistulae and found hearing loss or fluctuating hearing loss to be the most common symptom in 87% of cases. Moon [10] examined 49 cases of poststapedectomy perilymphatic fistulae and found that 71% of cases with primary fistulae, and 78% of cases with secondary

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perilymphatic fistulae presented with hearing loss as their chief complaint. Moon also reported that a pure sensorineural hearing loss is the most common type of loss in both primary and secondary fistulae. Rarely, mixed hearing losses and pure conductive hearing losses can occur from a perilymphatic fistula. Goodhill [11] noted that a perilymph fistula may present only as a fluctuating or persistent conductive hearing loss. He postulated that the ratio of the transducer effect of the prosthesis to the perilymph spillage effect is less than ideal in such patients, thus accounting for their symptoms. Vertigo may result from semicircular canal dysfunction leading to rotatory vertigo, or may have a utricular origin which results in a sense of falling. Harrison et al. [9] found that 35% of their patients complained of vertigo, while 39% had a sensation of imbalance. Moon [10] found that 77% of primary fistulae and 61% of secondary fistulae caused disequilibrium. Tinnitus was found in 28% of patients as reported by Harrison et al. [9]. Moon [10] found tinnitus to be present in 45% of patients who had a perilymph fistula. The signs and symptoms vary with the size of the fistula. Large fistulae result in rapid hearing loss, tinnitus, and vertigo. Morrison [12] noted that such large fistulae accompanied technical difficulties by the operating surgeon at the time of stapedectomy. Fluctuation in hearing loss is unlikely to be a feature in such a situation. In early perilymph fistulae, when the leak is small, the hearing loss may initially appear as a conductive hearing loss; then has a sensorineural component; then progressing to a total sensorineural hearing loss. When such a fistula is repaired late, the hearing does not improve, though vertigo may resolve. When a small fistula is present, the only evidence of the fistula may be failure to achieve adequate closure of the air– bone gap, with mild fluctuation in hearing and a small decreases in speech discrimination scores.

Cause of Primary Perilymph Fistula Improperly sealed oval window fenestra are the likely cause of such fistulae. Goodhill [11] stated that if a mucosal seal does not hermetically seal off the vestibule from the middle ear at the time of surgery, then the chances of such a fistula forming are high. Failure to reflect the mucoperiosteal flaps may allow the lacerated edges of tissue to extend down into the vestibule and prevent formation of a new endosteal membrane at the level of the oval window. A prosthesis that is too long may also prevent the fistula from sealing off. Numerous studies [13–15] have shown that the use of gelatin sponge (gelfoam) as a seal for the oval window fenestra is associated with a high incidence of perilymph fistula. Sheehy and Perkins [13] compared gelatin sponge, fat and fascia as seals for the fenestra and found that the incidence of perilymph fistula was 3.5% when gelatin sponge was used, 1.9% when fat was used, and 0.6% when fascia was used. Lippy and Schuring [16] compared the incidence of perilymph fistula formation with the use of gelatin sponge versus that of the Robinson vein graft prosthesis.

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They reported a significant difference: 50% for gelatin sponge and 4% for tissue seals. Gelatin sponge is thus inadequate as an oval window seal because: 1. It may be resorbed before the neomembrane has formed. 2. The gelatin sponge will get softened by the perilymph, and the prosthesis will penetrate through the gelatin sponge causing a perilymph fistula. 3. The neomembrane that forms with a gelatin sponge is very thin and gets perforated repeatedly by the prosthesis leading to the formation of a perilymph fistula. Linthicum [17] in his report provided evidence that gelatin sponge when used as an oval window seal is more likely to cause perilymph fistula. Causse et al. [18] recommended using a tissue seal over the oval window fenestra to prevent perilymph fistula formation.

Late (Delayed or Secondary) Perilymphatic Fistula Such a fistula can occur long after a successful stapedectomy. Morrison [12] states that this is often the cause of sensorineural deafness that sometimes occurs long after a successful stapedectomy. Most authorities state that the longer stapedectomy patients are followed up, the greater the chances of perilymphatic fistula occurring. He found that in 50% of late perilymphatic fistulae, no obvious cause could be discerned (in the other patients, mountaineering, lifting heavy objects, coughing, sneezing, pressure changes [barotrauma] from flying, and head injuries were suspected as the cause). Otitis media following stapedectomy is not likely to cause a perilymph fistula.

How Does a Perilymph Fistula Form? Glasscock [19] noted that the cochlear aqueduct is patent in a majority of human adults. It puts the cerebrospinal fluid (CSF) in potential communication with the perilymph. Pressure in the cerebrospinal fluid is transmitted directly to the perilymph. Shea [20] noted that CSF pressure in the lumbar spine is 150 mmH2O and that the pressure in the cistern through the cochlear aqueduct can be as high as 350 mmH2O (millimeter of water). In the event of the Eustachian tube getting blocked, negative pressure in the middle ear builds up and can reach minus 600 mmH2O. Thus, a potential gradient of 950 mmH2O is created, which has the potential to push the perilymph out of the vestibule. This can prevent the seal over the fenestra from healing, resulting in a perilymph fistula.

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Clinical Findings Clinical examination of the ear may appear normal in cases of even active PLF. Occasionally the tympanic membrane will be retracted indicative of underlying Eustachian tube dysfunction.

Audiometric Evaluation Pure tone audiometry in the setting of a PLF typically reveals sensorineural hearing loss in the low frequencies followed by a flat sensorineural hearing loss that fluctuates. Recruitment will be present in the initial stages and short increment sensitivity index (SISI) scores are often above 75%. In the early stages, speech discrimination scores fluctuate with the pure tone thresholds; later on they may lower disproportionately. A variable conductive hearing loss may be seen.

Vestibular Tests [21] Hallpike Caloric Tests Canal paresis or a hypoactive response is a likely finding in cases of PLF. However, because there is normally a high incidence of diminished caloric response after stapedectomy, it may become difficult to assess the true value of its significance in using it to diagnose the presence of a perilymph fistula. Electronystagmography (ENG) or Videonystagmography (VNG) ENG/VNG is relatively insensitive to the presence of a perilymphatic fistula. While it may reveal a direction fixed positional nystagmus, this finding in itself is not diagnostic of a perilymph fistula. Fistula Test Fistula tests with a pneumatic otoscope is a simple test that can be done as part of a routine clinical exam. It involves applying positive pneumatic pressure to the ear canal under a seal. In a positive test, nystagmus will develop. However, this test has been found to be negative in one-third of the cases. However, when the fistula test is combined with results from an ENG/VNG, a higher degree of accuracy for PLF diagnosis has been reported. Beales [21] studied 16 patients who had a negative

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fistula test but in whom a fistula was suspected were reoperated to rule out a fistula. Only one had a perilymph fistula; while out of six patients with a positive ENG fistula test, five were found to have a fistula. Thus, the incidence of false-positive and false-negative findings was low enough for the authors to conclude that this test was reasonably reliable.

Radiological Evaluation Kosling et al. [22] reported on the use of high-resolution CT scanning to detect the presence of perilymphatic fistula. They took high-resolution CT scans (1 mm slice thickness) in the axial and coronal planes They reported an air bubble (in the vestibule) at the end of the prosthesis to be an indirect sign of the presence of a perilymphatic fistula. This was the finding in six patients, and all six were found to have perilymphatic fistula. Thus, CT scans were found to be of value in detecting the presence of perilymphatic fistula poststapedectomy.

How Can a Perilymph Fistula Be Prevented? A number of suggestions have been put forward to reduce the likelihood of developing a poststapedectomy PLF: 1. Reflect the mucosa off the footplate completely before making a fenestra. 2. Some have suggested that a stapedotomy technique is less likely to result in perilymph fistula formation as compared to a partial or total stapedectomy, though definitive studies comparing these techniques with regard to the incidence of PLF has not been done. 3. A tissue graft seal over the fenestra acting as a barrier between the perilymph (vestibule) and the prosthesis is highly recommended. 4. The prosthesis should be securely placed on the incus to prevent it from migrating. 5. Avoid using gelatin sponge as a seal. Additional postoperative recommendations during the first several weeks after surgery that the patient can do to limit the development of PLF include: 1. Avoid trauma to the head. 2. Coughing and sneezing with the mouth wide open. 3. Avoid straining against a closed glottis. 4. Avoiding activities that may increase the risk of barotrauma. 5. Avoid lifting heavy weights. 6. Reporting to the surgical team immediately if symptoms such as vertigo, tinnitus, or hearing loss manifest themselves.

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Management of a Perilymph Fistula Surgical closure of the fistula is the treatment of choice. Many surgeons consider this to be a surgical emergency. It is important that the field be kept dry to inspect the oval window under high powered microscopy to assess for the presence of perilymph. If the leak is not visible, then the patient’s head should be lowered and the internal jugular vein on the same side compressed in an effort to make the leak visible. If the patient is under general anesthesia, then the anesthesiologist can also elicit a Valsalva maneuver to see if perilymph accumulates around the oval window. Causse et  al. [23] devised a test to help detect a perilymph fistula intraoperatively. They used a 1.0 mm diamond burr to remove fibrous adhesions from the oval window (this technique can also be performed with a laser). To confirm that a fistula is present, a small piece of gelfoam is placed at the site of the suspected fistula. This gelfoam is then tested on Clinitest glucose test paper. If the paper turns red, then perilymphatic fluid is present, indicating the presence of a perilymphatic fistula. Once the leak is detected, the fistulous tract is excised and the prosthesis removed. Lasers have proven to be immensely helpful and are excellent working tools in such a situation. The mucosa over the footplate is elevated completely. A fresh soft tissue seal is placed over an adequately created fenestra and a new prosthesis is placed over the seal. The patient is advised total bed rest for 48 h. Pirodda et al. [24], in a retrospective analysis of 26 cases, reported on their findings of their approach to the management of rapid deterioration in bone conduction thresholds following stapes surgery. Seven were treated conservatively with medication (pharmacologically with steroids steroids), and the other nineteen were treated with surgery and medication. Of the seven treated medically, improvement was seen in three, while in the other four hearing remained unchanged. In the nineteen cases managed with surgery and medication, in five cases a perilymphatic fistula was found at surgical exploration and four of these five improved. Of those where no fistula was found at surgery, four worsened, and eleven cases experienced no change. The authors concluded their study by advocating a combined medical and surgical approach to treating poststapedectomy perilymphatic fistula.

Results of Treatment of Poststapedectomy Perilymph Fistula Improvement of hearing, especially once sensorineural hearing loss is present, is minimal. Early repair of perilymph fistulae does help symptoms such as vertigo resolve. Tinnitus may not resolve completely. Thus ideally, PFL is diagnosed early, and treated as a surgical emergency.

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Spontaneous Perilymphatic Fistulae A spontaneous perilymphatic fistula is one that occurs without an obvious external influence. This includes the absence of any antecedent external events such as diving, flying or head trauma. Using this rigid definition, the medical literature documents only a very small percentage of patients developing a spontaneous perilymphatic fistula [25]. Symptoms of “spontaneous” PLF are similar to those of poststapedectomy PLF—vertigo and hearing loss with Valsalva-type maneuvers (bending, straining, coughing, etc.). In an attempt to explain the concept of spontaneous PLFs, Goodhill [26] proposed the following theory: An implosive (originating from Valsalva force-induced increased pressure in the middle ear) which then resulted in either the oval and or round window rupturing which then resulted in a PLF. He also postulated that an increased cerebrospinal fluid (CSF) pressure could result in an explosive force resulting in a PLF. There are some reports in which individuals were found to have PLF symptoms with no history of trauma or an antecedent event. The precise numbers of these “spontaneous” or “idiopathic” cases of PLF are hard to truly ascertain. Although many patients were termed to be suffering from PLF and were characterized as “spontaneous,” it is probably more accurate to refer to them as “idiopathic.” This is because the term “spontaneous” can have a small but significant difference in its categorization. Occasionally some of these “spontaneous” patients will cite a significant event which they will link to the onset of the suspected PLF, including something as trivial as sneezing, straining, nose blowing, laughing, or even bending over. This loose definition has thus spawned controversy over what constitutes an idiopathic PLF. One possible cause of idiopathic PLF may be from congenital malformations and microfissure formation. Microfissures can occasionally develop in multiple areas in the temporal bone. Microfissures that develop between the round window niche and the posterior canal ampulla and around the oval window have been described [5]. These microfissures are postulated to act as a possible cause of PLFs. Microfissures can also present as a variant of normal findings on radiological imaging [27] On occasion, defective temporal bone remodeling can contribute to the development of PLF [19]. Similarly, perilymph can leak through the fissula ante fenestram as well [9]. In normal human development, the fissula ante fenestram is a bony cleft present in all individuals that remodels and fills with cartilage and mesenchymal tissue in embryological development. Should this remodeling get altered in any way this could possibly result in a patent cleft through which perilymph can leak. An additional postulated cause of idiopathic perilymphatic fistula is elevations in intracranial pressure [26]. The theory holds that increased CSF pressure is transmitted to the labyrinthine fluids, which in turn leads to a leakage at the oval and/or round window.

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One challenge in diagnosing PLF without an obvious contributing event is that the audiovestibular symptoms of a PLF overlap with many other clinical conditions, including third mobile window syndromes (superior or posterior canal dehiscence), vestibular migraine, endolymphatic hydrops, Meniere’s disease, Eustachian tube dysfunction, and persistent postural-perceptual dizziness. Thus, clinicians should maintain high index of suspicion for a PLF when individuals with nonspecific audiovestibular symptoms do not respond to conventional medical treatments or vestibular rehabilitation. This is particularly true when there is a history of onset of symptoms after trauma or an antecedent inciting event. When patients present with vague auditory or vestibular complaints provided by movement, a full battery of audiologic and vestibular testing is warranted to rule out other potential causes of symptoms. These include 1. Audiometry in PLF it would demonstrate a sensorineural hearing loss 2. Cervical vestibular-evoked myogenic potential (cVEMP) 3. Electrocochleography 4. The fistula test, during videonystagmography These methods have varying sensitivity. They are helpful in  localizing the affected side or in distinguishing nystagmus invoked by noise or pressure changes. The fistula sign is a clinical finding that has traditionally been used; a positive fistula sign is defined as nystagmus when negative pressure is applied to the external auditory canal using Siegel’s speculum. These basic tests though they lack specificity must be performed as base line tests in the documentation of patients suspected to be suffering from PLFs.

Radiological Imaging High-resolution computed tomography (CT) and magnetic resonance imaging (MRI) have played a significant role in the detection of PLFs. One of the earliest described radiological signs of a PLF is a pneumolabyrinth. Small bubbles of air can be hard to visualize on a standard CT scan. Patients suspected to be suffering from PLFs should undergo high-resolution CT imaging with reformations in the coronal and sagittal planes. Fluid in the round and oval window is a reliable sign of a PLF. A study by Venkatasamy et  al. [28] found that high-resolution CT scanning of the temporal bone has a sensitivity for detection of PLFs of over 80% when compared to intraoperative visualization of the suspected perilymph leak. They reported that when CT scanning and MRI were used in patients suspected to be suffering from PLFs the specificity was reported to be close 100% of cases. Some authors have found that axial and coronal CISS (constructive interference in steady state) also called FIESTA (fast imaging employing steady-state acquisition) or MPR (magnetic resonance perfusion) sequence to be the most useful sequences in the detection of PLFs. MRI was found to be very helpful and accurate in identifying congenital abnormalities that contribute to PLF formation. MRI was also found to

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significantly reduce the need for CT imaging in children. While avoiding CT scanning in children will eliminate concerns with regard to radiation, MRI imaging in children will often require a general anesthetic. False-negative cases may be due to scarring or intermittent or slow leakage of fluid, whereas false-positive cases were likely caused by normal hypodensities seen in the cochlea motion artifacts, or inflammation. Furthermore it should be remembered that PLFs can be intermittent in nature, increasing the amount of false-negative cases. CT and MRI imaging have increased value in acute posttraumatic or postoperative patients with large PLFs. CT scanning is very helpful in ruling out other causes of third window syndrome such as superior or posterior canal dehiscence, enlarged vestibular or cochlear aqueduct, and carotid or facial nerve-cochlea fistula, all of which have similar presentations to that of PLFs.

Biomarkers The use of biomarkers for the detection of perilymph fluid has greatly increased the accuracy of the detection of PLF by its high sensitivity. Beta-2 transferrin is actively used around the world for the diagnosis of CSF leakage, and has recently been proposed as a marker for perilymph. Cochlin tomoprotein (CTP) was introduced by Ikezono et al. in 2009 [29], and has been recently approved in 2020 in Japan as an ELISA test for perilymph detection, though is not widely available for use. Beta-2 transferrin is a protein found in higher concentration in CSF, vitreous humor, and perilymph. While many consider it a promising biomarker for perilymph, some researchers have raised concerns regarding sample contamination with blood, blood plasma, CSF, and beta-1 transferrin. Unlike beta-2 transferrin, CTP is a protein found in perilymph. Its presence in CSF is negligible. Western blot and ELISA testing of fluid and lavages from the middle ear for CTP shows promise as a reliable diagnostic tool for PLFs. Currently, the test is limited by the presence of CTP in blood. This could possibly represent a route for sample contamination. Lavage techniques and centrifugation should dilute or remove any blood in the collected in the sample so as not to affect the final result of the CTP analysis.

Conclusions 1. Perilymphatic fistulae can present in diverse ways. 2. PLFs predominant symptoms are (a) fluctuating hearing loss, (b) tinnitus, (c) Vertigo, and (d) aural fullness. 3. Idiopathic PLFs are the most difficult to prove. 4. Radiological imaging using CT scans of the temporal bone and MRI has proved to be very valuable in the diagnosis of PLFs.

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5. Biomarkers such as Beta-2 transferrin and cochlin tomoprotein (CTP) are promising in confirming the presence of a PLF. 6. Surgery is the treatment modality of choice when treating a confirmed PLF that does not immediately respond to conservative measures.

Vertebral Artery Dissection Christopher de Souza, Aishan Patil, Rosemarie de Souza, Vimal Someshwar and Manish Srivastav

Introduction Vertebral artery dissection (VAD) is an unusual and rare cause of Cerebrovascular accident (CVA)/stroke. However, in patients younger than 45 years of age, the incidence of VAD has been found to be higher. Signs and symptoms of VAD are not pathognomonic which makes diagnosis difficult. While spontaneous dissections are known to occur, incidental, minor trauma is usually responsible for precipitating this potentially dangerous condition. Neck manipulation through chiropractic manipulation [30], bending of the neck, or blunt trauma causes the dissection. Spontaneous dissection is also known to occur but is far less common. The dissection of the artery may ultimately lead to a stroke which often can be delayed for days following the acute dissection. Most of VAD are intracranial. Several reports find that vertebral artery dissection may be responsible for around 20% of ischemic strokes in the young.

Etiology Patients often report minor, trivial precipitating events before the onset of symptoms. Coughing, vomiting, chiropractic procedures are frequently reported by patients before symptoms manifest themselves. Blunt trauma to the neck is also reported to be an initiating event in VAD [31]. Patients with connective tissue disorders like Ehlers–Danlos syndrome is the most common connective tissue disorder that can likely cause vertebral artery dissection. Twenty percent to 40% of patients with serious cervical cord injury or spine fractures will demonstrate VAD [32]. Other risk factors [33, 34] for vertebral artery dissection include: • Forceful nose blowing • Extension of neck for prolonged periods of time

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• • • • •

Wrestling Hypertension Fibromuscular dysplasia Oral contraceptives Vasculitis. Matrix metalloproteinase (MMP-9) [35] is thought to be one of the factors MMP 9 is a gelatinase involved in inflammation in several vascular diseases. Its role in VAD is unclear at this time although serum MMP 9 has been found to be grossly elevated in the acute phase of VAD. • Hypercholesterolemia and obesity • Migraine • Hypertension

Epidemiology Vertebral artery dissection is thought to be the likely cause of approximately 2% of all ischemic strokes. However, in young patients, the incidence is higher and 10%–25% of the population is affected by this condition. The combined incidence of both vertebral artery and carotid artery dissections is estimated to be 2.6 per 100,000 [36]. Carotid artery dissections are more three to five times more common than vertebral artery dissections [37].

Pathophysiology Dissections are caused by the penetration of blood into the arterial wall through the site of injury which is the intima of the arterial wall. Blood enters the media from the site of intimal injury, The dissection then extends cranially in the same direction as the bloodstream. The intramural hematoma causes compression and compromise of the lumen of the artery. This in turn causes enlargement of the external diameter of the artery. If the dissection extends toward the adventitia, then a pseudoaneurysm (dissecting aneurysm) will likely be the result. The resulting dissecting aneurysm could likely become a source for distal thromboembolism.

Vertebral Artery Anatomy Segment 1 starts at the first branch of the subclavian artery until the region of the foramina of C5–C6. Segment 2 runs within the transverse foramina from C5/C6 until C2. Segment 3 is the tortuous segment that begins at the transverse foramina of C2 and then loops around C1 and then passes between the atlas and the occiput. This

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segment of the artery is encased with nerves, muscles, and the atlanto-occipital membrane. Segment 4 is the intracranial segment; it pierces the dura at the foramen magnum runs until the junction of the medulla and pons where it merges with the basilar artery. The majority of spontaneous dissections occur in segment 3, which at times extends to involve segment 4. The arterial anatomy consists of three layers (a) the intima (innermost), (b) the media (middle), and (c) the adventitia (outermost layer). Dissection occurs when the structural integrity of the arterial wall is compromised. Intimal tears lead to arterial blood separating (dissecting) the layers of the arterial wall. The blood within the arterial wall results in a hematoma with clot formation. The resulting compromise in arterial blood flow results in stroke. Vertebral artery dissection can be either extracranial or intracranial. Extracranial dissections frequently occur at the distal extracranial segment near the atlas and axis. Intracranial dissections are frequently associated with subarachnoid hemorrhage and thus are associated with a much worse prognosis. Neurological sequelae of both extracranial and intracranial dissections result in cerebral ischemia caused by thromboembolism, hypoperfusion, or a combination of both [38].

History and Physical Examination History Patients typically present with an acute and severe unilateral neck pain and/or a headache. A history of trivial neck trauma preceding the pain will often be present. The pain is located in the occipital-cervical area of the neck. Neurological symptoms are often delayed in onset. However, 70% of patients will have some type of neurological deficit which may present late in the course of the disease. Lateral medullary syndromes (Wallenberg Syndrome) and cerebellar infarctions are often the most common sites for VAD related strokes. Wallenberg Syndrome is defined by sensory deficits affecting the trunk and extremities on the opposite side of the infarction and sensory deficits affecting the face and cranial nerves on the same side as the infarction. The major neurological symptoms that occur following VAD are, dizziness, ataxia, dysphagia (cranial nerves 9 and 10 are involved), disequilibrium, unilateral hearing loss, dysarthria and diplopia. Extracranial dissections often have a bruit present on palpation and are heard very clearly on auscultation. The bruit has even been reported on the contralateral

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side due to increased collateral blood flow that occurs secondarily. The distinguishing factor that separates patients suffering from cerebellar infarctions secondary to atherosclerotic disease is the age of the patient and the presence of pain. When the dissection is located intracranially, a subarachnoid hemorrhage is present 50% of the time [39]. This subset of patients have severe neurological symptoms and an accompanying poorer prognosis than those with extracranial dissections. Physical Exam The following are present in VAD • • • • • • • • • •

Nystagmus and vertigo Truncal ataxia Ipsilateral loss of taste (hypogeusia) and numbness Horner’s syndrome Impaired proprioception and fine touch Contralateral impairment in thermal and pain sensation in the extremities Tongue deviation to the side of the lesion Internuclear ophthalmoplegia Ipsilateral loss of taste (nucleus and tractus solitarius) Hiccups

Radiological Imaging MRI and CT angiography (Figs.  8.1, 8.2 and 8.3a, b) are the best modalities to evaluate VAD and remain the gold standard [40]. CT scanning and CT angiography are commonly used first line imaging modalities. CT scan can demonstrate posterior fossa ischemia along with subarachnoid hemorrhage. It can also identify the site where the occluded vertebral artery or mural thrombus occurs. CT Angiography are far superior to plain CT scans because of the information it yields and should be performed. CT Angiography will identify the irregularity of the vascular lumen or thickening of the arterial wall [41]. Vascular Duplex scanning demonstrates abnormal flow in 95% of patients. MRI is useful in detecting an intimal flap and luminal thrombosis. Hyperintensity of the vessel wall may be visualized on T1-weighted images and are considered pathognomonic of VAD. A cerebral angiogram may be required if the MRI and CT scan have failed to reveal any pathology.

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Fig. 8.1  Forty-eight-year-old female with recurrent posterior circulation strokes with V4 dissecting aneurysm. (a) Acute right cerebellar infarct. (b) MRI contrast angiogram Recon images showing outpouching at right V4. (c) DSA, right VA showing dissecting aneurysm at V4 level. (d) 4D angiogram showing right VA dissecting aneurysm

 ultisection CT Angiography Findings in Vertebral Artery M Dissection (Figs. 8.1, 8.2, and 8.3) Multisection CT angiography has been found to be a very sensitive and accurate technique for the diagnosis of vertebral artery dissection. The reported sensitivity was 100% and specificity was 98%. The reported findings are increased external diameter of the affected blood vessel and crescent-shaped mural thickening in patients suffering from vertebral artery dissection. It should be noted that these criteria should be applied with caution because both signs can be found in nondissected vertebral arteries as well. Multisection computed tomographic (CT) angiography provides very high-resolution and excellent high-contrast images of

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Fig. 8.2 Twenty-nine-­ year-old male developed sudden neck pain while dancing with friends, and MRI showed patchy right posterior cerebellar infarcts. Right VA DSA demonstrates, nonflow limiting short segment dissection of V2 segment (arrow)

the arterial lumen and wall. Two-dimensional (2D) and 3D visualization increase its value in helping diagnose the site and extent of dissection and vascular compromise. MR imaging too demonstrated excellent sensitivity and specificity of 84% and 99%, respectively, compared with conventional angiography in diagnosis of internal carotid dissection. The criteria were an increase in the external diameter of the artery and narrowing of the lumen. It should be noted that flow void narrowing is a much less useful indicator of dissection because it can be seen in many other conditions. Transcranial Doppler has been also been found to be a very useful tool in VAD [42]. Sonographic curves, microembolic signals (MES), and breath holding index (BHI) were found to be very useful parameters in predicting ischemic events. Routine blood work with specific reference to the patient’s coagulation profile should be obtained. Should radiological imaging reveal the absence of hemorrhage, anticoagulation can be then initiated.

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Fig. 8.3  Forty-year-old female with acute left cerebellar infarcts. (a) Left V4 dissection with underline thrombus. (b) Poststenting angiogram shows improved flow across stent and into the distal circulation

Management Outcomes Stenotic-type and almost completely occlusive dissections often and frequently heal with minor residual wall abnormalities. Occlusions are likely to recanalize early. However, the outer diameter of the dissected vessel will remain much smaller when compared to that of the normal contralateral vessel. Dissecting aneurysms behave in a similar fashion. However, improvement and recovery are not as remarkable as those which occur in a dissection. Treatment of patients suffering from a craniocervical artery dissection is controversial at this time because controlled studies are lacking. Administration of anticoagulants is the most frequent therapy to prevent thrombosis and embolism in extracranial dissections [43]. In intracranial artery dissections, the risks that accompany administration of anticoagulants may be high because of the possible risk of subarachnoid hemorrhage. Anticoagulant therapy is clearly contraindicated in cases of intracranial dissecting aneurysms with subarachnoid hemorrhage. Endovascular or surgical interventional procedures are considered [44, 45] for patients who still remain symptomatic due to thromboembolic events and in situations of dissecting aneurysm. Should recurrences occur they often occur within the first 4–6 weeks following the onset of symptoms. After the first month following dissection, the risk of

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recurrence is about 1% per year, and recurrent dissection occurs mainly in arteries not previously involved by dissection. Prognosis is usually good in those patients who survive the initial onset of VAD. Approximately 10% of patients succumb. The goal of management is to prevent stroke. Management is done with anticoagulants, the drug of choice being heparin. If there are no contraindications, then thrombolytic therapy can be started as long as the time is within 4.5 h from the onset of symptoms. Death is seen following extensive intracranial dissection, brainstem infarction, or subarachnoid hemorrhage. Most dissections will resolve over time with no neurological deficits. Should the dissection extend intracranially, the risk of subarachnoid hemorrhage increases significantly and anticoagulation is contraindicated. Endovascular or surgical treatments are reserved for patients with concomitant complications or those whose maximal medical therapy has been unsuccessful. Hospitalization is mandatory for all patients with vertebral artery dissection because close monitoring of all vital parameters is essential including that of evolving neurological deficits. Modern technological advances allow the use of endovascular therapies to manage vertebral artery dissection. The role of this therapy remains controversial at this time because most patients can be managed with anticoagulation therapy. Furthermore, most dissections resolve spontaneously. Endovascular therapy is best reserved for patients who are not candidates for thrombolytics and/or have a subarachnoid hemorrhage. Surgery in the form of bypass graft is rarely done and not always successful. Differential Diagnosis • • • • • • •

Cervical spine fracture Emergent management of subarachnoid hemorrhage Migraine headache Stroke Subarachnoid hemorrhage Vasculitis affecting the vertebrobasilar circulation Vertebrobasilar atherothrombotic disease

Prognosis For patients who do survive the initial acute extracranial dissection, the prognosis is excellent. Complete recovery in nearly 80%–90% of patients is expected. At least 10% of AD will develop recurrent attacks, a major stroke, or death. Patients who have severe neurological deficits at the time of presentation have a poor prognosis. Patients who present with an intracranial dissection have a poor prognosis. Those who present with altered consciousness and neurological deficits do poorly.

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Intracranial vertebral dissections are often associated with brainstem infarctions, subarachnoid hemorrhage, and death. Complications of VAD Cerebellar and brain stem infarction. Subarachnoid hemorrhage. Vertebral artery pseudoaneurysm leading to compression neuropathy of the cranial nerves.

Conclusions 1. VAD can be a cause of vertigo. 2. VAD should be diagnosed quickly and the physician should be aware of its presentation. 3. CT angiography and MRI angiography are radiological imaging modalities of choice. 4. If diagnosed early VAD can be treated effectively lessening the sequelae of compromised cerebral blood circulation which can lead to devastating consequences like stroke. 5. Treatment of VAD is usually through the administration of thrombolytics and anticoagulants. 6. Sequelae of VAD can be present in the form of aneurysms.

References 1. Newlands WJ.  Poststapedectomy otitis media and meningitis. Arch Otolaryngol. 1976;102(1):51–4. 2. Matz GJ, Lockhart HB, Lindsay JR.  Meningitis following stapedectomy. Laryngoscope. 1968;78:56–63. 3. Lewis ML. Inner ear complications of stapes surgery. Laryngoscope. 1961;71:377–83. 4. Crabtree JA, Britton BH, Powers WH. An evaluation of revision stapes surgery. Laryngoscope. 1980;90:224–7. 5. Derlacki EL.  Revision stapes surgery: problems with some solutions. Laryngoscope. 1985;95:1047–53. 6. Glasscock ME, McKennan KX, Levine SC. Revision stapedectomy. Otolaryngol Head Neck Surg. 1987;96:141–8. 7. Feldman BA, Schuknecht HF.  Experiences with revision stapedectomy procedures. Laryngoscope. 1970;80:1281–91. 8. Wiet RJ, Harvey SA, Bauer GP. Complications in stapes surgery: options for prevention and management. Otolaryngol Clin N Am. 1993;26(3):471–90.

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Chapter 9

Vestibular Ototoxicity Christopher de Souza, Rosemarie de Souza, and Aishan Patil

Introduction Available evidence demonstrates that early detection of toxicity through prospective monitoring allows for treatment modifications to minimize and prevent permanent hearing loss and balance impairment. Many monitoring protocols for the prevention of ototoxicity have been described, but their practical application is difficult to implement because of several variables. Current protocols when administering potentially ototoxic agents have been shown to be effective in recognizing early ototoxicity and thus allowing for the prevention of permanent, irreversible damage [1]. Implementation of these protocols (especially protocols to evaluate the vestibular system) is frequently difficult to carry out because of the incapacitated or obtunded status of the patient. Since the patient is seriously ill, they are unable to inform their physicians that they are experiencing symptoms of ototoxicity. Thus, it is only when the patient is recovering that they are able to perceive that the medications that they have received are ototoxic. At this time, there is no consensus regarding the choice of early ototoxicity identification methodology. C. de Souza (*) Lilavati Hospital, Mumbai, India Holy Family Hospital, Mumbai, India Holy Spirit Hospital, Mumbai, India Faculty SUNY Brooklyn, Brooklyn, NY, USA LSUHSC, Shreveport, LA, USA e-mail: [email protected] R. de Souza Department of Internal Medicine, BYL Nair Hospital, Mumbai, India A. Patil Vascular Surgery, Borders General Hospital, Melrose, Scotland, UK © The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 B. T. Crane et al. (eds.), Disorders of the Vestibular System, https://doi.org/10.1007/978-3-031-40524-2_9

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Historical Perspective Mercury was once thought to be a cure for syphilis. Hence the axiom, “Spend a night with Venus, and you’ll spend a lifetime with Mercury.” In this case, the cure proved far more terrible than the disease. Treatment with mercury resulted in severe vertigo, deafness, uncontrollable tremors, and insanity. When streptomycin was first discovered, it was thought to be a miracle cure for tuberculosis. It was soon seen that it resulted in severe cochlear and vestibular ototoxicity. This led to a search for a medication that was effective against tuberculosis but was far less vestibulotoxic. This led to the discovery of dihydrostreptomycin, which was as effective against tuberculosis but was mildly vestibulotoxic. In the 1960s, other aminoglycosides were discovered, and it was found that they were all ototoxic, some being more ototoxic to the cochlea while others affected the vestibular system much more than they damaged the cochlea. Subsequently, many ototoxic pharmacologic agents that are vestibular toxic have been discovered. They are loop diuretics, salicylates, quinidine, and other antibiotics, including minocycline, erythromycin, polymyxin, and chloramphenicol. Chemotherapeutic agents like cisplatin are also severely vestibulotoxic.

Epidemiology Ototoxicity can affect all age groups. The global incidence is not known. This may be due to a variety of reasons, like the existence of varied and diverse criteria to define. Ototoxicity  There could be a wide spectrum of reactions to a known ototoxic drug in different ethnic groups. The utilization of various audiological protocols for the evaluation of ototoxicity and the lack of referral for otological symptoms could account for the absence of a true incidence of ototoxicity. Cisplatin ototoxicity occurs in a range between 23% and 50% in adults and up to 60% in children. Some reports have found elevated hearing thresholds in up to 100% of cisplatin-treated cancer patients, while it is estimated to be 63% with aminoglycosides and 6–7% with furosemide. It should also be noted that the incidence and severity of ototoxic hearing loss appear to be dose-dependent and, at times, influenced by the cumulative buildup of ototoxic medication. Other considerations like age, gender, and comorbid conditions like congestive heart failure, renal failure, hypertension, genetic susceptibility, geographic factors, type of drug, route of administration, duration of therapy, bioavailability, and preexisting hearing loss also influence the course and severity of ototoxicity.

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Pathophysiology of Ototoxicity Animal studies have found damage to occur in the hair cells of the organ of Corti, the ampullary cristae, the maculae of the utricle, and the saccule. Inside the vestibular receptors, the most extensive damage occurs in the apex of the cristae and the striolar regions of the maculae. As ototoxicity increases, the progression of hair cell loss is seen to extend to the periphery of the vestibular receptors. In general, it is noted that vestibular type 1 hair cells are more susceptible to damage than type 2 hair cells. Aminoglycosides have been found to cause severe damage to the otoconial membrane and otolith structures. In end-stage ototoxicity, degeneration of ganglion cells is observed. Ototoxic medications enter the inner ear directly through intravenous injection, intramuscular injection, or topically when administered as ear drops. Some chemical toxins and solvents enter the bloodstream through alveolar oxygen transport following inhalation of toxic fumes. How exactly these toxins enter the inner ear through the bloodstream is not clear at this time. It has been postulated that these toxins enter the perilymph vascularis via the spiral ligament or into the endolymph via the stria vascularis. The round window membrane is another portal of entry for toxic substances to enter the inner ear. The round window membrane acts as a semipermeable and selective membrane. Factors that affect permeability include size, concentration, electrical charge, the thickness of the round window membrane, and facilitating agents that enhance transfer to the inner ear across the round window membrane. All the morphologic evidence available for the round window membrane suggests that it participates in the resorption and secretion of substances to and from the inner ear. The round window membrane acts as an active ionic pump for substances from the middle ear into the inner ear. It is thought that the membrane could very likely play a role in the defense system of the inner ear. Various substances, like antibiotics and tracers, when placed in the middle ear, traverse the membrane. Tracers placed in perilymph become incorporated into the membrane by the inner epithelial cell membrane. Substances traverse through the round window membrane through pinocytotic vesicles. Congenital ototoxicity can occur during pregnancy if the mother has been exposed to ototoxic agents. The ototoxic agent passes through the placenta to the developing fetus. The first trimester is the most vulnerable time for the developing fetus. In addition to the damage to the vestibular system and the cochlea, the child may be born with several birth defects as a direct consequence of being subjected to ototoxic medications.

Symptoms of Vestibular Ototoxicity Oscillopsia due to bilateral vestibular hypofunction is a dominant symptom that occurs in vestibulotoxicity. Oscillopsia is the perception that stationary objects or surroundings move coincidentally with head movement, resulting in dizziness, motion sickness, and unsteadiness when standing or walking, especially in the dark.

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With oscillopsia, illusory movements occur on the same plane as head movement but in the opposite direction. This usually gives the patient the impression that the environment is whirling around. This results in dizziness, motion sickness, and unsteadiness, especially when standing or walking. This worsens in the dark, where there are no visual cues to guide the patient. Unsteadiness when standing or walking can range from mild to severe, depending on the severity of the vestibular loss. Most patients with bilateral vestibular loss are completely dependent on visual and somatosensory input in order to maintain posture control. Therefore, disorders that adversely impact the function of one or both of these systems will have a greater negative functional impact. While it would be logical to assume that systemically administered medications would affect both ears equally, this has not always been true—vestibulotoxicity can also be unilateral or asymmetrical. Unilateral vestibular paresis, or non-lateralized vestibular loss, may include vertigo and nausea but is typically not associated with oscillopsia. With bilateral but asymmetric vestibular hypofunction, patients may present with a symptom profile that is consistent with both bilateral and unilateral vestibular loss, depending on the degree of asymmetry and the amount of loss in the better-functioning vestibular organ.

Vestibular Ototoxicity Vestibular ototoxicity occurs when the damaging effects of a chemical substance are felt on the labyrinthine hair cells and their supporting structures, the vestibular division of the eighth cranial nerve, and its central nervous system connections. The effects of this ototoxicity may be transient or permanent, and they can range from minimal to severe. The consequences for the person suffering from such a condition can be very debilitating. Vestibular ototoxicity typically does not occur exclusively by itself but is often also accompanied by cochlear symptoms (hearing loss or tinnitus). Vestibular ototoxicity is said to be present when the symptoms of vestibular disturbances are more pronounced than those related to the cochlea [2, 3].

Diagnosing Ototoxicity As previously noted, ototoxicity may present with symptoms related to the cochlea as well as the vestibular system. Evaluation of patients suspected of having ototoxicity requires a complete history and physical examination, including a comprehensive vestibular exam. Important elements of the vestibular exam to document vestibular hypofunction include head impulse testing in the planes of the three semicircular canals (see Halmgyi head impulse test below) and dynamic visual acuity testing.

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Comprehensive testing includes electronystagmography (ENG) and videonystagmography testing with calories. Caloric testing, in particular, is used to document unilateral versus bilateral vestibular hypofunction. Rotatory chair testing, if available, is also important in the diagnosis of vestibular hypofunction. Studies have shown that caloric and sinusoidal rotation tests are equally sensitive to monitoring the degree of nystagmus depression [4]. Some researchers have also demonstrated the distinct superiority of horizontal vestibular ocular reflex (VOR) rotational stimuli over caloric tests, especially when there is streptomycin-induced vestibular toxicity [5]. Another advantage of rotational testing is that high-frequency information unavailable from caloric testing can be obtained. Further, rotatory chair testing allows the clinician to track changes in the amplitude and symmetry of compensatory eye movements over a period of time. These can then be compared with normal values, which act as a referral, and the patient’s progress can be monitored. Dynamic posturography is an additional test that can be used. While it is generally insensitive to diagnosis, it is useful to document improvements in compensation over time. Further, it has made Romberg’s test a sensitive one for evaluating the vestibular spinal reflex. While the tests noted above are useful for the diagnosis and monitoring of vestibular compensation over time, in many instances, patients suffering from vestibular disturbances are quite ill and confined to bed. Thus, tests like complete ENG, rotation, and dynamic posturography cannot be easily performed on such patients. Longridge and Mallinson [6] described the “dynamic illegible E” for bedside evaluation of the VOR and VOR compensation. Its advantage is that it is simple to do, low cost, and can be performed at the bedside. Halmagyi and Curthoys [7] also describe a bedside test to determine the VOR. The examiner asks the patient to fix their gaze on the target while the examiner rapidly turns the patient’s head from side to side. A normal patient does not make saccadic eye movements during the head rotation, indicating that the VOR is intact and that the patient’s gaze has indeed been fixed. In contrast, patients with unilateral vestibular hypofunction can keep the gaze fixed on the target only when the head is tuned away from the abnormal side. When turning towards the side of the lesion, the patient must make one or more refixation saccades in the direction opposite to that of the motion of the head in order to allow his gaze to be fixed on the target. Patients with bilateral profound loss of vestibular function make saccadic refixation movements in both directions of passive head movements.

Audiometry Aminoglycosides affect the outer hair cells of the basal turn of the cochlea. This usually results in high-frequency sensorineural hearing loss and a loss of speech understanding out of proportion to the loss of pure tone thresholds.

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Electrocochleography has also been shown to be a very sensitive tool to determine hearing loss caused by ototoxic substances. It detects cochlear toxicity within minutes of an intravenous dose of intravenous aminoglycosides. Its disadvantage is that a needle has to be inserted through the tympanic membrane to make the measurement, limiting its widespread use.

Vestibulotoxicity Monitoring No widely accepted guidelines exist for identifying vestibulotoxicity. The challenge of vestibulotoxicity monitoring as compared to cochlear ototoxicity is the identification of these symptoms. These become apparent only once the patients are mobilized. Often, these symptoms are incorrectly attributed to the patient’s debilitated state. There is no single test that can identify vestibulotoxicity. Screening tests, such as dynamic visual acuity and head impulse testing, can be used to monitor patients over time. Vestibular diagnostic procedures are often not feasible due to the patient’s compromised health status.

Treatment The treatment of vestibular ototoxicity can be divided into two parts. 1. Vestibular ototoxicity is expected when administering a medication that is potentially vestibular toxic. This can occur when administering aminoglycosides. Baseline audiometry and neurologic examination with specific attention to equilibrium are recorded and kept as a source of referral once treatment has been initiated. When patients are ambulatory, it is far easier to detect. Patients will report disequilibrium and other deficits almost immediately once they occur. Usually, these will be early and therefore easier to reverse. Reversal is usually accomplished with the cessation of the ototoxic medication. Those patients who are not ambulatory and are obtunded are less likely to report symptoms promptly. Thus, the severity will increase before the patient reports it. Usually, such patients will have other far more serious health problems, and the treating physician will likely have to choose between continuing or discontinuing the medication, especially if it is a life-saving drug. 2. Protracted vestibular toxicity. This is caused by frequent and prolonged use of ototoxic medication. These patients are the most difficult to treat. They will also present with other symptoms like tinnitus, decreased hearing, ataxia, and oscillopsia. While cochlear implants and other devices can ameliorate symptoms like hearing loss and tinnitus, disequilibrium remains the symptom that is most difficult to treat. Medications like Meclizine, which suppress vestibular responses,

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generally are not much help in these circumstances after the acute phase of vertigo has resolved. Furthermore prolonged use of meclizine may result in other centrally mediated causes of imbalance and could complicate the treatment. Benzodiazepines are not the treatment of choice. They are reported to adversely affect eye movements through reduction of saccadic velocity, increase in saccadic duration, impairment of slow pursuit, decrease in VOR gain, and increase in VOR time constant. They are also addictive. Patients suffering from severe vestibular toxicity become visually and proprioceptor-­dependent. They need visual cues to navigate and depend excessively on proprioception to walk. While they are able to see, walking is feasible. It is in the dark that such patients experience major difficulties. Surgical options for this debilitating disorder are limited. Some have proposed either chemical (intratympanic gentamicin) or surgical labyrinthectomy to treat an ear that may be sending variable or abnormal balance signals to the brain, in the hopes that a better ear will allow improved vestibular compensation. However, such a procedure may in fact reduce the remaining vestibular function in a patient and make symptoms worse. The question then arises: when both ears are affected, what treatment options exist? At present, the primary treatment used is vestibular therapy to help the patient compensate for the vestibular loss, both by utilizing any remaining vestibular function and by coordinating proprioception and vision into the patient’s overall balance. One future avenue of treatment that holds great promise is the vestibular implant [8]. It is similar to the cochlear implant in that it is a surgically inserted device in the vestibular end organs (at present limited to the semicircular canals) and restores VOR in these patients. The device is currently in clinical trials [9].

Overview The diagnosis and effective treatment of ototoxicity are challenging. A stringent, practical protocol that encompasses all elements aimed at profiling the effects of ototoxicity is vital. Ototoxic drugs usually adversely affect both the cochlea and the vestibular systems simultaneously. Currently, over 600 categories of drugs that have the potential to cause ototoxicity have been listed. Aminoglycoside antibiotics, platinum-based chemotherapeutic agents, loop diuretics, macrolide antibiotics, and antimalarials are the commonly used medications that have documented ototoxic effects. On questioning the patient, it has often been found that the exact time of commencement of symptomatology is frequently unclear. High interindividual variability in symptomatology is often found because of differences in genetic factors, pharmacokinetics, the metabolic status of the individual, and comorbid medical conditions. Ototoxicity affecting the cochlea follows a relatively predictable pattern. The basal turn of the cochlea is involved first, involving its outer hair cells (responsible

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for high frequencies), and as ototoxicity progresses, it involves the apical portion, which is responsible for the lower speech frequencies. Although ototoxic-induced hearing loss is not a life-threatening condition, it can have a severely negative impact on communication and health-related quality of life issues, with significant adverse vocational, educational, and social consequences. It has been reported that in children, even mild hearing loss can severely impair speech and language acquisition and retard cognitive and social development. This, in turn, leads to poor scholastic performance and lowered psychosocial functioning. The goal of the management of ototoxicity is to minimize or prevent these complications and plan appropriate rehabilitation measures.

Preventive Measures When administering a medication that is potentially ototoxic, especially if it is to be given as a course, it is prudent to get baseline measures of the cochlear and vestibular systems before starting treatment. Baseline audiometric tests like pure tone, speech, and immittance audiometry need to be documented. The question arises as to whether baseline vestibular testing should be carried out. If the patient is without vestibular symptoms, then perhaps rotatory chair testing can be performed. And findings were noted and documented. At this time, there are no clear protocols for pretreatment. Caloric testing can also be considered if the patient does not present with perforations or infections of the ear. All aspects of treatment should and must be carefully explained to the patient in detail. The patient should be made aware of what the symptoms are that could herald the onset of either cochlear or vestibular toxicity. Then should the patient present with symptoms, tests can be performed using the baseline as a comparison to determine the level of toxicity. Some reports have described calcium as a competitive inhibitor of gentamycin. It was thought that an oral suspension of calcium could possibly be used as an oral supplement to avoid or ameliorate potential ototoxicity. It, in turn, could likely affect the efficacy of gentamycin. Thus, the pros and cons need to be carefully weighed before initiating it. Still, some other researchers have described using probenecid to reduce the level of perilymph penetration of furosemide, resulting in diminished cochlear toxicity. Fosfomycin has also been reported as being able to reduce the effects of cisplatin ototoxicity. There are several animal and in vitro studies that have reported the efficacy of otoprotective agents that can possibly prevent ototoxicity. Unfortunately, many of these studies lack appropriate control groups, positive clinical findings and longitudinal outcomes, and multicenter, large-scale clinical trials that would validate their results and recommendations. Agents designated as otoprotective medications such as sodium thiosulfate, amifostine, and N-acetylcysteine have been investigated for

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cisplatin otoprotection. While systemic administration of these agents has been described as having the ability to reduce cisplatin-induced hearing loss, it was also found that they simultaneously reduce cisplatin’s tumoricidal efficacy. Therefore, in an attempt to achieve otoprotection while simultaneously achieving tumoricidal activity, the administration of sodium thiosulfate was delayed for several hours following cisplatin administration. In addition, intra-tympanic administration of these agents was performed. There are reports of intratympanic administration of N-acetylcysteine, which adequately demonstrated otoprotection following the administration of cisplatin-induced ototoxicity. Intratympanic dexamethasone also yielded positive results following the administration of cisplatin. Cisplatin-induced ototoxicity causes permanent hearing loss in pediatric and adult cancer survivors. Understanding the mechanisms that cause cisplatin-induced hearing loss and the development of treatment modalities to reduce and possibly reverse cisplatin ototoxicity have been impeded by animal models that are not ideal. In a clinical setting, cisplatin is frequently administered in multidose, multicycle protocols. However, many studies conducted on animal models used single injections of high-dose cisplatin. This does not reflect the manner in which cisplatin is administered in clinical protocols. When these rodents were subjected to similar protocols that occur in real-life clinical settings, there was significant mortality that again presented a major impediment to understanding the mechanisms of ototoxicity. A Cochrane review of three randomized, controlled trials of amifostine agents reported that no conclusions could be drawn about their efficacy in otoprotection against cisplatin-induced ototoxicity in children. At this time, no medications have been approved by the US Food and Drug Administration that could play a role in the prevention of drug-induced ototoxicity during curative cancer treatment. More clinical research and trials are needed to study the otoprotective profile of these medications. Recent studies have demonstrated the successful promotion of cochlear gene therapy, adeno-associated virus-mediated delivery of brain-derived neurotrophic factors, and stem cells in animal models. These future therapeutics hold promise for the prevention and treatment of ototoxicity, though much work needs to be done to document their efficacy and feasibility in humans.

Drug Metabolizing Genes and Its Association with Ototoxicity Well-defined, clear associations have been established between chemotherapy and ototoxicity. Inter-individual variabilities have also been found in the development of chemotherapy-related hearing loss [10]. These interindividual variations can likely be explained by individual genetic variations toward the effects of chemotherapy, which in turn can potentially exacerbate the compound’s ototoxic effects. Understanding these genetic variants as a way to predict which patients are most susceptible to ototoxicity could thus provide important information for clinical decision-making.

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Candidate gene pharmacogenetic studies have explored the relationship between drug-induced hearing loss and several genotypes such as thiopurine methyltransferase, ATP-binding cassette transporter C3 (ABCC3), glutathione-S-transferase subclasses (GSTP1, GSTM1, and GSTT1), catechol-O-methyltransferase, and megalin [11–17]. These are results that are largely inconsistent. It was found that mutations in the mitochondrial DNA, such as the A1555G mutation, have been associated with increased susceptibility to aminoglycoside-related ototoxicity [18]. A recent genome-wide association study has identified the association between cisplatin-­ induced hearing loss and genetic variants such as superoxide dismutase 2 (SOD2) and Acylphosphatase-2 (ACYP2) ([19]).

Conclusions 1. Ototoxicity involves both the cochlea and the vestibular system. 2. There are no universally accepted, clearly defined protocols to evaluate and manage ototoxicity. 3. Most of the patients who are exposed to potentially ototoxic agents are obtunded and thus cannot complain of dizziness or hearing loss. When they do complain, ototoxicity is advanced, making treatment measures difficult. 4. There are a few medications available to ameliorate ototoxicity. However, they adversely affect the effectiveness of the medication that causes ototoxicity.

References 1. Handelsman JA.  Vestibulotoxicity: strategies for clinical diagnosis and rehabilitation. Int J Audiol. 2018;57(sup4):S69–77. https://doi.org/10.1080/14992027.2018.1468092. 2. Black FE, Pesznecker SC. Vestibular ototoxicity. Clinical considerations. Otolayngol Clin N Am. 1993;26(5):713–36. 3. Black FO, Gianna-Poulin C, Pesznecker SC.  Recovery from vestibular ototoxicity. Otol Neurotol. 2001;22(5):662–71. https://doi.org/10.1097/00129492-­200109000-­00018. 4. Ganesan P, Schmiedge J, Manchaiah V, Swapna S, Dhandayutham S, Kothandaraman PP.  Ototoxicity: a challenge in diagnosis and treatment. J Audiol Otol. 2018;22(2):59–68. https://doi.org/10.7874/jao.2017.00360. Epub 2018 Feb 26. PMID: 29471610; PMCID: PMC5894487. 5. Llorens J, Callejo A, Greguske EA, Maroto AF, Cutillas B, Martins-Lopes V. Physiological assessment of vestibular function and toxicity in humans and animals. Neurotoxicology. 2018;66:204–12. https://doi.org/10.1016/j.neuro.2018.02.003. Epub 2018 Feb 8. PMID: 29428870. 6. Longridge NS, Mallinson AI. The dynamic illegible E (DIE) test: a simple technique for assessing the ability of the vestibular ocular reflex to overcome vestibular pathology. J Otolaryngol. 1987;16:97–100.

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7. Halmagyi GM, Curthoys IS. A clinical sign of canal paresis. Arch Neurol. 1988;45:737. 8. Guyot JP, Perez Fornos A. Milestones in the development of a vestibular implant. Curr Opin Neurol. 2019;32(1):145–53. https://doi.org/10.1097/WCO.0000000000000639. 9. Guyot JP, Guinand N, Perez Fornos A. Tribute to Bernard Cohen - whose pioneering work made the vestibular implant possible. Front Neurol. 2020;11:452. https://doi.org/10.3389/ fneur.2020.00452. 10. Ross CJ, Katzov-Eckert H, Dubé MP, Brooks B, Rassekh SR, Barhdadi A, et  al. CPNDS. Consortium genetic variants in TPMT and COMT are associated with hearing loss in children receiving cisplatin chemotherapy. Nat Genet. 2009;41:1345–9. 11. Choeyprasert W, Sawangpanich R, Lertsukprasert K, Udomsubpayakul U, Songdej D, Unurathapan U, et  al. Cisplatin-induced ototoxicity in pediatric solid tumors: the role of glutathione S-transferases and megalin genetic polymorphisms. J Pediatr Hematol Oncol. 2013;35:e138. 12. Oldenburg J, Kraggerud SM, Cvancarova M, Lothe RA, Fossa SD. Cisplatin-induced long-­ term hearing impairment is associated with specific glutathione s-transferase genotypes in testicular cancer survivors. J Clin Oncol. 2007;25:708–14. 13. Palodetto B, Postal M, Grignoli CR, Sartorato EL, Oliveira CA. Influence of glutathione s transferase on the ototoxicity caused by aminoglycosides. Braz J Otorhinolaryngol. 2010;76:306–9. 14. Peters U, Preisler-Adams S, Hebeisen A, Hahn M, Seifert E, Lanvers C, et  al. Glutathione S-transferase genetic polymorphisms and individual sensitivity to the ototoxic effect of cisplatin. Anticancer Drugs. 2000;11:639–43. 15. Pussegoda K, Ross CJ, Visscher H, Yazdanpanah M, Brooks B, Rassekh SR, et al. Replication of TPMT and ABCC3 genetic variants highly associated with cisplatin-induced hearing loss in children. Clin Pharmacol Ther. 2013;94:243–51. 16. Riedemann L, Lanvers C, Deuster D, Peters U, Boos J, Jürgens H, et al. Megalin genetic polymorphisms and individual sensitivity to the ototoxic effect of cisplatin. Pharmacogenomics J. 2008;8:23–8. 17. Yang JJ, Lim JY, Huang J, Bass J, Wu J, Wang C, et al. The role of inherited TPMT and COMT genetic variation in cisplatin-induced ototoxicity in children with cancer. Clin Pharmacol Ther. 2013;94:252–9. 18. Fernandez K, Wafa T, Fitzgerald TS, Cunningham LL. An optimized, clinically relevant mouse model of cisplatin-induced ototoxicity. Hear Res. 2019;375:66–74. https://doi.org/10.1016/j. heares.2019.02.006. Epub 2019 Feb 22. 19. Hagleitner MM, Coenen MJ, Patino-Garcia A, de Bont ES, Gonzalez-Neira A, Vos HI, et al. Influence of genetic variants in TPMT and COMT associated with cisplatin induced hearing loss in patients with cancer: two new cohorts and a meta-analysis reveal significant heterogeneity between cohorts. PLoS One. 2014;9:e115869.

Chapter 10

Balance and Vestibular Disorders in Children and Adolescents Joshua Gurberg, Henri Traboulsi, and Jacob R. Brodsky

Introduction Children with vestibular dysfunction will most commonly present with dizziness or imbalance, though a multitude of other symptoms and clinical presentations may also occur. Pediatric vestibular medicine is an area that has received little attention until quite recently. However, this new field of clinical practice and research has begun to grow rapidly as a result of increasing awareness of the significant negative impacts that vestibular dysfunction can have on children’s development and quality of life. Awareness of the importance of addressing vestibular function in the congenital hearing loss and concussion populations has played a major role in fuelling the recent expansion of this field. The establishment of numerous dedicated pediatric vestibular programs around the world in recent years has led to increasing awareness of the significant prevalence of vestibular disorders in children and has allowed research in this area to expand exponentially.

J. Gurberg Department of Otolaryngology—Head & Neck Surgery, Pediatric Surgery, Montreal Children’s Hospital, Montreal, QC, Canada e-mail: [email protected] H. Traboulsi Division of Pediatric Otolaryngology, Department of Surgery, Texas Children’s Hospital, Baylor College of Medicine, The Woodlands, TX, USA e-mail: [email protected] J. R. Brodsky (*) Department of Otolaryngology and Communication Enhancement, Boston Children’s Hospital, Boston, MA, USA Department of Otolaryngology, Harvard Medical School, Boston, MA, USA e-mail: [email protected] © The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 B. T. Crane et al. (eds.), Disorders of the Vestibular System, https://doi.org/10.1007/978-3-031-40524-2_10

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Dizziness and imbalance impact approximately 2.0% and 3.7% of children in the United States, respectively [1]. Other studies have found similar prevalences in other countries [2, 3]. However, awareness of the most common causes of vestibular symptoms in children and their appropriate work-up and management is greatly lacking. Data from the 2016 United States National Health Interview Survey demonstrated that 5.6% of a nationally-representative cross-sectional sample of 9247 children had reported symptoms of dizziness and/or imbalance [1]. However, none of those children were given a causative diagnosis of migraine by their health care providers, despite overwhelming evidence from the medical literature that migraine is the most common cause of pediatric dizziness [1, 4–13]. Thus, it is important that any pediatric provider that could be involved in the evaluation of children with dizziness or imbalance be aware of the general work-up and most common diagnoses to cause vestibular symptoms in children. Although migraine is the most common cause of dizziness in children, peripheral vestibular disorders are also quite common causes of dizziness and/or imbalance in children, as summarized in further detail later in this chapter, and vestibular impairment is particularly common in children with congenital hearing loss. Thus, pediatric otolaryngologists should also become familiar with how to appropriately manage these patients. Pediatric vestibular disorders are treatable, but only if the provider knows what they are treating and how best to manage it.

Embryology, Anatomy, Physiology, and Development In order to understand how best to evaluate and treat pediatric vestibular disorders, it is important to first have at least a general understanding of the development of the vestibular system. Embryologically speaking, the semicircular canals and otolith organs develop as part of the inner ear. This begins at 3 weeks gestational age (GA) when a focus of ectoderm, the otic placode, invaginates in the region of the embryonic hindbrain to form the otic pit and eventually the otic vesicle, which will form the membranous labyrinth [14]. At 5 weeks GA, the otic vesicle develops into an otocyst and is divided into cranial, intermediate, and caudal portions. The intermediate portion, or “utriculosaccular area,” is comprised of a saccular and utricular region, which form the vestibule and semicircular canals, respectively. At 6 weeks GA, the superior semicircular canal, utricle, and saccule develop, followed by the posterior canal, and finally the lateral canal at 21–23 weeks. This order of canal development explains why lateral canal dysplasia is the most common vestibular end organ anomaly, since it is the last to complete its development. Between 19 and 23 weeks GA, the membranous labyrinth is surrounded by the osseous labyrinth through ossification of the surrounding precartilage, which is derived from embryonic mesoderm and neural crest cells. The sensory epithelia of the vestibular system are the three cristae within the ampullated ends of the semicircular canals and the maculae of the otolith organs [14, 15]. These structures begin to develop at 3  weeks GA from otocyst ectoderm. By 7 weeks GA, otoconia and vestibular hair cells have begun to develop in these sensory regions, which first become active at 8–9 weeks. The vestibulocochlear nerve, which innervates these structures, develops from a collection of neural crest cells known as

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fascioacoustic primordium at 5 weeks gestation. The vestibulocochlear ganglia arise from otocyst ectoderm as well as neural crest cells and are divided into a superior division, innervating the superior semicircular canal, lateral semicircular canal, and the utricle, and an inferior division innervating the posterior semicircular canal and saccule. The remaining portion makes up the spiral ganglion of the cochlea. The vestibular system begins sensing linear and angular acceleration as early as 32 week GA. The vestibulo-ocular reflexes are functional at birth as evidenced by the presence of primitive newborn reflexes such as the dolls eye response. The absence of such reflexes may indicate a deficiency in the vestibular system. This system is also essential in normal motor development. The child should be able to lift their head by 3–4 months of age, sit by 6–7 months, pull to stand at 9 months, and walk at 12–14 months [16]. Failure to meet these milestones may indicate a problem with the vestibular system, though these delays can also be due to other areas of dysfunction. As the child meets these milestones and interacts more with his or her environment, the vestibular system continues to develop until fully mature at 15 years of age.

History The history and physical examination are generally the highest yield component of the medical evaluation in establishing a diagnosis and treatment plan for pediatric patients with vestibular symptoms. A common misconception is that most children are unable to provide an effective history regarding vestibular symptoms. We have anecdotally found that this is often not the case. Many children can actually provide a very helpful history, if the provider knows what to ask. Some general guidelines are provided in the following paragraphs to help optimize the efficacy and efficiency of this sometimes-challenging assessment. Firstly, it should be noted that there are generally two major categories of pediatric patients that present with vestibular complaints [1, 17]. Younger children more often present with imbalance or motor delay, often in the setting of congenital hearing loss, otitis media, or global developmental delay. Older children (grade school through adolescence) more often present with complaints of dizziness or vertigo, sometimes accompanied by imbalance, often in the setting of concussion or migraine. Although these categories are not mutually exclusive, it can be helpful to think in these general terms when acquiring the history, since the diagnoses to consider differ significantly between these two groups. For young children with imbalance, it is particularly important to ask about motor milestones, as summarized above, as well as about speech development and signs of hearing loss or otitis media [16]. Vision plays a particularly important role in balance in young children, so it is also essential to ask about signs/symptoms of visual impairment and to confirm that an optometric/ophthalmologic evaluation has been completed. Birth history is also important to discuss, including any perinatal infections that could suggest a diagnosis of neonatal cytomegalovirus infection or meningitis, significant hyperbilirubinemia that could have resulted in kernicterus, and perinatal antibiotic exposure that could have resulted in vestibulo/ototoxicity.

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Table 10.1  Dizziness history factors and common associated diagnoses Dizziness character

Lightheadedness/ Disequilibrium

Vertigo

Episode duration

Provoking factors

Associated symptoms

Seconds–minutes

Hours Days to weeks Weeks to months (or “constant”/chronic) Position changes/head movements

•  Hemodynamic intolerance/dysautonomia •  Panic disorder/anxiety • PPPD •  Acute vestibular syndrome (recovery phase) •  Vestibular migraine • BPPV • BPVC •  Acute vestibular syndrome (acute phase) • BPPV • BPVC •  Hemodynamic intolerance/dysautonomia •  Panic disorder/anxiety •  PPPD (symptom flares) •  Vestibular migraine •  Acute vestibular syndrome/vestibular neuritis • PPPD

• BPPV •  Hemodynamic intolerance/dysautonomia •  Vestibular migraine •  Acute vestibular syndrome/vestibular neuritis • PPPD Visual flow • PPPD Stress •  Vestibular migraine • PPPD •  Panic disorder/anxiety Lack of sleep, diet changes, •  Vestibular migraine menses Headache, photophobia, •  Vestibular migraine phonophobia, visual aura Tunnel vision, paresthesias, •  Panic disorder/anxiety tinnitus •  Hemodynamic intolerance/dysautonomia • PPPD Nausea/vomiting •  Vestibular migraine •  Acute vestibular syndrome/vestibular neuritis Hearing loss • Labyrinthitis

PPPD persistent postural perceptual dizziness, BPPV benign paroxysmal positional vertigo, BPVC benign paroxysmal vertigo of childhood

The history can be more challenging with children and adolescents presenting for evaluation of dizziness or vertigo. Both the child and the parent should participate in the discussion, whenever possible, as characterization of the subjective features of the symptoms is paramount. A structured intake questionnaire for vestibular patients can greatly improve efficiency in a busy clinic. The highest yield questions for these patients pertain to the character, timing, and provoking factors for the dizziness, as well as any associated symptoms. Table 10.1 outlines which of the most common causes of pediatric dizziness should be considered when particular

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responses are given regarding each of these factors. Parents may make inaccurate assumptions about what the child is experiencing, so direct involvement of the patient in the interview can be very helpful, when feasible.

Physical Examination Cooperation with examination and testing of younger children can be enhanced by saving invasive components for the end and by using games and light-up toys. The examination should include assessment of the ears, eyes, neurological function, balance, vestibulo-ocular reflex (VOR), and nystagmus. Gait and stance can often be observed during the interview in younger children, and older children should also be evaluated with eyes closed in Romberg, tandem, and one-leg stance positions. The single leg stance with eyes closed is a particularly useful screen for vestibular impairment, as it reduces the child’s ability to rely on other systems (vision and proprioception) to balance and forces them to use their vestibular inputs. Cushing and colleagues demonstrated that inability to maintain a single-leg stance with eyes closed for >3 s is highly sensitive and specific for predicting bilateral vestibular loss in children >3 years old with bilateral sensorineural hearing loss [18, 19]. The head impulse test (HIT) can be facilitated in toddlers and infants by having an assistant hold a light-up toy, sticker, or smartphone/tablet as a target for the child to focus on while the examiner performs the head thrusts. The presence of spontaneous nystagmus without fixation suggests that an uncompensated vestibular loss is present. Assessment of spontaneous and gaze-evoked nystagmus ideally should be performed both with and without fixation (using Frenzel or videonystagmography goggles), whenever possible, since visual fixation on a target will typically suppress nystagmus from peripheral vestibular dysfunction. Thus, if Frenzel or videonystagmography (VNG) goggles are not available, then it should be noted that nystagmus of peripheral etiology cannot be definitively ruled out. Evaluation of positional nystagmus should include bilateral Dix–Hallpike maneuvers, bilateral supine head-roll maneuvers, and a midline head-hang maneuver, as benign paroxysmal positional vertigo (BPPV) can affect any of the semicircular canals in pediatric patients [20, 21]. Providers should have a low threshold for performing positional testing, as BPPV in children is likely much more common than previously thought, but is often missed. VNG goggles should also be used for diagnostic positional maneuvers, if available, as their use significantly increases the sensitivity of this evaluation.

Vestibular Testing Indications for vestibular testing in children and adolescents are summarized in Table 10.2. Vestibular testing alone will not yield a diagnosis without a careful history and physical examination. Pediatric vestibular testing can be challenging, and

184 Table 10.2  List of indications for vestibular testing

J. Gurberg et al. •  •  •  •  •  •  •  •  • 

Differentiate vestibular from nonvestibular conditions Differentiate peripheral from central vestibular dysfunction Determine if vestibular loss is unilateral versus bilateral Confirm a suspected diagnosis Quantify degree and etiology of imbalance Planning vestibular rehabilitation strategies Assessing response to vestibular rehabilitation Evaluate for functional disorder Evaluate for fictitious disorder (malingering)

Table 10.3  Vestibular testing ages for senior author’s testing lab. Note that ages vary widely between different pediatric vestibular testing centers Minimum age 6 months

3 years 4 years 6 years 10 years

Tests •  Vestibular-evoked myogenic potentials (VEMP), cervical •  Videonystagmography (VNG) •  Rotary chair •  Vestibular-evoked myogenic potentials (VEMP), ocular •  Video head impulse testing (VHIT), horizontal canals •  Computerized dynamic posturography (sensory organization test) •  Video head impulse testing (VHIT), vertical canals •  Subjective visual vertical, static •  Caloric test •  Subjective visual vertical, dynamic

many adult vestibular testing centers will not test young children. Fortunately, the number of pediatric vestibular testing centers is steadily growing and some adult centers are willing to test younger patients with encouragement. In addition to the tests summarized below, audiometry is also a key component of the assessment of most pediatric patients with vestibular complaints, though it is not routinely necessary in adolescents with specific complaints of dizziness/vertigo in the absence of audiological or otological concerns. Age ranges for each test vary with each testing center. The ages at which each test can be performed at the senior author’s lab are summarized in Table 10.3, though the tests available and ages at which they can be done varies greatly between different testing centers. Note that both the rotary chair and caloric tests only assess the lateral canal VOR, but the latter test is avoided in children when possible, as it can induce nausea/vomiting and can be difficult for young children to tolerate. It should also be noted that the interpretation of vestibular testing results is beyond the scope of this chapter and can be found in other resources on this topic [11, 16, 22–25]. • Videonystagmography (VNG): Video-goggles are used to assess for spontaneous, gaze-evoked, optokinetic, and positional nystagmus, as well as pursuits and saccades. Caloric testing is included in the adult VNG battery, but it is often avoided in children. In the absence of spontaneous nystagmus or BPPV, the yield of VNG in children is generally low. Horizontal and/or torsional nystagmus without fixa-

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tion suggests an uncompensated peripheral vestibular loss, while vertical or direction-changing nystagmus, particularly when present with and without fixation, suggest a central cause. Abnormal saccades and pursuits also suggest a central vestibular and/or oculomotor disorder. Caloric Test: Caloric testing typically involves sequential, binaural, bithermal (warm and cold) water irrigation of the ear canals, though variations of increased tolerance but decreased sensitivity are available (e.g., air, monothermal, monaural). A reduced vestibular response (or unilateral weakness) score is calculated, which indicates impairment of the ipsilateral horizontal canal if greater than a designated set value (usually 20%). This test is often difficult to perform in young children and can induce nausea/vomiting, so it is generally avoided in pediatric patients whenever possible. Ice water calorics can be helpful to confirm a suspected diagnosis of vestibular areflexia in children with congenital hearing loss. Rotary Chair Test: This test evaluates the horizontal canal VOR and is the gold standard for diagnosing bilateral vestibular loss. The child is rotated side-to-side in an arc at varying frequencies in a dark room or cylindrical enclosure. The VOR response is tracked using an infrared camera in young children and with VNG goggles in older children (typically 4 years of age and older). Computer software calculates VOR gain, phase lead, and asymmetry scores, which can collectively be used to determine if a child has VOR impairment of the lateral canal on the left and right sides. Young children can sit in a parents lap or in a car seat for this test. An infrared camera mounted to the chair can be used in children who are too small to wear goggles. Video Head Impulse Test (VHIT): VHIT objectively evaluates the HIT using VNG goggles with an accelerometer. It can evaluate each semicircular canal individually and is generally better tolerated than caloric or rotary chair testing, but is of limited sensitivity for mild vestibular losses [23]. Younger children (2° to one side averaged over multiple trials suggests an ipsilateral peripheral vestibular loss involving the utricle [22, 26]. Although abnormalities on SVV can also be indicative of acute central vestibular losses (mostly cerebrovascular accidents), such events are very

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rare in children, making this test a more consistent assessment of peripheral vestibular function in children than in adults. This test requires active participation of the patient and is generally difficult for children younger than 7 years of age to perform reliably. Dynamic variations of this test exist, which increase its sensitivity and specificity, but are very difficult for children and even many adolescents to tolerate. • Computerized dynamic posturography (CDP): Sway is evaluating using a force plate during different balance conditions allowing objective evaluation of balance compared to age-specific norms and a breakdown of balance impairment into visual, vestibular, and somatosensory components. Children less than 4 years of age are often unable to fit into the harness or follow the instructions for this test.

Pediatric Vestibular Disorders The relative prevalence of causes of pediatric dizziness and imbalance varies between studies, though it is well-accepted that migraine represents the most common cause. Table 10.4 shows a list of the most common causes from a recent study of >1000 patients seen for dizziness and/or imbalance at the senior author’s pediatric vestibular program [17]. Notably, although the majority of cases in this study were found to be migraine in origin, a large proportion were also due to peripheral vestibular dysfunction and other causes. Of particular note is that BPPV may be more common in children than previously recognized. Also notable is the fact that there are many nonvestibular causes of dizziness and imbalance in children, as well. This study also found that nearly half of patients had more than one concurrent causative diagnosis. In particular, the diagnoses of vestibular migraine, BPPV, and persistent postural perceptual dizziness (PPPD) were found to frequently cluster together in many patients, with BPPV and PPPD likely being secondary phenomena to vestibular migraine, especially in adolescent females. For the purposes of organization in this chapter, the different diagnoses will be broken down into otological disorders, neurological disorders, autonomic dysfunction, and functional/psychological disorders. Notably, many optometric/ophthalmologic conditions can also

Table 10.4 Relative prevalence of most common causes of pediatric dizziness (in patients without history of concussion (n = 757)) [17]

Diagnosis 1. Vestibular migraine 2. Benign paroxysmal positional vertigo (BPPV) 3. Primary dysautonomia 4. Persistent postural perceptual dizziness (PPPD) 5. Panic/anxiety disorder 6. Benign paroxysmal vertigo of childhood (BPVC) 7. Acute vestibular syndrome/vestibular neuritis

% 31.0 19.9 14.0 12.7 11.6 7.7 6.5

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cause dizziness and imbalance, but are beyond the scope of this chapter. Only the most common causes of pediatric dizziness and imbalance are included in this chapter, and this list is by no means exhaustive.

Otological Sensorineural Hearing Loss A large proportion of children with sensorineural hearing loss (SNHL) have vestibular impairment with associated imbalance and motor delay [27–30]. Many causes of pediatric hearing loss are known to cause significant vestibular impairment, while many that have previously been thought to not cause vestibular impairment are now being found to have vestibular impacts in many cases. This is also important to consider, because cochlear implantation can have variable impacts on vestibular function and balance in children [31, 32]. It should also be noted that Ménière’s disease is very rare in children, despite being one of the most common causes of vertigo in adults. Some of the most common congenital hearing loss disorders to cause concurrent vestibular impairment are summarized below. • Enlarged vestibular aqueduct (EVA) syndrome: An enlarged vestibular aqueduct is the most common inner ear malformation associated with sensorineural hearing loss [33]. Although less common than hearing loss, a vestibular deficit can be present with EVA2. Children can present with imbalance and poor coordination. EVA is often an isolated finding, but can also be associated with other ear anomalies, or part of syndromes. It can be sporadic or due to mutations in the SLC26A4 gene, which causes Pendred syndrome when mutations are homozygous. Patients with EVA can have progressive or fluctuating hearing loss and sometimes also have episodic vertigo. • Usher syndrome: There are three types of Usher syndrome, which are all characterized by SNHL and retinal degeneration. Type 1 is associated with congenital vestibular areflexia, type 2 typically has no (or minimal) vestibular dysfunction, and type 3 has variable and often late-onset vestibular dysfunction [34]. • CHARGE syndrome: The acronym for CHARGE refers to its most common associated anomalies of eye Colobomas, Heart defects, choanal Atresia, growth Retardation, Genitourinary anomalies, and Ear anomalies. It is most commonly due to a mutation in the CHD7 gene. Imbalance and vestibular dysfunction is common due to the presence of inner ear anomalies (often completely absent semicircular canals) in addition to the possible presence of cerebellar anomalies. CHARGE patients also frequently have SNHL that can be severe to profound [35]. • Congenital cytomegalovirus (CMV): Perinatal infection with CMV can cause either isolated SNHL or a constellation of multiple anomalies, including global developmental delay, microcephaly, and visual impairment. Peripheral vestibular impairment is relatively common in congenital CMV, particularly in the setting of SNHL, and cerebellar dysfunction can also occur, further impacting balance [36].

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• Cogan’s syndrome: This rare auto-inflammatory condition typically presents in adolescence and causes progressive uveitis that can result in blindness along with SNHL and vestibular impairment with associated vertigo. It can often be rapidly progressive, but can be treated with immune-modulator therapy, so prompt evaluation by an Ophthalmologist and Rheumatologist is essential whenever this condition is suspected [37]. Middle Ear Dysfunction Recurrent acute and/or chronic otitis media has been demonstrated to negatively impact balance in children, though the exact mechanism for this effect is yet to be definitely established [38, 39]. Tympanostomy tube insertion typically yields resolution of balance impairment, but there is increasing evidence that long-standing middle ear effusions can have more long-standing impacts on vestibular function [40]. Middle ear dysfunction can also rarely lead to complications that can further impact balance and vestibular function, such as labyrinthitis (see below), cholesteatoma with labyrinthine fistula, or meningitis. Benign Paroxysmal Positional Vertigo (BPPV) BPPV is due to the displacement of otoconia from the utricle into one or more of the semicircular canals. This causes episodic vertigo with movements of the head within the plane of the affected canal. Although less common than in the adult population, BPPV has been found to be more common than previously thought in children, and may impact as many as one in five children with dizziness and as many as one in three with postconcussive dizziness [16, 17, 20, 21, 41]. However, it should be noted that BPPV in children and adolescents is frequently a secondary condition, particularly in conjunction with concussion, vestibular migraine, and acute vestibular syndrome (vestibular neuritis). Children seem to more commonly have superior canal, lateral canal, and multiple canal involvement compared to adults [20, 21]. Diagnostic maneuvers are used to diagnose the condition and to determine the affected canal(s), and then therapeutic maneuvers can be performed in the office to treat it. This can often be done with an appropriately-trained vestibular physical therapist, if the treating clinician does not have adequate experience to do so. Labyrinthitis and Vestibular Neuritis (Acute Vestibular Syndrome) Vestibular neuritis typically causes acute onset vertigo with nausea, vomiting, and imbalance that can last for several days during its acute phase. This is followed by a recovery phase that can last for weeks where patients experience milder disequilibrium and imbalance. It is sometimes preceded by an upper

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respiratory tract infection, but this is certainly not ubiquitous. It is thought to be viral in origin, but this has still not been definitely established as the etiology of all cases, and some cases may even be related to vestibular migraine, hence the newer preferred term of “acute vestibular syndrome” [42]. Vestibular rehabilitation is the most effective treatment, though steroids have been demonstrated in some studies to be beneficial if given early on in the course of the illness [43]. Labyrinthitis causes a similar presentation to vestibular neuritis, but also causes hearing loss that can often be permanent, but may improve gradually over time. Labyrinthitis can sometime occur as a complication of middle ear disease, so a thorough ear examination and appropriate management of any concurrent middle ear dysfunction is paramount.

Neurological Vestibular Migraine Vestibular migraine is a migraine variant that causes episodic vertigo or motion intolerance along with concurrent migrainous symptoms. It is the most common cause of episodic vertigo in both children and adults and is diagnosed by clinical criteria (Table  10.5) [44]. Notably, migrainous symptoms must be present with vertigo episodes (e.g., light or sound sensitivity, visual aura, etc.), but headaches do not necessarily need to be concurrent with the vertigo episodes. First line treatment in pediatric patients consists of migraine hygiene (e.g., optimization of sleep, diet, hydration, stress management), though medical therapy with rescue medications and/or daily preventative medications is also effective and often necessary [4].

Table 10.5  Diagnostic criteria for vestibular migraine, International Classification of Headache Disorders, third Edition [67] A. At least five episodes fulfilling criteria C and D B. A current or past history of migraine without aura or migraine with aura C. Vestibular symptoms of moderate or severe intensity, lasting between 5 min and 72 h D. At least half of episodes are associated with at least one of the following three migrainous features:  1. Headache with at least two of the following four characteristics:    (a) Unilateral location    (b) Pulsating quality    (c) Moderate or severe intensity    (d) Aggravation by routine physical activity  2. Photophobia and phonophobia  3. Visual aura E. Not better accounted for by another ICHD-3 diagnosis or by another vestibular disorder

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Benign Paroxysmal Vertigo of Childhood (BPVC) BPVC is a pediatric migraine variant/precursor disorder that causes episodes of room-spinning vertigo that typically last for minutes at a time [45]. There is often no other associated symptoms and headaches do not typically occur with this condition. Episodes are also often accompanied by nystagmus, imbalance, and/or fearfulness. Children are asymptomatic between episodes. Age of onset is typically between 3 and 6  years of age. The condition usually resolves approximately 2–3  years after onset [46], but children with this condition have a higher risk of developing migraines in adolescence or adulthood than the general population. A family history of migraine is also common with this condition. Treatment is not usually necessary, since episodes are usually very brief and sporadic, but the medication cyproheptadine may be effective as daily preventative therapy in cases where episodes are very frequent, prolonged, or severe [45]. Benign Paroxysmal Torticollis of Infancy (BPTI) BPTI causes recurrent episodes of head tilting (torticollis) that can last from hours to days and occur every few days to weeks. It typically starts in infancy and almost ubiquitously resolves by 2–3  years of age [45]. It is typically accompanied by some migrainous features (e.g., light or sound sensitivity, irritability, nausea) as well as imbalance. Most children are asymptomatic between symptom flares. It does not require treatment, but the medication cyproheptadine may be effective as daily preventative therapy in cases where episodes are very frequent, prolonged, or severe [45]. It should also be noted that EVA can present with episodic torticollis, though usually without concurrent migrainous symptoms, and the torticollis episodes may precede the diagnosis of hearing loss, so audiological monitoring should be considered for children with paroxysmal torticollis, even when a migraine etiology is suspected [47].

Autonomic Dysfunction Autonomic dysfunction (a.k.a., dysautonomia) is a common cause of dizziness symptoms in the adolescent age group [17], and is typically a secondary phenomenon that can be triggered by multiple different primary conditions, including cardiac conditions, dehydration, nutritional deficiencies, acute/chronic infection, endocrine disorders, anemia, electrolyte deficiency, and anxiety. Thus, a thorough medical work-up may be warranted when dysautonomia is suspected and a clear source is not evident. Hemodynamic intolerance is a common primary cause of dysautonomia symptoms that are sensitive to orthostatic changes and physical exertion [48]. This is particularly common after concussion [17, 49]. In many adolescents this may also be due to postural orthostatic tachycardia syndrome (POTS), which may require a work-up by a cardiologist to diagnosis and treat. Anxiety and/

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or chronic stress are also common triggers of autonomic dysregulation, so chronic dizziness from other causes can often trigger secondary dysautonomia leading to different types of dizziness in a single patient [17]. The dizziness with dysautonomia is typically a lightheadedness, though room-spinning vertigo is sometimes also described. Concurrent symptoms during episodes include tunnel vision, tinnitus, decreased hearing, paresthesias in the hands/feet, chest tightness, palpitations, cognitive impairment, and sometimes syncope. With POTS or hemodynamic intolerance, the first-line treatment is optimizing hydration and increasing salt/electrolyte intake. Physical therapy with orthostatic/hemodynamic retraining as well as reconditioning therapy can also be beneficial [50]. When these treatments are unsuccessful, then medications to increase peripheral vascular tone can be helpful, such as midodrine or fludrocortisone, which are typically prescribed by a cardiologist. Treatments for secondary autonomic dysfunction are specific to the causative condition (e.g., anxiety management, correction of hormone/electrolyte derangements, etc.) and are typically outside of the realm of practice of the pediatric otolaryngologist.

Functional/Psychological Panic Disorder Panic attacks are a relatively common cause of episodic vertigo, and can occur in patients without a known history of baseline anxiety. These episodes are typically similar to the episodes seen in autonomic dysfunction, as summarized in the above section, though are typically also accompanied by hyperventilation with associated carbon dioxide retention, which can exacerbate the dizziness symptoms. Treatments for panic attacks include psychological therapies (e.g., cognitive behavioral therapy, biofeedback) and medical therapies (e.g., serotonin reuptake inhibitors, beta blockers, etc.). Persistent Postural Perceptual Dizziness (PPPD) PPPD is a functional neurological disorder (FND) that causes chronic dizziness that is reported as being either constant or intermittent throughout the majority of the day along with frequent symptom flares associated with particular triggers [51–53]. Common triggers include standing/walking and head movements. Additionally, patients are highly sensitive to settings that incorporate a degree of “visual flow” (e.g., grocery stores, shopping malls, hallways, etc.) and big, open spaces. Patients typically also report a constant fear of falling, but rarely exhibit any actual falls. It is typically triggered by an initial precipitating vestibular disorder (e.g., BPPV, vestibular migraine, concussion), and often can occur concurrently with the ongoing primary vestibular condition. The diagnostic criteria for this condition are summarized in

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Table 10.6  Bárány Society consensus criteria for the diagnosis of persistent postural perceptual dizziness [53]. Patients must meet all five of criteria A through E Criteria Additional details A. One or more symptoms of dizziness, 1. Symptoms last for prolonged (hours-long) unsteadiness, or nonspinning vertigo are periods of time, but may wax and wane in present on most days for 3 months or severity. more. 2. Symptoms need not be present continuously throughout the entire day. 1. Upright posture. B. Persistent symptoms occur without specific provocation, but are exacerbated 2. Active or passive motion without regard to by three factors: direction or position. 3. Exposure to moving visual stimuli or complex visual patterns. C. The disorder is precipitated by 1. When the precipitant is an acute or episodic conditions that cause vertigo, condition, symptoms settle into the pattern of unsteadiness, dizziness, or problems criterion A as the precipitant resolves, but they with balance including acute, episodic, may occur intermittently at first, and then or chronic vestibular syndromes, other consolidate into a persistent course. neurologic or medical illnesses, or 2. When the precipitant is a chronic syndrome, psychological distress. symptoms may develop slowly at first and worsen gradually. D. Symptoms cause significant distress or functional impairment. E. Symptoms are not better accounted for by another disease or disorder.

Table 10.6. PPPD is a relatively new umbrella term that incorporates a number of vestibular FND conditions that previously went by other names, including chronic subjective dizziness, space motion discomfort, visual vertigo, and phobic postural vertigo. In the pediatric age group it most commonly impacts adolescents, particularly females [51]. Pre-existing anxiety or depression are risk factors for developing PPPD, but it can also occur in people without any pre-­existing mental health conditions. However, secondary anxiety from the chronic dizziness and confusion between visual and vestibular inputs to maintain equilibrium is ubiquitous. Treatment for PPPD includes habituation-based vestibular physical therapy, cognitive behavioral therapy, and often also selective serotonin reuptake inhibitor (SSRI) or serotonin norepinephrine reuptake inhibitor (SNRI) medications. It is a challenging condition to treat and requires close, long-term follow-up to achieve successful recovery.

Vestibular Rehabilitation Vestibular rehabilitation is a core, workhorse treatment approach in the management of a majority of vestibular conditions that affect children and adolescents. Vestibular rehabilitation is typically conducted by a specially-trained physical therapist, though some occupational therapists also are appropriately trained in this area, as well. It

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involves a multitude of different strategies that must be tailored to the specific condition(s) that a given patient is afflicted by, as well as a given patient’s functional limitations, symptoms, triggers, and goals [16]. For this reason, a comprehensive evaluation prior to treatment is of the utmost importance, which should include an in-depth review of the medical history, developmental history, symptoms, and available vestibular testing. While the otolaryngologist’s assessment will focus more on the vestibular and the oculomotor systems, the physical therapist has the appropriate tools for a detailed assessment of the balance system as a whole, including the musculoskeletal system and the patient’s gait. Symptom questionnaires [54, 55] as well as balance and gait assessment tools [56, 57] are available for use in children, and are useful to monitor response to treatment. A course of vestibular rehabilitation typically lasts for a few weeks, but may be shorter or longer, depending on what is being treated and the patient’s response. Usually, the patient has weekly sessions with the therapist along with exercises to work on at home in between the visits. General categories of vestibular rehabilitation treatment approaches are summarized below: • Restoration—The goal of this approach is to restore an impaired vestibular system. This approach be used when residual function is present. This approach is primarily effective for partial, incompletely compensated, unilateral, peripheral vestibular losses. Much of this approach focuses on vestibulo-ocular reflex retraining exercises with combinations of visual fixation/tracking with head and/ or body movements. • Adaptation—The goal of this approach is to induce long-term changes in the neuronal response to head movements with the goal of reducing symptoms and normalizing gaze and postural stability. This approach is typically done in conjunction with restorative therapy and includes vestibulo-ocular reflex training and postural/balance retraining. • Habituation—This approach is primarily used for treating PPPD and similar conditions and consists of gradual, systematically increasing exposure to provocative stimuli to facilitate tolerance to such triggers. Common triggers involved in habituation therapy include position changes, head movements, and visual flow stimuli. • Substitution—This approach is typically reserved for patients with severe or complete bilateral vestibular loss (areflexia). The child is trained to use nonvestibular sensory systems to maintain balance and visual stability, including proprioception, vision, smooth pursuit, saccades, and/or assistive devices. Patients with bilateral vestibular areflexia can be especially challenging to rehabilitate, particularly since many of them may also have conditions that predispose them to concurrent visual compromise (e.g., CHARGE, Usher, CMV, etc.). Thus, this type of rehabilitation is often done over many months or years, in contrast to the other therapeutic approaches above that can often be highly effective in a matter of weeks. • Repositioning maneuvers—Many vestibular physical therapists are also experienced in performing repositioning maneuvers to treat BPPV, as discussed in further detail in the section on BPPV above.

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Other Treatments Although vestibular rehabilitation is generally considered to be the core treatment for most pediatric vestibular disorders, many of the most common vestibular conditions in children may not benefit from physical therapy (e.g., vestibular migraine) or may require a multimodal approach that includes both physical therapy and other, concurrent treatments.

Medication Many pediatric vestibular disorders benefit from pharmacological therapies, though typically these are ideally combined with other treatments. The use of medications to treat specific vestibular disorders in children are summarized in further detail under the section for each respective condition above. In particular, vestibular migraine is often treated with a combination of rescue medications, such as the triptans, and daily, preventative medications, such as cyproheptadine, tricyclic antidepressants, SNRI medications, beta blockers, and topiramate. PPPD is most effectively treated with a multimodal approach that includes SSRI/SNRI therapy along with vestibular rehabilitation and CBT. Hemodynamic intolerance also sometimes benefits from treatment with midodrine or fludrocortisone, when response to optimizing hydration and electrolyte intake is unsuccessful.

Surgery The need for surgical intervention with pediatric vestibular disorders is uncommon. Balance impairment in the setting of chronic middle ear dysfunction or recurrent acute otitis media can improve significantly after tympanostomy tube placement [38, 39]. Superior semicircular canal dehiscence is effectively treated with semicircular canal occlusion or resurfacing, either through a transmastoid or middle cranial fossa approach [58, 59]. Traumatic perilymphatic fistulas that do not require spontaneously will require middle ear exploration to confirm the diagnose and to repair to leak, which can typically be performed transcanal, often with an endoscopic approach [60]. Treatment resistant BPPV that does not resolve with repositioning maneuvers may require transmastoid occlusion of the offending canal to resolve, particularly when cupulolithiasis is suspected [61]. Although semicircular canal occlusion for treatment resistant BPPV has not been described in the medical literature in the pediatric population, the senior author has had good success with this procedure in two pediatric patients with treatment resistant BPPV as of the time of this writing. Rarely, Chiari malformations may cause balance impairment or even dizziness that may improve with surgical decompression by a neurosurgeon [11, 16]. Also, it has been

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demonstrated that children with severe vestibular impairment and poor balance in the setting of bilateral congenital SNHL may benefit greatly from cochlear implantation not only from a hearing standpoint, but also in terms of balance function [62]. Lastly, vestibular implants are currently showing great promise in adult human trials, and they will hopefully soon be an option for children with vestibular areflexia, as well [63].

Alternative Therapies Numerous alternative therapies play a vital role in the management of many pediatric vestibular disorders, as covered in further detail under the sections for each of these specific conditions above. Vestibular migraine can benefit greatly from “migraine hygiene,” including trigger identification/avoidance and optimizing sleep, hydration, diet and stress management. Hydration and electrolyte optimization are also the first line management strategies for hemodynamic intolerance. Magnesium supplements may also be helpful for patients with vestibular migraine, though this has not yet been well studied in the pediatric population [64]. CBT plays a central role in the management of PPPD and panic disorder, while it may also be beneficial for many patients with migraine [65, 66].

Accommodations and Follow-Up Many children with chronic vestibular disorders may benefit from accommodations in the classroom in order to optimize their ability to learn effectively. Children with VOR impairments may struggle with reading and with seeing activities at the front of the classroom. Children with balance impairment may have difficulty with navigating around the classroom or between classes, particularly in busy hallways. Children with PPPD or vestibular migraine may have frequent dizziness flares in the classroom and require breaks for recovery or even partial home schooling initially with gradual upward titration of in-person learning, as tolerated. Some examples of accommodations that may be beneficial for children with vestibular disorders are summarized in Table 10.7. Although the pediatric otolaryngologist often functions in a consultative role for the child with dizziness or imbalance, it is important to ensure adequate follow-up with either the otolaryngologist or an alternative appropriate provider (e.g., primary care physician or neurologist) to confirm that ongoing improvements are made and that medications are being tolerated appropriately. Although BPPV may resolve with maneuvers, many children may experience recurrences or may not resolve with initial maneuver attempts. Their symptoms also could persist after successful maneuvers if concurrent conditions, such as PPPD, vestibular migraine, or peripheral vestibular losses, are present. Vestibular migraine is a chronic condition that consistently requires long-term management and support. PPPD will often reach a

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Table 10.7  School accommodations that may be beneficial for children with chronic vestibular disorders •  Allowing use of a laptop or tablet or printed materials to convey materials presented at front of class •  Sitting in the middle or back of classroom to minimize arc of head movements between desk and front of class (unless concurrent hearing loss warrants front row seating) •  Providing extra time for taking tests and for completing assignments, including standardized exams •  Allowing brief breaks on a regular basis, if needed •  Minimizing excess sensory stimulation in the classroom (noise, unnecessary visual stimuli, etc.), whenever possible •  Minimizing need to participate in classroom activities that require moving about the classroom, whenever possible •  Maintaining a structured classroom setting with predictable routines and minimal distraction •  Using an enlarged font [16–18] and increased space between printed lines, when feasible •  Providing extra time for moving between classes •  Permitting transition between classes a few minutes early and/or late relative to classmates to walk next class, as busy/high traffic hallways can exacerbate dizziness and imbalance •  Facilitating transition between classes with a trusted friend and/or staff member, if needed and appropriate

point of complete recovery, but this can sometimes takes months or even years to occurs, so it is best managed like a chronic condition with relatively frequent follow-­up with a vestibular specialist to confirm that appropriate treatment strategies are being adhered to.

Conclusion Vestibular symptoms are surprisingly common in the pediatric population. Pediatric dizziness and imbalance are often multifactorial, so a multidisciplinary approach is often warranted. Although migraine is the most common cause of dizziness in children, many other conditions should also be considered. Vestibular testing can be helpful in some cases, but a careful history and physical examination alone is usually adequate to arrive at an accurate diagnosis. Vestibular disorders in children and adolescents can be effectively treated once diagnoses are reliably determined. Vestibular physical therapy is the core management strategy for most pediatric vestibular conditions, though medications, surgery, and/or alternative therapies are often warranted, as well.

References 1. Brodsky JR, Lipson S, Bhattacharyya N. Prevalence of pediatric dizziness and imbalance in the United States. Otolaryngol Head Neck Surg. 2020;162(2):241–7.

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2. Niemensivu R, Pyykko I, Wiener-Vacher SR, Kentala E. Vertigo and balance problems in children—an epidemiologic study in Finland. Int J Pediatr Otorhinolaryngol. 2006;70(2):259–65. 3. Humphriss RL, Hall AJ.  Dizziness in 10 year old children: an epidemiological study. Int J Pediatr Otorhinolaryngol. 2011;75(3):395–400. 4. Brodsky JR, Cusick BA, Zhou G. Evaluation and management of vestibular migraine in children: experience from a pediatric vestibular clinic. Eur J Paediatr Neurol. 2016;20(1):85–92. 5. Choung YH, Park K, Moon SK, Kim CH, Ryu SJ.  Various causes and clinical characteristics in vertigo in children with normal eardrums. Int J Pediatr Otorhinolaryngol. 2003;67(8):889–94. 6. Erbek SH, Erbek SS, Yilmaz I, et al. Vertigo in childhood: a clinical experience. Int J Pediatr Otorhinolaryngol. 2006;70(9):1547–54. 7. Gioacchini FM, Alicandri-Ciufelli M, Kaleci S, Magliulo G, Re M. Prevalence and diagnosis of vestibular disorders in children: a review. Int J Pediatr Otorhinolaryngol. 2014;78(5):718–24. 8. Jahn K. Vertigo and dizziness in children. Handb Clin Neurol. 2016;137:353–63. 9. Lee JD, Kim CH, Hong SM, et  al. Prevalence of vestibular and balance disorders in children and adolescents according to age: a multi-center study. Int J Pediatr Otorhinolaryngol. 2017;94:36–9. 10. McCaslin DL, Jacobson GP, Gruenwald JM.  The predominant forms of vertigo in children and their associated findings on balance function testing. Otolaryngol Clin N Am. 2011;44(2):291–307, vii. 11. O’Reilly RC, Greywoode J, Morlet T, et al. Comprehensive vestibular and balance testing in the dizzy pediatric population. Otolaryngol Head Neck Surg. 2011;144(2):142–8. 12. Wang A, Zhou G, Lipson S, Kawai K, Corcoran M, Brodsky JR. Multifactorial characteristics of pediatric dizziness and imbalance. Laryngoscope. 2021;131(4):E1308–14. 13. Wiener-Vacher SR. Vestibular disorders in children. Int J Audiol. 2008;47(9):578–83. 14. Wareing MJ, Lalwani AK, Anwar AA, Jackler RK. Development of the ear. In: Rosen CA, Johnson JT, editors. Bailey’s head and neck surgery: otolaryngology. 5th ed. Philadelphia, PA: Lippincott Williams & Wilkins; 2014. p. 2239–52. 15. Della Santina CC, Carey JP. Principles of applied vestibular physiology. In: Flint PW, Haughey BH, et al., editors. Cumming’s otolaryngology - head & neck surgery. 7th ed. Philadelphia, PA: Elsevier; 2020. p. 2466–94. 16. O’Reilly R, Morlet T, Brodsky JR, Cushing SL. Manual of pediatric balance disorders. 2nd ed. San Diego, CA: Plural Publishing, Inc.; 2020. 17. Wang A, Zhou G, Lipson S, Kawai K, Corcoran M, Brodsky JR. Multifactorial characteristics of pediatric dizziness and imbalance. Laryngoscope. 2020;131:E1308–14. 18. Cushing SL, Papsin BC. Taking the history and performing the physical examination in a child with hearing loss. Otolaryngol Clin N Am. 2015;48(6):903–12. 19. Oyewumi M, Wolter NE, Heon E, Gordon KA, Papsin BC, Cushing SL.  Using balance function to screen for vestibular impairment in children with sensorineural hearing loss and cochlear implants. Otol Neurotol. 2016;37(7):926–32. 20. Brodsky JR, Lipson S, Wilber J, Zhou G. Benign paroxysmal positional vertigo (BPPV) in children and adolescents: clinical features and response to therapy in 110 pediatric patients. Otol Neurotol. 2018;39(3):344–50. 21. Wang A, Zhou G, Kawai K, O’Brien M, Shearer AE, Brodsky JR. Benign paroxysmal positional vertigo in children and adolescents with concussion. Sports Health. 2021;13(4):380–6. 22. Brodsky JR, Cusick BA, Kenna MA, Zhou G. Subjective visual vertical testing in children and adolescents. Laryngoscope. 2016;126(3):727–31. 23. Hamilton SS, Zhou G, Brodsky JR. Video head impulse testing (VHIT) in the pediatric population. Int J Pediatr Otorhinolaryngol. 2015;79(8):1283–7. 24. Zhou G, Goutos C, Lipson S, Brodsky J. Clinical significance of spontaneous nystagmus in pediatric patients. Int J Pediatr Otorhinolaryngol. 2018;111:103–7. 25. Zhou G, Dargie J, Dornan B, Whittemore K. Clinical uses of cervical vestibular-evoked myogenic potential testing in pediatric patients. Medicine (Baltimore). 2014;93(4):e37.

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26. Brodsky JR, Cusick BA, Kawai K, Kenna M, Zhou G. Peripheral vestibular loss detected in pediatric patients using a smartphone-based test of the subjective visual vertical. Int J Pediatr Otorhinolaryngol. 2015;79(12):2094–8. 27. Cushing SL, Gordon KA, Rutka JA, James AL, Papsin BC. Vestibular end-organ dysfunction in children with sensorineural hearing loss and cochlear implants: an expanded cohort and etiologic assessment. Otol Neurotol. 2013;34(3):422–8. 28. Cushing SL, Papsin BC, Rutka JA, James AL, Gordon KA. Evidence of vestibular and balance dysfunction in children with profound sensorineural hearing loss using cochlear implants. Laryngoscope. 2008;118(10):1814–23. 29. Rine RM, Braswell J, Fisher D, Joyce K, Kalar K, Shaffer M. Improvement of motor development and postural control following intervention in children with sensorineural hearing loss and vestibular impairment. Int J Pediatr Otorhinolaryngol. 2004;68(9):1141–8. 30. Rine RM, Cornwall G, Gan K, et al. Evidence of progressive delay of motor development in children with sensorineural hearing loss and concurrent vestibular dysfunction. Percept Mot Skills. 2000;90(3 Pt 2):1101–12. 31. De Kegel A, Maes L, Van Waelvelde H, Dhooge I. Examining the impact of cochlear implantation on the early gross motor development of children with a hearing loss. Ear Hear. 2015;36(3):e113–21. 32. Jang JH, Kim H, Choo OS, Park HY, Choung YH. Changes in vestibular symptoms and function after cochlear implantation: relevant factors and correlations with residual hearing. Clin Exp Otorhinolaryngol. 2020;14:69. 33. Gopen Q, Zhou G, Whittemore K, Kenna M. Enlarged vestibular aqueduct: review of controversial aspects. Laryngoscope. 2011;121(9):1971–8. 34. Tsang SH, Aycinena ARP, Sharma T.  Ciliopathy: usher syndrome. Adv Exp Med Biol. 2018;1085:167–70. 35. Hsu P, Ma A, Wilson M, et  al. CHARGE syndrome: a review. J Paediatr Child Health. 2014;50(7):504–11. 36. Goderis J, De Leenheer E, Smets K, Van Hoecke H, Keymeulen A, Dhooge I. Hearing loss and congenital CMV infection: a systematic review. Pediatrics. 2014;134(5):972–82. 37. Shamriz O, Tal Y, Gross M.  Autoimmune inner ear disease: immune biomarkers, audiovestibular aspects, and therapeutic modalities of Cogan’s syndrome. J Immunol Res. 2018;2018:1498640. 38. Casselbrant ML, Villardo RJ, Mandel EM. Balance and otitis media with effusion. Int J Audiol. 2008;47(9):584–9. 39. Cohen MS, Mandel EM, Furman JM, Sparto PJ, Casselbrant ML. Tympanostomy tube placement and vestibular function in children. Otolaryngol Head Neck Surg. 2011;145(4):666–72. 40. da Costa Monsanto R, Erdil M, Pauna HF, et al. Pathologic changes of the peripheral vestibular system secondary to chronic otitis media. Otolaryngol Head Neck Surg. 2016;155(3):494–500. 41. Brodsky JR, Shoshany TN, Lipson S, Zhou G. Peripheral vestibular disorders in children and adolescents with concussion. Otolaryngol Head Neck Surg. 2018;159(2):365–70. 42. Kerber KA. Acute vestibular syndrome. Semin Neurol. 2020;40(1):59–66. 43. Le TN, Westerberg BD, Lea J. Vestibular neuritis: recent advances in etiology, diagnostic evaluation, and treatment. Adv Otorhinolaryngol. 2019;82:87–92. 44. Headache Classification Committee of the International Headache Society. The international classification of headache disorders, 3rd edition (beta version). Cephalalgia. 2013;33(9):629–808. 45. Brodsky J, Kaur K, Shoshany T, Lipson S, Zhou G.  Benign paroxysmal migraine variants of infancy and childhood: transitions and clinical features. Eur J Paediatr Neurol. 2018;22(4):667–73. 46. Batuecas-Caletrio A, Martin-Sanchez V, Cordero-Civantos C, et al. Is benign paroxysmal vertigo of childhood a migraine precursor? Eur J Paediatr Neurol. 2013;17(4):397–400. 47. Brodsky JR, Kaur K, Shoshany T, et al. Torticollis in children with enlarged vestibular aqueducts. Int J Pediatr Otorhinolaryngol. 2020;131:109862.

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48. Kim HA, Bisdorff A, Bronstein AM, et al. Hemodynamic orthostatic dizziness/vertigo: diagnostic criteria. J Vestibular Res. 2019;29(2–3):45–56. 49. Shah AS, Raghuram A, Kaur K, et al. Specialty-specific diagnoses in pediatric patients with postconcussion syndrome: experience from a multidisciplinary concussion clinic. Clin J Sport Med. 2021;32:114. 50. Fedorowski A. Postural orthostatic tachycardia syndrome: clinical presentation, aetiology and management. J Intern Med. 2019;285(4):352–66. 51. Wang A, Fleischman KM, Kawai K, Corcoran M, Brodsky JR. Persistent postural-perceptual dizziness in children and adolescents. Otol Neurotol. 2021;42(8):e1093–100. 52. Popkirov S, Staab JP, Stone J.  Persistent postural-perceptual dizziness (PPPD): a common, characteristic and treatable cause of chronic dizziness. Pract Neurol. 2018;18(1):5–13. 53. Staab JP, Eckhardt-Henn A, Horii A, et al. Diagnostic criteria for persistent postural-perceptual dizziness (PPPD): consensus document of the committee for the Classification of Vestibular Disorders of the Barany Society. J Vestibular Res. 2017;27(4):191–208. 54. McCaslin DL, Jacobson GP, Lambert W, English LN, Kemph AJ.  The development of the Vanderbilt pediatric dizziness handicap inventory for patient caregivers (DHI-PC). Int J Pediatr Otorhinolaryngol. 2015;79(10):1662–6. 55. Pavlou M, Whitney SL, Alkathiry AA, et al. Visually induced dizziness in children and validation of the pediatric visually induced dizziness questionnaire. Front Neurol. 2017;8:656. 56. Almutairi AB, Christy JB, Vogtle L.  Psychometric properties of clinical tests of balance and vestibular-­ related function in children with cerebral palsy. Pediatr Phys Ther. 2020;32(2):144–50. 57. Christy JB, Payne J, Azuero A, Formby C. Reliability and diagnostic accuracy of clinical tests of vestibular function for children. Pediatr Phys Ther. 2014;26(2):180–9. 58. Lee GS, Zhou G, Poe D, et al. Clinical experience in diagnosis and management of superior semicircular canal dehiscence in children. Laryngoscope. 2011;121(10):2256–61. 59. Weinreich HM, Carey JP. Perilymphatic fistulas and superior semi-circular canal dehiscence syndrome. Adv Otorhinolaryngol. 2019;82:93–100. 60. Rawal RZX, Lipson S, Brodsky JR. Endoscopic repair of traumatic perilymphatic fistula in children: a case series. J Adv Otol. 2021;17:182–5. 61. Beyea JA, Agrawal SK, Parnes LS.  Transmastoid semicircular canal occlusion: a safe and highly effective treatment for benign paroxysmal positional vertigo and superior canal dehiscence. Laryngoscope. 2012;122(8):1862–6. 62. Wolter NE, Gordon KA, Campos JL, et al. BalanCI: head-referenced cochlear implant stimulation improves balance in children with bilateral cochleovestibular loss. Audiol Neurootol. 2020;25(1–2):60–71. 63. Azevedo YJ, Ledesma ALL, Pereira LV, Oliveira CA, Bahmad F Jr. Vestibular implant: does it really work? A systematic review. Braz J Otorhinolaryngol. 2019;85(6):788–98. 64. Avery J, Etheridge L. Is high-dose magnesium supplementation helpful in adolescents with migraine? Arch Dis Child. 2021;106(10):1027–30. 65. Popkirov S, Stone J, Holle-Lee D.  Treatment of persistent postural-perceptual dizziness (PPPD) and related disorders. Curr Treat Options Neurol. 2018;20(12):50. 66. Rettig EK, Ergun G, Warfield JR, et  al. Predictors of improvement in pediatric chronic migraine: results from the cognitive-behavioral therapy and amitriptyline trial. J Clin Psychol Med Settings. 2021;29:113. 67. Headache Classification Committee of the International Headache Society (IHS). The international classification of headache disorders, 3rd edition. Cephalalgia. 2018;38(1):1–211.

Chapter 11

Vestibular Migraine Danielle M. Gillard and Jeffrey D. Sharon

History The first possible description of vestibular migraine has been attributed to Aretaeus of Cappadocia, who connected vertigo, headache, and tinnitus. Writing in the first century CE, he noted “… if the head be whirled round with dizziness, and the ears ring as from the sound of rivers rolling along with a great noise, or like the wind when it roars among the sails, or like the clang of pipes or reeds, or like the rattling of a carriage, we call the affection Scotoma (or Vertigo); a bad complaint indeed, if a symptom of the head, but bad likewise if the sequela of cephalæa….” In 1961, Bickerstaff associated migraine with vertigo with a proposal for “basilar artery migraine” [1]. At the time, it was thought that migraine predominantly resulted from alterations in intracranial vasculature, causing ischemia followed by arterial dilation. Bickerstaff noted that if the basilar artery was affected, then reversible brainstem dysfunction would occur, marked by visual loss, vertigo, dysarthria, tinnitus, unsteadiness of gait, alterations in consciousness, and paresthesias. In the current version of the International Classification of Headache Disorders (ICHD-3), this entity is referred to as “migraine with brainstem aura,” and includes a migraine with at least two transient brainstem symptoms, including dysarthria, vertigo, tinnitus, decreased hearing, diplopia, ataxia (not attributable to a sensory deficit), and/ or decreased level of consciousness. While they share similarities, migraine with brainstem aura and vestibular migraine are separate entities. The vast majority of patients with vestibular migraine don’t fit the definition for migraine with brainstem aura. We prefer the term vestibular migraine, unless clear transient neurologic deficits referable to the brainstem, such as dysarthria, are present during attacks.

D. M. Gillard · J. D. Sharon (*) Department of Otolaryngology/Head and Neck Surgery, University of California, San Francisco, CA, USA © The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 B. T. Crane et al. (eds.), Disorders of the Vestibular System, https://doi.org/10.1007/978-3-031-40524-2_11

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In 1917, Boenheim first coined the term “vestibular migraine” [2]. Associations between vertigo and migraine were highlighted by Heveroch [3], Symonds [4], Richter [5], Levy [6], and Friedman [7]. In 1960, Shelby and Lance [8] published a large case series of patients with migraine, and noted that one-third of the time vertigo was present during the headache phase. Kayan and Hood published a study in 1984, finding that 59% of patients with migraine had vestibulocochlear symptoms, and that half had a history of motion sickness [9]. In 1992, Cutrer and Baloh published a paper on “migraine associated dizziness,” which described a cohort of patients with dizziness, who had a history of migraine, and whose dizziness could not be ascribed to another disorder [10]. In the late 90s, other authors used similar terms, including “migraine associated vertigo” [11], and “migraine-related vestibulopathy” [12]. In 1999, Dieterich and Brandt [13] published a case series of 90 patients with episodic vertigo, thought to be a variant of migraine. They noted that only 7.8% of patients in their cohort fit the definition of basilar artery migraine, and therefore argued that vestibular migraine is a more inclusive diagnostic entity. In 2001, Neuhauser et al. proposed the first widely used diagnostic criteria for vestibular migraine [14]. However, the disorder was not included in the 2004 International Classification of Headache Disorders (ICDH-2), but was included as a migraine disorder in the ICDH-3 published in 2018. The Barany Society, an international consortium of vestibular specialists, published diagnostic criteria for vestibular migraine in 2012 [15].

Epidemiology Migraine headaches are one of the most commonly diagnosed diseases in the world. Roughly 33% of women and 13% of men will suffer from migraine at some point in their life [16]. Migraine without aura is defined by the International classification of Headache Disorders third edition (ICDH-3) as a headache lasting 4–72 h that has two of the four following characteristics: unilateral, pulsating, moderate or severe intensity, and aggravated by activity. It also has either nausea/vomiting and/or photophobia or phonophobia [17]. Migraines can be accompanied by an aura that is usually visual in nature, often described as scotoma (area of visual loss) or perceptual disturbance, such as seeing flashing zig zag lines or other iridescent patterns that usually move across the visual field. Migraine without aura is far more common than migraine with aura. In a 2001 study of patients presenting to both dizziness and migraine clinics, there was a large overlap discovered between patients [18]. In the dizziness clinic 38% of patients met the criteria for migraine, and in the migraine clinic 16.5% reported episodic vertigo. Vestibular migraine (VM) has an estimated prevalence is between 1% and 2.7% of adults [19, 20]. Depending on the study population, VM is the first or second most common cause of dizziness after benign positional paroxysmal vertigo (BPPV). Using the 2008 National Health Interview Survey data, Formeister et al. found that 11.9% of US adults had a problem with dizziness or imbalance in the prior year. Of those, 23% met a case definition for vestibular migraine, representing

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2.7% of the adult US population. Sixty-four percent were female. Of those with VM, 60% had missed work or school, and 52% had experienced a fall in the prior year (both higher than population averages, and also averages for subjects with dizziness without VM). Remarkably, of those given a diagnosis, only 10% were told that vestibular migraine was the cause of their symptoms, suggesting that underdiagnosis is common. Vestibular migraine is most likely to present between the third to sixth [18, 21] decade of life, and it can present either as the initial migraine manifestation or after a prior diagnosis of migraine headache [13, 21]. Dizziness, like migraine, is also a common symptom. Up to 4% of ER visits [22] and 5% of primary care provider visits [23] every year are for dizziness as the chief complaint. Dizziness represents a large economic and quality of life burden in the United States. The total annual medical expenditure for vertigo and dizziness is almost $50 billion [24]. Costs for the workup of dizziness make up roughly 4% of Emergency Department (ED) costs per year and exceed $4 billion with $360 million for the cost of CT scans and $110 million for the cost of MRI in the ED alone [25]. Dizziness has also been shown to increase missed work days which leads to decreased productivity, an additional economic burden [25, 26]. Vertigo and dizziness also increase the risk of falls, which can lead to resulting injury, especially in an aging population. In individuals over 40, those with vestibular complaints had 12-times higher odds of falling compared to older individuals without vestibular complaints [27]. Dizziness, especially in the elderly, is linked to increased disability and lower quality of life independent of other comorbidities [28].

Migraine Variants While migraine is predominantly associated with headaches, it’s important to note that there are several migraine variants that don’t involve a headache and have predominant symptoms that differ from the classical migrainous features. Typical aura without headache, or acephalgic migraine, is a migraine variant that presents with the usual migraine aura without associated headache [29]. So, for example one could experience a visual aura by itself, without any other symptoms. Hemiplegic migraine is a type of migraine with aura that presents with motor weakness symptoms [30]. Basilar artery migraine presents with symptoms of brainstem dysfunction including dysarthria, vertigo, tinnitus, hyperacusis, diplopia, ataxia and altered consciousness [31]. Therefore, it’s clear that while headache is a major feature of migraine, it’s only one of numerous neurologic manifestations of the disease. There are also several episodic syndromes in children that are now thought to be migrainous symptoms or precursors to classical migraine. This includes abdominal migraine, which presents as recurrent abdominal pain in children [32] and cyclical vomiting syndrome [33]. Furthermore, it’s now understood that both benign paroxysmal vertigo of childhood and benign paroxysmal torticollis of childhood are migraine variants [34]. In benign paroxysmal torticollis of infancy children present in the morning with direction-varying head tilt that improves at

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night-time [35]. Benign paroxysmal vertigo of childhood is a pediatric migraine syndrome that has predominantly vertiginous symptoms. Benign paroxysmal vertigo of childhood generally presents between ages 2 and 4, with discrete episodes of vertigo that last seconds to minutes in otherwise healthy children. This disorder is usually self-­limited over the course of several years and usually resolves by age 7 or 8 [36]. It was first described by Basser in 1954 [37] and was first associated with migraine headache in 1967 by Fenichel [37, 38]. These pediatric disorders are now well recognized as a migraine variants and it has been shown that these children are at an increased risk of developing typical migraine later in life [37– 39]. They are categorized in the ICHD-3 as “episodic syndromes that may be associated with migraine.” Furthermore, migraines can have a variety of associated otolaryngologic symptoms including neck pain, sinus pressure, nasal congestion, lacrimation, conjunctival infection, eyelid swelling, facial flushing and aural pressure. Many patients with “rhinosinusitis”—especially those with clear CT scans—have been shown to suffer instead from a migraine variant [40]. Additionally, the majority of individuals with “sinus headache” meet the criteria for migraine or probable migraine [41]. These patients frequently report facial pain, nasal congestion and rhinorrhea, which could be confused with a primary sinus etiology. Interestingly, these patients have been shown to have symptomatic improvement with classic migraine treatments, including response to empiric treatment for migraine with triptans [42]. It is clear that there are a variety of atypical migraine syndromes and there are many that present with otolaryngologic symptoms and findings, underscoring the fact that one must be familiar with migraine to understand many otolaryngologic symptoms.

 ssociation of Migraine and Vestibular Migraine with Other A Vestibular Diseases VM and migraine are commonly associated with a variety of other causes for vertigo. Those who suffer from BPPV, the most common cause of dizziness in the general population, have between 38% and 56% incidence of concomitant migraine symptoms [18, 43, 44]. In a cohort of posterior canal benign positional paroxysmal vertigo (BPPV) patients at UCSF, those with migraine presented with BPPV about 5 years earlier than the non-migraine cohort [45]. However, there was no difference in severity of dizziness symptoms based on DHI score and no significant differences in the rate of self-reported falls or BPPV recurrence in the migraine versus nonmigraine group. In Meniere’s, another common otolaryngologic disorder that causes symptoms of vertigo, 38%–56% of patients also have a history of migraine [46]. Migraine history has also been shown to be associated with bilateral vestibular loss; up to 50% of cases of idiopathic bilateral vestibular loss have a positive migraine history [47]. The number of vestibular diseases associated with migraine is quite remarkable, and highlights the need to understand how migraine affects the vestibular periphery.

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Pathophysiology The pathophysiology for vestibular migraine is not currently fully understood. It seems logical that any pathophysiologic model should explain all of the following: (1) Why there is an association between migraine and vertigo/dizziness; (2) Why some patients with migraine headaches get vertigo, and some do not; (3) Why some patients can have vertigo/dizziness without a prior headache history; (4) Why acute attacks of minutes to hours of spinning vertigo can occur; (5) Why variable amounts of symptoms can occur between episodes, including motion sensitivity, disequilibrium, dizziness, aural pressure, tinnitus, visual vertigo, and motion sickness; (6) Why vestibular migraine is linked to other vestibular diseases, including Meniere’s disease, BPPV, vestibular neuritis, and bilateral vestibular loss; (7) Why there is frequently, but not always a family history of migraine. To date, no complete explanation is available. Much of the current researches on the mechanisms that underlie vestibular migraine use the framework of classical migraine research. Migraine headache was originally thought to involve arterial spasm and dilation. Therefore, it was hypothesized that alterations of the labyrinthine artery could explain the pathophysiology of VM. However, this theory does not explain the wide range of clinical manifestations that are seen in those that suffer from vestibular migraine [48, 49], or the prolonged duration of vestibular symptoms both during and between acute migraine episodes. Furthermore, it’s been shown that migraines do not just involve arterial spasm, but instead a complex interplay of neurologic events in susceptible patients. One theory is that vestibular migraine is really a vestibular aura. Migraine with aura includes neurologic symptoms which are most frequent visual but can also be other sensory or central nervous system symptoms such as paresthesias. These aura symptoms gradually progress over several minutes to an hour and are often accompanied by or shortly followed by headache. Currently, migraine aura is thought to be a result of spreading cortical depolarization—which is an expanding wave of neuronal depolarization in the brain. This wave suppresses electrical activity and leads to a delayed restoration of transmembrane concentration gradients. Cortical spreading depolarization, in addition to aura, is thought to be responsible for the disorientation and brain fog that occur in migraine. A similar pathway has been investigated as a potential mechanism for VM if this cortical spreading depression reaches central vestibular centers. It’s possible that spreading depression may reach the vestibular brainstem nuclei, thalamus or other higher order vestibular centers including multisensory integrative areas, or other vestibular processing centers, leading to vertigo [13]. This explanation could potentially explain acute vertigo lasting minutes to hours, but may not be sufficient to explain the interictal symptoms. Another migraine mechanism that has been investigated as a potential cause for VM is the trigeminovascular inflammatory system. Headache and facial pain in migraine are caused by aberrant activation of the nociceptive sensory portion of the trigeminal nerve. These nerve efferents innervate the dura and intracranial blood vessels leading to the classic headache symptoms [50]. Trigeminal efferents also provide sensory input for the face and sinuses which may explain some of the other

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otolaryngological symptoms that can be associated with migraine. It is thought that trigeminovascular inflammatory peptides that are released may also affect the inner ear, leading to vestibular symptoms [51]. Animal models of guinea pigs have shown that electrical stimulation of the trigeminal nerve leads to plasma extravasation in the spiral modiolar artery within the cochlea [52]. Therefore this activation of the trigeminal nerve may lead to vascular changes and release of inflammatory peptides within the ear, possibly explaining the vestibular symptoms in VM. Once the trigeminal-vascular system is sensitized it releases a host of vasoactive and inflammatory peptides, including substance P, calcitonin gene-related peptide (CGRP), and neurokinin A. These peptides lead to vasodilation, mast cell degranulation, and neurogenic inflammation [53]. CGRP released by the trigeminal system leads to vasodilation and plasma extravasation [50] creating a positive feedback loop that furthers inflammation in the migraine state. Infusions of CGRP in humans have been shown to precipitate acute migraine attacks in both patients who have migraine with [54] and without aura [55]. There are multiple anti-CGRP antibodies that bind to the CGRP receptor or ligand including, galcanezumab (Eli Lilly and Company), fremanezumab (Teva Pharmaceuticals), and erenumab (Amgen/ Novartis) that have been approved for the treatment of migraine [56], highlighting the important role of the trigeminovascular inflammatory system in the pathophysiology of migraine. CGRP has been studied extensively in classical migraine and researchers have been looking into its role in vestibular migraine. CGRP has been demonstrated within vestibular brainstem efferents and in terminals that make synaptic contact with vestibular end organs in rat and chinchilla models [57–59]. More recently, CGRP has also been demonstrated in the human vestibular system, validating these earlier animal models [60, 61]. CGRP positive neurons located near the vestibular nuclei project directly to the vestibular end-­ organs [62, 63] as well as the vestibular nucleus and vestibular cerebellum [59, 64]. CGRP is expressed in peripheral vestibular organs as well, where it is co-located with choline acetyl-transferase, which makes acetylcholine, the primary neurotransmitter of the efferent vestibular system. In animal models CGRP infusion has been shown to cause photophobia [65], so there is some thought that CGRP release could also be responsible for hypersensitivity in the ear which may lead to some of the vestibular phenomena seen in VM. CGRP knockout mice have reductions in sound-evoked activity in the cochlear nerve [66], which implies a roll for CGRP in the response to external stimulus in the ear as well as the eye. Additionally, loss of CGRP has been shown to cause perturbations of the vestibular system. CGRP receptor knockout mice had a reduced vestibulo-­ocular reflex (VOR) gain, with no effect in VOR phase [67]. CGRP negative mouse models also show reduced otolith activation timing and impaired balance [68]. The connection between the trigeminovascular inflammatory peptide CGRP, migraine and the vestibular system remains an exciting pathway for further investigations into the underlying pathophysiology of VM. The central sensory sensitization theory has been utilized to help explain the chronic symptoms in patients with VM, and help provide insights as to why they can have vertigo and motion sensitivity that is prominent even in between acute migraine episodes. It is thought that VM sufferers have lower thresholds for sensory stimuli, including motion. This process is thought to be responsible for some of the chronic

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symptoms of VM, such as dizziness and motion sickness that is present between acute migraine episodes. Functional MRI studies of classical migraine show that migraine sufferers have atypical responses to visual, olfactory and painful cutaneous stimuli [69] and it is thought that this relationship may hold true for vestibular inputs in patients with VM. Sensory hypersensitivity to light, sound and motion is thought to be caused by alteration of circuitry in the thalamus which leads to an overall altered multisensory integration. Patients with VM often report that their vertigo is associated with headaches movements and this dizziness occurs even outside of acute vertigo attacks highlighting that they also share this abnormal sensory integration. The ventral posterior lateral and ventral posterior medial nuclei of the thalamus are relay nuclei for somatosensory information, which includes vestibular inputs [70]. The thalamus has increased activation in vestibular migraine [71] which highlights this as an important pathway for sensory sensitization in VM sufferers. Testing in patients with VM has provided some support for this theory of abnormal multisensory integration. Although there are a variety of papers that show minor abnormalities on vestibular testing alone (see section “Work-Up”) results across studies have been inconsistent and neither sensitive nor specific for VM. However, there is some thought that the true deficits can be seen in multisensory information processing and that these may point to possible mechanisms for VM. In a study of the effects of static head tilt on upright perception on VM patients and healthy controls perception of head tilt was measured in a dark room using a subjective visual vertical paradigm at three head tilt positions. Interestingly, patients with VM showed larger subjective visual vertical errors with head tilt to the right, but not with upright head position or head tilt to the left. On head tilt to the right VM patients tended to overestimate the tilt magnitude compared to controls suggesting these patients have abnormal sensory integration for spatial orientation processing [72]. Additional evidence to support that multisensory integration abnormalities cause central sensory sensitization is that VM sufferers have abnormal sensitivity to roll-­ tilt testing. In a study of the VOR and perception of self-motion in VM patients and healthy controls, researchers found that VM patients were abnormally sensitive to roll tilt. This test involves both semicircular canal and otolith activity. They were not more sensitive to tests that activated the canals or the otoliths in isolation [73]. Again, these results show that investigation of multisensory inputs reveals abnormalities which could be used to elucidate the mechanisms behind VM.

Functional Neuroimaging Functional imaging studies of VM patients are providing new clues to the mechanisms that may underlie the pathophysiology of VM. In a small study of two patients, regional brain metabolism of VM was recently assessed [74]. During a migraine attack, 18F-fluorodeoxy glucose-PET studies showed that compared to the interictal period there was increased activation in the temporo-parietal-insular areas and bilateral thalami and decreased activation of the occipital cortex. It was thought that this pattern of metabolism represents activation of the vestibulo-thalamo-cortical

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pathway and inhibition between the vestibular and visual systems which may explain some of the vestibular symptoms of VM. Another study conducted in between acute attacks showed similar activation of the bilateral insular cortex, thalamus, cerebellum and brainstem during caloric testing [71]. The thalamus continues to be examined in VM, as it is involved in pain processing and cortical excitability. It is posited that dysfunction in the integration and processing of vestibular and pain information through vestibulo-thalamo-­cortical pathways that lead to the symptomatic attacks in VM.  Whole brain imaging in migraine sufferers has also shown grey matter changes in regions of the brain important in pain and vestibular processing implying that VM may lead to permanent structural changes in the brain in relation to pain and vestibular inputs which may help explain the vestibular hypersensitivity present during and between episodes [75]. In another imaging study of VM patients, 12 patients with VM underwent whole-­ brain blood oxygen level-dependent fMRI during cold water calorics and results were compared with patients with migraine without aura and healthy controls. VM patients had increased thalamic activation compared to the other groups, providing additional support for the abnormal thalamic activation theory of VM [71]. Although there are not many functional neuroimaging studies the current body of research shows that in VM has structural and functional abnormalities that are similar to those seen in classical migraine. They also have additional abnormalities in vestibular systems which may show a connection between classic migraine mechanisms and vestibular symptoms. More neuroimaging studies will be needed to further elucidate these structural and functional changes.

Genetics of Vestibular Migraine Genetic analysis in VM has been done to help guide theories on the pathophysiology of the disease. There does appear to be some genetic component to VM, as patients with VM often have a positive family history [76]. Genetic variations in ion channels and membrane transporters have been investigated in the pathophysiology of migraine [77] and could potentially present a common pathway for the VM variant. Ionic homeostasis in the inner ear is important for the maintenance of endocochlear potential and alterations could lead to a variety of vestibular and cochlear symptoms. In addition, ion channel dysfunction in the cerebellum is also thought to lead to imbalance, incoordination and nystagmus. Familial hemiplegic migraine, a rare form of migraine that presents with motor weakness, aura, paresthesias and sensory changes and aphasia can also present with a variety of otolaryngologic symptoms including vertigo, tinnitus and imbalance [78]. Genetic analyses of familial hemiplegic migraine have identified mutations in CACNA1A, a calcium channel gain of function mutation [79], ATP1A2, a loss of function mutation in the sodium potassium-ATPase transporter [80] and SCN1A, a gain of function mutation in a voltage gated sodium channel [81]. These ion channelopathies present in familial hemiplegic migraine are being investigated as potential mechanisms for classical migraine. These mutations in the voltage-gated calcium channel CaV2.1 promote cortical spreading depression in

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migraine as well as in vestibular migraine [82]. Unfortunately, a link between these ion channelopathies discovered in familial hemiplegic migraine and VM has not been discovered [83]. However, a recent variant of ATP1A2 has been identified in a family with progressive hearing loss and migraine [84]. In a genome-wide association study (GWAS) of 38 loci involved in migraine, two genes were identified that are involved in the notch pathway for hair cell development which could provide an underlying genetic connection between classical migraine and vestibular symptoms. Additional genetic analyses of migraine have not identified specific genetic mutations in VM. Despite this lack of findings genetic analyses of VM and calcium channelopathies represent a possible area for future research on the pathophysiology of VM.

Presentation The hallmark symptoms of vestibular migraine (VM) are vertigo (a subjective sense of motion when there is none occurring, or altered sense of motion when motion is occurring) and/or dizziness (an altered sense of spatial orientation without vertigo) [85]. This helps to distinguish vestibular migraine from migraine headaches occurring with vertigo. If the predominant symptom that causes the patient to seek medical attention is vertigo, then we prefer the label vestibular migraine. The presentation of VM is highly variable, not only between individuals, but also between different attacks in the same individual. Symptoms can even fluctuate within a single attack. The vestibular symptoms can often be difficult to describe for patients and thus hard for the practitioner to interpret in the office. The vertigo in VM is often worsened by head movement and position changes. The duration of an acute vertigo episode is highly variable and can last anywhere from minutes to days, or even longer. As covered in the diagnostic criteria below, there are different forms of vestibular migraine. In the author’s clinic, they are equally divided. Some patients have a history of migraine headaches, and then develop episodic vertigo, with or without migrainous symptoms (photophobia or phonophobia or aura). Other patients do not have a history of migraine headache, but develop episodic vertigo with migrainous symptoms. VM patients may have nystagmus present during their VM episodes. The nystagmus can be quite variable between patients and even within the same patient. One study using a vestibular event monitor found that VM patients had spontaneous horizontal upbeating or downbeating nystagmus, positional nystagmus, or no nystagmus. In this study spontaneous vertical nystagmus was shown to be highly specific for VM. Their positional nystagmus was also persistent and did not extinguish with time [86].This is important to note, because not all positional vertigo is BPPV; vestibular migraine can cause identical symptoms. Around 60% of patients with VM have evidence of central ocular motor disorders between acute VM attacks including gaze-evoked nystagmus with saccadic smooth pursuit, horizontal or vertical spontaneous nystagmus and central positional nystagmus [13]. Patients with VM may have other associated otolaryngologic symptoms in addition to their vestibular symptoms. These include tinnitus, which can be pulsatile,

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aural fullness and subjective hearing loss [87]. Neck stiffness, facial numbness, and facial pressure can all occur as well. Cognitive dysfunction is a frequent complaint for patients with VM. One study looked at the Cognitive Failures Questionnaire, which is an indicator of cognitive dysfunction measured by the frequency of everyday cognitive slips (e.g., forgetting names, or what you were trying to do). Subjects with VM patients had elevated scores compared to normative controls, Meniere’s disease patients, and those with BPPV [88–90]. They also have increased rates of reported brain fog and fatigue [89]. VM triggers are generally the same as for regular migraine triggers, including stress, skipped meals, specific foods or beverages, bright lights, allergies, barometric pressure changes, loud sounds or busy visual scenes. They are also shown to have hormonal triggers, for example hormonal changes at menopause may be a trigger for an initial episode of VM, much like for migraine in women [91]. Patients with VM will often have a positive family history for migraine. In the author’s clinic, 45% have a first-degree family member with a history of migraine. Therefore, this can be an important diagnostic clue for VM. The vertigo and motion sensitivity seen in VM patients is often long-standing and can even be present between migraine attacks. In general, patients with VM are hypersensitive to movement and suffer from motion sickness at high rates [10]. This may help explain some of the chronic symptoms of VM. In addition, it can be more difficult to treat those with motion sensitivity, as physical therapy may paradoxically worsen symptoms. VM significantly reduces the quality of life for sufferers. Using 2008 NIHS data, 60% of VM patients had missed work or school because of their diagnosis, 37% called their diagnosis at least a moderate problem, and 52% had a fall [20]. Comparatively, the rate of falls in the non VM population was only 17%. In the author’s practice, the rate of comorbid depression is 48% and anxiety is 45%. In clinical practice we often find that patients have a lot of hesitation and mistrust toward this diagnosis. Patients often do not think vestibular attacks are migraines and see them as distinct symptoms from their usual migraines. We also find several common myths about migraines within the VM population. Many patients and providers believe that migraines have to cause headache, although we now know that there are several known migraine variants that do not cause headache including acephalgic or ocular migraine, abdominal migraine and hemiplegic migraine. It is also thought that migraines are episodic and can’t be continuous so the persistent vestibular symptoms between episodes cannot represent migraines. However, chronic migraine is diagnosed when migraines occur 14 or more days per month, and status migrainosus refers to a migraine lasting 72 h or longer, proving that migraine attacks and symptoms can last longer than the classic teaching of 72  h. Patients often think that migraine is an obvious diagnosis and that since other providers did not give them a migraine diagnosis that it cannot be the cause of their vestibular symptoms. Although as demonstrated previously, VM is likely highly underdiagnosed. Many patients also share the belief that migraines cannot possibly be as severe or life altering as their symptoms, which prior research shows is false. VM can be a very severe diagnosis causing significant morbidity for patients.

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In a UCSF cohort of 67 patients who presented to the UCSF Balance and Falls Center with dizziness, a plurality of subjects felt neutral as to whether or not their provider would figure out the cause of their dizziness, 31% were neutral as to whether or not treatment would help. About one third of patients who met ICHD-3 criteria for migraine did not believe that migraines could cause dizziness. Finally a majority of subjects did not believe that migraines could be chronic [92]. Figure 11.1 shows vertigo triggers, associated symptoms, episode length, episode frequency, and secondary vestibular diagnoses for a cohort of 51 VM patients in the author’s practice. Triggers 100 90 80 70 60 50 40 30 20 10 0

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Fig. 11.1  Clinical characteristics of vestibular migraine. Unpublished from a UCSF study of 51 subjects with VM. (a) Most common triggers of VM, (b) Associated symptoms during dizziness, (c) Dizziness duration (d) Dizziness frequency per month, (e) Secondary vestibular diagnoses. MD Meniere’s disease, BPPV benign paroxysmal positional vertigo, VH vestibular hypofunction, PPPD persistent perceptual postural dizziness, MdDS mal débarquement syndrome

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Diagnostic Criteria The first diagnostic criteria for VM were described by Lempert and Neuhauser in 2001 [93–95]. They proposed four basic criteria for the diagnosis of VM were (1) recurrent vestibular symptoms, (2) migraine based on the International Headache Society (IHS) criteria, (3) migraine symptoms such as headache, photophobia, phonophobia or auras, during vertigo attacks, (4) other possible causes have been ruled out. Currently, many clinicians use the newer but similar Barany Society Criteria for Diagnosis to diagnose VM [96] (Table  11.1). Definite vestibular migraine can be diagnosed with at least five episodes of vestibular symptoms with migrainous features and history of migraine. Probable VM can be diagnosed even if the patient does not have a positive history of classical migraine or consistent migrainous symptoms along with their vestibular symptoms. In order to use the Barany society criteria, one must be familiar with current ICHD criteria for the diagnosis of migraine headache. The ICHD-3 criteria for migraine without aura are presented in Table 11.2.

Work-Up At the time of writing, there is no definitive diagnostic work-up for VM. Imaging and routine laboratory testing in these individuals is generally normal. A variety of vestibular tests have been used to evaluate patients with VM, with inconsistent results. A meta-analysis by Furman in 2003 found that about one quarter of

214 Table 11.1  Barany Society criteria for the diagnosis of vestibular migraine

D. M. Gillard and J. D. Sharon A. Vestibular migraine  (a) At least 5 episodes with vestibular symptoms   (i) Severity: moderate–severe    (ii)  Timing: 5 min–72 h  (b) History of migraine ± aura according to ICHD-3  (c) ≥  1 of the following migraine features occurring with at least 50% of vestibular episodes    (i)  Headache with at least two of the following characteristics: unilateral, pulsing, moderate or severe pain intensity, aggravation by routine physical activity   (ii) Photophobia and phonophobia    (iii)  Visual aura  (b) Not better accounted for by ICHD-3 diagnosis B. Probable  (a) At least 5 episodes with vestibular symptoms   (i) Severity: moderate–severe    (ii)  Timing: 5 min–72 h  (b) Has either (b) or (c) from “Definite” criteria but NOT both  (c) Not better accounted for by ICHD-3 diagnosis Diagnostic criteria for definite and probable vestibular migraine from the Barany Society criteria [96]

Table 11.2 International Classification of Headache Disorders-3 Vestibular Migraine Criteria

A. At least five episodes fulfilling criteria C and D B. Current or past history of migraine without aura or migraine with aura C. Headache of moderate to severe intensity, lasting between 5 min and 72 h D. At least half of episodes are associated with at least one of the following three migrainous features:   (1) Headache with at least two of the following four characteristics:    (a) Unilateral location    (b) Pulsating quality    (c) Moderate or severe intensity    (d) Aggravation by routine physical activity   (2) Photophobia and phonophobia   (3) Visual aura E. Not better accounted for by another ICHD-3 diagnosis or by another vestibular disorder. Migraine without aura is the most common migraine disorder presenting as a recurrent headache with migraine features as described above. Available at https://ichd-3.org/

patients with migraine or migraine with significant associated vestibular symptoms have abnormalities of the peripheral vestibular system, but these results were inconsistent among studies [97]. In a study that directly compared migrainerelated dizziness with nonmigraine-related dizziness, there were no significant

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differences in the majority of neuro-otological tests. However, VM patients had significantly increased emetic response (more likely to have nausea and/or vomiting) during caloric testing compared to patients with other causes of dizziness [98]. The majority of patients with VM have normal electronystagmography results. In some studies there have been a number of patients with a unilaterally reduced vestibular response, abnormal directional preponderance on rotational chair testing, reduced vestibular response on caloric testing [12], increased postural sway [99, 100] or reduced amplitudes of vestibular myogenic evoked potentials [101, 102]. These results suggest that there is both peripheral and central vestibular dysfunction present in VM. However, none of these results are sensitive or specific for the diagnosis of VM.  It has been considered that testing of combined stimuli to assess vestibular-­visual processing may reveal abnormalities more consistent with the VM diagnosis. Testing of visually enhanced vestibulo-ocular reflex (VVOR) has been analyzed in migraine patients with vestibular symptoms. In VVOR testing the rotational chair evaluation of the vestibulo-ocular reflex is performed in a lighted setting with an optokinetic visual stimulus to produce eye motion. VVOR gain (nystagmus velocity relative to chair rotation speed) has been found to be elevated in patients with VM [103]. There are no other consistent responses to caloric or vestibular testing in these patients [93, 94]. Thus, proper diagnosis relies primarily on the astute clinician interpreting the patient’s clinical symptoms. Patients and their symptoms can be evaluated with the Dizziness Handicap Inventory (DHI) [104] a survey used in vestibular disorders to evaluate patient symptoms and handicap. The average DHI score in a UCSF population of patients with VM was 49. Recently, a validated disease specific survey from UCSF was developed specifically for use in VM. The Vestibular Migraine Patient Assessment Tool and Handicap Inventory (VM-PATHI) was validated in 2020 to measure disease severity in vestibular migraine patients [105]. The VM-PATHI is available on the UCSF Balance and Falls website (https://ohns.ucsf.edu/balance-­falls/ vestibular-­migraine). The survey covers cognition, emotional disturbance, disequilibrium symptoms, anxiety, motion sensitivity and headache equivalents (Fig. 11.2). The survey was developed in three phases: in the first phase a library of questions for inclusion were developed with experts in neurotology, neurology, audiology and biostatistics, with the aim of high face and content validity. In the second phase the questions were trialed in a small cohort to determine readability and ease of use. In the final phase it was administered to a large group of patients to determine reliability, internal consistency, test-retest liability, and was given to controls to assess discriminant validity. It was also compared against the DHI and quality of life measure (Short Form-36). The final, validated survey has 25 questions about symptoms that are scored on a Likert scale ranging from “no problem” to “problem as bad as it can be.” For the final survey, Cronbach’s a was 0.92 and test retest reliability was high (r = 0.90, p 11.1 s, with a sensitivity of 80% and specificity of 56% in falls prediction [78]. Dynamic Gait Index (DGI): The DGI is an 8-item scale that was developed initially to identify fall risk in older adults [79]. The DGI is a sensitive assessment tool to identify people at risk of falls due to vestibular disorders [80]. Participants are scored on an ordinal score (0–3) while performing a variety of ambulatory tasks such as walking with head turns or walking around/over obstacles. Scores of 19 points or less indicates an increased risk of falling [80]. Some patients may score above the 19 point cut-off, and may benefit from a more challenging version of the test known as the Functional Gait Assessment [81]. A final category of behavioral tests that are helpful for identifying impairments for individuals with vestibular disease evaluate behavioral performance of the VOR. The most common and low tech clinically friendly version of these tests that quantify gaze stability is the Dynamic Visual Acuity test (DVA) [82]. Computer aided testing allows for separately evaluating (1) how small a target can be recognized at specified head velocities [83], (2) the fastest velocity that an object of specified size can be recognized [84, 85], and a combined evaluation of the VOR gain and DVA [86, 87]. Here we briefly describe the clinical version of the DVA. Dynamic Visual Acuity (DVA) test: Vestibular hypofunction leads to impaired gaze stability due to increased retinal slip during head movement. The DVA test is a behavioral assessment of gaze stability [82]. The clinical DVA starts with an evaluation of static visual acuity using a Snellen or EDTRS chart by asking the patient to read the smallest line that they can see clearly without moving their head. Then the patient is instructed to read the lines from the top down while the examiner passively oscillates the patient’s head ±15° to 20° at 2 Hz. A difference of 2 lines or more between the static acuity and the dynamic acuity suggests uncompensated gaze instability [88, 89]. Computerized versions of the DVA test were found to be more valid [83].

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Vestibular Conditions Manifesting These Symptoms Unilateral Vestibular Hypofunction Unilateral vestibular hypofunction (UVH) is the partial or complete loss of function of one or more of the vestibular organs and/or vestibular nerves on one side [8, 30]. Acute unilateral vestibular hypofunction is most commonly due to vestibular neuritis but other causes include: trauma, surgical nerve transection, ototoxic medication, vestibular schwannoma, superior canal dehiscence, or Meniere’s disease [8, 30, 90, 91]. Acute asymmetry in resting vestibular tone leads to sudden onset of vertigo, nausea, and imbalance symptoms and transient spontaneous nystagmus [90, 92]. Although visible nystagmus and vertigo usually subside within hours to 14 days, uncompensated UVH results in imbalance, blurry vision with head movement, dizziness, spatial disorientation, and difficulty with path instability when walking [92– 96]. UVH may affect a person’s ability to drive, perform typical daily activities, and work [97, 98]. Negative changes in quality of life may also lead to secondary problems such as depression and anxiety as well as secondary deconditioning likely due to reduction in activity participation [99–104]. Importantly, individuals with more complete hypofunction may take longer to rehabilitate and may continue to report subjective symptoms after apparent recovery of balance ability [65]. For some people, this may result in a chronic condition called persistent postural-perceptual dizziness (PPPD) [105, 106]. Vestibular rehabilitation is very effective at addressing the impairments and symptoms related to unilateral vestibular hypofunction [6, 8].

Bilateral Vestibular Hypofunction BVH is a condition caused by absent or reduced function of the vestibular organs and/or nerves of both ears. Most instances of BHV are idiopathic [107, 108]. Other causes of BVH include: trauma, aging, infectious disease, ototoxic medication, bilateral Meniere’s disease, neurodegenerative disorders, autoimmune disease, and congenital or genetic abnormalities [107–110]. Common symptoms include oscillopsia with head movement and imbalance, especially in the dark or on unlevel/ uneven surfaces [55, 57–59, 109]. Most individuals with severe BVH do not complain of vertigo. Individuals with BVH often experience difficulty walking in the dark [111]. Herdman and colleagues (2000) reported that about 50% of patient with BVH had fallen since the onset of the vestibular deficit [39]. Quality of life is often negatively impacted and individuals with BVH report a high socioeconomic burden due to work-related disabilities [41, 57]. Vestibular rehabilitation is effective at addressing the impairments and symptoms related to bilateral vestibular hypofunction, although the rehabilitation duration typically takes longer and the level of recovery may be less complete [6, 8].

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Benign Paroxysmal Positional Vertigo Benign paroxysmal positional vertigo (BPPV) is one of the most common causes of vestibular vertigo [112–114]. Loose otoconia dislodged from the utricle that end up free-floating in the semicircular canals (canalithiasis) or attached to the cupula (cupulolithiasis) are considered to be the primary cause of BPPV symptoms [115– 120]. BPPV symptoms of vertigo and imbalance are triggered by change in head orientation to gravity (i.e., bending over, looking up, lying down, rolling in bed) [121]. Thus, the methods for differential diagnosis depend on changes in head orientation while aligning a set of semicircular canals in the plane of gravity [122, 123]. Many factors including age, acute vestibular loss, and trauma contribute to otoconia becoming dislodged [124, 125]. Although BPPV has been reported in some children [126, 127], this is relatively rare and BPPV is much more common in adulthood with prevalence increasing with age [125, 128, 129]. BPPV occurs in all three semicircular canals, with the posterior canal being most commonly affected and the anterior canal being the rarest form, and each variant has many distinct treatment options [130, 131]. It is paramount for clinicians to accurately identify the affected semicircular canal since the canalith repositioning treatments are canal specific [123, 131–133]. The Dix–Hallpike test is the clinical standard for diagnosing posterior canal BPPV (see Fig. 14.1) [122, 130, 134]. Some individuals may not be able to tolerate the traditional Dix–Hallpike positions, thus a modified testing position in side-lying was developed that can be used in those instances (see Fig. 14.2) [135–137]. The “Supine-Roll Test” (Fig. 14.3) and/or the “Bow and Lean Test” are recommended for differential diagnosis of lateral canal BPPV [123, 138]. Readers are encouraged to reference the most current BPPV clinical practice guideline for an extensive review of recommended differential diagnostics and a

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Fig. 14.1  Example of Dix–Hallpike testing for BPPV on the right side, (a) shows the starting position with the head rotated 45° to the right, (b) shows the testing position maintaining a 45° rightward head rotation with 20° of neck extension. The testing position should be held for 30–60 s while waiting for symptoms or nystagmus. Infrared goggles can be used to improve visualization of nystagmus as shown in (b)

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Fig. 14.2  Example of modified side-lying Dix–Hallpike testing for BPPV on the right side, (a) shows the starting position with the head rotated 45° to the left to place the right posterior canal into the plane of movement, (b) shows the testing position maintaining a 45° leftward head rotation with 20° of neck extension. The testing position should be held for 30–60 s while waiting for symptoms or nystagmus. Infrared goggles can be used to improve visualization of nystagmus as shown in (b)

treatment strategies [130]. In this section we provide a brief overview of the most commonly used diagnostic tests and the nystagmus characteristics typical for each subtype of BPPV, see Table 14.1. Selected treatment strategies are described later in this chapter.

Vestibular Migraine Vestibular migraine is a migraine in the company of vestibular symptoms. In the past it was described by other terms such as migraine-associated dizziness, migraine related vestibulopathy and migrainous vertigo. Today, the acceptable term by the Barany Society and the International Headache Society is “Vestibular Migraine” [139, 140]. Vestibular migraine is characterized by episodic events of vertigo and/or dizziness and/or unsteadiness with or without experiencing other symptoms such as nausea, tinnitus, sound sensitivity, light sensitivity, and visual disturbance [140, 141]. The symptoms can last for minutes to days with occurrences ranges from every day to twice a year [142, 143]. Vestibular migraines can negatively affect an individual’s activity and participation, reduce quality of life, lead to work absences, and interfere with daily activities [142, 144]. Rehabilitation programs for vestibular migraine are exercise-based. There is some evidence that symptoms and functional abilities improve with vestibular rehabilitation [145–147]. However, vestibular rehabilitation is relatively underutilized, and patients should also receive appropriate medical management for optimum results [143].

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Fig. 14.3  Example of Supine Roll testing for lateral canal BPPV, (a) shows the starting position with the head in midline and elevated 30°, (b) shows the testing position with the right ear down, (c) shows the head back in the neutral midline position, (d) shows the head turned with the left ear down. Each position should be held for 30–60 s while waiting for symptoms or nystagmus. Infrared goggles can be used to improve visualization of nystagmus

Persistent Postural-Perceptual Dizziness Persistent postural-perceptual dizziness (PPPD) is a functional vestibular disorder, not a structural or psychiatric vestibular disorder. PPPD is characterized with a persistent dizziness, nonspinning vertigo aggravated by postural challenges with reported sensitivity to space-motion stimuli [105]. PPPD often develops after peripheral or central vestibular disorders. However, it might also develop due to vestibular migraine, panic or anxiety attacks, concussion, whiplash injuries and even by autonomic disorders [148]. Many patients with PPPD report that upright posture, standing and walking, worsen their symptoms [149, 150], interfering with participation in typical daily functions. There is emerging evidence for the importance of vestibular rehabilitation to address the symptoms reported by patients with PPPD [151–153].

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Table 14.1  Summary of positional tests and nystagmus characteristics for different types of BPPV Canal Positional test Canalithiasis Posterior Dix–Hallpike or side-lying Lateral Supine Roll Test or Bow & Lean Anterior Dix–Hallpike or Deep Head Hang Cupulolithiasis Posterior Dix–Hallpike or side-lying Lateral Supine Roll Test or Bow & Lean Anterior Dix–Hallpike or Deep Head Hang

Nystagmus direction Up-beating and geotropic torsional nystagmus Horizontal geotropic nystagmus Down-beating ± geotropic torsional nystagmus

Up-beating and geotropic torsional nystagmus Horizontal apogeotropic nystagmus Down-beating ± geotropic torsional nystagmus

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Concussion Concussion is a mild traumatic brain injury, with a complex pathophysiological process leading to rapid onset of short lived neurological impairments that typically resolve spontaneously [154]. Etiology of dizziness postconcussion varies. Patients might be dizzy due to post traumatic BPPV [155] or peripheral vestibular dysfunction [156]; however, video head impulse testing suggests lateral semicircular canal function remains intact for many concussed adolescents [157, 158]. Whether from central or peripheral pathology gaze stability is impaired postconcussion [156, 159, 160]. Oculomotor functions such as smooth pursuit, saccades, convergence motion of the eyes and accommodation are frequently abnormal after a mild head injury [161], leading to symptoms of dizziness. In many cases posttraumatic migraine with aura of dizziness/vestibular migraine might be a result of concussion [160]. Most patients postconcussion return to their prior level of functional within days to weeks, yet some patients have prolonged recovery that may be associated with psychiatric comorbidities such as anxiety, social withdrawal, inter personal sensitivity, and fearfulness [162–164]. Concussed individuals experiencing dizziness, imbalance, and oculomotor symptoms benefit from symptom management using vestibular rehabilitation [165–168].

Mal de Debarquement Syndrome (MdDS) MdDS, sickness of disembarkation, is a subjective perception of an oscillatory sensation of swaying or rocking [169–171]. Possible triggers for MdDS are disembarking from a moving water, air or land-based vessel (boats, airplanes, trains, etc.)

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[169]. History of migraine, stress, medication changes, and sleep deprivation serve as contributing factors [169]. Symptoms include persistent motion when standing or lying down, especially with eyes closed. Symptoms often abate slightly during movement like walking or driving [169]. MdDS patients report reduced confidence during activities of daily living [172]. There are some promising technology driven treatments for MdDS, but at the moment they remain primarily experimental [173– 176]. Traditional vestibular rehabilitation has been used to address the symptoms of MdDS; however, reports of effectiveness are inconsistent and additional research is needed [177, 178].

Symptom-Based Treatment Approaches Education Patient education is a key element in vestibular rehabilitation. Patients are educated about their symptoms and impairments, the underlying mechanism of their pathology, potential risks, and the importance of symptom provocative treatment strategies improving patient buy-in and participation in home exercises [179]. In addition, patient education facilitates better self-management of aggravating factors [6]. Hillier and McDonnell reported in their Cochrane review that even a minimal approach to patient education enhances the effectiveness of vestibular rehabilitation [7].

Positional Vertigo Benign paroxysmal positional vertigo (BPPV) is one of the most common forms of vertigo [114], and the primary treatments for BPPV emphasize using gravity to reposition otoconia debris from the affected semicircular canal [130]. Here we discuss canalith repositioning treatments for the most common subtypes of BPPV followed by a brief discussion on habituation as a less preferred form of treatment for BPPV. As we mentioned earlier, the most common type of BPPV involves loose otoconia in the posterior semicircular canal, diagnosed by the Dix–Hallpike test. The two most common treatment approaches for canalithiasis are the Epley (canalith repositioning) maneuver and the Semont maneuver [133, 180–183]. A description of the performance for the canalith repositioning maneuver (Epley) and the Semont maneuver are provided in the captions for Fig. 14.4 (Epley) and Fig. 14.5 (Semont). The efficacy (>85%) of the Epley and Semont maneuvers have been shown to be equivalent when combining the results of two studies [180]. Current evidence supports canalith repositioning treatments as having greater efficacy over other techniques such as the Brandt–Daroff exercises [184].

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Fig. 14.4  Example of the Epley treatment for left posterior canal BPPV, (a) shows the starting position with the head turned 45° to the left, (b) shows the second position with the left ear down and approximately 20° of neck extension, (c) shows the third position with the right ear down (head turned 45° to the right) and approximately 20° of neck extension, (d) shows the fourth position in side-lying with the right ear down and approximately 10° of neck flexion, (e) shows the final position seated at the edge of the mat. Each position should be held for 30–45 s after vertigo/nystagmus stops

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Fig. 14.5  Example of the Semont treatment for right posterior canal BPPV, (a) shows the starting position with the head turned 45° to the left, (b) shows the second position with the right ear down and approximately 20° of neck extension, (c) shows the third position with the nose and left ear down and approximately 10° of neck flexion, (d) shows the final position seated at the edge of the mat. Transitions between positions are fast with abrupt stops to dislodge stuck on otoliths. Positions b and c should be held for 1–2 min each after vertigo/nystagmus stops

The second most common form of canalithiasis involves the lateral or horizontal canal. The differential diagnosis is based on horizontal (head referenced) nystagmus during the Supine Roll Test [123]. The Bow and Lean Test can be helpful in determining the affected ear [138]. Lateral canal canalithiasis can be treated with either the Supine Roll technique or the Gufoni (Vannucchi) maneuvers [185, 186]. A description of the performance for the Supine Roll technique and the Gufoni maneuver are provided in the captions for Fig. 14.6 (Supine Roll) and Fig. 14.7 (Gufoni). The least common form of canalithiasis involves the anterior canal [187]. There are two recommended treatment techniques to address canalithiasis involving the anterior canal. The Epley maneuver has been successfully applied to treat anterior canalithiasis [188], and more recently a technique developed by Yacovino and colleagues has met with similar success [189]. The overall effectiveness of these techniques for resolving positional vertigo complaints is >75% [187]. A description of the performance for the deep head hanging maneuver is provided in the captions for Fig. 14.8.

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Fig. 14.6  Example of the Supine Roll treatment for left lateral canal BPPV, (a) shows the starting position with the head turned 90° to the left elevated 30°, (b) shows the second position with the head in midline elevated 30°, (c) shows the third position with the head turned 90° to the right elevated 30°, (d) shows the fourth position with the head in midline and nose down with approximately 30° of chin tuck, (e) Left side-lying position, (f) Supine with head midline, (g) final position seated on the mat. Positions a, b and c should be held for 30–45 s after vertigo/nystagmus stops

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Fig. 14.7  Example of Gufoni for left lateral canal BPPV. (a) Shows the starting position with the head in midline and the patient crossing their arms to grasp the forearms of the clinician, (b) shows the second position with the head in midline and right side-lying holding for 1 min, (c) shows the third position with the head turned 45° to the right (nose down) holding for 1–2 min, (d) shows the final position seated on the mat

In some cases particle repositioning maneuvers do not successfully resolve complaints of positional vertigo. For those individuals a habituation approach should be considered as a final conservative approach [190]. Habituation exercises can take the form of an appropriately selected repositioning technique as described above, Cawthorne–Cooksey exercises [191], or Brandt–Daroff exercises [192]. Habituation prescription for positional vertigo may include 5–10 repetitions daily of motion provoking movements. In rare cases, surgical intervention may be appropriate [193].

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Fig. 14.8  Example of deep head hang technique for anterior canal BPPV. (a) Shows the starting position with the head in midline and the patient sitting upright, (b) shows the second position with the head in midline with approximately 60° of head/neck extension, holding for 1 min, (c) shows the third position with the head in midline brought up to a chin-tuck, (d) shows the final position seated on the mat

Treatments for Nonspecific Dizziness Exposure Therapy The primary goal for habituation exercises is to desensitize nonspecific dizziness by gradual repeated exposure to provocative stimuli such as self-movement or visual stimulating surroundings. The symptom of nonspecific dizziness has been referred to in several ways including motorists’ disorientation syndrome motorists’ disorientation syndrome [194], space and motion discomfort [103, 195], visual vertigo [196], and visual-vestibular mismatch [197–199]. Over time, exposure to vestibular and visual motion stimuli leads to reduced vestibular responses, probably due to changes in velocity storage mechanisms that mediate ocular and perceptual responses, therefore, reducing sensitivity to

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visual-­vestibular mismatches [56, 200, 201]. Vestibular rehabilitation exercises may include a range of visual environments, virtual reality, and supplementary immersive settings [26, 202, 203]. Incorporating optokinetic stimuli concurrent with vestibular rehabilitation exercises has better outcomes than treatments without optokinetic stimuli [25, 204]. Vestibular and visual motion stimulation for habituation can also be induced by self-motion, and has been successfully used to address motion sensitivity aspects of vestibular hypofunction [24].

Cognitive Behavioral Therapy Anxiety, depression, and other psychological conditions often present as comorbid conditions for individuals with dizziness. About 50% of dizzy patients experience psychiatric comorbidity [99]. Both nonspecific dizziness and psychological disorders can lead to functional limitations. Not surprisingly, habituation principles are similar for both conditions. The main element of vestibular habituation exercises is gradual and controlled exposure to sensory input that provokes symptoms. The main component of cognitive behavior therapy (CBT) is progressively and controlled exposure to the individual’s challenging factors [104, 205, 206]. Psychotherapy such as CBT, together with vestibular rehabilitation, can be a very effective treatment combination for a dizzy patient, as has been shown in a systematic review [207]. Even for patients with persistent dizziness, this combination of treatments is feasible and promising; however, the optimal intervention strategy still needs to be identified [152, 208]. Patients who suffer only from dizziness, without measurable balance impairments benefit even more from CBT treatments [209].

Gaze Instability The purpose of VOR adaptation exercises is to improve gaze stability by “strengthening” vestibular responses and recruiting substitution mechanisms such as preprogramming eye movements, and the cervico-ocular reflex to compensate for the vestibular hypo function in order to gain stable vision and therefore also improve postural stability [23, 210–212]. An error signal that causes retinal slip during head movement is the VOR adaptation’s key stimulus [213–215]. Human VOR adaptation abilities are phenomenal due to neuroplasticity [216, 217]. It has adaptive capabilities for concurrent and opposing directions, i.e., increased VOR response when moving the head to one side and decreased response as moving the head to the other side. VOR adaptation is context-specific and depends on the error signal that drives the adaptation process [218]. The basic clinical VOR adaptation exercise is VOR X1 viewing exercise. For VOR X1 exercise a patient holds a target in front of the eyes, moves the head side to side or up and down in a small amplitude but as fast as possible while maintaining a

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perception of a clear and stationary target. To advance in treatment and add extra challenge to the VOR, a patient can move the target and the head in opposite directions at approximately the same velocity. This kind of exercise is known as VOR X2 viewing. Because of the target movement, the eyes will need to move faster than the head, increasing the VOR gain [213, 215, 219]. These techniques are very easy to deliver in the clinic as well as for patients to practice at home. Examples of X1 and X2 viewing are presented in Fig. 14.9. Importantly, these gaze stabilization exercises can be progressed in difficulty starting with sitting and progressing to standing or walking. During vestibular rehabilitation, the brain recruits alternative strategies to achieve better function and gaze stability by substitution mechanisms and central preprogramming eye movements [15, 22]. The level of vestibular recovery determines the brain strategy to improve gaze stability. Patients with sufficient vestibular end-organ functional recovery use fewer compensatory saccades [220]. On the other hand, patients with chronic vestibular hypofunction depend on compensatory saccades to improve gaze stability [221–223]. Improvement of DVA is a significant outcome that indicates better gaze stability. Vestibular rehabilitation exercises that include head and eye movements lead to better results than general exercises not based on actions that require visual fixation [21, 224]. Additional exercises for improving gaze stability can include eye and head movements between several targets and even by moving the head while keeping fixation on a remembered target, for examples Figs. 14.10 and 14.11 [225]. Isolated saccades or pursuit eye movement only exercises are not effective for treating peripheral vestibular hypofunction and should not be prescribed [6]. For effective vestibular rehabilitation, patients should participate in daily exercises that include head-eye movements for 12–20 min per day of combined gaze stabilization exercises [6]. This recommendation was based on interpretation of studies that were not designed to evaluate dosage, and additional research is needed to clarify the optimum exercises and dosage parameters to improve gaze stability.

Disequilibrium Balance problems and falls are common for individuals with vestibular dysfunction [35, 40, 226]. Balance problems may manifest while standing still or when in motion such as while walking [227–229]; thus, balance interventions need to be specifically targeted. Balance exercises must be sufficiently challenging [230, 231], or individuals may not improve. Normal balance ability depends on having an intact and functional musculoskeletal system and intact peripheral systems and central sensory processing [232–234]. Balance rehabilitation often incorporates both a strengthening and a sensory reweighting approach for individuals with vestibular dysfunction. Sensory reweighting is facilitated by systematically reducing the availability or reliability of specific sensory inputs that are relevant for balance control [18, 235–238].

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Fig. 14.9  Example of X1 viewing (a–c) and X2 viewing (d–f) exercises. For X1 viewing, the target or “X” is world fixed and the head is either continuously or impulsively rotated in pitch or yaw. For X2 viewing, the target is moved in the opposite direction of head motion at approximately the same velocity which can be done either continuously or impulsively

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Fig. 14.10  Example of eye-then-head exercises to promote substitution. From a to c, progressively the eyes move to the new target and then stay there as the head is turned. In d and e, this process is reversed moving the eyes then head back to the original target

Standing balance can be progressively challenged in a variety of ways starting with altering the shape and size of the base of support, wider is more stable [229]. Different surfaces such as foam, tilting boards, narrow beams, or different surface heights are used to artificially create instability leading to a change in how balance is controlled [239–241]. Sensory availability can be manipulated to increase the balance challenge by closing the eyes [241–243], standing on a foam cushion [241], or watching optic flow patterns [204]. Altered head position or adding continuous

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Fig. 14.11  Example of remembered target exercise for gaze stability. (a) The target is visualized, (b) the eyes are closed maintaining position on the remembered target location, (c) the head is turned away while the closed eyes continue looking where the target is, (d) the eyes are opened for visual feedback to see whether they stayed on the target

head motion can further create challenges to standing balance leading to increased sway [244, 245]. Similar exercise manipulations are often also applied during walking based on identified task difficulty on balance tests like the Functional Gait Assessment or Dynamic Gait Index [79, 81]. Obstacles to step over or navigate around are also often incorporated into rehabilitation exercises as those are commonly encountered in daily life [246, 247]. Current recommendations for balance exercises include at least 20 minutes per day for 4-6 weeks or 6-9 weeks for unilateral or bilateral vestibular hypofunction respectively [248]. Additionally, Klatt and colleagues theorized that 8–12 min of focused balance exercises 2–3 times per week may be beneficial [231]. Research based guidelines on balance exercise dosage are needed.

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Frontiers in Vestibular Rehabilitation Cognition Although the specific mechanisms are still being elucidated [249], the vestibular system influences cognition in several ways [250–256]. Vestibular signals from both the semicircular canals and otoliths are found in the hippocampus and entorhinal cortex highlighting the impact of vestibular afferent signals on spatial orientation/ navigation [257–259]. Reduced vestibular function either caused by aging or disease leads to worse performance on tests of spatial orientation and spatial navigation compared to healthy adults [96, 260–264]. In fact, individuals with dementia are more likely to have vestibular dysfunction compared to older adults with normal cognition [265]. Because of the broad vestibular connection to cognition, some have proposed vestibular exercises to improve both cognition and balance [266, 267]. At present, there is insufficient evidence supporting enhanced cognition from vestibular rehabilitation, but promising research is on the horizon [268, 269].

Innovations Novel vestibular rehabilitation approaches, especially for patients who do not respond well to traditional vestibular rehabilitation (e.g., severe BVL patients), are needed. Some of these promising approaches include the use of invasive vestibular implants and noninvasive devices that use vibrotactile stimuli to improve balance control.

Vestibular Prosthesis One promising approach is providing electrical stimulation via a vestibular prosthesis to mimic vestibular sensation [270–272]. Research using animal models demonstrated that vestibular reflexes could be effectively driven by direct electrical stimulation of vestibular afferent neurons [273, 274]. Similar results have been reported in humans with BVH who have received a vestibular implant and been tested in laboratory settings [271, 275–277]. The Labyrinth Devices MVI™ Multichannel Vestibular Implant system is currently the only human vestibular implant with the prosthesis on continuously 24 h/day. Long-term use of this implant produced stable improvements in VOR eye movement responses [278], more importantly, a phenomenal improvement in quality of life, walking abilities, and postural control of BVL patients [279]. The potential benefits of vestibular rehabilitation exercises for implanted patients remains to be determined.

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Vibrotactile Stimuli The idea behind vibrotactile belts or shoes is to promote sensory substitution by “replacing” or augmenting the information that should be provided by a defective vestibular system by using sensory input from augmented tactile cues. For example, a belt fitted with actuators that deliver vibrotactile stimulus to the waist when the subject leans significantly from an upright position [280]. By using such a belt, patients with UVH showed better control of their body sway during perturbed standing and tandem walking [281]. Even patients with BVH report improved quality of life as their mobility and balance control are improved after using a vibro-tactile belt [282]. Interestingly, community-dwelling elderly who used vibrotactile stimulus for 8 weeks as part of their balance training improved their vestibular reliance during postural testing [283]. However, even though vibrotactile stimuli are simple noninvasive devices as well as showing promising results, the effect of vestibular rehabilitation together with vibrotactile stimuli remains to be determined.

Virtual Reality/Augmented Reality Virtual reality has long been available to researchers in the field of vestibular science and rehabilitation [203, 284–286], and with the recent availability of low cost consumer systems it is now more available for home and clinic use [287–290]. Immersive virtual reality games that require head motion lead to improvements in the vestibulo-ocular reflex and also improvements in balance [291–294]. Nonimmersive virtual reality game play such as the Nintendo Wii™ has also been shown to improve outcomes after vestibular rehabilitation [295]. Augmented reality glasses may also be helpful in certain circumstances for individuals with vestibular loss to address oscillopsia [296] or imbalance and falls [297]. Additional studies are needed to determine whether technology driven vestibular rehabilitation consistently leads to better outcomes [284, 293], but it may lead to greater participation because of higher engagement and adherence [298].

Incremental VOR Adaptation The downside of more traditional gaze stability exercises is that they cause an immediate large error signal for large deficits in VOR gain. A gradually increasing error signal drives the VOR more efficiently [299]. A novel rehabilitation device for patients who suffer from reduced VOR gain due to vestibular hypo function showed promising results by using the incremental VOR adaptation (IVA) paradigm [300, 301]. An interesting case report demonstrates the IVA paradigm’s benefits presents a 51 years-old patient who suffered for 20 years from bilateral vestibular loss. The

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patient had daily training with an IVA device, for 15 min, for 645 days. He demonstrated dramatically improved VOR gains. Additionally, his gait and balance ability also improved. These results suggest a transfer effect from VOR adaptation training to balance performances [302].

Team Approach to Vestibular Rehabilitation Optimal rehabilitation management for persons with vestibular disorders requires a team approach [303]. Since rehabilitation strategies often depend on accurate differential diagnosis, multiple specialists may need to be involved [304, 305]. Comorbid symptoms of anxiety/depression and inappropriate compensatory strategies or catastrophizing should be identified and addressed concurrently with appropriate referrals [208, 306], hoping to prevent a transition to PPPD [105, 304, 307]. Open communication between vestibular rehabilitation providers and referring physicians is important especially for individuals who are not progressing along an expected trajectory or may need additional medical management [306]. Ultimately, a team approach is highly recommended and only serves to enhance patient care for individuals with symptoms and impairments caused by vestibular dysfunction [308].

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Chapter 15

Vestibular Implants E. Loos, N. Verhaert, E. Devocht, N. Guinand, A. Perez-Fornos, C. Desloovere, and R. van de Berg

Introduction During the last few decades, much research has been performed to develop an implantable vestibular prosthesis to artificially restore vestibular function. The concept is similar to a cochlear implant (CI), which has already been used for many years for treating severe sensorineural hearing loss. The vestibular implant (VI) aims to provide the E. Loos (*) Department of Neurosciences, Research Group ExpORL, KU Leuven, University of Leuven, Leuven, Belgium Department of Otorhinolaryngology-Head and Neck Surgery, University Hospitals Leuven, Leuven, Belgium Department of ENT/Audiology, School for Mental Health and Neuroscience (MHENS), Maastricht University Medical Center, Maastricht, The Netherlands e-mail: [email protected] N. Verhaert · C. Desloovere Department of Neurosciences, Research Group ExpORL, KU Leuven, University of Leuven, Leuven, Belgium Department of Otorhinolaryngology-Head and Neck Surgery, University Hospitals Leuven, Leuven, Belgium e-mail: [email protected]; [email protected]; christian.desloovere@ uzleuven.be E. Devocht · R. van de Berg Department of ENT/Audiology, School for Mental Health and Neuroscience (MHENS), Maastricht University Medical Center, Maastricht, The Netherlands e-mail: [email protected]; [email protected] N. Guinand · A. Perez-Fornos Division of Otorhinolaryngology and Head-and-Neck Surgery, Department of Clinical Neurosciences, Geneva University Hospitals, Geneva, Switzerland e-mail: [email protected]; [email protected] © The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 B. T. Crane et al. (eds.), Disorders of the Vestibular System, https://doi.org/10.1007/978-3-031-40524-2_15

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central nervous system with information about head spatial orientation and movement. The pioneering work of Bernard Cohen and Jun-Ichi Suzuki in the 1960s, who first described eye movements originating from electrically stimulating the ampullary nerves of rabbits, pigeons, cats, and monkeys [1], inspired Gong and Merfeld, who described the first vestibular prosthesis that was tested in guinea pigs [2]. Those animal experiments paved the way for human research. In 2004, the first human patients underwent vestibular stimulation before undergoing surgery for cochlear implantation or surgical labyrinthectomy [3]. In these trials, it was confirmed that electrical stimulation of the ampullary nerves could produce a nystagmic response aligned with the plane of the stimulated canal. After this proof of concept, Guyot et al. performed the first vestibular implantation in humans in 2007 [4]. This implant was a modified CI (MED-EL, Innsbruck, Austria), in which one electrode was removed from the cochlear array and implanted in the vicinity of the posterior ampullary nerve. It was demonstrated that a patient could adapt to electrical stimulation of the vestibular system without too much discomfort and that, once the adaptation was completed, the electrical stimulation could be modulated to artificially evoke smooth eye movements [5]. As these prerequisites for developing a VI were fulfilled, the implant was modified into a multichannel prosthesis and implanted for the first time in 2012 by the Geneva-Maastricht Group [6]. At the moment, two main types of VIs exist: the semicircular canal implants and the otolith implants. There are two subtypes of semicircular canal (SCC) implants: pure VIs and cochleovestibular implants, which combine a CI with a VI. In this chapter, we provide an overview of current knowledge concerning VI candidacy, operative techniques, device programming, clinical outcomes, possible complications, and a future outlook.

Candidacy To date, VIs are only available in a research setting, and therefore no reimbursement criteria exist. They are mainly developed to treat patients with bilateral vestibulopathy (BV). This is a very debilitating disorder that can lead to a broad spectrum of symptoms like, for example, postural instability, impairment of spatial orientation, and distorted vision in dynamic conditions (i.e., while walking), commonly known as oscillopsia. It has been conservatively estimated that more than 1.8 million people worldwide have severe bilateral vestibular loss, but this is probably an underestimation [7]. To date, BV has a poor prognosis, as more than 80% of the patients experience no significant improvement despite vestibular rehabilitation [8]. Vestibular implantation could be the solution for treating this debilitating condition. To facilitate comparison of results from different studies, VI-implantation criteria were proposed by van de Berg et al. [9] (Table 15.1) in cooperation with all current research groups. The diagnostic criteria for BV, according to the Bárány Society, were modified and extended because they are solely based on the horizontal vestibular-­ ocular reflex (VOR) function. As vestibular implantation is practically irreversible and can cause a deterioration of residual vestibular functions, it was important to include

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Table 15.1  VI implantation criteria for BV as described by van de Berg et al. [9] A. Chronic vestibular syndrome with the following disablinga symptoms:  •  Unsteadiness when walking or standing plus at least one of the following:    –  Movement-induced blurred vision or oscillopsia during walking or quick head/body movements, and/or    –  Worsening of unsteadiness in darkness and/or on uneven ground B. Symptoms greatest during head movement C. Bilaterally reduced or absent angular VOR function documented by at least one of the following major criteria:  •  Bilaterally pathological horizontal angular VOR gain ≤0.6 and at least bilaterally one vertical angular VOR gain