Neurogenic Dysphagia 3030421392, 9783030421397

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Neurogenic Dysphagia Tobias Warnecke Rainer Dziewas Susan Langmore

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Neurogenic Dysphagia

Tobias Warnecke • Rainer Dziewas Susan Langmore

Neurogenic Dysphagia

Tobias Warnecke Department of Neurology University of Münster Münster Germany Susan Langmore Department of Otolaryngology Boston University Boston, MA USA

Rainer Dziewas Department of Neurology and Neurorehabilitation Klinikum Osnabrück Osnabrück Germany

Originally published in German: Neurogene Dysphagien by Tobias Warnecke, Rainer Dziewasc © W. Kohlhammer GmbH 2013, second extended and revised edition 2018. All rights reserved ISBN 978-3-030-42139-7    ISBN 978-3-030-42140-3 (eBook) https://doi.org/10.1007/978-3-030-42140-3 © Springer Nature Switzerland AG 2021 This work is subject to copyright. All rights are reserved 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

“Over the next 20 years, the face of dysphagia evaluation and treatment may change drastically. […] It is an exciting and stimulating area in which to practice. Our patients benefit from our efforts, and we derive pleasure from witnessing their progress. The rewards are great; after all, to many people, fewer pleasures are more satisfying than a glass of wine and a good meal.” (Langmore 2001, p. 249) “The best answer to the question of who should perform FEES is whoever understands oropharyngeal dysphagia best. […] FEES now has a secure place in the armamentarium of tools used to evaluate and manage this disorder. As the scoring system becomes better validated and technology allows more quantification of findings, its use will become ever more valuable.” (Langmore 2017, pp. 34–35)

Preface

Neurological disorders, such as stroke, dementia, Parkinson’s disease, or neuromuscular diseases, are the most common causes of swallowing disorders. Neurogenic dysphagia has significant consequences for those affected as it impacts on the quality of life, and is associated with malnutrition, aspiration pneumonia, and even death. According to recent data, up to 50% of all neurological patients suffer from a swallowing disorder. Today, neurogenic dysphagia plays an important role in the daily practice of acute-care hospitals, rehabilitation clinics, nursing homes, and outpatient care. With the aging of the population and the greater emergence of neurodegenerative diseases, neurogenic dysphagia will take on an even more important role in the future. In the next few years, the demographic changes in our population will lead not only to a steady increase in neurological diseases but thereby also to a corresponding increase in the frequency of neurogenic dysphagia. Against this background, a rapid development of different diagnostic modalities and new treatment options for neurogenic dysphagia has taken place. Over the years, the use of flexible endoscopic evaluation of swallowing (FEES) has grown incrementally. When Susan Langmore first published on this procedure in 1988, there were only a handful of clinicians using this tool to assess swallowing. Today, FEES is a well-established procedure done throughout the world. It has been embraced by clinical specialists who evaluate dysphagia, including speech and language pathologists (SLPs), gastroenterologists, otolaryngologists, phoniatrists, vii

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geriatricians, rehabilitation physicians, physiatrists, and neurologists. There have been very few textbooks written about FEES in general (Langmore 2001; Aviv and Murray 2005). The content of the present book is focused on neurological disorders but will be relevant to practitioners who see other patients as well. The main approach presented here is to customize the exam in order to uncover the nature of the disorder and to address the specific purpose of the exam. This means not to adhere to the “one size fits all” principle at all and this may be a refreshing change from some overly rigid protocols in use. The use of FEES to assess neurogenic dysphagia has become firmly established in neurology and has significantly enhanced the clinical understanding of the complex patterns of neurogenic dysphagia by enabling a direct visualization of the act of swallowing. Today, specific endoscopic protocols allow standardized examinations of special subtypes of neurogenic dysphagia. In the future, swallowing endoscopy is likely to become just as common as the instrumental procedures routinely used by neurologists, such as EEG, EMG, and ultrasound. In order to take account of the increased knowledge in the field and to enable a broad spectrum of training in swallowing endoscopy, a FEES training curriculum for neurogenic dysphagia was first developed by the German Neurological Society, the German Stroke Society and the German Society for Geriatrics. A similar FEES training program was recently also established by the European Society for Swallowing Disorders (ESSD). This book covers all content requirements of these FEES training curriculums. With the aid of FEES and other modern instrumental methods of investigation, it is becoming increasingly possible to classify the various forms of dysphagia both phenomenologically and pathophysiologically. These findings are facilitating the development of completely novel therapeutic approaches in the future. Due to the specific and complex combination of different symptoms that result from underlying neurological disorders, it is becoming clear that neurogenic dysphagia is not a simple symptom but rather a multi-etiological syndrome. Analogous to aphasia syndromes, it is now possible to speak of neurogenic dysphagia syndromes, although etiology is considerably more heterogeneous than in the field of aphasias. In this book, modern neurological systematics are consistently applied to neurogenic dysphagia syndromes, whose clinical relevance is emphasized. The modern diagnosis of and therapy for neurogenic dysphagia are thus a highly differentiated, expansive, and extremely exciting field of medicine in which different specialist groups work together in an interdisciplinary manner. The aim of this book is to impart practical knowledge on the current state of clinical research. Wherever possible, practical guidance is provided for diagnostics and therapy in the daily care of patients with neurogenic dysphagia. The supplemental electronic material makes use of video samples to demonstrate various patterns of neurogenic dysphagia that have direct practical relevance. In addition to already available diagnostic and therapeutic procedures, the various chapters of the book also reveal the areas in which there is a particularly urgent need for additional research. The book is also intended to provide easy access and fast information to colleagues who have no special knowledge in this field. We would also be very pleased to see the work used as a reference source that can prove helpful to its readers.

Preface

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In medical textbooks, drawings provided by illustrators with special medical expertise are very rare. We are therefore proud that Heike Blum and Esther Gollan have created numerous informative illustrations for this book that considerably enhance readers’ understanding of the highly complex process of swallowing and its coordination. These images are not mere schematic drawings but rather extremely precise and detailed representations that are intended to aid in the understanding of even more complex relationships by visually depicting the described details. Despite our careful attention to detail, this book will naturally contain room for improvement. It is therefore our great wish that readers inform us of any mistakes, send suggestions and comments, and contribute constructively to the further optimization of a future edition. We are most grateful to Andrea Ridolfi from Springer for his exceptional collaboration and patient support during the completion of this book. We would like to thank Ryan DeLaney for expert help with the English translation. We also wish to thank our families for their continued support and understanding of the requirements of our work. Finally, we are impressed by the enthusiasm and motivation with which neurogenic dysphagia is today being examined and treated by multidisciplinary teams consisting of SLPs and physicians of various disciplines. These dysphagia teams have recently been described as ideal “think tanks” because they can examine issues from a variety of perspectives and thereby generate creative ideas and solutions together. In this sense, we hope that the readers of this book will profit from its lessons. Münster, Germany Osnabrück, Germany  Boston, MA, USA 

Tobias Warnecke Rainer Dziewas Susan Langmore

Contents

1 Neuroanatomy and Physiology of Deglutition������������������������������������������   1 1.1 The Unimpaired Swallow ������������������������������������������������������������������   1 1.2 The Impaired Swallow������������������������������������������������������������������������   8 1.3 Central Coordination of Swallowing��������������������������������������������������  11 1.3.1 Brainstem Swallowing Centers����������������������������������������������  11 1.3.2 Supramedullary Coordination of Swallowing������������������������  13 1.3.3 Hemispheric Specialization����������������������������������������������������  14 1.3.4 Cortical Plasticity: Compensation of Disease-Related Dysfunction����������������������������������������������������������������������������  18 1.3.5 Cortical Plasticity: Sensory Stimulation to Enhance Reorganization������������������������������������������������������������������������  29 References����������������������������������������������������������������������������������������������������  34 2 Clinical Procedures��������������������������������������������������������������������������������������  39 2.1 Introduction����������������������������������������������������������������������������������������  39 2.2 History������������������������������������������������������������������������������������������������  40 2.3 Aspiration Screening��������������������������������������������������������������������������  43 2.4 The Clinical Swallowing Examination ����������������������������������������������  49 References����������������������������������������������������������������������������������������������������  51 3 FEES and Other Instrumental Methods for Swallowing Evaluation ����  55 3.1 FEES ��������������������������������������������������������������������������������������������������  56 3.1.1 Introduction����������������������������������������������������������������������������  56 3.1.2 Equipment ������������������������������������������������������������������������������  58 3.1.3 Standard FEES Protocol ��������������������������������������������������������  59 3.1.4 Specific Neurological Protocols����������������������������������������������  64 3.1.5 Key Findings and Their Rating ����������������������������������������������  68 3.1.6 Endoscopic Classification of Neurogenic Dysphagia ������������  75 3.1.7 Documentation of Endoscopic Findings��������������������������������  76 3.1.8 Training Curriculum: “FEES for Neurogenic Dysphagia” ����  80 3.2 Videofluoroscopic Swallowing Study (VFSS)������������������������������������  81 3.2.1 Indications������������������������������������������������������������������������������  81 3.2.2 Technique��������������������������������������������������������������������������������  82 3.2.3 Radiation Exposure����������������������������������������������������������������  82

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3.2.4 Contrast Agents����������������������������������������������������������������������  82 3.2.5 Procedure��������������������������������������������������������������������������������  83 3.2.6 Findings����������������������������������������������������������������������������������  85 3.2.7 Comparing VFSS and FEES ��������������������������������������������������  88 3.3 Manometric Evaluation of Swallowing����������������������������������������������  89 3.3.1 Conventional Manometry�������������������������������������������������������  90 3.3.2 High-Resolution Manometry��������������������������������������������������  90 3.4 Electromyographic Evaluation of Swallowing ����������������������������������  94 3.5 Sonographic Evaluation of Swallowing����������������������������������������������  95 3.6 Magnetic Resonance Imaging and Computed Tomography ��������������  97 3.7 Differential Indication of Instrumental Dysphagia Diagnostics ��������  99 References���������������������������������������������������������������������������������������������������� 100 4 Special Findings in Neurogenic Dysphagia������������������������������������������������ 109 4.1 Stroke�������������������������������������������������������������������������������������������������� 110 4.2 Dementia �������������������������������������������������������������������������������������������� 116 4.2.1 Alzheimer’s Disease��������������������������������������������������������������� 117 4.2.2 Vascular Dementia������������������������������������������������������������������ 119 4.2.3 Frontotemporal Dementia ������������������������������������������������������ 119 4.2.4 Dementia with Lewy Bodies�������������������������������������������������� 120 4.2.5 Presbyphagia �������������������������������������������������������������������������� 121 4.3 Movement Disorders�������������������������������������������������������������������������� 124 4.3.1 Parkinsonian Syndromes�������������������������������������������������������� 124 4.3.2 Chorea ������������������������������������������������������������������������������������ 138 4.3.3 Dystonias�������������������������������������������������������������������������������� 140 4.3.4 Wilson’s Disease �������������������������������������������������������������������� 146 4.4 Inflammatory Diseases of the Central Nervous System��������������������� 147 4.4.1 Multiple Sclerosis ������������������������������������������������������������������ 147 4.4.2 Bacterial and Viral Meningoencephalitis�������������������������������� 150 4.4.3 CNS Listeriosis ���������������������������������������������������������������������� 150 4.4.4 Poliomyelitis and Post-polio Syndrome �������������������������������� 150 4.4.5 Tetanus������������������������������������������������������������������������������������ 151 4.5 Tumors������������������������������������������������������������������������������������������������ 153 4.5.1 Brain Tumors and Metastases ������������������������������������������������ 153 4.5.2 Neoplastic Meningitis ������������������������������������������������������������ 154 4.5.3 Paraneoplastic Syndromes������������������������������������������������������ 154 4.6 Motor Neuron Disorders �������������������������������������������������������������������� 156 4.6.1 Amyotrophic Lateral Sclerosis ���������������������������������������������� 156 4.6.2 Hereditary Spastic Paraplegia ������������������������������������������������ 161 4.6.3 Spinal and Bulbar Muscular Atrophy (Kennedy’s Disease) �� 162 4.7 Polyneuropathy ���������������������������������������������������������������������������������� 163 4.7.1 Guillain–Barré Syndrome ������������������������������������������������������ 164 4.7.2 Critical Illness Polyneuropathy and Myopathy���������������������� 165 4.8 Neuromuscular Transmission Disorders �������������������������������������������� 167

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4.8.1 Myasthenia Gravis������������������������������������������������������������������ 167 4.8.2 Lambert–Eaton Myasthenic Syndrome���������������������������������� 170 4.8.3 Botulism���������������������������������������������������������������������������������� 171 4.9 Myopathies������������������������������������������������������������������������������������������ 172 4.9.1 Myositis���������������������������������������������������������������������������������� 172 4.9.2 Oculopharyngeal Muscular Dystrophy ���������������������������������� 176 4.9.3 Oculopharyngodistal Myopathy��������������������������������������������� 177 4.9.4 Metabolic Myopathies������������������������������������������������������������ 178 4.9.5 Facioscapulohumeral Muscular Dystrophy���������������������������� 179 4.9.6 Myotonic Dystrophies������������������������������������������������������������ 180 4.10 Trauma������������������������������������������������������������������������������������������������ 182 4.10.1 Traumatic Brain Injury����������������������������������������������������������� 182 4.10.2 Spinal Cord Trauma���������������������������������������������������������������� 184 4.11 Psychogenic Dysphagia���������������������������������������������������������������������� 185 4.12 Others�������������������������������������������������������������������������������������������������� 187 4.12.1 Hereditary Ataxias������������������������������������������������������������������ 187 4.12.2 Niemann–Pick Disease, Type C���������������������������������������������� 188 4.12.3 Chiari Type I Malformation���������������������������������������������������� 189 4.12.4 Palatal Myoclonus (Palatal Tremor) �������������������������������������� 190 4.12.5 Diffuse Idiopathic Skeletal Hyperostosis�������������������������������� 191 4.12.6 Surgery������������������������������������������������������������������������������������ 193 4.12.7 IgLON5 Syndrome����������������������������������������������������������������� 194 4.12.8 Internal Diseases �������������������������������������������������������������������� 195 4.13 Algorithm for a Structured Assessment of Patients with Neurogenic Dysphagia���������������������������������������������������������������� 196 References���������������������������������������������������������������������������������������������������� 202 5 Using FEES in the Treatment and Management of Neurogenic Dysphagia: General Principles and Methodologies���������������������������������� 223 5.1 Introduction���������������������������������������������������������������������������������������� 223 5.2 FEES as a Therapeutic Examination (in Comparison to VFSS)�������� 224 5.2.1 Use of Behavioral Strategies During the Examination ���������� 225 5.2.2 Selecting the Appropriate Therapeutic Strategy �������������������� 226 5.2.3 The Weak or Ineffective Swallow with Reduced Bolus Clearance�������������������������������������������������������������������������������� 226 5.2.4 The Misdirected Swallow: Impaired Airway Protection Due to Incomplete Valving������������������������������������ 231 5.2.5 The Delayed or Mistimed Swallow���������������������������������������� 234 5.2.6 Ice Chip Protocol�������������������������������������������������������������������� 235 5.2.7 FEES as an Educational Tool to Increase Patient Compliance ���������������������������������������������������������������������������� 236 5.2.8 FEES as Biofeedback Tool in Therapy ���������������������������������� 237 5.2.9 FEES as a Tool to Reevaluate Patients (Serial FEES)������������ 239 References���������������������������������������������������������������������������������������������������� 240

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6 Using FEES in the Stroke Unit and the Intensive Care Unit ������������������ 241 6.1 Stroke Unit������������������������������������������������������������������������������������������ 242 6.1.1 Dysphagia Management in the Stroke Unit���������������������������� 242 6.1.2 Classification and Management of Post-Stroke Dysphagia���� 249 6.2 Intensive Care Unit ���������������������������������������������������������������������������� 253 6.2.1 Epidemiology and Complications of Critical Illness Dysphagia ������������������������������������������������������������������������������ 253 6.2.2 Etiology and Pathophysiology of Critical Illness Dysphagia 253 6.2.3 Applications of FEES in the ICU������������������������������������������� 256 References���������������������������������������������������������������������������������������������������� 263 7 Treatment of Neurogenic Dysphagia���������������������������������������������������������� 267 7.1 Evidence-Based Medicine������������������������������������������������������������������ 268 7.2 General Treatment Options ���������������������������������������������������������������� 269 7.2.1 Behavioral Swallowing Therapy�������������������������������������������� 270 7.2.2 Pharmacotherapy�������������������������������������������������������������������� 279 7.2.3 Surgical Treatment Options���������������������������������������������������� 283 7.3 Disease-Specific Therapy�������������������������������������������������������������������� 285 7.3.1 Stroke�������������������������������������������������������������������������������������� 285 7.3.2 Dementia �������������������������������������������������������������������������������� 295 7.3.3 Parkinson’s Disease���������������������������������������������������������������� 296 7.3.4 Progressive Supranuclear Paralysis���������������������������������������� 308 7.3.5 Multiple System Atrophy�������������������������������������������������������� 309 7.3.6 Dystonias�������������������������������������������������������������������������������� 310 7.3.7 Wilson’s Disease �������������������������������������������������������������������� 310 7.3.8 Huntington’s Disease�������������������������������������������������������������� 310 7.3.9 Multiple Sclerosis ������������������������������������������������������������������ 312 7.3.10 Tetanus������������������������������������������������������������������������������������ 313 7.3.11 Brain Tumors�������������������������������������������������������������������������� 314 7.3.12 Amyotrophic Lateral Sclerosis (ALS)������������������������������������ 314 7.3.13 Spinobulbar Muscular Atrophy (Kennedy’s Disease)������������ 318 7.3.14 Guillain–Barré syndrome�������������������������������������������������������� 318 7.3.15 Myasthenia Gravis������������������������������������������������������������������ 319 7.3.16 Myopathies (Including Myositis)�������������������������������������������� 320 7.3.17 Traumatic Brain Injury����������������������������������������������������������� 323 7.3.18 Hereditary Ataxia�������������������������������������������������������������������� 324 7.4 Neurostimulation�������������������������������������������������������������������������������� 324 7.4.1 Transcranial Magnetic Stimulation���������������������������������������� 325 7.4.2 Transcranial Direct-Current Stimulation�������������������������������� 327 7.4.3 Pharyngeal Electrical Stimulation������������������������������������������ 330 7.4.4 Neuromuscular Electrical Stimulation������������������������������������ 335 References���������������������������������������������������������������������������������������������������� 337 8 Nutritional Requirements in Patients with Neurogenic Dysphagia�������� 353 8.1 Introduction���������������������������������������������������������������������������������������� 353 8.2 Pathophysiology of Malnutrition�������������������������������������������������������� 354

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8.3 Diagnostics������������������������������������������������������������������������������������������ 355 8.4 Treatment of Malnutrition������������������������������������������������������������������ 356 8.4.1 Oral Nutritional Therapy�������������������������������������������������������� 357 8.4.2 Artificial Nutrition������������������������������������������������������������������ 362 References���������������������������������������������������������������������������������������������������� 364 Appendix. Scales and Scores ���������������������������������������������������������������������������� 367 Swallowing Quality-of-Life Questionnaire (SWAL-QoL), based on Dysphagia 2000, 15(3):115–121, and Dysphagia 2000; 15(3):122–133, Courtesy of Prof. McHorney���������� 367 Instructions for Completing the SWAL-QOL Survey���������������������������������� 367 Swallowing Disturbance Questionnaire (SDQ), from Manor et al. Movement Disorders 2007; 22(13):1917–1921, with permission�������������������������������������������������� 377 Munich Dysphagia Test: Parkinson’s Disease (MDT-PD), simons 2012, Courtesy of Dr. Janine Simons�������������������������� 378 Gugging Swallowing Screen (GUSS), from Trapl et al, Stroke 2007; 38(11):2948–2952, with permission�������������������������������������� 381 Flexible Endoscopic Dysphagia Severity Scale for Acute Stroke Patients (FEDSS), from Dziewas et al., Cerebrovasc Dis. 2008;26:41–7, with permission �������������������������������������� 383 FEES Levodopa Test, from Warnecke et al., Mov Disord. 2010;25:1239–45, with permission���������������������������������������� 384 FEES Tensilon Test (Tensilon = Edrophonium Chloride), from Warnecke et al., J Neurol. 2008;255:224–30, with permission�������������������������������������������������������������� 386 Murray Secretion Rating Scale (Short version), from Murray et al., Dysphagia 1996; 11:99–103, with permission�������������������������������������������� 387 Murray Secretion Rating Scale (Long Version), from Murray et al. Dysphagia 1996; 11:99–103, with permission�������������� 388 Penetration-Aspiration Scale (PAS), from Rosenbek et al., Dysphagia 1996; 11:93–98, with permission���������������������������������������������� 389 Functional Oral Intake Scale (FOIS), from Crary et al., Arch Phys Med Rehabil 2005; 86:1516–1520, with permission ���������������� 390 Dysphagia Outcome and Severity Scale (DOSS), from O’Neil et al. Dysphagia 1999; 14:139–145, with permission������������ 391 Standardized Endoscopic Swallowing Evaluation for Tracheostomy Decannulation in Critically Ill Neurologic Patients (SESETD Protocol), from Warnecke et al., Crit Care Med, 2013; 41(7):1728–1732, with permission�������������������������� 392 Index�������������������������������������������������������������������������������������������������������������������� 393

Abbreviations

AD AFM ALS AWMF

Alzheimer’s disease Airflow method Amyotrophic lateral sclerosis Arbeitsgemeinschaft der Wissenschaftlichen Medizinischen Fachgesellschaften e.V. [Association of Scientific Medical Societies in Germany] ÄZQ Ärztliche Zentralstelle für Qualitätssicherung [German Agency for Quality in Medicine] BMD Becker muscular dystrophy BMI Body mass index BODS Bogenhausener Dysphagia Score BRACS Boston Residue and Clearance Scale CBD Corticobasal degeneration CBS Corticobasal syndrome CEA Carotid endarterectomy CIM Critical illness myopathy CIP Critical illness polyneuropathy CNS Central nervous system COPD Chronic obstructive pulmonary disease CPEO Chronic progressive external ophthalmoplegia CPG Central pattern generator CRT Cough Reflex Test CSS Collet–Sicard syndrome DES Diffuse esophageal spasm DGEM Deutsche Gesellschaft für Ernährungsmedizin [German Society for Nutritional Medicine] DGN Deutsche Gesellschaft für Neurologie [German Neurological Society] DISH Diffuse idiopathic skeletal hyperostosis DM Dermatomyositis DMD Duchenne muscular dystrophy DSG Dorsal swallowing group DSI Digital spot imaging DTI Diffusion tensor imaging xvii

xviii

Abbreviations

EBM Evidence-based medicine EDSS Expanded disability status scale EEG Electroencephalography EMG Electromyography EMGBF EMG biofeedback EMST Expiratory muscle strength training EPI Echo-planar imaging ESPEN European Society for Clinical Nutrition and Metabolism F.O.T.T.® Facial-Oral Tract Therapy FDT Functional dysphagia therapy FEDSS Flexible endoscopic dysphagia severity scale for acute stroke patients; FEES Flexible endoscopic evaluation of swallowing FEESST Flexible endoscopic evaluation of swallowing with sensory testing fMRI Functional magnetic resonance imaging FSHD Facioscapulohumeral muscular dystrophy FST Fatigable swallow test FTD Frontotemporal dementia FTLD Frontotemporal lobar degeneration GBS Guillain–Barré syndrome GCS Glasgow Coma Scale GUSS Gugging Swallowing Screen HBE Harris–Benedict equation HRM High-resolution manometry HSP Hereditary spastic paraplegia IBM Inclusion body myositis ICU Intensive care unit IDDSI International Dysphagia Diet Standardisation Initiative KD Kennedy’s disease KSS Kearns–Sayre syndrome LBD Lewy body dementia LEMS Lambert–Eaton myasthenic syndrome LGMD Limb-girdle muscular dystrophy Lee Silverman Voice Treatment LSVT® LTD Long-term depression LTP Long-term potentiation LTV Long-term ventilation MBS Modified barium swallow MC Myasthenic crisis MDS Münster Dysphagia Score MDT Munich Dysphagia Test MEBDT Modified Evan’s blue dye test MEG Magnetoencephalography MEP Motor-evoked potential MFS Miller Fisher syndrome

Abbreviations

MG Myasthenia gravis MJD Machado–Joseph disease MM Mendelsohn maneuver MNA Mini nutritional assessment MNDs Motor neuron diseases MS Multiple sclerosis MSA Multiple system atrophy mSv MilliSievert MUST Malnutrition Universal Screening Tool NA Nucleus ambiguus NAS Neuroacanthocytosis syndromes NBIA Neurodegeneration with brain iron accumulation NMES Neuromuscular electrical stimulation NMO Neuromyelitis optica NMT Neuromyotonia NPC Niemann–Pick disease, type C NPD Niemann–Pick disease NRS Nutritional risk screening OFC Orbitofrontal cortex OM Overlap myositis OPDM Oculopharyngodistal myopathy OPMD Oculopharyngeal muscular dystrophy OPP Oral preparatory phase ORL Otorhinolaryngology OSAS Obstructive sleep apnea syndrome OTT Oral transit time PAS Penetration–Aspiration Scale PD Parkinson’s disease PEG Percutaneous endoscopic gastrostomy PES Pharyngeal Electrical Stimulation PET Positron-emission tomography PKAN Pantothenate kinase-associated neurodegeneration PM Polymyositis PNS Peripheral nervous system PPA Primary progressive aphasia PSP Progressive supranuclear palsy PTT Pharyngeal transit time RASSS Rapid Aspiration Screening for Suspected Stroke RLN Recurrent laryngeal nerve rTMS Repetitive transcranial magnetic stimulation SBMA Spinal and bulbar muscular atrophy SCA Spinocerebellar ataxia SCLC Small-cell lung cancer SD Semantic dementia SGSM Supraglottic swallow maneuver

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xx

SjS Sjögren syndrome SLE Systemic lupus erythematosus SMA Supplementary motor areas SN Solitary nucleus SPT Swallowing Provocation Test SSA Standardized Swallowing Assessment SSGSM Super supraglottic swallow maneuver SU Stroke unit TBI Traumatic brain injury tDCS Transcranial direct-current stimulation TMS Transcranial magnetic stimulation TOR-BSST© Toronto Bedside Swallowing Screening Test UES Upper esophageal sphincter UPDRS Unified Parkinson’s Disease Rating Scale VAST Video-assisted swallowing therapy VD Vascular dementia VFS Videofluoroscopy VFSS Videofluoroscopic swallowing study VLM Ventrolateral medulla oblongata VPC Velopharyngeal closure VSG Ventral swallowing group VVST Volume-Viscosity Swallow Test WD Wilson’s disease YPRSRS Yale Pharyngeal Residue Severity Rating Scale

Abbreviations

List of Videos

Video 3.1 Normal velopharyngeal closure Video 3.2 Incomplete velopharyngeal closure Video 3.3 Saliva pooling in the pyriform sinus Video 3.4 Fasciculations Video 3.5 Normal base of tongue movement Video 3.6 Normal pharyngeal squeeze maneuver Video 3.7 Pharyngeal palsy on the left side Video 3.8 Normal vocal cord movement Video 3.9 Vocal cord palsy on the left side Video 3.10 Premature spillage Video 3.11 Test of oral containment Video 3.12 Delayed swallowing reflex Video 3.13 Absent swallowing reflex Video 3.14 Penetration and aspiration Video 3.15 Vallecular residue Young IPG

S1 M1

IFG MFG

SFG MFG M1 & IFG

MFG

MFG

IFG Tri Y: 4

X: 58 S1

Z: 6

Young > Old MFG

S1 S1

X: -50

Y: -38 p < 0.05

Z: 59 3.88

T

9.60

p80–90%) or to rule it out (specificity: >50%; Doggett et al. 2002). As of yet, however, only a few of the screening methods proposed in the literature fulfill these criteria, meaning that a combination of several tests may be needed to achieve sufficiently founded clinical guidance (Bours et al. 2009). One of the key underlying issues with aspirations screening is the fact that only indirect signs of aspiration can be detected with these tests. However, about 50% of patients who aspirate do not cough, and this silent aspiration therefore goes unnoticed by the examiner. It should also be noted that most of the tests have been developed and validated for specific groups of patients, and the results are not easily transferable to other groups. Several studies have attempted to predict the occurrence of aspiration or penetration based on various clinical findings and constellations (Daniels et  al. 1997; Logemann et al. 1999; McCullough et al. 2001). For example, Logemann et al. (1999) used a detailed test with 28 items from five categories: (1) medical history, (2) behavioral data, (3) general motor skills, (4) oral motor examination, and (5) swallowing evaluation. As part of a relatively detailed clinical swallowing examination combined with a water swallow test, Daniels et al. (1997) observed that at least two of the following six symptoms were predictive of aspiration in acute stroke patients (sensitivity: 92%; specificity: 67% compared to videofluoroscopy as gold standard): dysphonia, dysarthria, an impaired voluntary cough, a pathological gag reflex, coughing, or a change in voice quality within 1 min of the water test. In the water test used here, the patients had to drink a total of 70 ml from a cup (if necessary, with a straw) in quantities of 5, 10, and 20 ml. Each volume was tested twice, and immediately after swallowing, the patient was asked to phonate to assess voice quality. However, in many studies, the clinical findings have displayed insufficient sensitivity and/or specificity (Bours et al. 2009). In order to provide a better overview, the

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various screening methods can be roughly summarized in four categories, although there are overlaps in several variants: • Water swallow tests: –– 50-ml water test (Gottlieb et al. 1996; Kidd et al. 1993) –– 50-ml water test combined with pulse oximetry (Smith et  al. 2000; Lim et al. 2001) –– 70-ml water test (Daniels et al. 1997) –– 90-ml water test (DePippo et al. 1992; Suiter and Leder 2008) –– 100-ml water test (Wu et al. 2004) –– Timed water swallow test (Nathadwarawala et  al. 1992; Hughes and Wiles 1996; Hinds and Wiles 1998) –– Dysphagia limit test (Ertekin et al. 1996) –– Standardized swallowing assessment (SSA) (Perry 2001a, b) –– Toronto bedside swallowing screening test (TOR-BSST©; Martino et al. 2009; Martino et al. 2014). • Tests with multiple food consistencies: –– Gugging swallowing screen (GUSS) (Trapl et al. 2007) –– Semi-solid bolus swallow test (Schultheiss et al. 2011) –– Volume-viscosity swallow test (VVST) (Clavé et al. 2008) • Protective reflex provocation tests: –– Swallowing provocation test (SPT) (Teramoto et  al. 1999; Teramoto and Fukuchi 2000; Warnecke et al. 2008a) –– Cough reflex test (CRT; Wakasugi et al. 2008, Miles et al. 2013) • Tests for patients with a tracheal cannula: –– Modified Evan’s blue dye test (MODS; Cameron et  al. 1973; Thompson-­ Henry and Braddock 1995; Brady et al. 1999). The different water tests vary in the amount of water tested and the way water is given to the patient. They also differ in terms of the risk to which the patient is exposed. For example, some authors advise against screening methods that are referred to in the literature as “timed water swallow tests” (Hughes and Wiles 1996; Hinds and Wiles 1998; Wu et al. 2004) and that require a certain amount of water (usually 100–150 ml) to be drunk as quickly as possible. In these tests, both the required time to drink the water and the number of swallows are counted. From the obtained values the volume and duration of a swallow and the swallowing capacity (in ml/s) are calculated and compared with are-related normative data. In the so-­called dysphagia limit test, the maximum amount of water per swallow is determined (i.e., the volume that can be swallowed at once without piece-meal deglutition). Testing is done with gradually increasing bolus volumes (1, 3, 5, 10, 15, 20, and 25 ml). The normal value for healthy individuals is ≥20 ml (Ertekin et al. 1996). For patients with Parkinson’s disease, a modified water test has been recommended as a clinical screening tool to measure the maximum swallowing volume and/or the swallowing speed (Kalf et  al. 2011a, b; Sect.

2.3  Aspiration Screening

45

4.3.1). With regards to interpreting test results, one needs to keep in mind that patients with limited awareness of their swallowing impairment tend to swallow large quantities very quickly, which can lead to serious misinterpretations of the results in the timed water swallow tests (cf. Prosiegel and Weber 2013, p. 120). Smithard et al. (1998) begin their test much more cautiously with 5 ml of water given with a teaspoon and then administer 60 ml of water over 2 min as long as there are no clinical signs of aspiration. In the three-ounce water swallow test (equivalent to 90  ml), the patient is asked to drink the entire volume of a cup without stopping (DePippo et al. 1992; Suiter and Leder 2008). Both tests consider coughing or choking as well as a wet voice as clinical indicators of aspiration. Patients who cannot drink the entire volume are also considered to have an increased risk of aspiration. Due to the low specificity and the high rate of false positive results, however, not all patients failing these tests are actually at risk of aspiration with liquids. For the 50-ml water test, 50 ml of water is administered in 5-ml sips while watching out for signs of aspiration, in particular choking, coughing, and change in the patient’s vocal quality. Pharyngeal sensitivity is examined by touching the left and right pharyngeal walls with a cotton swab with the patient being asked. Whether and where the contact is felt. If at least one of these two tests is positive, there is a high risk of aspiration (Kidd et al. 1993; Martino et al. 2000). However, in the absence of further studies supporting this approach, testing for pharyngeal sensitivity cannot currently be recommended as a screening procedure (Bours et al. 2009). Alternatively, the 50-ml water test can be combined with pulse oximetry (Lim et al. 2001). Zaidi et al. (1995) suggested that pulmonary aspiration leads to measurable oxygen desaturation through reflex-induced bronchoconstriction. Based on this assumption this screening method was the first to be potentially capable of uncovering silent aspiration. Methods-wise, oxygen saturation is continuously measured during the water test via a finger clip. In addition to the clinical signs of aspiration, a decrease in oxygen saturation of more than 2% is considered pathological. In an initial study of acute stroke patients, the combined test achieved a sensitivity of 100% and a specificity of 71% for the detection of aspiration compared with gold standard FEES (Lim et al. 2001). However, since then several studies have been published that cast considerable doubt on the ability of pulse oximetry to detect (silent) aspiration (Colodny 2000; Leder 2000). Thus, in another study, the positive predictive value of a decrease in oxygen saturation of >3% was only 39.1% for the presence of aspiration, and the negative predictive value was 59.4% (Wang et al. 2005). Sensitivity and specificity were also relatively low (33% and 62%, respectively) in a similar subsequent study (compared with the detection of aspiration by VFSS). A combination of the water test with pulse oximetry displayed a sensitivity of 60% and a specificity of 41% and therefore also failed to demonstrate a sufficient improvement of this result (Ramsey et al. 2006). In the most recent pulse oximetry study, Marian et al. examined 50 acute stroke patients with moderate to severe dysphagia on whom a standardized FEES had been performed while oxygen saturation was monitored. In the blinded swallow-by-swallow analysis, there was no correlation between

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aspiration and measured oxygen saturation (Marian et al. 2017). Thus, the use of pulse oximetry in the context of aspiration screening can no longer be recommended. Perry (2001a, b) developed the Standardized Swallowing Assessment (SSA) as a screening tool for nurses (sensitivity: 97%; specificity: 90%). The stepwise algorithm first establishes whether the patient can remain awake and in an upright position for at least 15  min. If so, the patient’s mouth is cleaned (if necessary). Subsequently, the patient is asked to cough and lick his lips. Respiration, saliva control, and vocal quality are assessed. Only if no abnormalities are detected the water test is carried out by administering liquid from a teaspoon. The test is considered to indicate severe dysphagia if there is no swallowing, water runs out of the mouth, the patient coughs or chokes, there is an increase in the respiratory rate, the patient has a wet voice up to 1  min after swallowing, or the patient makes “an unwell impression” on the examiner. If none of these symptoms occurs, the patient is asked to drink half a glass of water (about 100 ml) and is reassessed using the same criteria. If the patient also passes this second examination without any signs of aspiration, a careful oral intake can be initiated with a test meal under a nurse’s supervision. Although a simple water test has the advantage of being able to identify more patients at risk of aspiration compared with all other types of tests, many patients who could, in principle, eat a modified diet, would initially be placed at an nothing per os regimen due to the test result. Therefore, screening instruments that involve different food consistencies and thereby allow for a more differentiated approaches have recently become increasingly implemented. This new trend may represent a paradigm shift. Tohara et al. (2003) combined a 3-ml water test with a 4-g pudding test and two voluntary saliva swallows without any bolus. On the basis of the findings, a comprehensive score of swallowing impairment is defined ranging from a score of 1 (inability to swallow), over 2 (shortness of breath), to 3 (coughing, dysphonia, a pudding residue of >25% of the bolus), 4 (water and pudding were successfully swallowed but only one saliva swallow was possible), and 5 (test successfully completed). In a mixed population the sensitivity and specificity were 90% and 56%, respectively. The Volume-Viscosity Swallow Test (VVST) tests nectar (295  mPa  s), liquid (21  mPa  s), and pudding (3.682  mPa  s) consistencies  in sequential order with increasing bolus volumes (5, 10, and 20 ml). Whenever during the testing of nectar and liquid consistencies signs of aspiration appear, the procedure switches to the testing of pudding consistency—which is usually safer to swallow. The aim of the VVST is not only to determine the risk of aspiration but also to identify food consistencies that are safe for the patient to swallow. The test has a sensitivity of 88.2% and a specificity of 64.7% for the detection of penetration and/ or aspiration. Trapl et al. (2007) developed the Gugging Swallowing Screen (GUSS; Sect. 5.1), which distinguishes different risk groups and related nutritional recommendations. This stepwise screening test was also designed to minimize the risk of aspiration during the examination. Only after a successfully completed native saliva swallow is the less risky semi-solid consistency (5 half-teaspoons of thickened

2.3  Aspiration Screening

47

liquid) tested. This test is followed by the administration of water from a cup with increasing volumes (3, 5, 10, 20, and 50 ml). Finally, the patient receives up to five bites of dry bread to swallow. Compared with the results of a FEES examination, the GUSS achieved a sensitivity of 100% and a specificity of 50–69% in a group of acute stroke patients. These results were recently reproduced in a larger study population (n = 100) by another research group (sensitivity: 96.5%; specificity: 55.8%; Warnecke et al. 2017). The GUSS is thus the best-evaluated screening tool for acute stroke patients. The recently published CADN (Clinical Assessment of Dysphagia in Neurodegeneration) also includes a multiple-consistency test in conjunction with a standardized questionnaire (Vogel et al. 2017; Appendix: Scales and Scores). Its validity was evaluated in patients with Parkinson’s disease (n = 60) and neurodegenerative ataxias (n = 65). The multiple-consistency test displayed a sensitivity of 84% and a specificity of 69%.

Based on the available literature different tests may be recommended for the acute phase after a stroke, such as the Standardized Swallowing Assessment (SSA; Perry 2001a, b), the Gugging Swallowing Screen (Trapl et al. 2007), the 3-ounce Water Swallow Test (Suiter and Leder, 2008) or the Daniels Test (Daniels et  al. 1997). Pulse oximetry should not be used for  aspiration screening.

In a  single center prospective study of 144 consecutive acute stroke patients, however, the SSA- and Daniels criterium (“2 out of 6”)—which were used as a method of aspiration screening—revealed only insufficient sensitivity (76.0% and 68.0%, respectively; the FEES served as the gold standard). According to these data, a negative result of the SSA screening procedure—or “2 out of 6”—does not allow for full oralization (Lindner-Pfleghar et al. 2017). Schultheiss et al. (2011) concluded in their prospective randomized study that tests that include solid consistencies are potentially superior to pure water tests, especially when testing for neurogenic dysphagia. In combination with an initial native saliva swallow test, their bolus swallow test displayed a sensitivity of 90% and a specificity of 73% in a mixed patient population with neurogenic and non-­ neurogenic dysphagias. In addition, the inter-rater reliability was good, and the results correlated with the findings of the FEES, which had been run in parallel. The Swallowing Provocation Test (SPT) can be performed on incooperative bedridden patients. 0.4 ml (Step 1) or 2.0 ml (Step 2) of water is applied intrapharyngeally via a thin transnasal catheter. The time from bolus injection to the beginning of visible swallow-related laryngeal movement is measured. A latency of more than 3 s until the start of the reflexive swallow is considered pathological (Teramoto et al. 1999; Teramoto and Fukuchi 2000). A case-control study on a mixed patient population found a sensitivity of 72–75% (Step 1) and 13–17% (Step 2) as well as a

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specificity of 38–44% (Step 1) and 80–98% (Step 2) for detecting (silent) aspiration and penetration, respectively (Kagaya et al. 2010). Compared with FEES, however, the first step of the SPT in acute stroke patients achieved a sensitivity of just 74.1% (specificity 100%) (Warnecke et al. 2008a). The cough reflex test (CRT) assesses the sensitivity  of the respiratory tract which is supposed to mirror pulmonary protective reflexes in case of aspiration. The CRT should thus be able to identify patients with silent aspiration (Wakasugi et al. 2008). The test—which can be carried out at the bedside—usually involves exposing the respiratory tract to citric acid or capsaicin in precisely defined, increasing concentrations via a nebulizer and waiting for the patient’s reaction (in the case of healthy individuals, this process would immediately trigger a cough reflex). In a study of more than 200 patients with suspected dysphagia, the sensitivity for  the detection of silent aspiration (compared with the FEES or the VFSS) was 87%, and the specificity was 89% (Wakasugi et al. 2008). Despite increasing evidence for the validity of the method (Addington et al. 1999; Sato et al. 2012; Miles et al. 2013), the inhalative agents, the inhalation modalities, and the assessment criteria defining a pathological response vary widely. Initial attempts to standardize the method and establish normal values (Monroe et al. 2010) have been undertaken but have not yet been sufficiently validated for routine use. The cough reflex test continues to be applied, especially in Australia and New Zealand. The so-called blue dye test assesses the risk of aspiration in patients with a tracheal cannulae. For this purpose, blue food coloring is added to the test bolus. A bluish secretion seen during subglottic suctioning immediately after swallowing indicates aspiration. This method, however, is not sensitive enough to reliably detect minor aspiration, which is why a negative finding does not allow for a definitive conclusion (Brady et al. 1999). If there is a suspicion of aspiration due to gastric reflux, it is also possible to color the patient’s enteral nutrition or—alternatively—to perform a glucose oxidase test on the aspirated tracheal secretion. Increased glucose content in the secretion due to gastroesophageal reflux is made visible by a conventional test strip.

In contrast to simple water tests, swallow tests using multiple consistencies allow to derive more differentiated recommendations for further diagnostic and therapeutic procedures. The swallowing provocation test is a suitable alternative for neurological patients who are incapable of cooperating during the test. The blue dye test is available for patients with tracheal cannulae. When using these screening methods to assess the aspiration risk of patients with neurogenic dysphagia, the often-insufficient sensitivity and specificity of the individual test procedures should always be kept in mind before making a decision in daily clinical practice.

2.4  The Clinical Swallowing Examination

49

Fig. 2.1 Clinical assessment of hyoid movement during swallowing

2.4

The Clinical Swallowing Examination

The detailed clinical swallowing examination (CSE) falls within the domain of appropriately trained SLP. In addition to the assessment of the aspiration risk, the CSE also provides as accurate an assessment of the severity and phenomenological pattern of the swallowing impairment as possible as a basis for further diagnostics, dietary recommendations, and treatment planning. The detailed CSE can be divided into: • Part 1: Examination of the oropharyngeal structures in the following order: –– resting observation (atrophy, paresis, tone, fasciculations, tremor) –– examination of reflexes (especially coughing, choking, and swallowing reflex and pathological oral primitive reflexes) –– assessment of voluntary movements (force, velocity, fluidity and accuracy, symmetry, diadochokinesis) –– sensory testing (tactile stimuli with cotton swabs) • Part 2 (if no contra-indications exist): Several swallows, usually in the order of semi-solid food (puree), liquid, and solid food An increased risk of aspiration is assumed in the case of disturbed soft palate mobility, a disturbed voluntary cough, a wet voice, or reduced laryngeal elevation. The latter finding is confirmed by the examiner via a clinical assessment of hyoid movement. In this four-finger palpation, the index finger is placed submentally, the middle finger at the level of the hyoid, the ring finger at the upper edge of the thyroid cartilage, and the little finger at the lower edge of the thyroid cartilage (Fig. 2.1).

50

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The clinical examination of hyoid movement also serves to assess the duration of the oral phase and the timing of the reflexive swallow response. During the swallowing examination, it is necessary to pay extra attention to anterior leaking (saliva running out of the patient’s mouth), nasal penetration, aspiration, and the amount and location of residue. We would also like to refer readers to textbooks with detailed descriptions of the comprehensive CSEs (Bartolome and Schröter-Morasch 2013; Logemann 1983). However, it should be pointed out that methodologically sound studies that use the criteria of evidence-based medicine to examine the specific benefit and validity of CSEs in neurogenic dysphagia do not yet exist. In addition, the methods used may vary widely depending on the individual examiner’s experience and education (Carnaby-­Mann and Lenius 2008; Langmore 2003). Leder and Espinosa (2002) compared the results of a CSE with those of FEES (as a gold standard) in 49 acute stroke patients. They concluded that the CSE underestimated the aspiration risk in patients who were actually at risk of aspiration (14% false negative results) and overestimated the aspiration risk in true non-aspirators (70% false positive results). Therefore, in that study the sensitivity of the CSE was 86%, but the specificity was only 30%. In a review, Carnaby-Mann and Lenius stated in line with this observation, “Within the field of dysphagia, there is an urgent need for a standardized and accepted clinical assessment tool, grounded in current neurophysiologic swallowing theory, that reflects both dysphagia and aspiration outcomes and has been evaluated through rigorous research design” (Carnaby-Mann and Lenius 2008, p. 765). In a recent retrospective study recruiting patients with stroke-related dysphagia (n = 60), Rangarathnam and McCullough (2016) found that the CSE only matched with the VFSS in terms of laryngeal elevation and did not correctly assess other parameters of swallowing physiology. Although the CSE has a greater diagnostic value than does a simple aspiration screening, prospective studies are urgently needed to investigate the additional clinical value of the CSE in different types of neurogenic and non-neurogenic dysphagia (Rangarathnam and McCullough 2016). Findings of the detailed CSE should be carefully documented. Various standardized protocols have recently been proposed for this purpose. The Bogenhausener Dysphagia Score (BODS)—which is widely used in Germanspeaking countries—also provides a severity grading of neurogenic oropharyngeal dysphagia (Bartolome and Schröter-Morasch 2013). This score consists of two eight-point scales that separately record the impairment of saliva swallowing and food intake. The BODS was additionally designed to take findings from instrumental swallowing assessment into account (Appendix: Scales and Scores). Carnaby-Mann has published a standardized clinical exam called MASA (Mann Assessment of Swallowing Ability). It was originally validated on stroke patients and has later been used for other conditions  as well (Mann 2002).

References

51

References Addington W, Stephens R, Gilliland K. Assessing the laryngeal cough reflex and the risk of developing pneumonia after stroke: an interhospital comparison. Stroke. 1999;30(6):1203–7. Bartolome G, Schröter-Morasch H.  Schluckstörungen. Diagnostik und Rehabilitation. 5th ed. München: Elsevier, Urban & Fischer; 2013. Bateman C, Leslie P, Drinnan MJ. Adult dysphagia assessment in the UK and Ireland: are SLTs assessing the same factors? Dysphagia. 2007;22(3):174–86. Belafsky PC, Mouadeb DA, Rees CJ, Pryor JC, Postma GN, Allen J, Leonard RJ. Validity and reliability of the eating assessment tool (EAT-10). Ann Otol Rhinol Laryngol. 2008;117(12):919–24. Bours GJ, Speyer R, Lemmens J, et al. Bedside screening tests vs. videofluoroscopy or fibreoptic endoscopic evaluation of swallowing to detect dysphagia in patients with neurological disorders: systematic review. J Adv Nurs. 2009;65:477–93. Brady SL, Hildner CD, Hutchins BF. Simultaneous videofluoroscopic swallow study and modified Evans blue dye procedure: an evaluation of blue dye visualization in cases of known aspiration. Dysphagia. 1999;14:146–9. Cameron JL, Reynolds J, Zuidema GD. Aspiration in patients with tracheostomies. Surg Gynecol Obstet. 1973;136:68–70. Carnaby-Mann G, Lenius K. The bedside examination in dysphagia. Phys Med Rehabil Clin N Am. 2008;19:747–768, viii. Cheney DM, Siddiqui MT, Litts JK, Kuhn MA, Belafsky PC. The ability of the 10-item eating assessment tool (EAT-10) to predict aspiration risk in persons with dysphagia. Ann Otol Rhinol Laryngol. 2015;124(5):351–4. Clavé P, Arreola V, Romea M, et al. Accuracy of the volume-viscosity swallow test for clinical screening of oropharyngeal dysphagia and aspiration. Clin Nutr. 2008;27:806–15. Cohen JT, Manor Y. Swallowing disturbance questionnaire for detecting dysphagia. Laryngoscope. 2011;121(7):1383–7. Colodny N. Comparison of dysphagics and nondysphagics on pulse oximetry during oral feeding. Dysphagia. 2000;15:68–73. Daniels SK, McAdam CP, Brailey K, et al. Clinical assessment of swallowing and prediction of dysphagia severity. Am J Speech Lang Pathol. 1997;6:17–24. DePippo K, Holas MA, Reding MJ. Validation of the 3-oz water swallow test for aspiration following acute stroke. Arch Neurol. 1992;49:1259–61. Doggett DL, Turkelson CM, Coates V.  Recent developments in diagnosis and intervention for aspiration and dysphagia in stroke and other neuromuscular disorders. Curr Atheroscler Rep. 2002;4:311–8. Ertekin C, Aydogdu I, Yüceyar N. Piecemeal deglutition and dysphagia limit in normal subjects and in patients with swallowing disorders. J Neurol Neurosurg Psychiatry. 1996;61:491–6. Gottlieb D, Kipnis M, Sister E, et al. Validation of the 50 ml3 drinking test for evaluation of poststroke dysphagia. Disabil Rehabil. 1996;18:529–32. Hinds NP, Wiles CM. Assessment of swallowing and referral to speech and language therapists in acute stroke. QJM. 1998;91:829–35. Hughes TA, Wiles CM. Clinical measurement of swallowing in health and in neurogenic dysphagia. QJM. 1996;89:109–16. Kagaya H, Okada S, Saitoh E, et al. Simple swallowing provocation test has limited applicability as a screening tool for detecting aspiration, silent aspiration, or penetration. Dysphagia. 2010;25:6–10. Kalf H, de Swart B, Bonnier-Baars M, et al. Guidelines for speech-language therapy in Parkinson’s disease. ParkinsonNet/NPF; 2011a. Kalf JG, de Swart BJ, Bloem BR.  Difficulty with pill swallowing in Parkinson’s disease. Mov Disord. 2011b;26(Suppl. 2):S191.

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Kidd D, Lawson J, Nesbitt R, et al. Aspiration in acute stroke: a clinical study with videofluoroscopy. Q J Med. 1993;86:825–9. Langmore SE.  Evaluation of oropharyngeal dysphagia: which diagnostic tool is superior? Curr Opin Otolaryngol Head Neck Surg. 2003;11:485–9. Leder SB. Use of arterial oxygen saturation, heart rate, and blood pressure as indirect objective physiologic markers to predict aspiration. Dysphagia. 2000;15:201–5. Leder SB, Espinosa JF. Aspiration risk after acute stroke: comparison of clinical examination and fiberoptic endoscopic evaluation of swallowing. Dysphagia. 2002;17(3):214–8. Leder S, Warner H, Suiter M. Comparing simultaneous clinical swallow evaluations and fiberoptic endoscopic evaluations of swallowing: findings and consequences. Dysphagia. 2015;30:639. Lim SHB, Lieu PK, Phua SY, et al. Accuracy of bedside clinical methods compared with fiberoptic endoscopic examination of swallowing (FEES) in determing the risk of aspiration in acute stroke patients. Dysphagia. 2001;16:1–6. Lindner-Pfleghar B, Neugebauer H, Stösser S, Kassubek J, Ludolph A, Dziewas R, Prosiegel M, Riecker A. Management of dysphagia in acute stroke: a prospective study for validation of current recommendations. Nervenarzt. 2017;88(2):173–9. Logemann JA.  Evaluation and treatment of swallowing disorders. San Diego: College-Hill Press; 1983. Logemann JA, Veis S, Colangelo L.  A screening procedure for oropharyngeal dysphagia. Dysphagia. 1999;14:44–51. Mann G.  MASA: the Mann assessment of swallowing ability. Clifton Park: Singular/Thomson Learning; 2002. Manor Y, Giladi N, Cohen A, et  al. Validation of a swallowing disturbance questionnaire for detecting dysphagia in patients with Parkinson’s disease. Mov Disord. 2007;22:1917–21. Marian T, Schröder J, Muhle P, Claus I, Oelenberg S, Hamacher C, Warnecke T, Suntrup-Krüger S, Dziewas R. Measurement of oxygen desaturation is not useful for the detection of aspiration in dysphagic stroke patients. Cerebrovasc Dis Extra. 2017;7(1):44–50. Martino R, Pron G, Diamant N.  Screening for oropharyngeal dysphagia in stroke: insufficient evidence for guidelines. Dysphagia. 2000;15:19–30. Martino R, Silver F, Teasell R, et  al. The Toronto Bedside Swallowing Screening Test (TORBSST): development and validation of a dysphagia screening tool for patients with stroke. Stroke. 2009;40:555–61. Martino R, Maki E, Diamant N. Identification of dysphagia using the Toronto Bedside Swallowing Screening Test (TOR-BSST©): are 10 teaspoons of water necessary? Int J Speech Lang Pathol. 2014;16(3):193–8. Mathers-Schmidt BA, Kurlinski M.  Dysphagia evaluation practices: inconsistencies in clinical assessment and instrumental examination decision-making. Dysphagia. 2003;18(2):114–25. McCullough GH, Wertz RT, Rosenbek JC, et al. Inter- and intrajudge reliability of a clinical examination of swallowing in adults. Dysphagia. 2000;15:58–67. McCullough GH, Wertz RT, Rosenbek JC. Sensitivity and specificity of clinical/bedside examination signs for detecting aspiration in adults subsequent to stroke. J Commun Disord. 2001;34:55–72. McCullough GH, Rosenbek JC, Wertz RT, et al. Utility of clinical swallowing examination measures for detecting aspiration post-stroke. J Speech Lang Hear Res. 2005;48:1280–93. McHorney CA, Bricker DE, Kramer AE, et  al. The SWAL-QOL outcomes tool for oropharyngeal dysphagia in adults: I.  Conceptual foundation and item developmen. Dysphagia. 2000a;15:115–21. McHorney CA, Bricker DE, Robbins J, et al. The SWAL-QOL outcomes tool for oropharyngeal dysphagia in adults: II. Item reduction and preliminary scaling. Dysphagia. 2000b;15:122–33. McHorney CA, Robbins J, Lomax K, et al. The SWAL-QOL and SWAL-CARE outcomes tool for oropharyngeal dysphagia in adults: III. Documentation of reliability and validity. Dysphagia. 2002;17:97–114. Miles A, Moore S, McFarlane M, et al. Comparision of cough reflex testing against instrumental assessment of aspiration. Physiol Behav. 2013;118:25–31.

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Monroe M, Robb M, Huckabee ML. Citric acid inhalation cough challenge: establishing normative data. Dysphagia. 2010;25:354–87. Nathadwarawala KM, Nicklin J, Wiles CM. A timed test of swallowing capacity for neurological patients. J Neurol Neurosurg Psychiatry. 1992;55:822–5. Perry L.  Screening swallowing function of patients with acute stroke. Part one: identification, implementation and initial evaluation of a screening tool for use by nurses. J Clin Nurs. 2001a;10(4):463–73. Perry L. Screening swallowing function of patients with acute stroke. Part two: detailed evaluation of the tool used by nurses. J Clin Nurs. 2001b;10(4):474–81. Prosiegel M, Weber S, editors. Dysphagie. Diagnostik und Therapie. 2nd ed. Berlin: Springer; 2013. Ramsey DJ, Smithard DG, Kalra L. Can pulse oximetry or a bedside swallowing assessment be used to detect aspiration after stroke? Stroke. 2006;37:2984–8. Rangarathnam B, McCullough GH. Utility of a clinical swallowing exam for understanding swallowing physiology. Dysphagia. 2016;31(4):491–7. Rofes L, Arreola V, Mukherjee R, Clavé P. Sensitivity and specificity of the Eating Assessment Tool and the Volume-Viscosity Swallow Test for clinical evaluation of oropharyngeal dysphagia. Neurogastroenterol Motil. 2014;26(9):1256–65. Rosenbek JC, McCullough GH, Wertz RT. Is the information about a test important? Applying the methods of evidence-based medicine to the clinical examination of swallowing. J Commun Disord. 2004;37:437–50. Sasaki CT, Steve B, Leder PD. In memoriam. Dysphagia. 2016;31:597. Sato M, Tohara H, Iida T, et al. Simplified cough test for screening silent aspiration. Arch Phys Med Rehabil. 2012;93(11):1982–6. Schröter-Morasch H.  Anamnesebogen zur klinischen Erfassung von Schluckstörungen nach Hirnverletzung. Dortmund: Bergmann Publishing; 1994. Schultheiss C, Nusser-Muller-Busch R, Seidl RO.  The semisolid bolus swallow test for clinical diagnosis of oropharyngeal dysphagia: a prospective randomised study. Eur Arch Otorhinolaryngol. 2011;268:1837–44. Smith HA, Lee SH, O’Neill PA, et al. The combination of bedside swallowing assessment and oxygen saturation monitoring of swallowing in acute stroke: a safe and humane screening tool. Age Ageing. 2000;29:495–9. Smithard DG, O’Neill PA, Park C, et al. Can bedside assessment reliably exclude aspiration following acute stroke? Age Ageing. 1998;27:99–106. Speyer R, Cordier R, Kertscher B, Heijnen BJ. Psychometric properties of questionnaires on functional health status in oropharyngeal dysphagia: a systematic literature review. Biomed Res Int. 2014;2014:458678. Suiter DM, Leder SB. Clinical utility of the 3-ounce water swallow test. Dysphagia. 2008;23:244–50. Teramoto S, Fukuchi Y. Detection of aspiration and swallowing disorder in older stroke patiens: simple swallowing provovation test versus water swallowing test. Arch Phys Med Rehabil. 2000;81:1517–9. Teramoto S, Matsuse T, Fukuchi Y.  Simple two-step swallowing provocation test for elderly patients with aspiration pneumonia. Lancet. 1999;353:1243. Thompson-Henry S, Braddock B. The modified Evan’s blue dye procedure fails to detect aspiration in the tracheostomized patient: five case reports. Dysphagia. 1995;10:172–4. Tohara H, Saitoh E, Mays KA, et al. Three tests for predicting aspiration without videofluorography. Dysphagia. 2003;18:126–34. Trapl M, Enderle P, Nowotny M, et al. Dysphagia bedside screening for acute-stroke patients: the Gugging Swallowing Screen. Stroke. 2007;38:2948–52. Vogel AP, Rommel N, Sauer C, Horger M, Krumm P, Himmelbach M, Synofzik M.  Clinical assessment of dysphagia in neurodegeneration (CADN): development, validity and reliability of a bedside tool for dysphagia assessment. J Neurol. 2017;264(6):1107–17. Vogels B, Cartwright J, Cocks N. The bedside assessment practices of speech-language pathologists in adult dysphagia. Int J Speech Lang Pathol. 2015;17(4):390–400.

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Wakasugi Y, Tohara H, Hattori F, Motohashi Y, Nakane A, Goto S, Ouchi Y, Mikushi S, Takeuchi S, Uematsu H.  Screening test for silent aspiration at the bedside. Dysphagia. 2008;23(4):364–70. Wang TG, Chang YC, Chen SY, et al. Pulse oximetry does not reliably detect aspiration on videofluoroscopic swallowing study. Arch Phys Med Rehabil. 2005;86:730–4. Warnecke T, Teismann I, Meimann W, et  al. Assessment of aspiration risk in acute ischaemic stroke – evaluation of the simple swallowing provocation test. J Neurol Neurosurg Psychiatry. 2008a;79:312–4. Warnecke T, Im S, Kaiser C, Hamacher C, Oelenberg S, Dziewas R.  Aspiration and dysphagia screening in acute stroke  - the Gugging Swallowing Screen revisited. Eur J Neurol. 2017;24(4):594–601. Wu MC, Chang YC, Wang TG, et al. Evaluating swallowing dysfunction using a 100-ml water swallowing test. Dysphagia. 2004;19:43–7. Zaidi NH, Smith HA, King SC, et al. Oxygen desaturation on swallowing as a potential marker of aspiration in acute stroke. Age Ageing. 1995;24:267–70.

3

FEES and Other Instrumental Methods for Swallowing Evaluation

Contents 3.1  FEES 3.1.1  Introduction 3.1.2  Equipment 3.1.3  Standard FEES Protocol 3.1.4  Specific Neurological Protocols 3.1.5  Key Findings and Their Rating 3.1.6  Endoscopic Classification of Neurogenic Dysphagia 3.1.7  Documentation of Endoscopic Findings 3.1.8  Training Curriculum: “FEES for Neurogenic Dysphagia” 3.2  Videofluoroscopic Swallowing Study (VFSS) 3.2.1  Indications 3.2.2  Technique 3.2.3  Radiation Exposure 3.2.4  Contrast Agents 3.2.5  Procedure 3.2.6  Findings 3.2.7  Comparing VFSS and FEES 3.3  Manometric Evaluation of Swallowing 3.3.1  Conventional Manometry 3.3.2  High-Resolution Manometry 3.4  Electromyographic Evaluation of Swallowing 3.5  Sonographic Evaluation of Swallowing 3.6  Magnetic Resonance Imaging and Computed Tomography 3.7  Differential Indication of Instrumental Dysphagia Diagnostics References

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Electronic Supplementary Material The online version of this chapter (https://doi. org/10.1007/978-3-030-42140-3_3) contains supplementary material, which is available to authorized users. © Springer Nature Switzerland AG 2021 T. Warnecke et al., Neurogenic Dysphagia, https://doi.org/10.1007/978-3-030-42140-3_3

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3.1

3  FEES and Other Instrumental Methods for Swallowing Evaluation

FEES

3.1.1 Introduction The fiberoptic (or flexible) endoscopic evaluation of swallowing was first described in 1988 by American speech and language pathologist (SLP) Susan Langmore and colleagues in the journal Dysphagia (Langmore et al. 1988). In 1997, the acronym FEES was copyrighted as a registered trademark to distinguish this particular endoscopic swallow examination technique from conventional ORL laryngoscopy without an evaluation of swallowing (Langmore 2001a, b). The copyright has since expired without being renewed. A recent review by Susan Langmore describes the international development of the FEES procedure from its first description to the present situation (Langmore 2017). Table 3.1 summarizes important milestones in the history of FEES with a focus on Germany (Table 3.1).

Table 3.1  FEES history Year 1988 1991

1997 2001

2005

2010

2012

2012 2015

2017

Event Susan Langmore publishes the 1st scientific article on FEES as a new method of dysphagia diagnosis and therapy in the journal Dysphagia (Langmore et al. 1988) The American Speech Language Hearing Association put FEES in the scope of practice for SLPs in the USA The acronym FEES is copyrighted. Later, the copyright is not renewed The standard reference on FEES, entitled Endoscopic Evaluation and Treatment of Swallowing Disorders, by Susan Langmore is published by Thieme Publishing House (Langmore 2001a) In the 3rd Edition of the German Guidelines for Diagnostics and Therapy in Neurology, FEES and the videofluoroscopic swallowing study (VFSS) are considered the most important instrumental methods of “determining the cause, type, and severity of neurogenic dysphagia” as well as for “developing a therapy plan and monitoring the effectiveness of the therapy” (Prosiegel 2008, p. 748) The German Institute of Medical Documentation and Information (Deutsches Institut für Medizinische Dokumentation und Information; DIMDI) includes a separate code (1-613) for FEES in the Operation- and Procedure Code (Operationen- und Prozedurenschlüssel; OPS) Guidelines for dysphagia management in the acute stroke from the German Stroke Society and the German Neurological Society: “In acute stroke, FEES is preferable to VFSS and is almost always sufficient” (Prosiegel et al. 2012; translated by Ryan DeLaney) FEES is used in 52% of certified German stroke units (SUs) for standardized dysphagia diagnostics (Suntrup et al. 2012) Inception of the FEES training curriculum for neurogenic dysphagia from the German Neurological Society and the German Stroke Society (Dziewas et al. 2014), which was also endorsed by the German Society of Geriatrics (Deutsche Gesellschaft für Geriatrie) in 2016 Inception of the FEES Accreditation Program for Neurogenic and Geriatric Oropharyngeal Dysphagia from the European Society for Swallowing Disorders (ESSD) (Dziewas et al. 2017)

3.1 FEES

57

In the 1980s and 1990s, the gold standard of instrumental dysphagia evaluation was the radiological examination of swallowing, which is referred to as the videofluoroscopic swallowing study (VFSS) and which was developed primarily by American SLP Jeri Logemann (1983). Langmore originally intended FEES to be an alternative in situations in which VFSS was not available (e.g., in smaller hospitals without a radiology department, in intensive care units, or in nursing homes) or was impractical (e.g., for seriously ill patients who are not capable of complying with the examination and/or cannot sit upright; Langmore et  al. 1988). However, along with its increasing clinical use over the past 15 years, in addition to VFSS, FEES has now established itself as an independent and efficient method of studying swallowing and has become an indispensable component in the diagnosis and therapy of neurogenic dysphagia (Langmore 2001a, b, 2017; Warnecke et al. 2009b). Today, FEES and VFSS are considered complementary instrumental methods for the objective evaluation of swallowing (Langmore 2003; Tabaee et  al. 2006; Prosiegel 2008). In some regions of the world, FEES has even become the primary tool for studying the pharyngeal phase of deglutition (Langmore 2017). Historically, the endoscopic evaluation of swallowing was used primarily in otolaryngology settings, in which non-neurogenic dysphagias (e.g., structural dysphagia resulting from malformations, inflammations, or tumors) constitutes a large proportion of swallowing disorders (Langmore 2001a, b). However, in particular in neurology endoscopic dysphagia evaluation has gained increasing clinical and scientific significance in recent years (Langmore 2017), and many neurological acute care and rehabilitation hospitals now have their own FEES units. In these settings, FEES is frequently performed by teams of specially trained neurologists and SLPs (Warnecke et al. 2009b). In 2013, recommendations for implementing FEES as part of dysphagia diagnostics in stroke units were published for the first time with the aim of ensuring a high quality of care and consistent standards of quality (Dziewas et al. 2013). Outside of neurology, FEES is used in a variety of other disciplines, including phoniatrics, gastroenterology, pulmonology, rehabilitation, dentistry, and geriatrics (Langmore 2001a, b). The increased clinical significance of FEES is also evident in the fact that in 2010, the German Institute of Medical Documentation and Information (Deutsches Institut für Medizinische Dokumentation und Information; DIMDI) assigned a separate code to Chap. 1 of the Operation- and Procedure Code (Operationen- und Prozedurenschlüssel; OPS; 2010 Version; 1-613: Evaluation of swallowing with a flexible endoscope; DIMDI 2009). As neither the specialist training in neurology nor the education program of SLPs includes systematic instructions or a practical introduction to this examination technique, the German Neurological Society and the German Stroke Society developed a training curriculum that is open to doctors of all disciplines as well as to SLPs (Dziewas et al. 2014, 2016). Since January 2015, more than 800 physicians and SLPs have earned a FEES certificate or FEES instructor status (Sect. 3.1.8). In 2017, the European Society for Swallowing Disorders (ESSD) also established a similar education program (Dziewas et al. 2017).

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3  FEES and Other Instrumental Methods for Swallowing Evaluation

3.1.2 Equipment For many years, flexible fiberoptic laryngoscopes with a diameter of ca. 2.4–3.5 mm were used in the endoscopic evaluation of swallowing. At the distal end of the insertion portion of these endoscopes—which continue to be used in many institutions until today—is an objective lens that focuses the image on one end of an array of clad optical fibers. Each bundle contains several thousand optical fibers of approximately 10 μm in diameter, and each of these fiberoptic bundles transmits one pixel of the image from the distal to the proximal lens, enabling the observer to view the entire array as a coherent image. The fiberoptic endoscope allows a viewing angle of up to 100° and can be angled by about 130° during the examination (Murray 2001). The light is passed through a diffusing lens system on the distal end along a fiberoptic bundle that is separate from the image-carrying bundle, and illuminates the area of interest. The examiner can use the endoscope by looking directly through the eyepiece or attaching a camera, which converts the light into a video signal so that the examination can be tracked on the monitor, digitally recorded with the laptop, and saved as a movie file. The fiberoptic laryngoscope is usually part of an examination unit that contains a light source, a camera, a monitor, and either a laptop (Fig. 3.1) or a stand-alone system (Fig. 3.1). In the USA, an adapter has been available since 2014 that even

Fig. 3.1  Mobile FEES examination units

3.1 FEES

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allows the examiner to view and record FEES directly on a smartphone rather than on a monitor. The complete FEES unit can be moved directly to the patient’s bed on an endoscopy trolley (Murray 2001). Since the image transmission through the fiberoptic bundles in the endoscope leads to a loss of image sharpness, in recent years video endoscopes have grown in use. Here, greater resolution can be achieved via a chip camera, which is located on the tip of the endoscope (“chip on the tip”) and directly transmits the image without the need for a separate camera. The price difference between a fiberoptic laryngoscope and a video laryngoscope is no longer significant. The diameter of the video endoscopes has also decreased and is now comparable with that of fiberoptic endoscopes. If a video endoscope is used instead of the “classic” fiberoptic endoscope, the acronym FEES can still be used. In this case, it stands for “flexible endoscopic evaluation of swallowing.” Apart from the endoscopes also the light sources have been refined over the years. Today, small LED light sources have replaced the previously used halogen or xenon lights (Langmore 2017). In the USA, flexible endoscopes with an additional channel designed to deliver a defined air pulse stimulus for sensitivity testing were used for some time (pulse duration: 50  ms; intensity or air pulse pressure: 0–15  mmHg; Aviv et  al. 1993, 2005). However, the equipment needed for this examination technique (using the sensory box for delivering air pulses) is no longer available. Some researchers have developed their own sensory equipment (Hammer 2009). In clinics today, the air pulse test has been largely replaced by the ‘touch test’ where the tip of the laryngoscope briefly and lightly touches the arytenoids to assess sensation. The Touch Test is sometimes still called FEESST and is a recognized code in the US.

3.1.3 Standard FEES Protocol The extensive standard FEES protocol was first published in 2001 by Susan Langmore in her book “Endoscopic Evaluation and Treatment of Swallowing Disorders” (Langmore 2001a, b), and is considered the gold standard in terms of conducting endoscopic evaluations of swallowing. However, it has not yet been validated and therefore serves as more of a general guide (Langmore 2017). As extension to the FEES standard protocol the ice-chip protocol has been developed that is particularly suited to examine patients with high risk of aspiration (Langmore 2001) (see chapter 5). Before beginning FEES, the following preparatory measures should be taken (Langmore 2001a, b): 1. Informing the patient The patient and—if applicable—the relatives/caregivers should be informed about the different examination steps. During this time, the patient should be shown the endoscope and how deep it will enter the throat. Of course, the patient or—if applicable—his legal guardian must give consent before beginning the examination, but this consent does in the opinion of the authors not have to be in written form.

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2. Positioning the patient If the circumstances allow, the patient should always be examined in a natural posture or the most optimal posture for eating. The patient should ideally sit upright in a chair. For bedridden patients, the head of the bed should be raised to at least 45° unless contraindicated. For patients who are not fully compliant, caregivers may be necessary to provide additional assistance and keep the patient’s head in a suitable position during the examination. One of the authors’ studies revealed that this type of assistance was required in about 10% of all acute stroke patients in a stroke unit (Warnecke et al. 2009d). In rare cases, in order to assess airway safety, critically ill patients in the neurological intensive care unit or stroke unit must be examined endoscopically while lying down if they are unable to be placed in another position. This approach may be appropriate when checking the indication for protective intubation/tracheotomy. For patients who are fully compliant, different positions can also be tested during the examination to determine the optimal swallowing posture for eating and/or feeding (Langmore 2001a, b). 3. Cleaning the patient’s mouth If necessary, the cheeks, teeth, and tongue should be cleaned before beginning FEES. On the one hand, this procedure can reduce the risk of pathogenic microorganisms entering the lungs in the event of aspiration during FEES (Langmore et al. 1998); on the other hand, it enables the patient to better feel and taste the administered bolus, which facilitates swallowing (Langmore 2001a, b). 4. Using local anesthesia The use of topical anesthesia (e.g. with lidocaine gel or spray) in the nares that will be traversed endoscopically is optional. Anesthesia can reduce the sensation of pressure and/or pain that may occur during the insertion of the endoscope (Johnson et al. 2003a, b). However, the evidence for this benefit is mixed. Some studies did not find a benefit of local anesthesia, in fact FEES was even deemed more unpleasant after local anesthesia had been applied (Frosh et al. 1998; Leder et al. 1997). A Cochrane review in 2011 on the use of surface anesthesia or vasoconstrictors during nasal pharyngolaryngoscopy concluded that there was no evidence for an added benefit of these two procedures. However, the number of patients in the analyzed studies was small (a total of 8 randomized controlled trials recruiting 746 patients), which could be a possible reason for the neutral outcome (Sunkaraneni and Jones 2011). In a recent meta-­analysis with somewhat less “strict” inclusion criteria, more studies (n = 10) and patients (n = 837) were considered. In these studies, pain and discomfort were found to have been significantly reduced, but an unpleasant taste was associated with the use of a topical anesthetic (Hwang et al. 2015). The direct application of 0.4 mL of a 2% lidocaine gel in a double-blind randomized controlled crossover study on 36 healthy control subjects did not result in an increased risk of penetration/aspiration during the subsequent FEES (Kamarunas et al. 2014). The question as to whether and—if so—what dosage of lidocaine spray should be used for surface anesthesia of the nasal mucosa has also been investigated. In a series of three studies where the patients received 2 exams; one with lidocaine and

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the other with a sham spray, these questions were directly assessed. In the first study, applying 1 mL of a 4% lidocaine spray resulted in a worsening of the average score on the penetration–aspiration scale (from 1.05 to 1.21) in 20 healthy control subjects during FEES; however, FEES was perceived as being less uncomfortable and was better tolerated overall (Lester et al. 2013). In the second study, the dose was decreased to 0.5 mL of a 4% lidocaine spray. This lowered dose was also associated with better tolerability of FEES in 25 dysphagic patients, but there was a tendency—albeit not statistically significant—for the penetration–aspiration scale score to increase (Fife et al. 2015). In the third and final study, using only 0.2 mL of a 4% lidocaine spray (combined with oxymetazoline) in FEES on 17 patients with dysphagia, there was no worsening of swallowing as measured by the PAS scale or a rating of residue. In addition, patient-reported level of discomfort was significantly reduced (O’Dea et al. 2015). As consequence of these fi ­ ndings, lidocaine was deemed safe as long as the dose was kept to 0.2ml. When FEES is combined with a standard ORL laryngoscopy examination—which is usually done with significantly higher doses of lidocaine—it should be performed either before or at least 1 h after the laryngoscopy (O’Dea et al. 2015). 5. Preparing the food consistencies During the examination, patients should receive at least three different food consistencies (liquid–semi-solid–solid) to swallow. Liquids must be mixed with a few drops of blue or green food coloring to enable better visualization. Dark-­ colored liquids such as coffee or cola may be difficult to differentiate from the pharyngeal mucosa and should be avoided. Milk, on the other hand, is well-­suited for the examination because it reflects light and slightly coats the mucose, enabling better visualization. Another option is to use a few drops of white food color in whatever liquid is being used, even in water. It is superior to milk for visualization and is highly recommended. It can be purchased from bakery suppliers or over the internet. A study published in 2016 analyzed 40 FEES examinations of patients with neurological and non-neurological conditions and demonstrated that green-colored milk enabled a significantly better visualization of the depths of bolus penetration/aspiration (laryngeal vestibule and trachea) compared with uncolored white milk. In addition, intra-rater reliability improved (Marvin et al. 2016). Solid food consistencies only need to be dyed if the natural color of the test bolus cannot be clearly distinguished from the color of the pharyngeal mucosa (Leder et al. 2005). Ideally, the FEES examination should also include foods that the patient has the greatest difficulty swallowing in his daily life. A nasogastric tube in place should not be removed prior to FEES as the tube itself does usually not result in a clinically relevant impairment of swallowing or in an increase in aspiration (Fattal et al. 2011). However, if the feeding tube coiles in the pharynx and interferes with arytenoid and epiglottic movement, it should be repositioned (Dziewas et al. 2008a). After the mentioned preparatory measures FEES begins with the insertion of the laryngoscope into the lower, or more rarely middle nasal passage. The tip of the endoscope is first positioned in the posterior third of the nasal meatus. From this position, the mobility of the soft palate and the velopharyngeal closure can be

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assessed. The tip of the endoscope is then passed over the velum to the upper hypopharynx. From this position (the so-called home position), the base of the tongue, the valleculae, the pharyngeal musculature, the piriform sinus, the epiglottis, and the larynx can be studied. In order to take a closer look at the laryngeal vestibule, the vocal folds, and the subglottic space, the tip of the endoscope is advanced beyond the tip of the epiglottis (“close view”; Langmore 2001a). Figure 3.2 provides an overview of the anatomy of the hypopharynx from the perspective of the two examination positions (Fig. 3.2). The standard FEES examination is divided into three steps, which should be performed in succession: (1) the anatomical-physiological examination (without food), (2) the swallow examination (with food), and (3) an assessment of the effectiveness of selected therapeutic interventions (Langmore 2001b). In clinical practice, the individual steps of the standard FEES protocol should not be executed rigidly; rather, they should be modified depending on the concrete findings and the resulting questions during the examination. In some settings, the examination is best carried out by a team consisting of a SLP and a physician; in other settings, either professional can conduct the examination—as long as that person is qualified to perform and interpret the exam. In other words, the endoscopist can be a physician or a SLP (Langmore 2001a). The endoscopic evaluation of swallowing should be carried out by qualified and trained professionals. Ideally, this team consists of a SLP and a physician. The standard FEES protocol should not be executed rigidly; rather, the examination should be adapted to the individual patient depending on the clinical problem and respective findings.

a

b

Fig. 3.2  Anatomy of the hypopharynx from the endoscopic perspective. (a) “home position”: (1) tip of the uvula; (2) valleculae; (3) epiglottis; (4) larynx; (5) piriform sinus; (6) posterior pharyngeal wall. (b) “close view”: (7) vestibular folds; (8) vocal folds; (9) subglottic region and trachea; (10) arytenoid cartilage

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Table 3.2  Endoscopic tests to evaluate different pharyngeal and laryngeal motor functions Task Dry swallowing, phonation [k] Phonation [hi]; alternated with inhalation Repetitive phonation [i-i-i] High pitch phonation Tight breath-holding, coughing, throat clearing Base of tongue phonation of postvocalic “l” words [c:] (e.g., “earl”, “ball”, “call”)

Motor function Velopharyngeal closure Glottic closure; adequacy of airway opening Diadochokinetic movement of vocal folds/arytenoid cartilage Pharyngeal contraction Closure of the airway by supraglottic structures Movement of base of tongue

Anatomical-Physiological Examination (Without Food) The anatomical-physiological examination begins with the inspection of the hypopharynx (resting state examination). The examiner should pay particular attention to irregularities on the mucosa, asymmetries, involuntary movements, and changes in the form and position of the vocal folds, the arytenoid cartilage, and the epiglottis as well as to accumulations of saliva, secretions, and food residues (Langmore 2001a, b). The resting state examination is followed by an examination of pharyngeal and laryngeal motor function and sensory responses. Table 3.2 provides an overview of the most important tests for evaluating motor functions (Langmore 2001a, b; Schröter-­Morasch 2006; Rodriguez et al. 2007). The examiner tests for sensitivity by gently touching both arytenoids with the tip of the endoscope. Alternatively, if specialized equipment needed for FEESST is available, airpuffs of defined pressure may be applied. Apart from the patient reporting whether he feels the stimulus, objective parameters like a triggered reflexive swallow, a cough reflex or a laryngeal adductor reflex  (brief medial movement of the arytenoids) are considered to be  physiological reactions (Schröter-Morasch 2006). The evaluation of adductor and cough reflexes is particularly important in neurological patients with impaired vigilance, inability to follow instructions, or severe aphasia. In the case of the airpuff method, the stimulus threshold can be determined by a continuous increase in pressure applied. Depending on their age, healthy volunteers perceive airflow at pressures between 2.0 and 2.7 mmHg (Aviv 1994, 1997a, b, 2005; Setzen et al. 2003; Perlman et al. 2004). As mentioned above, the air pulse method is not available in most clinics. In a study of 14 subjects that compared touching the arytenoid cartilage with the airpuff method, only the sensory impairment detected by the touch method was found to be significantly associated with penetration/aspiration. The airpuff method was able to identify minor abnormalities in sensory perception, but the clinical relevance was questionable. In addition, it was difficult for the investigators to maintain a constant distance between the tip of the endoscope and the arytenoid cartilage, which affected the reproducibility of the airpuff pressure (Kaneoka et al. 2014, 2015).

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Swallow Examination (With Food) In the second step of the standard FEES protocol, the swallowing process is directly studied with test boli of different consistencies (e.g., liquid, semi-solid (pudding), solid), and increasing bolus sizes (e.g., 2 mL up to normal cup or bite size) being given to the patient. During FEES, the food bolus is visualized on its way through the pharynx during the late oral and pharyngeal phases of swallowing. The physiological process of swallowing is not impaired by the endoscope in the pharynx (Suiter et al. 2006). Figure 3.3 shows the physiological process of swallowing from the endoscopic perspective. Assessment of the Effect of Therapeutical Interventions After  finishing the swallow examination, the effect of therapeutic interventions (especially dietary adjustment, postural changes, swallowing techniques, and biofeedback) are assessed based on the pathological findings from the second step of the standard FEES protocol (Langmore 2001a, b). Every FEES should be fully recorded as a video, which allows for later off-line analysis. Audio recording is also extremely important for later analysis of the examination, in particular when it comes to assessing reflexive cough or throat clearing. As has been shown in two recent studies, off-line analysis capitalizing on the possibility of a frame by frame review improved the reliability and validity of the detection of penetration and aspiration as compared with the “live” analysis, not using playback to review the findings (Hey et al. 2015; Pluschinski et al. 2015).

3.1.4 Specific Neurological Protocols Various protocols have been established that focus on disease-specific issues of different neurological disorders (Langmore 2017).  A summary of the FEES protocols discussed here is given in Table 3.3. Flexible Endoscopic Dysphagia Severity Scale for Acute Stroke Patients (FEDSS) The standard FEES protocol may be too extensive and time-consuming to integrate the endoscopic dysphagia evaluation into the highly specialized routine workflow of modern stroke units, in which numerous diagnostic and therapeutic procedures are performed by a multidisciplinary team on a tight timeframe (Ringelstein and Nabavi 2007a, b). Therefore, by taking the characteristic endoscopic findings of acute stroke patients into account, a standardized examination protocol and a dysphagia severity score derived from this protocol were developed for use in the stroke unit (Appendix: Scales and Scores). This protocol allows for a fast and focused yet differentiated endoscopic dysphagia evaluation in acute stroke patients (Dziewas et al. 2008b; Warnecke et al. 2009c). Depending on the endoscopic findings, FEDSS classifies post-stroke dysphagia into six degrees of severity (1 = no dysphagia, 2–5 = mild- to severe dysphagia, 6 = high-grade dysphagia with the inability to swallow saliva), to  which specific protective and rehabilitative strategies addressing the respective swallowing impairment are directly linked (Dziewas et al. 2008b). If the patient has an initial FEDSS of 4, 5, or 6, tube feeding is recommended, while

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a

b

c

d

e

Fig. 3.3  Physiological process of swallowing from the endoscopic perspective. (a) Larynx in resting position; (b) bolus enters oropharynx at end of oral phase and triggers swallow reflex; (c) pharyngeal muscles contract and press the tip of endoscope against the mucosa, thereby temporarily disrupting the view (“whiteout”); (d) pharyngeal muscles are relaxed, epiglottis is still inverted, bolus is in the esophagus, pharyngeal phase is complete; (e) epiglottis returns to resting position

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scores 1 to 3 allow for starting an oral diet, albeit with restrictions concerning solid food (score 2) and also liquids (score 3). Because of the rapidly changing nature of dysphagia in the acute stage after stroke, reevaluation of patients within the first days is recommended. The expert recommendations on “dysphagia management in the acute stroke phase” that were developed by the German Neurological Society (Deutsche Gesellschaft für Neurologie; DGN) and the German Stroke Society (Deutsche Schlaganfall-Gesellschaft; DSG) suggest using FEDSS in stroke units (Prosiegel et  al. 2012).  The guideline “Clinical nutrition in patients with stroke” issued by the German Society for Clinical Nutrition recommends to use the FEDSS for dysphagia management in acute stroke (Wirth et al. 2013) Section 5.1.2 details the practical application of FEDSS in the stroke unit. FEES Levodopa Test In order to evaluate the response of Parkinson-related dysphagia to dopaminergic medication, a standardized FEES levodopa test was developed (Appendix: Scales and Scores). In the first section of this examination protocol, an endoscopic evaluation of dysphagia is performed in the off-state, for which the dopaminergic medication is discontinued overnight for at least 12 h. Following the off-state examination, patients receive an oral test dose of fast-dissolving L-DOPA. This dose corresponds to 1.5 times the regular morning dose, de novo patients are given 200 mg of L-DOPA. To make sure the patient has successfully swallowed the test dose, the endoscope is left in the hypopharynx until the L-DOPA solution has entered the esophagus. The second step of the study consists of an endoscopic dysphagia evaluation in the on-­state. This evaluation is performed about 60 min after the application of the L-DOPA test dose (Warnecke et al. 2010a, 2016). During the on- and off-state evaluation of dysphagia, nine swallows are assessed consecutively. The following bolus consistencies are administered three times each: 8 mL of pudding, 5 mL of water, and 3 × 3 × 0.5 cm slices of white bread. For each of the swallows, three main parameters of swallowing function (premature spillage, penetration/aspiration, and residue) are analyzed and ranked on a 5-point scale (0–4) based on their severity: • Premature spillage (bolus localization at the time when the swallow reflex is triggered): 0 = behind the tongue; 1 = at the base of tongue or valleculae, 2 = at the tip of the epiglottis or lateral channels, 3 = in the piriform sinus or touching laryngeal rim, 4 = in the laryngeal vestibule • Penetration/aspiration: 0 = none, 1 = penetration with protective reflex, 2 = penetration without protective reflex, 3 = aspiration with protective reflex, 4 = aspiration without protective reflex • Residue: 0 = none, 1 = coating, no pooling, 2 = mild pooling in less than half of the cavities, 3 = moderate pooling that fills the cavities, 4 = severe pooling that overflows from the cavities The points obtained from the nine swallows are added separately for the on- and off-state (0–108 points; the higher the score, the worse the swallowing function).

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Subsequently, the sums of both conditions are compared. If the on-state shows an improvement of >30% compared to the off-state, the FEES L-DOPA test is considered positive, which means that the respective dysphagia is considered L-DOPA-­ sensitive (Warnecke et  al. 2010a). In a pilot study, the FEES L-DOPA test was employed without complications as part of the clinical routine in 13 patients with Parkinson’s disease (PD), progressive supranuclear palsy (PSP), and multiple system atrophy (MSA) (Warnecke et al. 2010b; Suttrup et al. 2011). A follow-up study that evaluated 15 PD patients with motor fluctuations and dysphagia revealed excellent inter- and intra-rater reliability for the test as a whole as well as for all subscales in both the on- and off-states (Warnecke et al. 2016). As an alternative to the FEES L-DOPA test, a FEES apomorphine test can be carried out analogously. The advantage of this test is that apomorphine is administered subcutaneously, and the drug absorption thus does not depend on swallowing function or gastric emptying. FEES Fatigable Swallow Test In order to demonstrate the presence of fatigable neurogenic dysphagia (the subtype that is typically found in myasthenia gravis (MG)), a standardized FEES fatigable swallow test (FST) was developed (Dziewas et al. 2006). For the FST, a patient is offered up to 30 pieces of white bread, each about 3 × 3 × 0.5 cm3 (equivalent to a small meal). The patient is asked to chew the bread and then swallow the bolus completely. Immediately after swallowing, the patient receives the next piece of bread. The examination continues until the patient has swallowed all the pieces of bread or until severe residue occurs in the hypopharynx (Dziewas et al. 2006). In fatigable myasthenia-related dysphagia, increasing amounts of residue can be observed after about 5–10 swallows, eventually leading to the discontinuation of the examination. The number of swallows until the assessment needs to be stopped is used to quantify the severity of dysphagia (Dziewas et  al. 2006; Warnecke et al. 2008). FEES Tensilon® Test The standardized FEES Tensilon® test can also be used for the diagnosis and treatment of myasthenic dysphagia (Appendix: Scales and Scores). Analogous to the conventional Tensilon® test, FEES examines whether dysphagia improves after intravenous administration of a cumulative dose of up to 10 mg of edrophonium chloride (Tensilon®). The FEES Tensilon® test is performed according to a standardized procedure that also includes the fatigable swallow test (FST; Fig. 3.4; Warnecke et al. 2008). The FEES Tensilon® test can contribute significantly to the diagnosis of myasthenia gravis in patients with isolated dysphagia and negative acetylcholine receptor antibodies (Llabres et al. 2005; Warnecke et al. 2008). Other clinical indications for the FEES Tensilon® test in myasthenia gravis include the differentiation between myasthenic and cholinergic crisis and the adequate titration of cholinergic medication (Warnecke et al. 2008).

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FEES with simultaneous Tensilon application

pureed food

FEES following a standard protocol

penetration or aspiration

improvement

Result of FEES-Tensilon-Test

positive

pureed food no improvement

negative

no penetration and aspiration

soft solid food + thin liquids

moderate or severe pathological findings

food consistency with the most severe pathological finding

improvement

positive

negative no improvement

no or mild pathological findings Fatigable swallowing test (FST)

thirty consecutive small pieces of white bread

pathological

thirty consecutive small pieces of white bread

normal

improvement

no improvement

positive

negative

negative

Fig. 3.4  Standardized protocol of FEES Tensilon® test. The examination begins by testing puree, as in the standard FEES protocol (see box in top left). Depending on the findings, the examination continues as indicated by the arrows. A positive result is indicative of myasthenic dysphagia

3.1.5 Key Findings and Their Rating This section describes general findings of FEES in patients with neurogenic dysphagia. In addition, different grading scales are presented. A detailed description of disease-specific dysphagia findings is provided in Chap. 4. Anatomical-Physiological Examination During initial anatomic-physiological examination, it is important to assess the extent of saliva accumulation as this parameter offers conclusions about the presence and severity of neurogenic dysphagia. Significant saliva accumulation in the laryngeal vestibule is a valid predictor of severe neurogenic dysphagia (Murray et al. 1996; Donzelli et al. 2003; Dziewas et al. 2008b). In order to semiquantitatively score saliva pooling, the four-point scale developed by Murray (and modified by Langmore) can be used (Appendix: Scales and Scores; Table  3.3, Murray et al. 1996). In addition, the frequency of spontaneous swallowing should be documented. Healthy subjects swallow on average about three times per minute during endoscopy (Murray et al. 1996). As a rule of thumb, less than one spontaneous swallow per minute is considered pathological (Langmore 2001a, b). During the initial anatomic-physiological examination, it is important to ensure that any nasogastric

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Table 3.3  Summary of different types of FEES protocols Type of protocol Patient population Setting All settings Patients with General FEES suspected/manifest protocols standard dysphagia of all protocol severity grades

Diseasespecific protocols

Ice-Chip protocol

All patients with severe dysphagia and high risk of aspiration

All settings

FEDSS

Acute stroke patients

Inpatients, stroke unit

SESETD Tracheotomized (see chapter 6) intensive care patients weaned from the respirator FEES-LDopa-Test

FEESTensilon-Test

Patients with suspected/manifest Parkinson’s disease and atypical Parkinsonism Patients with suspected/manifest Myasthenia gravis

Intensive care unit, high-care rehab facilities Movement disorder clinics (in- and outpatients) Neurological inpatients

Conclusion • Dysphagia grading • Pathomechanism • Recommendations regarding:   – Airway safety   – Feeding strategy   – Behavioral procedures   – Follow-up investigations • Dysphagia grading • Pathomechanism • Recommendations regarding:   – Airway safety   – Feeding strategy   – Behavioral procedures   – Follow-up investigations • Dysphagia grading • Recommendations regarding:   – Airway safety   – Feeding strategy •R  eadiness for decannulation • I nitial feeding strategy after decannulation • Etiology of dysphagia • Change of dopaminergic medication

• Etiology of dysphagia •C  hange of myasthenia specific medication • Treatment monitoring

tubes are adequately positioned. In one study, the authors found that a nasogastric tube had been incorrectly positioned in five of 100 acute stroke patients (Fig. 3.5), which resulted in additional impairment of the swallowing act. On the other hand, a correctly positioned nasogastric tube does not lead to a clinically relevant swallowing impairment (Dziewas et al. 2008a). Laryngeal sensory function is tested by touching the arytenoids on both sides with a laryngeal adductor reflex and/or a reflexive cough or swallow being scored as physiological reactions. Reduced sensation detected by this “touchtechnique” has been shown to be associated with penetration and aspiration and

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Fig. 3.5  Position of nasogastric tubes in hypopharynx. (left upper picture) Correct position of nasogastric tube; (right upper picture) loop formation of nasogastric tube around epiglottis; (left lower picture) nasogastric tube enters laryngeal vestibule and trachea

appears to be clinically more meaningful than the airpuff-method (Kaneoka et  al. 2015). The airpuff method provides sensory thresholds in mmHg, and there is a positive correlation of this threshold with increasing age (Sect. 4.2.5; Aviv et al. 2005). The so-called pharyngeal squeeze maneuver first described by Bastian et al. in 1993 is performed during FEES in order to detect pharyngeal paresis (Bastian 1993). During this procedure, patients are asked to produce a loud, high-pitch “eee” phonation. Endoscopically, a narrowing of the hypopharyngeal lumen due to bilateral contraction of the pharyngeal constrictors can be observed (Langmore 2001a, b). The pharyngeal squeeze maneuver has a particularly good inter- and intra-rater reliability for dichotomous differentiation between normal and abnormal conditions. On the other hand, inter- and intra-rater reliability is much worse if a more sophisticated categorization into uni- or bilateral absent, reduced, or normal movement is applied (Rodriguez et al. 2007). A vigorous pharyngeal squeeze maneuver was found to be a valid surrogate for an effective pharyngeal contraction during swallowing (Fuller et al. 2009). In the same study, an abnormal pharyngeal squeeze maneuver was only moderately predictive of poor pharyngeal contraction during swallowing, possibly because there are several reasons for a poor  voluntary “squeeze” maneuver (in particular not fully understanding or executing the task). On the other hand, an impaired pharyngeal squeeze maneuver was shown to be a risk factor for laryngeal penetration and aspiration (Satow et  al. 2004; Aviv et al. 2002). Specific findings from the anatomical-physiological examination listed below can provide information on the possible lesion location within the nervous system

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(peripheral vs. central) in patients with neurogenic dysphagia and thereby help to stratify further diagnostic and therapeutic steps: • Pharyngeal fasciculations, which may be difficult to detect, indicate a peripheral etiology of pharyngeal weakness. • In patients with velopharyngeal paresis of  central origin (for example due to brainstem stroke), i.e. impaired voluntary elevation of the soft palate, involuntary elevation of the soft palate during coughing and/or swallowing is frequently preserved as opposed to patients with peripheral lesion location (Bartolome et al. 2013). • A narrowing of the piriform sinus indicates a spasticity (central lesion), while a widening suggests a flaccid paresis (peripheral lesion) of the pharyngeal musculature (Bartolome et al. 2013). • A peripheral or nuclear lesion of the recurrent laryngeal nerve or vagus nerve leads ipsilaterally to a flaccid, excavated vocal fold, which remains in the intermediate position during respiration (Bartolome et al. 2013). • Central paresis is accompanied by a characteristic change in the position of the vocal fold during the examination. At the beginning, the affected vocal fold is in a paramedian position during respiration. After maximum relaxation during the course of the examination, complete abduction is possible. During phonation, both vocal folds adduct bilaterally. Following phonation, the affected vocal fold remains in an adducted position (Bartolome et al. 2013). • Muscle twitches with a frequency of 1–3/s in the soft palate, the posterior pharyngeal wall, or the larynx are referred to as velopharyngolaryngeal myoclonus. These myocloni are characterized by rapid adduction and slow abduction movement and always indicate a central lesion (especially a cerebellar and/or brainstem infarction; Deuschl et al. 1990). While unilateral myoclonus does not affect swallowing, bilateral myoclonus may be associated with aspiration as a result of insufficient glottal closure (Schröter-Morasch and Hoole 1998). • Isolated myoclonus of the vocal folds has been found after pontine infarctions. Myoclonus may be unilateral (ipsilateral to the lesion) or bilateral and is spontaneous and irregular, with a frequency of 19–420 twitches/min. Myoclonus stops during swallowing, and isolated myoclonus of the vocal folds does not contribute to a worsening of swallowing function (Marom et al. 2013). It should be noted that in neurological diseases, the findings of the anatomical-­ physiological examinations are insufficient to adequately assess the severity and phenomenology of dysphagia. Therefore, as suggested in the Langmore protocol, an examination of food and liquid swallows needs to be performed in each patient (Seidl et al. 2008).

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Table 3.4  Definitions of endoscopically observable pathological findings Symptom Leakage of liquid during oral containment Timely/delayed/absent swallow reflex Penetration Aspiration Silent penetration/aspiration Residue/retention

Table 3.5 Standard values for time until swallow reflex is triggered as function of bolus consistency and localization

Definition Premature spillage of bolus from the mouth into the hypopharynx Time until triggering of swallow reflex (with regards to bolus consistency, size, and depth of bolus penetration) Bolus is in the laryngeal vestibule above vocal folds Bolus is below the vocal folds in the subglottal region or trachea Penetration/Aspiration without reflexive cough Remaining bolus material is in the hypopharynx after swallowing

Liquid Solid consistency

Valleculae (s) 3.2 ± 0.5 2.1 ± 0.3

Piriform sinus (s) 1.4 ± 0.6 1.5 ± 0.7

Swallow Examination Table 3.4 summarizes the definitions of important pathological findings that may be detectable during FEES and are of particular importance for the evaluation of neurogenic dysphagia. To help distinguish premature spillage (an impairment of the oral phase) from a delayed swallow reflex (an impairment of the pharyngeal phase), the test of oral containment described by Langmore can be carried out in a slightly modified form (Langmore 2001a, b). In the first step of the test, the patient is instructed to keep a liquid bolus in the mouth. In the second step of the test, the patient is asked to swallow. If the test bolus spills in the hypopharynx during the first step of the test, this is interpreted as an indication of impaired oral bolus control during the oral preparatory phase. If there is an uncontrolled transfer of the liquid bolus into the hypopharynx in the second step of the test, this is an indication of an impairment of the oral phase. According to Dua’s work, a delayed swallow reflex can be diagnosed if the pharyngeal dwell times  (i.e. time from bolus entry into the hypopharynx until begin of whiteout) summarized in Table 3.5 are exceeded (Dua et al. 1997). It should be noted that the times given for food boluses are much shorter than reported by Heiimae and Palmer (1999) and discussed earlier in this chapter. As a rule of thumb, a liquid bolus that reaches the valleculae during eating or drinking should trigger the swallow reflex within about 3 s. Accordingly, a latency of more than 3 s until the swallow reflex is triggered is also considered pathological in the so-called swallowing provocation test (SPT), which measures this latency while bypassing the oral phase of swallowing (Sect. 2.3). On the other hand, when a subject is given the task of swallowing a water bolus with a volume of between 5 and 20 mL from a cup “all at once,” according to Butler’s work, the average “bolus dwell time” in the valleculae is less than 1 s (Butler et al. 2011).

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Table 3.6  Penetration–aspiration scale (PAS) Score Description 1 Material does not enter the airway 2 Material enters the airway, remains above the vocal folds, and is ejected from the airway 3 Material enters the airway, remains above the vocal folds, and is not ejected from the airway 4 Material enters the airway, contacts the vocal folds, and is ejected from the airway 5 Material enters the airway, contacts the vocal folds, and is not ejected from the airway 6 Material enters the airway, passes below the vocal folds, and is ejected into the larynx or out of the airway 7 Material enters the airway, passes below the vocal folds, and is not ejected from the trachea despite effort 8 Material enters the airway, passes below the vocal folds, and no effort is made to eject

For the endoscopic assessment of premature spillage and a delayed swallow reflex, it is critical that the examiner always takes the instruction given to the patient into account (e.g., “Keep the bolus in your mouth.” “Please swallow the bolus.” and “Eat and drink as you would at home and swallow whenever you want.”) when interpreting the findings. In the future, additional endoscopic studies on healthy volunteers are needed to establish standard values of premature spillage and delayed swallow reflex for different swallowing tasks. The endoscopic detection of penetration and/or aspiration should indicate whether an event occurs before, during, and/or after swallowing (pre-, intra-, and/or post-deglutitively; Langmore 1997, 2001a, b). The severity of penetration and aspiration is classified using Rosenbek’s ordinal penetration–aspiration scale (PAS), which was originally developed for VFSS but has since  then been validated for FEES (Table 3.6; Rosenbek et al. 1996a; Colodny 2002). The inter- and intra-rater reliability of the PAS is excellent, regardless of the investigator’s experience with FEES (Appendix: Scales and Scores; Butler et al. 2015). FEES studies by Butler and co-workers have shown that occasional penetration and even aspiration can also be detected in healthy volunteers without dysphagia. While in a group of young subjects (mean age 30 years) out of 184 swallows one incidence each of penetration and aspiration were found, in the group of older subjects (mean age of 75), 19 incidences of penetration and 11 incidences of aspiration were found in a total of 168 examined swallows (Butler et al. 2009a). In a follow-­up study, older healthy volunteers (mean age: ~79) demonstrated within a total of 545 swallows 82 with penetration and 15 with aspiration (Butler et al. 2009b). The correlation of increasing numbers of penetration and aspiration events with increasing age likely signals an age-related worsening of swallowing function (presbyphagia; Sect. 4.2.5). In a recent study, a change in head position during FEES (right or left rotation and tilting the head up or down) did not result in a change in PAS scores in healthy subjects with no dysphagia (n = 84; Badenduck et al. 2014). In addition,

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Table 3.7  Endoscopic rating of residue

Score 0 = normal 1 = mild residue 2 = moderate residue 3 = severe residue

Definition no residue or coating only Up to approximately 25% of cavities are filled 25–75% of cavities are filled Cavities filled or overflow into laryngeal vestibule

swallowing of milk and larger bolus volumes resulted in higher risk of penetration/ aspiration than water swallow and lower bolus volumes. By contrast, the method of administering the bolus (via a cup or straw) did not affect the risk of airway invasion (Butler et al. 2011). Residue is the most important post-deglutitive pathological finding. Following Kelly and Langmore’s work, the classification given in Table 3.7 is proposed here for the endoscopic quantification of pharyngeal residue (Kelly et  al. 2006, 2008; Langmore et al. 2007): Kelly et al. (2008) were able to show that the endoscopic detection of relevant (meaning more than a trace amount) residue is always a pathological finding, even for patients of older age (>65). However, after age of 40, healthy subjects may also experience abnormal residue depending on the position of the head during swallowing, especially when the head is tilted backward or is in the chin-up position (Badenduck et al. 2014). Because of this, the examination situation and the resulting head- and body posture maintained during FEES must always be taken into account when assessing residue. In a study that included 15 patients with Parkinson’s disease and motor fluctuations, the endoscopic rating of the residue described above was shown to have excellent inter- and intra-rater reliability in both the on-state and the off-state (Warnecke et al. 2016). In addition, two other residue scales for FEES have been published in recent years: • the Boston Residue and Clearance Scale (BRASC; Kaneoka et al. 2013) • the Yale Pharyngeal Residue Severity Rating Scale (YPRSRS; Neubauer et al. 2015) The Boston Residue and Clearance Scale—developed by Susan Langmore’s group—is an 11-point ordinal residue rating scale. The scale distinguishes between two zones in which the location and severity of the residue should be assessed. Zone 1 comprises the lateral and posterior pharyngeal walls, the base of the tongue, the valleculae, and the tip of the epiglottis. Zone 2 includes the lateral channels adjacent to the epiglottis, the left and right piriform sinuses, and the postcricoid region. A severity level of 0–3 should be specified for each localization (0 = no residue; 1 = mild residue: 2/3 filled). In addition, the assessment also includes the effectiveness of spontaneous or externally cued clearing swallows, the perception of residue by the patient and possible penetration of the residue in the laryngeal vestibule. In one study, excellent inter-rater- and test-retest reliability, good compliance, and internal coherence were demonstrated with 63 swallows recorded using FEES and scored twice by 4 raters (Kaneoka et al. 2013).

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The Yale Residue Scale, developed by Steven B.  Leder’s group, involves assessing the extent of residue at two locations (in the valleculae and piriform sinus) via a 5-point ordinal scale: • valleculae: I = 0%, no residue; II = trace residue, 1–5%, trace coating of the mucosa; III = mild residue, 5–25%, epiglottic ligament visible; IV = moderate residue, 25–50%, epiglottic ligament covered; V = severe residue, >50%, filled to epiglottic rim • piriform sinus: I = 0%, no residue; II = trace residue, 1–5%, trace coating of mucosa; III = mild residue, 5–25%, up wall to quarter full; IV = moderate residue, up wall to half full; V = severe residue, >50%, filled to aryepiglottic fold In a validation study with 20 participants, very good to excellent inter- and intra-­ rater reliability and excellent construct validity were demonstrated for both scales (Neubauer et al. 2015, 2016). In order to quantify pharyngeal residue, software-based analysis methods are also being developed that could be used in the future to determine the percentage of residue that fills in the cavities (Pisegna et al. 2017; Langmore 2017). Following each FEES, in addition to documenting the different single findings, a summary report should be prepared that includes information on (1) salient findings, (2) grading of severity, (3) pathomechanisms, (4) classification, and (5) recommendations for the further diagnostics and treatment strategies. In Sect. 3.1.7, detailed recommendations for the documentation of neuroendoscopic findings are proposed.

3.1.6 Endoscopic Classification of Neurogenic Dysphagia Capitalizing on the results of published FEES studies on the specific forms of dysphagia in different neurological diseases, a classification of neurogenic oropharyngeal dysphagia based on salient endoscopic findings was developed for everyday clinical practice (Warnecke et al. 2011). The severity of neurogenic dysphagia (vertical axis; Sect. 3.1.7) is determined by the extent of penetration and/or aspiration: (0) no neurogenic dysphagia, (1) mild neurogenic dysphagia without relevant penetration/aspiration, (2) moderate neurogenic dysphagia with penetration/aspiration of one bolus consistency, and (3) severe neurogenic dysphagia with penetration/aspiration of two or more bolus consistencies. The other salient endoscopic findings allow for a description of the pathomechanism or phenotype that leads to penetration/aspiration (horizontal axis): (1) dysphagia caused by pronounced premature spillage, (2) dysphagia caused by a delayed/absent swallow reflex, (3) dysphagia caused by insufficient pharyngeal bolus clearing with residue predominantly in the valleculae, (4) dysphagia caused by an impaired opening of the upper esophageal sphincter with residue predominantly in the piriform sinus, and (5) dysphagia caused by a combination of premature spillage, pathological swallow reflex, and/or residue in the valleculae and/or the piriform sinus. Due to their specific endoscopic-neurological features, (6) dysphagia caused by

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Table 3.8  Endoscopic phenotyps of neurogenic dysphagia Main findings (1) Premature bolus spillage

(2) Delayed swallowing reflex (3) Insufficient pharyngeal bolus clearance (residue in valleculae >>> piriform sinus)

(4) Impaired opening of upper esophageal sphincter (residue in piriform sinus >>> valleculae) (5) Complex disorder (combination of I–IV, at least two equivalent phenotypes) (6) Combination of one phenotype (I–IV) with a pharyngolaryngeal movement disorder (7) Combination one phenotype(I–IV) with fatigable pharyngeal weakness

Neurological diseases Peripheral Early-stage ALS

Spinobulbar muscular atrophy, myotonic dystrophy type II, (critical illness neuropathy/myopathy) Early-stage ALS Inclusion body myositis (IBM) Severe myasthenia gravis, late ALS (Guillain–Barré syndrome (GBS)), myotonic dystrophy type I –

Myasthenia gravis

Central Early-stage ALS, early-stage PSP, frontotemporal dementia, SPG7-HSP, acute strokea Acute strokea Early-stage ALS, early-stage PD

Dorsolateral medulla oblongata infarction Late ALS, advanced PD and PSP

Neuroleptic-induced dysphagia,PD, multiple system atrophy, (Huntington’s disease) (PD, ALS)

ALS amyotrophic lateral sclerosis, PSP progressive supranuclear palsy, HSP hereditary spastic paraplegia, PD Parkinson’s disease () = There have not yet been any FEES studies for the neurological diseases listed in parentheses. The classification is based on our own clinical experience a All infarction- and bleeding sites except the dorsolateral medulla oblongata

(extrapyramidal) pharyngeal movement disorder and (7) dysphagia caused by fatigable pharyngeal weakness can be differentiated as special forms. Finally, based on the underlying disease and/or the findings of the clinical and endoscopic examination of the cranial nerves involved in the coordination and execution of swallowing, the respective phenotypes can be subdivided into those with a peripheral or a central etiology. Table 3.8 summarizes the different endoscopic phenotyps of neurogenic dysphagia and provides examples of related neurological disorders.

3.1.7 Documentation of Endoscopic Findings It is essential to adequately document findings of FEES.  Detailed reports enable other examiners to understand the relevant results of endoscopic swallowing

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Fig. 3.6 Documentation software for FEES examination. Image courtesy of Rehder/Partner Medizintechnik. Reproduced with permission

Fig. 3.7 Post-processing of recorded FEES videos. Image courtesy of Rehder/Partner Medizintechnik. Reproduced with permission

diagnostics and compare them with their own findings. We therefore recommend to digitally store reports and the accompanying swallowing videos. This also allows researchers to re-evaluate the endoscopic videos frame by frame, which has been demonstrated to optimize the reliability and validity of assessments (at least regarding penetration and aspiration) as compared with a “real-time” analysis only (Pluschinski et al. 2015). Various manufacturers offer documentation- and data-management software with their FEES units that can also be used to generate detailed reports (Figs. 3.6 and 3.7). Integrated CD/DVD archives enable long-term archiving, and the databases can be adapted to individual requirements. By using an electronic

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documentation system, the time required for generating report can be nearly halfed, and in addition reports tend to be more comprehensive (Hey et al. 2010, 2011). In addition to the detailed documentation of individual findings, which can be done using Langmore’s report form of the standard FEES protocol, a summary assessment should be provided that succinctly and thoroughly characterizes the phenotype of dysphagia and defines the further diagnostic and therapeutic work-­up. In the event of a normal finding, an abbreviated version is sufficient. From the authors’ point of view, this summary assessment should include the following five elements: 1. Salient findings The occurrence and severity of premature spillage, penetration, and/or aspiration as well as of residue should be documented. Different, commonly used grading systems of these salient findings were presented in Sect. 3.1.5. In case of penetration and/or aspiration, it need additionally be noted whether these events occur predominantly pre-, intra-, or post-deglutitively. In addition, it is important to specifically document which tested consistencies lead to which findings. 2. Grading of Severity At present, there is no uniformly used comprehensive FEES-based grading of dysphagia severity available. The most commonly applied classification is Rosenbek’s penetration–aspiration scale (PAS; Rosenbek et  al. 1996a). From the authors’ point of view, scoring severity exclusively with the PAS is inadequate because less severe forms of dysphagia that are characterized by premature spillage and/or residue and do not exhibit penetration/aspiration are not fully represented. Therefore, the following more multidimensional classification of dysphagia severity (Table 3.9)—which has been proven helpful in clinical practice and has also been used in clinical studies—is recommended (Warnecke et al. 2009a, 2010a; Suttrup et al. 2017): While this score is in principle  applicable to all diagnostic groups, for acute stroke patients the more differentiated FEDSS may be considered (Sect. 3.1.4). Table 3.9  FEES-based severity grading of neurogenic dysphagia Level 0 = no clinically relevant neurogenic dysphagia Level 1 = mild neurogenic dysphagia: relevant premature spillagea and/or residue, buta no penetration/aspiration Level 2 = moderate neurogenic dysphagia: penetration/aspiration of one food consistency Level 3 = severe neurogenic dysphagia: penetration/aspiration of two or more food consistencies a In the case of very pronounced premature spillage and/or severe residue, a higher classification (i.e., Level 2) can be applied in individual cases, even without direct evidence of penetration/aspiration

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3. Pathomechanism The main pathomechanisms associated with the previously described salient findings should be documented next. In addition it should be noted whether the specific impairment occurs predominantly during the oral, pharyngeal, or esophageal phase. Pathophysiological considerations should also take findings of the anatomical-­ physiological examination into account. 4. Classification Next, dysphagia should be classified according to the endoscopic phenotypes of neurogenic dysphagia and linked to a causative neurological disease (see Sect. 3.1.6). Following this strategy it possible to identify patients in whom the endoscopic phenotype does not match the underlying neurological disorder. In such cases, further differential diagnostic steps should be undertaken (Sect. 4.13).

Example 3.2 65-Year-Old Patient with Progressive Supranuclear Palsy (PSP; Sect. 4.3.1)

Summary assessment of FEES: Salient findings: premature spillage of liquid with pre-deglutitive aspiration, no improvement of dysphagia in FEES levodopa test Severity: moderate neurogenic dysphagia Pathomechanism: impaired oral bolus control Classification: neurogenic dysphagia with pronounced premature spillage (type I), findings in line with early-stage PSP Procedural recommendations: 1. swallow liquids in small sips 2. chin-tuck maneuver to reduce premature spillage 3. regular behavioral swallowing therapy 4. follow-up appointment in 3 months

Example 3.1 52-Year-Old Patient with Spinal and Bulbar Muscular Atrophy (Kennedy’s Disease, Sect. 4.6.3)

Summary assessment of FEES: Salient findings: moderate residue of solid food in the valleculae Severity: mild neurogenic dysphagia Pathomechanism: bilateral pharyngeal palsy and reduced mobility of the base of the tongue Classification/Phenotype: neurogenic dysphagia with insufficient pharyngeal bolus clearance (type III), phenotype consistent with spinal and bulbar muscular atrophy

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Recommendations: 1. no change in diet required 2. solid food consistencies should be ingested with liquid to improve pharyngeal bolus clearance when ingesting solid food consistencies; the patient should have clearing swallows with liquids in between 3. regular behavioral swallowing therapy 4. follow-up appointment in 6 months

5. Recommendations  for further dysphagia management Finally, where necessary, recommendations for the further evaluation of the phenotype of swallowing impairment (e.g., by VFSS and/or manometry) and also for the diagnosis of the underlying neurological disease should be provided. In addition, therapeutic strategies specifically addressing the swalloing problem in question should be suggested. As said above and detailed in Sect. 7.2.1 behavioral interventins should ideally have been directly tested and found effective during FEES.

3.1.8 Training Curriculum: “FEES for Neurogenic Dysphagia” In light of the numerous possible applications of FEES in neurological disorders and clinical scenarios and due to the recognized (DGN) demand for qualified dysphagia diagnostics, the German Neurological Society and the German Stroke Association designed a comprehensive FEES training curriculum that provides systematic education in endoscopic dysphagia diagnostics (Dziewas et al. 2014, 2016). The German Geriatric Society also approved this program in 2016. By defining quality standards, the FEES curriculum aims to help ensure that FEES is conducted consistently and at an appropriate level. In addition, the intended standardization of terminology, examination algorithms, and interpretation of findings are designed to promote and facilitate interprofessional communication within the individual treatment teams and will also contribute to the optimisation of understanding between the various sites involved in the treatment of an individual patient over time, e.g. acute clinic, rehabiliation clinic, and outpatient care. Since the diagnostics and therapy of swallowing disorders are relevant to many disciplines, this training curriculum is not only intended for neurologists but is open to all clinicians with an interest in this topic. In addition, it offers SLPs the opportunity to acquire additional qualification in the field of instrumental dysphagia diagnostics and thus to expand their range of activities. Figure 3.8 gives an overview of the different educational steps leading to the FEES certificate and the FEES instructor certificate. More detailed information can be found on the DGN’s homepage (https:// dgn.org/fortbildungen/fees-fortbildungen/informationen-zu-fees/) and in the corresponding article (Dziewas et  al. 2014, 2016). In 2017, the European Society for Swallowing Disorders (ESSD) decided to offer a FEES accreditation program for neurogenic and geriatric oropharyngeal dysphagia in a slightly adapted form at the European level (Dziewas et al. 2017).

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aApplying for an authorisation to administer FEES-instructor examinations implies a minimum of 2 years of activity in this field, the verifiable performance of at least 500 FEES, the participation in the organization, and realisation of, at least one curricular FEES workshop, the training of at least five FEES-certificate holders and, optionally, a relevant scientific contribution

Fig. 3.8  Training steps of FEES curriculum created by DGN, DSG, and DGG

3.2

Videofluoroscopic Swallowing Study (VFSS)

The videofluoroscopic swallowing study (VFSS) is a contrast based  radiological swallow examination of the entire swallowing act. This method has its roots in the classical radiological barium swallow, which, mainly driven by the American SLP Jeri A. Logemann, was modified to meet the requirements of dysphagia diagnostics (Logemann 1998)  thereby coining the term, “modified barium swallow”. VFSS, which is carried out according to the so-called Logemann standard, was generally accepted as the sole gold standard of instrumental dysphagia diagnostics until the introduction of FEES. VFSS allows for a detailed analysis of all phases of swallowing (Langmore 2003). A detailed comparison of the advantages and disadvantages of VFSS and FEES—which are today considered to be complementary instrumental procedures for dysphagia evaluation—can be found at the end of this section. For additional information on methodology and evaluation, the articles on VFSS in neurogenic dysphagia by Gates et al. (2006), Rugiu (2007), and Wuttge-Hannig and Hannig (2007) are recommended.

3.2.1 Indications VFSS allows for a sensitive detection of aspiration, enables a precise  temporal assignment of these events in relation to the initiation of swallowing and also provides a related severity grading of aspiration, which may be relevant, for example,

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to assess the efficacy of rehabilitative measures. Moreover, swallowing pathologies without aspiration, in particular impairments of the closing and propulsion mechanisms during the oral, pharyngeal, and esophageal phases can be reliably identified. In addition to precisely identifying the pathomechanisms of dysphagia, VFSS can also be used to monitor treatment effects during specific interventions and to help determine nutritional and therapeutic strategies (Logemann 1998).

3.2.2 Technique In general, three dynamic recording methods are available: (1) high-frequency cinematography, (2) videofluoroscopy, and (3) digital spot imaging (DSI). High-­ frequency cinematography allows for the recording of fast motion sequences with frame rates of 50–200/s, which are recorded with a 35 mm cinema camera and have a relatively high spatial resolution. High-frequency cinematography is predominantly reserved for scientific questions and is only indicated in clinical diagnostics in special cases of fast movement phenomena. Videofluoroscopy can be performed at a conventional fluoroscopy workstation. The images are recorded either on videotape or—much more common  today—digitally (DSI). For digital recordings, a frame rate of about 25–30 images/s is sufficient to achieve the necessary temporal resolution for a proper analysis of the rapid processes of swallowing.

3.2.3 Radiation Exposure A diagnostic DSI fluoroscopy with a frame rate of 30/s and three series of about 150–400 images per series is associated with an effective radiation exposure of about 3–5  mSv (MilliSievert). Up to 7  mSv may be acquired with higher frame rates. In comparison, exposure to natural ambient radiation is about 2.4 mSv/year and radiation exposure of a CT scans of the thorax and abdomen ranges between 5 and 15 mSv. Like all examinations that uses X-ray, VFSS applies the so-called ALARA principle (“as low as reasonably achievable”), which refers to the careful use and minimization of radiation exposure by limiting examination times and by focussing on the target area.

3.2.4 Contrast Agents When planning the investigation the most suitable contrast agent for the given patient needs to be determined with anticipated aspiration risk being the most important factor here. In principle, non-water-soluble barium sulfate suspensions (Micropaque® liquid) have to be distinguished from water-soluble hyperosmolar contrast agents that contain iodine (Gastrografin®) and from non-ionic iso-osmolar contrast agents (Isovist®, Ultravist®).

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In the absence of episodes of aspiration in the patient's history and without clinical signs of aspiration during a preceding water swallow test, barium sulfate should be used for VFSS. In the case of a high risk of aspiration, non-ionic, iso-osmolar contrast agents are preferred, such as iopromide (Ultravist®), which does not carry any relevant pulmonary risk due to its pharmocological properties (Gmeinwieser et al. 1988). Aspiration usually results in the absorption of the contrast agent into the periphery of the lungs within half an hour. For the gas-soluble hyperosmolar contrast agent Gastrografin®, severe cases of pulmonary edema with  reflectory cardiovascular arrest have been described subsequent to the aspiration of larger volumes during computer tomography of the thorax and abdomen; therefore, the use of this contrast agent during VFSS should be critically assessed (Trulzsch et  al. 1992). However, the use of small amounts of water-soluble hyperosmolar contrast agents is considered acceptable in this scenario (Awounou and Stanschus 2009). Any of the mentioned contrast agents can be thickened according to the requirements of the examination (see below).

3.2.5 Procedure Ideally, the examination should be carried out in close collaboration between a radiologist and a SLP. In addition to the diagnostic focus aiming to uncover the pathophysiology of dysphagia, the SLP can use the knowledge gained from the preliminary clinical examination to modify the type and order of the tested food consistencies as well as to provide specific instructions for compensatory techniques (e.g., a change in posture). On the basis of the jointly collected findings, the SLP can determine what further therapy and nutrition are needed and—if necessary—arrange any necessary check-ups (Awounou and Stanschus 2009). VFSS can be conducted with the patient either standing or sitting. During the procedure, the patient is placed between the X-ray tube and the detector block and should be investigated in a natural eating posture. The instruction to sit very still and avoid any movement—which is normally used in radiological diagnostics—is not indicated here. Nevertheless, the examination situation never corresponds entirely to reality for several reasons: (1) The patient must first keep the bolus in the mouth and be allowed to swallow only on command, (2) the contrast agent’s viscosity does not match that of normal food, and (3) due to the unusual flavor of most contrast agents, the patient’s normal swallowing behavior may change. If a feeding tube has already been inserted, it should be left alone during VFSS as it only slightly affects the findings and disturbing the patient by re-inserting the tube after the examination thus does not appear to be justified (Awounou and Stanschus 2009). On the one hand, the diagnostic procedure should be as standardized as possible; on the other hand, the examination should be adapted to the concrete clinical situation and also take existing findings into account. VFSS usually tests liquids, semi-­solids, and solid foods sequentially. Since evaluating the effectiveness of swallowing therapies (for example change in posture, sensory stimulation

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techniques, swallowing maneuvers, modifications of volume and consistency) is also an important part of VFSS, the consistency and size of the bolus and the patient’s posture should—if necessary—be adjusted to match the patient’s pattern  of swallowing impairment and his experience in previous examinations. During the entire VFSS, protection against aspiration has the highest priority, and if necessary, it is possible to bypass the testing of the individual’s diet. The aim of the study is to create a test load sufficient to detect any decompensation while simultaneously avoiding any complications. These aspects are taken into account in the protocol established by Jeri A. Logemann and are known as the Logemann standard (Logemann 1993). Logemann’s Standard VFSS Protocol 1. Lateral view The examination begins in the lateral view. The following structures are usually used as anatomical landmarks for defining the optimal image section: • • • •

anterior: lips superior: soft palate posterior: posterior pharyngeal wall and cervical spine inferior: seventh cervical vertebra

The oral cavity and pharynx should be visible throughout the entire swallowing cycle. If this is not possible, the focus during the assessment of the pharyngeal phase should initially be on the base of the tongue, the pharynx, the larynx, and the upper esophageal sphincter. Subsequently, the examination can be focused on the oral cavity during the observation of the oral phase. At the beginning of VFSS, a brief initial observation without swallowing can be made of the oropharyngeal structures with respect to movement disorders (for example tremor and myoclonus). Since pronounced osteophytes and diffuse idiopathic skeletal hyperostosis (DISH; Sect. 4.12.5) may affect swallowing, the patient’s anatomy, and in particular the cervical spine should also be carefully  assessed. When studying the swallow, the patient first receives a few liquid boli of increasing volume (1, 3, 5, and 10 mL). Small volumes are applied with a teaspoon. Boli of 5 mL or more are dispensed in a small plastic cup or carefully placed in the patient's mouth using a syringe. Importantly, the patient is instructed before to only swallow when instructed to do so by the examiner. The initial small amounts of contrast agent only slightly moisten the anatomical structures, which improves their visibility and assessability. In addition, starting with small bolus volumes also reduces the risk the patient is exposed to in case of massive aspiration. If there is no evidence of an increased risk of aspiration even after increasing bolus volumes, consecutive drinking from a cup should be tested. This stress test requires a persistent glottal closure and is much closer to natural drinking than are the single swallows on comand. The test also serves to detect a myasthenic syndrome, which often results in aspiration only during the stress test (Wuttge-Hannig and

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Hannig 2010). In the next step, 1/3 teaspoon of a semi-solid, pudding-like consistency is tested two to three times. If these items are also successfully swallowed, the patient receives a solid bolus (e.g., a piece of a cracker coated in barium paste) and is requested to chew and swallow it as usual. In individual cases, it may be necessary to study mixed consistencies and extend the examination to several uncued swallows during VFSS, it is important to pay attention to the amount and localization of residues and to residue management, such as spontaneous clearing swallows, the lack of a protective reflex as a sign of a sensory disturbance, laryngeal penetration, and the occurrence and timing of aspiration. 2. Anterior-posterior view Finally, the patient is examined in the anterior-posterior view, which is particularly appropriate to detect lateral asymmetries (e.g., unilateral residues in the case of one-sided pharyngeal paresis), and general pharyngeal weakness with resulting bilateral residues. This examination step can be complemented by a “Valsalva maneuver” to depict hypotonic parts of the pharyngeal constrictors. To minimize radiation exposure, only consistencies with pathological findings in the lateral view are tested here.

3.2.6 Findings The localization and movement of the bolus in relation to the radiologically visible movements of the oropharyngeal structures are made visible by the contrast agent (Krauß 2009). The image sequences are evaluated qualitatively (descriptively) as well as quantitatively by determining the following specific parameters. (Stanschus 2002; Awounou and Stanschus 2009; Prosiegel and Weber 2013): • oral onset time (the time between the instruction to swallow and the beginning of oral transit) • oral transit time (norm: 60-year-old group. In addition, FEES studies by Butler et  al. (2009a, b) have shown that in older subjects (with a mean age of 75 and 79, respectively) with no subjective dysphagia, penetration and aspiration are present in 11–15% of subjects and 2.75–6.5% of all swallows, respectively. Kelly et al. (2008) used FEES to compare the amount of residues of 30 healthy subjects aged >65 with that of 21 healthy

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subjects aged 65  years)—and should not be interpreted as an expression of age-related changes in swallowing function. Radiological Findings Alterations resulting from presbyphagia affect all phases of swallowing. Elderly healthy volunteers display a prolonged oral phase (Kim et al. 2005), decreased isometric tongue pressure (Robbins et  al. 1995), slower tongue movements (Rofes et al. 2010), a delayed initiation of the swallow reflex (Tracy et al. 1989), a smaller bolus volume per swallow, premature spillage of liquid into the pharynx, an accumulation of pharyngeal residue, a higher rate of laryngeal penetration (Yoshikawa et al. 2005), and delayed laryngeal closure compared with younger healthy subjects (Rofes et al. 2010). In a review on this topic, Ney et al. (2009) assumed that there is progressive disconnection of the voluntary oral phase from the involuntary pharyngeal phase as a result of age-related changes in swallowing. Alzheimer-related dysphagia is characterized by an orotactile “agnosia/swallowing apraxia” with predominant impairment of the oral phase and the transition from the oral to the pharyngeal phase (predominant disturbance of the sensory components of swallowing). The pattern of neurogenic dysphagia in vascular dementia is heterogeneous and depends on the distribution of the vascular lesions and predominantly affects the motor components of swallowing. Frontotemporal dementia causes neurogenic dysphagia that is characterized by marked premature spillage and/or insufficient pharyngeal bolus clearance. Neurogenic dysphagia may be the first symptom of Lewy body dementia. The pharyngeal phase of swallowing is more frequently impaired in Lewy body dementia than is the oral phase of swallowing. Presbyphagia (age-related changes in swallowing function) should be differentiated from dementia-related dysphagia.

4.3

Movement Disorders

4.3.1 Parkinsonian Syndromes Parkinsonian syndromes are clinically characterized by the onset of cardinal motor symptoms, including bradykinesia, rigor, tremor, and postural instability. Atypical and symptomatic Parkinsonism should be differentiated from idiopathic Parkinson’s disease (Schwarz and Storch 2007). In all types of Parkinsonian syndromes, neurogenic dysphagia is a major risk factor for pneumonia which in turn is the leading

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cause of death in these patients (Prosiegel et al. 2012). In addition, neurogenic dysphagia in Parkinson’s disease can lead to significant impairment of the quality of life, insufficient response to dopaminergic treatment, and severe malnutrition (Miller et al. 2006). Parkinson’s Disease Parkinson’s disease (PD) is a very common neurological disease with an incidence of 10/100,000 and a prevalence of 300/100,000 (Ceballos-Baumann 2005b). Depending on the presence of cardinal motor symptoms, an akinetic-rigid subtype, a tremor-dominant subtype, and a mixed subtype can be distinguished. More than 50% of PD patients develop neurogenic dysphagia during the course of the disease (Edwards et al. 1992, 1993; Pfeiffer 1998). Swallowing disorders that patients subjectively recognize and complain of usually appear in more advanced stages of PD (on average after 10–11 years of illness), at which point the average life expectancy is 24 months (Müller et al. 2001). In individual cases, however, subjective swallowing impairment have also been reported as the first symptom of PD (Thomas and Haigh 1995). A significant reduction in the speed of swallowing was demonstrated during the early stages of Parkinson’s disease (n  =  66; mean disease duration = 1.26 years) in comparison with control subjects, although the affected patients did not complain of dysphagia (Moreau et al. 2016). Between 1979 and 2010 PD patients in the USA were 3.8-fold more likely to suffer from aspiration pneumonia than a control group. Overall, aspiration pneumonia occurred in 3.6% of PD (Akbar et al. 2015). In a smaller Canadian study covering the period from 1994–1999, there was even a 6.34-­fold increased risk for PD patients to acquire aspiration pneumonia (Guttman et al. 2004). In a retrospective single-center study, 212 PD inpatients (mean age = 74.1; mean disease duration = 6 years) had a rate of nosocomial aspiration pneumonia of 2.4% during 339 hospital stays. Only 12.5% of patients had previously undergone a swallow examination, and overall less than one-­quarter of all patients had received a dysphagia evaluation (MartinezRamirez et al. 2015). PD patients who were advised to exclusively receive enteral feeding due to their dysphagia and yet continued to eat orally displayed an increased risk of aspiration pneumonia over the subsequent 12 months (Goh et al. 2016). Swallowing disorders are often not perceived by PD patients themselves. In addition, even if they are recognized by them, swallowing problems are only rarely reported spontaneously (Bushmann et al. 1989; Bird et al. 1994). When instrumental methods were used in addition to a clinical examination, dysphagia was found in more than 50% of cases of subjectively asymptomatic PD patients (Bird et al. 1994; Fuh et al. 1997; Manor et al. 2007). A recent meta-analysis by Kalf et al. found that the prevalence of oropharyngeal dysphagia in PD patients increased from 35% via subjective assessments to 82% when objective examination techniques had been used (Kalf et al. 2012). Silent penetration and aspiration have been detected by means of instrumental diagnostics in about 20% of PD patients with sialorrhea (Nobrega et  al. 2008a). These PD patients have a significantly increased risk of respiratory infections within the subsequent year (Nobrega et al. 2008b), and the swallowing-related quality of life decreases significantly with the progression of the movement disorder

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(van Hooren et al. 2016). In the so-called Barcelona and Lisbon cohort, 68% of latestage PD patients (Hoehn and Yahr Stages 4 and 5; mean disease duration = 17.9 years) were shown to have on-state dysphagia. Subjectively, patients judged dysphagia to severely affects their health (Coelho et al. 2010). Recent studies have also shown that PD patients with dysphagia are significantly more likely to have affective symptoms such as anxiety and depression compared with PD patients without dysphagia (Manor et al. 2009; Han et al. 2011). Clinical Diagnostics The following clinical criteria indicate a significantly increased risk of dysphagia in PD patients and should therefore be given special attention: 1 . Hoehn and Yahr Stages IV and V (Coelho et al. 2010) 2. Unintentional weight loss over several months or a body mass index of G mtDNA mutation was not associated with dysphagia (Hedermann et al. 2017). Radiological Findings In one case series, ten patients with CPEO-plus and two patients with KSS (mean age: 46) were examined consecutively by VFSS. In total, ten patients had neurogenic dysphagia. As radiological key finding, cricopharyngeal obstruction (cricopharyngeal achalasia) was detected in nine patients. Three of these patients displayed >50% constriction of the upper esophageal sphincter during the swallow. In addition, pharyngo-esophageal manometry was performed in eight of these patients. In the subgroup of patients with cricopharyngeal achalasia, pressure in the upper esophageal sphincter was elevated before and after the swallow. However, normal relaxation of the upper esophageal sphincter was detectable intra-deglutitively in the majority of patients (Kornblum et al. 2001). In a recent study, swallowing function in 14 CPEO patients examined via VFSS was compared with that of 16 healthy control subjects. CPEO patients had significantly shorter pharyngeal transit times of semi-solid and solid food consistencies (Domenis et al. 2015).

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Manometric Findings 14 CPEO patients (five men, nine women; mean age: 35.3), seven of whom had been subjectively complaining of impaired deglutition, were examined by esophageal manometry. Manometric findings were compared with those of 16 healthy controls. CPEO patients featured a lower amplitude and shorter duration of contractions in the proximal esophagus as well as an increase in peristaltic velocity in the distal esophagus (Domenis et al. 2011). Mitochondrial myopathies, especially CPEO-plus and KSS, can lead to severe neurogenic dysphagia characterized predominantly by an opening disorder of the upper esophageal sphincter.

4.9.5 Facioscapulohumeral Muscular Dystrophy Facioscapulohumeral muscular dystrophy (FSHD) is an autosomal dominant disease with a prevalence of 1/20,000. The disease typically manifests during the 2nd–3rd decade of life. Clinically, FSHD is characterized by a slowly progressive, asymmetric atrophy and weakness of the facial, shoulder, and arm muscles. Muscle enzymes are usually slightly elevated, and the diagnosis is confirmed by the detection of a deletion of D4Z4 repeats on chromosome 4q35 (Sieb et  al. 2009). While severe neurogenic dysphagia is not a typical feature of FSHD, mild swallowing impairment may develop during the course of the disease as a result of poor oral function, tongue weakness, and/or tongue atrophy (Wohlgemuth et al. 2006). Endoscopic Findings Based on the authors’ clinical experience, reduced retraction of the tongue base with resulting mild to moderate residue in the valleculae can be endoscopically detected in FSHD patients. Radiological Findings Wohlgemuth et al. (2006) used VFSS to examine eight FSHD patients (mean age: 39) who had been complaining of swallowing problems. A clinical examination revealed a weakness of the chewing and/or tongue muscles in all patients. Seven patients also had radiographic signs of mild oropharyngeal dysphagia. In one patient, an impaired esophageal transit was detected. The main pathological findings of oropharyngeal dysphagia were fragmented swallowing, delayed pharyngeal transport, decreased retraction of the tongue base, and pharyngeal residue. In two patients, aspiration with a subsequent sufficient cough reflex was detected. In another study, swallowing function in 20 FSHD patients (mean age: 38) was radiologically examined. Ineffective pharyngeal contractions, pharyngeal diverticula, and reduced relaxation of the cricopharyngeal musculature were detected in two of the patients (Stubgen 2008).

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Manometric Findings In the same study, swallowing function in the 20 FSHD patients was also examined manometrically. Evidence of non-specific esophageal dysmotility was found in three patients (Stubgen 2008). FSHD may be associated with mild oropharyngeal dysphagia, which is most often characterized by weakness of the tongue base resulting in residues in the valleculae.

4.9.6 Myotonic Dystrophies Myotonic dystrophies are clinically and genetically heterogeneous disorders that are multisystemic in nature and feature an autosomal dominant inheritance. Their main clinical signs and symptoms are muscle weakness, myotonia, and cataracts. Myotonia is characterized by abnormally slow or delayed muscle relaxation following normal muscle contraction with a characteristic neurophysiological signature in electromyographic testing. To elicit grip myotonia, the patient is instructed to grip the examiner’s fingers firmly and then to let go rapidly: In the case of myotonia, the relaxation of the fingers is delayed. Percussion myotonia is induced by firmly percussing the thenar eminence, which causes the thumb to abduct and then relax slowly in the presence of myotonia. There are two forms of myotonic dystrophies (Sieb et al. 2009). Myotonic Dystrophy Type 1 (DM1; Dystrophy Curschmann–Steinert) With a prevalence of 5.5/100,000, DM1 is the most common form of adult muscular dystrophy in Europe. Clinically, DM1 is characterized by distal muscle weakness, muscular atrophy, ptosis, myotonia, cataracts, a receding hairline, cognitive disorders, dilated cardiomyopathy, cardiac arrhythmias, and various endocrine disorders, such as diabetes mellitus and testicular atrophy. There are congenital and infantile forms, forms in early adulthood, and an adult form that typically manifests between the ages of 20 and 40. A trinucleotide expansion can be detected on chromosome 19q13.3 via genetic testing (Sieb et al. 2009). Several studies have found a prevalence of neurogenic dysphagia of between 25% and 80% in DM1 patients, and dysphagia is often not adequately perceived by DM1 patients (Bellini et al. 2006). Pneumonia is the leading cause of death in DM1 patients in adulthood (de Die-Smulders et al. 1998). Only a subgroup of dysphagic DM1 patients has been found to have percussion myotonia of the tongue in the neurological examination. DM1-related dysphagia is often associated with fragmented and repetitive swallowing (Ertekin et al. 2001b). Dysphagia has been identified as the main reason for impairment of drug intake in DM1 patients (Fitzgerald et al. 2016). Interestingly, caregivers of DM1 patients often describe dysphagia as being relatively mild despite the fact that this symptom limits the patients’ life expectancy (LaDonna et al. 2016).

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Endoscopic Findings In FEES, DM1 patients often display salivary accumulation that cannot be completely cleared as well as silent saliva penetration and residue of semi-solid and solid food consistencies in the valleculae and piriform sinus (Jungheim et al. 2015b). In a Dutch study, 45 consecutive DM1 patients (mean age: 46; mean disease duration: 14 years) were compared with ten healthy control subjects. All salient findings seen in FEES were frequently detectable in the group of DM1 patients for all three tested food consistencies (liquid, thickened liquid, cookie). These findings were a delayed swallow reflex, residue in valleculae and piriform sinus, penetration and aspiration, and fragmented swallowing. Most of these findings were more pronounced with liquids than with the other food consistencies. Aspiration of liquids was detected in 17 patients (Pilz et al. 2014a). Radiological Findings In a VFSS study, swallowing function in 18 DM patients (12 men, 6 women; ages between 24 and 58) was compared with that of 60 healthy control subjects. A prolonged oral and pharyngeal transit time was observed in the DM1 group. As a possible correlate of a myotonic reaction, a significantly delayed reconfiguration of the hyolaryngeal complex with a marked slowing of the epiglottis’s return to the resting position after the swallow was demonstrated in DM1 patients without any associated impairment of the swallowing process. Furthermore, hypopharyngeal residue was found as a result of weakened pharyngeal muscle contraction. An early and prolonged opening of the upper esophageal sphincter in DM1 patients was interpreted as a compensatory mechanism. Overall, it was concluded that pharyngeal muscle weakness is more critical to the severity of dysphagia than is pharyngeal myotonia (Leonard et al. 2001). Manometric Findings Pharyngo-esophageal dysmotility has been detected in studies that have examined DM1 patients with conventional esophageal manometry. The main pathological findings have included reduced amplitudes of the peristaltic esophageal contractions, a complete esophageal atony, decreased pharyngeal contractions, and reduced resting pressure in the upper esophageal sphincter (Pilz et al. 2014b). Some studies have also found decreased resting pressure in the lower esophageal sphincter, which thereby increased the risk of gastroesophageal reflux (Bellini et al. 2006). In two DM1 patients, high-resolution esophageal manometry (HRM) was able to detect an esophageal dysmotility, which was classified as type I achalasia (missing contractions) according to the Chicago classification (Paris et al. 2012b). Furthermore, by employing HRM, reduced pharyngeal contractility resulting in reduced pharyngeal bolus pressure was described in DM1 patients (Jungheim et al. 2015b). Electromyographic Findings Ertekin et al. (2001b) studied swallowing function in 18 DM1 patients electromyographically (mean age: 38.8, mean disease duration: 14.3 years). The main findings were (1) a delayed onset of the pharyngeal swallow, (2) prolonged duration of the

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involuntary pharyngeal stage of swallowing, and—in a minority of patients—(3) hyperreflexia of the upper esophageal sphincter. The following possible pathophysiological mechanisms were attributed to these findings: (1) oropharyngeal myotonia, (2) oropharyngeal muscular dystrophy, and (3) involvement of the medullary swallowing centers during the course of the disease. In a recent study, surface EMG used on DM1 patients (n  =  20) also showed a prolonged activation of the pharyngeal musculature during swallowing as main characteristic finding compared with healthy control subjects (Ercolin et al. 2013). Myotonic Dystrophy Type 2 (DM2; Proximal Myotonic Myopathy, PROMM) DM2 usually takes a less severe clinical course than DM1 and is characterized by proximal muscle weakness, myotonia, muscle pain, cardiac conduction defects, cataracts, and testicular atrophy. The onset of the disease is usually between the 20th and 50th years of life, and congenital forms do not exist. In terms of molecular genetics, there is a tetranucleotide repeat on chromosome 3q2.1 (Sieb et al. 2009). Dysphagia has been reported in 14–52% of DM2 patients (Day et al. 1999; Tieleman et  al. 2008). Difficulties in swallowing solid consistencies have been more frequently reported than problems with liquids (Tieleman et  al. 2008); however, because dysphagia seems to be more mild in DM2 as compared with DM1, there is no increased risk of aspiration pneumonia, even in advanced stages of the disease (Tieleman et al. 2008, 2009). Endoscopic Findings Tieleman et al. used FEES to study eight patients with genetically confirmed DM2 who had been complaining of impaired deglutition. Seven of these patients had mild dysphagia. The most frequent pathological findings included residues with solid consistencies (88%) and milk (75%). Rarely, salivary retentions (25%) and premature spillage of solid consistencies (25%) and milk (13%) were found. Penetration or aspiration did not occur in any of the patients. The severity of dysphagia correlated with the patients’ age but not with the disease duration (Tieleman et al. 2009). While DM1 is often associated with severe pharyngeal dysphagia, mild pharyngeal dysphagia without an increased risk of aspiration is found in DM2. A delayed reconfiguration of the hyolaryngeal complex post-swallow can occasionally be observed in patients with DM1 and is interpreted as myotonic pharyngeal response.

4.10 Trauma 4.10.1 Traumatic Brain Injury In Germany, about 150,000–250,000 people suffer from a traumatic brain injury (TBI) every year, and up to 40,000 cases involve severe trauma. The incidence rate of intracranial injury is 29 cases per 100,000 inhabitants. The most common cause

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(40–50%) is traffic accidents. TBI can lead to brain damage through various pathophysiological mechanisms: (1) primary damage: diffuse axonal injury and focal damage (coup and contrecoup) with brain contusion and/or hematomas and (2) secondary damage: cerebral edema, increased intracranial pressure, hypoxia, ischemia, inflammation (Wallesch et al. 2005). Neurogenic dysphagia is a common and serious symptom of TBI. Severe TBI causes clinically relevant dysphagia in approximately 60% of patients during the acute phase (Leder 1999; Mackay et al. 1999b; Morgan and Mackay 1999). A low Glasgow Coma Scale (GCS) score (especially 14  days (Mackay et  al. 1999b). Hospitals that provide care for TBI patients should have a standard diagnostic algorithm for dysphagia management (Schurr et  al. 1999). Because dysphagic TBI patients, much like other patients with neurogenic dysphagia, often have silent aspiration, a clinical swallow examination alone is insufficient and needs to be complemented by an instrumental swallowing evaluation (Leder 1999; Schurr et al. 1999). Dysphagic TBI patients require an approximately threefold amount of time on artificial ventilation, and oral intake is delayed for approximately three times (11 days vs. 28 days) compared with non-dysphagic TBI patients (Mackay et al. 1999a). In a recent study, independent risk factors for the persisting need for artificial feeding upon discharge from an acute care facility were higher age, the presence of a tracheostomy, and aphonia during the initial swallowing examination (Mandaville et al. 2014). Endoscopic Findings Leder (1999) examined swallowing function in 47 TBI patients during the acute phase of the illness (30 men, 17 women; mean age: 34). Aspiration was detected in 17 patients (36%), 53% of which was silent. The 17 aspirators were initially unable to take an oral diet. Of the remaining 30 patients, ten received a modified oral diet, and 20 managed a regular diet immediately after swallowing evaluation with FEES. Overall, the authors concluded FEES to be a particularly suitable method in this clinical context since it can be used flexibly and on short notice for follow-up examinations given that the neurological condition in TBI patients is prone to change rapidly, and it considerably helps in determining the type of oral diet (Leder 1999). Radiological Findings In a VFSS study, 54 TBI patients were evaluated during early rehabilitation immediately following acute care (45 men, nine women; mean age: 26.8 years). The key inclusion criterion for study participation was sufficient cognitive function to allow for completion of the radiological swallow examination. 21 patients were tracheotomized at the time of VFSS, and dysphagia was detected in 61% of patients. The five most common swallowing abnormalities (≥45% of the dysphagia patients) were a lack of oral bolus control, reduced tongue control, decreased

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retraction of the tongue base, a delayed pharyngeal swallow response, and impaired closure of the laryngeal vestibule. Only one patient displayed cricopharyngeal dysfunction. Aspiration was seen in 41% of all TBI patients (Mackay et  al. 1999b). A recent study retrospectively compared VFSS findings from 41 TBI patients with a control group consisting of stroke patients. There were no significant differences between both groups regarding to the severity of dysphagia. In brain trauma patients, the most common symptoms were penetration or aspiration (73.2%), decreased laryngeal elevation (68.3%), and reduced epiglottic inversion (61%; Lee et al. 2016).

4.10.2 Spinal Cord Trauma In industrialized countries, the annual incidence rate of acute spinal cord lesions is about 10–30/1,000,000 inhabitants. Traumatic spinal cord lesions are most likely to affect young people between 16 and 30  years of age (Wallesch et  al. 2005). Injuries to the cervical spine may result in mechanical and/or neurogenic dysphagia due to the close anatomical vicinity to the larynx and the esophagus. In addition, dysphagia is a common complication in cervical spine surgery (especially with an anterior approach; up to 79% of patients in the first week after surgery and 13–21% 1  year after surgery; Riley et  al. 2010). In surgeries with an anterior approach at the level of C3 and C4, lesions of the hypoglossal nerve, the superior laryngeal nerve, and the recurrent laryngeal nerve at the level of C6 have been described as contributing factors to subsequent dysphagia (Martin et  al. 1997; Abel et al. 2004). Age, an anterior surgical approach, artificial ventilation, and tracheotomies have been identified as predictors of dysphagia after spinal cord injury (Kirshblum et al. 1999). About one-third of all patients with acute cervical spinal cord trauma have been estimated to suffer from dysphagia (Abel et al. 2004). These patients have an increased risk of pneumonia late in the course of the disease (>2 weeks after the trauma; Abel et  al. 2004). Seidl et  al. (2010) found clinically relevant dysphagia in 28% of 175 patients with severe cervical spinal cord trauma resulting in tetraplegia in a recent retrospective study. Similarly, another retrospective cohort study of patients with spinal cord trauma treated in a trauma center revealed clinically characterized dysphagia in 26% of cases. Significant predictors of dysphagia were older age (>65 years) and spinal cord lesions. However, the majority of patients with dysphagia did not have a spinal cord lesion subsequent to the trauma (Lee et al. 2016). Lesions at the level of C3 to C5 resulted most frequently in swallowing disorders. Mechanical and neurogenic changes in the pharynx were claimed to be the causes of dysphagia. Tissue swelling as well as the impairment of sensation, motor functions, and laryngeal elevation are commonly assumed to cause dysphagia. To diagnose dysphagia, a standardized clinical swallowing evaluation was recommended in combination with FEES (Seidl et al. 2010). The additional costs incurred by dysphagia in this patient group were estimated at €40,000 (Seidl et al. 2010).

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Endoscopic Findings In a longitudinal observational study, 51 patients suffering from acute cervical spinal cord injury were examined in the intensive care unit using FEES (35 men, 16 women; mean age: 43.4 years). At the time of admission, 21 patients had severe dysphagia with significant aspiration, and 20 patients showed mild dysphagia (a laryngeal edema or minor aspiration with a sufficient cough reflex). Overall, the prognosis of dysphagia was good. Only three patients still had severe dysphagia at discharge (Wolf and Meiners 2003). Radiological Findings One study retrospectively analyzed the VFSS outcomes of 13 patients who had undergone cervical spinal surgery with an anterior approach and presented with a new onset of dysphagia thereafter. The following pathomechanisms were identified: pre-vertebral swelling of the soft tissue with insufficient movement of the pharyngeal posterior wall and impaired opening of the upper esophageal sphincter, an absent or weak pharyngeal swallow, impaired oral bolus control, and reduced tongue motility (Martin et al. 1997). The risk factors for TBI-related dysphagia include a low score on the Glasgow Coma Scale, severe post-traumatic cognitive impairment, a midline shift, brainstem involvement, and the need for emergency surgery and artificial ventilation >14 days. In cervical spine surgery with an anterior approach at the C3- and C4 level, lesions of the hypoglossal and superior laryngeal nerves are responsible for postoperative dysphagia, while surgery at the C6 level is associated with lesions to the recurrent laryngeal nerve. In spinal cord injuries, lesions at the C3–C5 level are particularly prone to causing neurogenic dysphagia. Dysphagia can also occur even without detectable lesions confined to the spinal cord.

4.11 Psychogenic Dysphagia To date, there is no reliable information on the incidence rates of psychogenic or functional dysphagia (i.e., subjective impairments of swallowing without an underlying pathophysiological mechanism or structural lesion) in the literature. Psychogenic dysphagia often manifests in early or middle adulthood, and women are reported to have these symptoms more often than men. Apart from weight loss, typical complications of dysphagia (particularly aspiration pneumonia) do not occur, and the neurological examination is typically normal (Buchholz 1994). Triggering psychological stress often persists for a very long time and is complex in nature and difficult to uncover. Depression, anxiety, and an introverted personality are more prevalent in affected individuals than in healthy controls (Deary et al. 1995a, b). Occasionally, oral dysfunctions are found in the clinical swallow examination and are phenomenologically similar to

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swallowing apraxia. When analyzed with VFSS, these findings include a complex impairment of tongue movement resulting in no effective bolus propulsion. There is initial evidence that psychogenic dysphagia has a neurobiological correlate. In a pilot study, Suntrup et al. compared cortical activation during swallowing in five subjects with psychogenic dysphagia and five healthy controls subjects using MEG. In this study, patients with psychogenic dysphagia displayed a significantly altered cortical activation pattern. Whereas the rostromedial sensorimotor cortex of both hemispheres was activated in the healthy subjects, in subjects with psychogenic dysphagia, prominent activation of the right insular cortex, the dorsolateral prefrontal cortex, and the lateral premotor, motor, and inferolateral parietal cortex was found. In addition, activation was significantly reduced in the left medial primary sensory cortex as well as in the right medial sensorimotor cortex and the adjacent supplementary motor area. Therefore, psychogenic dysphagia seems to be associated with distinctive changes in the swallowrelated cortical activation pattern, which may reflect exaggerated activation of a widely distributed vigilance, self-monitoring, and salience rating network that interferes with downstream deglutitive sensorimotor control (Suntrup et al. 2014). The clinical spectrum of psychogenic dysphagia includes globus pharyngis and phagophobia, whereas eating disorders such as anorexia nervosa and bulimia need to be differentiated from these entities (Barofsky and Fontaine 1998). Globus Pharyngis Globus pharyngis was formerly called globus hystericus and belongs to the group of conversion disorders. Patients report the sensation of having a lump or constriction in their throat that is typically not associated with food intake. In some cases, food intake even leads to an improvement in symptoms, and patients do not complain about pain. However, psychosocial stress often triggers or leads to a worsening of the condition; thus, the intensity of the disorder can vary widely (Deary et  al. 1995a, b). Phagophobia Phagophobia, which was described as a new entity by Shapiro et al. in 1997, is characterized by the fear of swallowing while eating. Phagophobia is associated with a pronounced fear of breathlessness and suffocation. Two-thirds of phagophobic patients are women, and their restricted eating behavior can lead to weight loss as a clinical consequence. The disease is frequently associated with panic disorders (41%) and obsessive-compulsive disorders (22%) and is therefore often misdiagnosed as an eating disorder. Affected patients seldom seek professional help (Shapiro et  al. 1997). A universal definition of phagophobia does not yet exist. In the literature, the terms “phagophobia,” “suffocation anxiety,” and “psychogenic dysphagia” in combination with “bolus sensation” or a “lump in the throat” are used to describe the same phagophobic phenomena (Baijens et al. 2013a). The fact that psychogenic dysphagia is probably much less common than “true” neurogenic dysphagia, which is misinterpreted as psychogenic, is of great clinical importance. After a detailed instrumental re-evaluation, an organic correlate was found in 65% of patients initially suspected of having a psychogenic swallowing

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disorder or a globus hystericus (Ravich et al. 1989). In addition, the study revealed that once it had been made, the diagnosis of psychogenic dysphagia was critically re-evaluated far too rarely during follow-up (Ravich et  al. 1989). Another study included 58 patients diagnosed with various forms of psychogenic dysphagia. After extensive follow-up investigations, other etiologies (achalasia, esophageal spasm, pharyngo-esophageal discoordination) could be detected and defined as the cause of the symptoms in all cases (Stacher 1986). Even in a recent study in which 32 patients with the diagnosis of psychogenic dysphagia were included, the diagnosis was confirmed in fewer than 44% of cases. Pathological changes in swallowing-­related EMG patterns were shown to be indicative of an organic correlation in supposedly nonpsychogenic patients (Vaiman et al. 2008). Therefore, even if a clear temporal relationship to psychosocial stress is obvious in suspected psychogenic dysphagia, a thorough diagnostic workup that searches for other etiologies of the patient’s symptoms is always required (Buchholz 1994). The diagnosis of psychogenic dysphagia should only be made when the clinical swallowing assessment and instrumental dysphagia diagnostics—including FEES, VFSS, and esophageal manometry—have reliably excluded disorders of the oral, pharyngeal, and esophageal phases of swallowing. FEES that is used as a kind of biofeedback is suitable in combination with behavioral swallowing therapy and psychotherapy for “disruptive” dysfunctional swallowing patterns of psychogenic dysphagia (Thottam et al. 2015). Psychogenic dysphagia represents a diagnosis by exclusion and is much less common than “true” neurogenic dysphagia when misinterpreted as psychogenic. Psychogenic dysphagia, which should be distinguished from eating disorders, clinically manifests itself primarily as globus pharyngis or phagophobia.

4.12 Others 4.12.1 Hereditary Ataxias Autosomal Dominant Ataxias Autosomal dominant spinocerebellar ataxias (SCAs) are a heterogeneous group of neurodegenerative diseases that have the common clinical feature of progressive ataxia. In addition, a variety of other neurological symptoms can occur. More than 25 genetic subtypes have now been identified, the most common form being SCA3, which is also known as Machado–Joseph disease (MJD). In Central Europe, subtypes SCA 1, 2, 3, and 6 account for about 70% of all cases (Schols et al. 2004). Neurogenic dysphagia has been described in subtypes SCA 1, 2, 3, 6, and 7 (Burk et al. 1996; Rub et al. 2006). Dysphagia occurring in these SCA subtypes may affect all phases of swallowing, and aspiration pneumonia is the leading cause of death in these patients (Rub et al. 2006). In a genotype-phenotype study, 89% of all SCA1 patients had dysphagia, whereas only 54% of SCA2 patients and 34% of SCA3

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patients showed impaired deglutition (Burk et  al. 1996). A recent VFSS study described the course of dysphagia in six patients with SCA3 (mean age: 48.0  ±  21.1  years). The mean disease duration until the onset of dysphagia was 12 ± 2.5 years. Thus, dysphagia occurred significantly later than in a control group of seven patients with cerebellar multiple system atrophy (Isono et  al. 2015). Another VFSS study revealed that dysphagia is much more pronounced in SCA3 (n = 7) than in SCA 6 (n = 13; Isono et al. 2013). A pathoanatomical study found extensive neurodegeneration of the central brainstem regions (which are known to be involved in the control of swallowing) in all dysphagic SCA patients of subtypes 2, 3, 6, and 7 (Rub et al. 2006). For patients suspected of suffering from SCA and who also have neurogenic dysphagia, mutation analyses should be performed for SCA 1, 2, 3, 6, and 7 subtypes. Autosomal Recessive Ataxias Autosomal recessive Friedreich’s ataxia (FA) is the world’s most common form of hereditary ataxias. A prevalence of 1/20,000 to 1/125,000 is assumed for several Western European countries. FA is caused in 95% of patients by a homozygous GAA repeat expansion in the frataxin gene. Usually, the clinical onset of the illness is between the ages of 5 and 25. The classic phenotype is characterized by a progressive ataxia of all four limbs and gait, impaired proprioception, loss of deep tendon reflexes, pyramidal tract signs, eye movement abnormalities, and dysarthria. Non-neurological manifestations include skeletal deformities, cardiomyopathy, and diabetes mellitus (Parkinson et al. 2013). The frequency of neurogenic dysphagia reported in the literature varies from 27 to 74%. In advanced stages, the initially mild dysphagia may lead to aspiration pneumonia, which is considered a major cause of death in FA patients (Parkinson et  al. 2013). In a recent Australian study, 36 FA patients were systematically examined for clinically relevant dysphagia, but an instrumental dysphagia assessment was not performed. Clinical signs of dysphagia were detected in 97.2% (n = 35) of the included FA patients. Both the oral and pharyngeal phases of swallowing were affected, and dysphagia was suggested to be associated with impaired coordination, weakness, and spasticity. The most commonly reported symptom was coughing/choking on liquids (58.33%). 19 patients reported using swallowing maneuvers for safety reasons. Patients reported specifically focusing on certain elements of the swallowing process as the most frequent strategy (Vogel et al. 2014).

4.12.2 Niemann–Pick Disease, Type C Autosomal recessive Niemann–Pick type C (NPC) is a rare neurovisceral lipid storage disease caused by mutations in the NPC1 gene (>95% of patients) or the NPC2 gene. As a result of the genetic defects, the intracellular transport of cholesterol,

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glycolipids, and phospholipids (sphingomyelin) is impaired, causing an accumulation of these lipids in lysosomes. NPC affects 1/150,000 people, and the clinical spectrum ranges from a fatal infantile form to an adult-onset, chronic neurodegenerative disease (adult form). For most patients, disease severity and prognosis are determined by the neurological symptoms. The mean age at the onset of neuropsychiatric symptoms is 25. The following symptoms occur in decreasing order of frequency: cerebellar ataxia, supranuclear vertical gaze palsy, dysarthria, cognitive disorders, movement disorders, splenomegaly, psychosis, dysphagia, epilepsy, and cataplexy. The drug miglustat (Zavesca®) was approved in January 2009 for the treatment of neurological symptoms. Miglustat is a glucosylceramide synthase inhibitor and thus leads to a substrate reduction (reduced production of glycolipids; Sevin et al. 2007; Vanier 2010; Mengel et al. 2013). According to the available data, the frequency of severe neurogenic dysphagia is at least 37% in NPC patients (Sevin et al. 2007), and aspiration pneumonia is considered the leading cause of death (Walterfang et al. 2012). In an observational study, swallowing function in four pediatric NPC patients from 1–12  years of age was studied with VFSS prior to beginning of miglustat therapy and was evaluated over 3–4 years. Initially, two patients had severe oropharyngeal dysphagia with aspiration, and one patient had mild oropharyngeal dysphagia without aspiration. After 6 months of drug treatment, a significant improvement in swallowing, and particularly a normalization of the pharyngeal phase, was found in both NPC patients with initially severe dysphagia. Aspiration was no longer detected, and only a slight dysfunction of the oral phase remained. Even at a followup of 36 months, no further worsening of swallowing function was observed, but the oral dysfunction persisted. In the NPC patient with initially mild dysphagia, swallowing function initially worsened after miglustat therapy over 6–9  months, and even aspiration occurred, which necessitated PEG feeding. After 14 months, a complete normalization of swallowing function was demonstrated. Even after 48 months, no swallowing disorder had reoccurred, and the PEG tube could thus be removed. In the NPC patient without dysphagia, no impairment of swallowing was detected under miglustat therapy, even at a follow-up of over 40  months (Fecarotta et  al. 2011). The effect of miglustat on swallowing function in NPC patients was evaluated in a systematic review. The limited data available on clinical and videofluoroscopic swallowing function in the course of the drug treatment suggest that swallowing function stabilizes or improves, leading to a prolonged life expectancy (Walterfang et al. 2012). In line with this finding, a small randomized controlled study (n = 25) showed a stabilization or improvement in the ability to swallow four different food consistencies (water, puree, noodles, cookies) in most NPC patients after 24 months. These findings persisted for all consistencies except for water in 40–50% of patients, even after 48–96 months (Fecarotta et al. 2015).

4.12.3 Chiari Type I Malformation Chiari malformation is an early embryonic malformation of the craniocervical junction that occurs in about 1/25,000 births. Downward displacement of the cerebellum

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into the upper cervical canal may result in aqueduct stenosis with concomitant hydrocephalus, brainstem compression, and cranial neuropathies. Type I often becomes symptomatic only in adulthood between the ages of 40 and 50 and may be associated with syringomyelia. Accompanying symptoms include caudal cranial neuropathy, torticollis, neck pain and headache, dizziness, and downbeat nystagmus. Therapy consists of a suboccipital decompression and/or the implantation of a ventriculo-peritoneal shunt. Bulbar dysphagia may also be the only or the predominant symptom in Chiari type I malformation. Such a clinical manifestation of Chiari type I has been misdiagnosed in several case reports as bulbar amyotrophic lateral sclerosis (Gamez et al. 2003). In one case, bulbar dysphagia was accompanied by rapidly progressive bilateral tongue atrophy (Paulig and Prosiegel 2002). A recent case also described fluctuating dysphagia that was dependent on body position. In a 38-year-­old female patient suffering from this malformation, severe pharyngeal dysphagia with aspiration was shown in FEES with the patient in an upright sitting position, while swallowing without aspiration occurred in the supine position. After decompression surgery, swallowing normalized completely (White et al. 2010). Chiari type 1 malformation can lead to bulbar dysphagia, the severity of which may vary with changing body positions: It increases in the upright position and improves in the supine position. Any bulbar dysphagia requires an MRI of the head to exclude Chiari type 1 malformation as a rare differential diagnosis.

4.12.4 Palatal Myoclonus (Palatal Tremor) Palatal myoclonus is characterized by unilateral or bilateral, mostly rhythmic myoclonus of the soft palate with a frequency of 1–3 Hz. In addition, myoclonus of the pharyngeal posterior wall and larynx can also occur (pharyngolaryngeal myoclonus). A distinction can be made between essential palatal myoclonus (involving the levator veli palatini and typically accompanied by a clicking noise in the ear) and symptomatic palatal myoclonus (in which the M. levator veli palatini is affected), which is caused by lesions in the so-called Guillain–Mollaret triangle (the functional connections of the following grey matter areas in the brainstem and cerebellum: the nucleus ruber, the inferior olivary nucleus, and the dentate nucleus), especially in brainstem- and cerebellar infarctions (Deuschl et al. 1990, 1994a, b). Palatal myoclonus may be associated with dysphagia (especially with liquids), which often cannot be reliably clinically diagnosed. Endoscopically and/or videofluoroscopically, premature spillage of liquids with pre- and intra-deglutitive penetration and/or aspiration has been demonstrated in such cases (Drysdale et al. 1993; van de Loo et al. 2010; Juby et al. 2014). Myoclonus of the soft palate may interfere with oral bolus control. Pharyngolaryngeal myoclonus can also prevent timely closure of the laryngeal vestibule (van de Loo et al. 2010).

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Palatal myoclonus can be associated with neurogenic dysphagia featuring premature spillage of liquids and consecutive pre- and intra-deglutitive aspiration. In addition, if pharyngolaryngeal myoclonus persists, timely closure of the laryngeal vestibule may also be disturbed, thereby further increasing the risk of aspiration.

4.12.5 Diffuse Idiopathic Skeletal Hyperostosis Diffuse idiopathic skeletal hyperostosis (DISH) is a noninflammatory disorder characterized by the calcification and ossification of spinal ligaments and entheses. Men are affected more frequently than women. DISH typically manifests in the fifth or sixth decade of life, and risk factors include obesity, diabetes mellitus, and arterial hypertension. Its predominant location is the anterior longitudinal ligament of the spine. Hyperostosis on the anterior surface of the vertebral body causes ventral cervical spondylophytes and can result in severe dysphagia; however, the vast majority of patients with ventral cervical spondylophytes do not feel any impairment of deglutition. About 20–30% of all elderly people show such changes of the cervical spine without suffering from dysphagia. It is therefore of great clinical importance that other causes of dysphagia be excluded prior to diagnosing a swallowing disorder due to cervical spondylophytes. However, in some patients, this hyperostosis of the anterior vertebral surface causes mechanical constriction of the hypopharynx and upper esophagus, neuropathy due to injury to the recurrent laryngeal nerve, and chronic inflammation and fibrosis of the pharyngo-esophageal musculature (Goh et al. 2010; Papadopoulou et al. 2013). In order to adequately assess the impact of spondylophytes on swallowing physiology, FEES, VFSS, and esophageal manometry should be performed in respective patients (Figs.  4.9 and 4.10). In case of severe dysphagia with critically impaired oral intake and consecutive weight loss, cervical spine surgery with resection of the spondylophytes may improve patients’ swallowing function (Ozgursoy et al. 2010). Dysphagia caused by ventral cervical spondylophytes is a differential diagnosis of neurogenic dysphagia; however, the majority of radiologically detectable ventral cervical spondylophytes do not result in clinically relevant dysphagia.

Cervical scoliosis and other deformities of the cervical spine can also lead to dysphagia (Papadopoulou et al. 2013).

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4  Special Findings in Neurogenic Dysphagia

Fig. 4.9 Radiographic image of a ventral cervical spondylophyte. Image courtesy of the Department of Radiology at Münster University Hospital (Director: Prof. Dr. W. Heindel). Reproduced with permission

Fig. 4.10 Endoscopic evidence of hypopharyngeal narrowing by a ventral cervical spondylophyte

G

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4.12.6 Surgery Different surgical procedures can result in neurogenic dysphagia as a complication. Endarterectomy of the Carotid Artery According to current guidelines, carotid endarterectomy (CEA) is the treatment of choice for high-grade symptomatic stenosis of the internal carotid artery. Because the vagus nerve is in close anatomical proximity to the internal carotid artery, it may be damaged during this surgical procedure, resulting in ipsilateral vocal fold- and/ or ipsilateral pharyngeal palsies with neurogenic dysphagia. The combination of vocal fold paresis and pharyngeal dysphagia is also referred to as “double trouble.” Oral dysphagia can occur if damage to the hypoglossal nerve with concomitant ipsilateral tongue paresis occurs as a side effect of surgery. A lesion on the hypoglossal nerve is the most common form of cranial nerve damage due to CEA. In addition, surgical lesions of cranial nerves V, VII, and IX have been described. Cranial nerve palsy occurs in approximately 5.5% of patients post CEA (Greenstein et al. 2007). Endoscopic Findings Masiero et al. (2007) prospectively examined 19 patients suffering from dysphagia after CEA both 5 days and 3 months post-surgery (13 men, six women; mean age: 71.7 years). While 15 patients had dysphagia with liquids and solid food, four patients had problems only with solid consistencies. Eight patients required parenteral nutrition. Aspiration was detected in the first FEES in six patients, and rehabilitation began after 6 days on average. In ten patients, swallowing function fully normalized within 1 month, and three additional patients fully recovered from dysphagia within 3 months. Only one patient displayed aspiration in the second FEES (after 3 months). Cervical Spine Surgery via an Anterior Approach Cervical spine surgery via an anterior approach can lead to neurogenic dysphagia, and all phases of the swallowing cycle can potentially be disturbed (Sect. 4.10.2). The cause of dysphagia may be an affection of the hypoglossal and/or the vagal nerve. Access above C6 is more likely to cause impairment of the hypoglossal and the superior laryngeal nerve, whereas access at C6 and below more frequently leads to recurrent laryngeal nerve lesions (Martin et al. 1997). Postoperative laryngeal neuropathies, which can be detected by laryngeal electromyography, are associated with more severe dysphagia (Ryu et al. 2012). In a prospective observational study, the prevalence of neurogenic dysphagia was 54.0% 1 month after surgery and 13.6% at 24 months after surgery (Lee et al. 2007). Other case studies have described a prevalence of dysphagia of just above 50% in post-­cervical spine surgery in addition to comparable improvement rates over the course of 1  year (Papadopoulou et al. 2013). Pain during swallowing (odynophagia) post-­surgery is usually caused by local swelling and/or a hematoma in the prevertebral space. Swallowing disorders may also occur as late as weeks or months after surgery via

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4  Special Findings in Neurogenic Dysphagia

an anterior approach, or they may reoccur again after an initial improvement (Vanderveldt and Young 2003). Dysphagia in post-cervical spine surgery is associated with longer hospitalizations and higher healthcare costs (Singh et al. 2013; Starmer et al. 2014). Cardiac Surgery Dysphagia is a potential complication after open-heart surgery. In a FEESST study by Aviv et  al. (2005) on 1340 consecutive patients with congestive heart failure, open-heart surgery was the leading cause of dysphagia in 26.9% of cases. In addition to peri-operative stroke and the resulting dysphagia, intra-operative transesophageal echocardiography and an age >65 have been identified as additional risk factors for postoperative dysphagia in patients without a cerebrovascular event (Rousou et al. 2000). Furthermore, FEESST has demonstrated moderate to severe pharyngolaryngeal hypesthesia in nearly 90% of patients with postoperative dysphagia but without a peri-operative stroke (Aviv et al. 2005). This observation has been interpreted as an indication that unrecognized and hence insufficiently treated reflux disease may have caused this sensory disruption detected by FEESST and may even have been the main cause of dysphagia after open-heart surgery (Aviv et al. 2000, 2005). Hypoglossal Nerve Palsy Following Intubation Hypoglossal nerve palsy with consecutive tongue dysmotility and oral dysphagia is described as a rare complication after orotracheal intubation as well as after a bronchoscopy and the use of a laryngeal mask (Dziewas and Lüdemann 2002). In the majority of cases, a rapid improvement of symptoms is observed, but deficits persist beyond 4 months in about 20% of cases. Hypoglossal palsy is associated with ipsilateral damage to the lingual nerve in one-quarter of affected patients. This coincidence suggests that direct compression of the nerves at the lateral margin of the tongue is the most likely pathomechanism. In light of the generally good prognosis (with spontaneous recovery occurring in most cases), surgical revision of the nerve is generally not indicated.

4.12.7 IgLON5 Syndrome In 2014, a new neuroimmunological syndrome was described that is characterized by sleeping disorders (non-REM parasomnia and REM parasomnia, sleep-related breathing disorders), dysarthria, dysphagia, ataxia, and chorea and is associated with IgLON5 antibodies. Neuropathologically, tau deposits were found in the brainstem and the hypothalamus (Sabater et al. 2014). In the authors’ clinic, a patient with antiIgLON5 syndrome was treated and became symptomatic with a slowly progressive neurogenic dysphagia. FEES revealed severe oropharyngeal dysphagia with impaired oral bolus control, premature spillage, a critically delayed swallow reflex, residue in the valleculae and piriform sinus, as well as pre- and post-­deglutitive penetration and

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aspiration. VFSS and high-resolution manometry (HRM) also revealed an upper esophageal sphincter dysfunction and esophageal dysmotility. During further inpatient care, progressive dysfunction of multiple cranial nerves developed (including bilateral vocal fold paresis), whereupon intubation and tracheostomy were necessary (Schröder et al. 2016).

4.12.8 Internal Diseases In recent years, methods of instrumental dysphagia diagnostics have become increasingly used for primarily internal diseases. As a result, chronic respiratory diseases (especially chronic obstructive pulmonary disease (COPD) and obstructive sleep apnea syndrome (OSAS)) have been demonstrated to be associated with an increased prevalence of oropharyngeal dysphagia (Ghannouchi et  al. 2016). In COPD, a FEES study revealed that dysphagia was characterized by decreased pharyngolaryngeal sensitivity and residue in the valleculae and piriform sinus. Aspiration was found in 25% of the studied COPD patients (n = 20), and the self-­ perception of swallowing impairment was reduced in them (Clayton et al. 2014). In another FEES study, Schindler et al. (2014) investigated swallowing function in 72 OSAS patients without subjective dysphagia. About half of all patients showed signs of subclinical dysphagia. The most frequent FEES findings were premature spillage (64%), residue (44%), penetration (36%), and fragmented swallowing (28%). There were no differences between patients with moderate and severe OSAS. An impaired sensory function of the mucosa of the upper airway (including the oropharynx) is assumed to be the key driver of dysphagia in this condition. This sensory impairment is thought to be caused by the low-frequency vibration of snoring subsequently leading to a disruption of the neuronal regulation of microcirculation in the mucosa. According to the results of this study, the symptom subscale of the SWAL-­QOL is suitable for detecting subclinical dysphagia in OSAS patients (Schindler et al. 2014). In another FEES study, swallowing function in patients with Sjögren syndrome (n = 69) was compared with that of healthy control subjects (n = 40). Patients with Sjögren syndrome showed significantly more frequently thickened liquid and solid residue in different parts of the hypopharynx than healthy controls. Relevant penetration/aspiration was not found in the Sjögren patients (Eyigör et al. 2017). Oropharyngeal and esophageal dysphagia are also common in other autoimmune rheumatic diseases (systemic lupus erythematosus, rheumatoid arthritis, scleroderma, etc.; Amos et al. 2016). 70% of all scleroderma patients suffer from esophageal symptoms resulting from smooth muscle atrophy and muscle fibrosis in the distal two-thirds of the esophagus (Amos et al. 2016). Because the patterns of dysphagia in these conditions may be similar to those of primary neurogenic diseases, it is critically important to also systematically evaluate the patient’s history for the presence of these internal diseases and to also consider them when evaluating findings of instrumental dysphagia diagnostics.

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4.13 A  lgorithm for a Structured Assessment of Patients with Neurogenic Dysphagia In order to introduce adequate protective and rehabilitative measures in patients with neurogenic dysphagia (Chap. 7), it is essential to correctly diagnose the underlying neurological disease. In addition, the individual patients’ prognosis can only be assessed and communicated with the patients and relatives once the etiology of the neurogenic dysphagia has been clarified. If neurogenic dysphagia occurs together with other neurological symptoms, the underlying etiology can often be clarified on the basis of the additional symptoms and its generally characteristic combination. Due to the growing knowledge about dysphagia over the past 25 years (Chap. 3), however, the specific pattern of neurogenic dysphagia can also contribute significantly to determining the diagnosis. A typical example is the sudden onset of dysphagia in Wallenberg’s syndrome, which may present variably with ipsilateral paresis of cranial nerves V, IX, and X, ipsilateral Horner’s syndrome, ipsilateral hemiataxia, and contralateral dissociated sensory loss. In addition, a characteristic pattern of swallowing impairment that almost never occurs in other stroke localizations is the impaired opening of the upper esophageal sphincter with (mostly) prominent salivary and bolus residues in the piriform sinus (Sect. 4.1). Table 4.5 provides an overview of the differential diagnoses of neurogenic dysphagia that takes additional neurological symptoms into account. The pattern of dysphagia observed in the different diseases can be found in the corresponding chapter of this book. Table 4.5  Differential diagnosis of neurogenic dysphagia guided by additional neurological symptoms. Additional neurological symptoms Differential diagnoses Acute CNS symptoms Cerebral infarctions/bleeding Relapse of multiple sclerosis Slowly progressive CNS Brain tumors symptoms Chronic progressive multiple sclerosis Brainstem symptoms Brainstem infarctions/bleeding Multiple sclerosis Listeria rhombencephalitis Paraneoplastic brainstem encephalitis Neurocognitive disorders Alzheimer’s disease Vascular dementia Frontotemporal lobar degenerations Lewy body dementia Progressive supranuclear palsy Extrapyramidal motor symptoms Parkinson’s disease Huntington’s disease Dystonias Neuroleptic-induced dysphagia Wilson’s disease

Chapter section Sect. 4.1 Sect. 4.4.1 Sect. 4.5.1 Sect. 4.4.1 Sect. 4.1 Sect. 4.4.1 Sect. 4.4.2 Sect. 4.5.3 Sect. 4.2.1 Sect. 4.2.2 Sect. 4.2.3 Sect. 4.2.4 Sect. 4.3.1 Sect. 4.3.1 Sect. 4.3.2 Sect. 4.3.3 Sect. 4.3.3 Sect. 4.3.4

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197

Table 4.5 (continued) Additional neurological symptoms Differential diagnoses Progressive bulbar paralysis Amyotrophic lateral sclerosis Pseudobulbar paralysis Primary lateral sclerosis Arnold–Chiari malformation, type I Kennedy’s disease Post-polio syndrome IgLON5 bulbar paralysis Cerebellar symptoms Multiple sclerosis Hereditary ataxias Niemann–Pick disease, type C Subacute cerebellar degeneration Cranial nerve palsies Skull base tumors Meningeosis neoplastica Basal meningitis Special forms of Guillain–Barré syndrome Ptosis and/or ocular symptoms Special forms of Guillain–Barré syndrome Myasthenia gravis Lambert–Eaton myasthenic syndrome Botulism Oculopharyngeal muscular dystrophy Mitochondrial myopathies Oculopharyngodistal myopathy Neuropathy Guillain–Barré syndrome Critical illness neuropathy Myopathy Myositis Myotonic dystrophies Duchenne muscular dystrophy Oculopharyngeal muscular dystrophy Mitochondrial myopathies Facioscapulohumeral muscular dystrophy Oculopharyngodistal myopathy Myotonic syndrome Myotonic dystrophies Trismus and/or risus sardonicus Tetanus

Chapter section Sect. 4.6.1 Sect. 4.12.3 Sect. 4.6 Sect. 4.4.4 Sect. 4.6.3 Sect. 4.4.4 Sect. 4.12.7 Sect. 4.4.1. Sect. 4.12.1 Sect. 4.12.2 Sect. 4.5.3 Sect. 4.5.1 Sect. 4.4.2 Sect. 4.5.2 Sect. 4.7.1 Sect. 4.7.1 Sect. 4.8.1 Sect. 4.8.2 Sect. 4.8.3 Sect. 4.9.2 Sect. 4.9.4 Sect. 4.9.3 Sect. 4.7.1 Sect. 4.7.2 Sect. 4.9.1 Sect. 4.9.6 Sect. 4.9 Sect. 4.9.2 Sect. 4.9.4 Sect. 4.9.5 Sect. 4.9.3 Sect. 4.9.6 Sect. 4.4.5

However, when dysphagia is the sole or predominant symptom of a neurological disease, the differential diagnosis is often more difficult, and the risk of making an incorrect diagnosis is particularly high. In such cases, esophageal diseases or psychogenic dysphagia are frequently suspected and represent common misdiagnoses. David W. Bucholz referred to this fact in his 1994 review “Neurogenic Dysphagia: What Is the Cause When the Cause Is Not Obvious?” About 5% of all neurological patients in an emergency room present with a leading symptom from the group of speech and swallowing disorders as summarized by Royl and co-workers (Royl et al. 2010). In the following paragraphs, a step-by-step diagnostic procedure that has proven effective in the authors’ clinical work is presented for difficult, non-obvious cases in

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which dysphagia is the main symptom (see also Fig. 4.11). The aim of the first three steps of this structured procedure is to assign the form of neurogenic dysphagia to a neurological syndrome so that a definite diagnosis can be made via a targeted selection of additional diagnostics in the fourth step. If it is not possible to make a definitive diagnosis during an initial diagnostic “workup,” reevaluations should be carried out at regular intervals and if symptoms progress or when additional neurological symptoms appear. This approach also pays tribute to the fact that—analogously to other neurological symptoms—a diagnosis is sometimes only possible during a follow-up examination. Merely diagnosing dysphagia without performing adequate research on its etiology is entirely inadequate; nevertheless, according to the authors’ experience, such a symptom-centered approach is still quite common in daily practice and is clearly more common than with other key symptoms of neurological disorders, such as dysarthria or aphasia. 1st Step: Taking Medical History Medical history is as important for neurogenic dysphagia as it is for all other neurological symptoms. Data from the patient’s history (current complaints, pre-existing conditions, and family, social, and drug history) may be crucial for making the diagnosis. It is also important to include dysphagia-specific questions in the interview (Sect. 2.2). In addition, attempts should be made to characterize dysphagia based on certain criteria:

Complaints and/or clinical symptoms of dysphagia

Initial diagnostic work-up: • Detailed history • Neurological examination • FEES following standard protocol Diagnosis of neurogenic dysphagia suspected

Advanced diagnostic workup I: • MRI of the brain • Cerebrospinal fluid analysis • FEES-Tensilon-Test No specific findings allowing to determine the etiology of dysphagia

Advanced diagnostic workup II: • VFSS • HRM • Neurophysiological examination • Whole-Body-Muscle-MRI • MRI of the cervical spine • Antibody-testing • Muscle biopsy

Fig. 4.11  Step-wise diagnostic workup to target neurogenic dysphgia of undetermined etiology

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199

• temporal dynamics of symptom development: acute—subacute—chronicprogressive—chronic-relapsing • subjectively perceived localization of the swallowing disorder: oral—pharyngeal—esophageal (patient should point to the “problematic” area!) • variability of symptoms related to specific conditions: physical stress, psychological stress, time of day • family history of dysphagia 2nd Step: Clinical-Neurological Examination The clinical-neurological examination should search for (subtle) additional symptoms that may indicate a specific neurological disease. With regard to neurogenic dysphagia, a particularly detailed examination of cranial nerves V3, VII, IX, X, and XII—which are relevant to swallowing—is required. In addition, aspiration screening is part of the clinical neurological examination (Sect. 2.3). 3rd Step: Instrumental Dysphagia Diagnostics Instrumental dysphagia diagnostics allow for directly and objectively visualizing the suspected swallowing impairment and to identify the pattern of dysphagia, which in turn often provides further clues to clarifying the underlying etiology. Because of its availability and its diagnostic value, in the authors’ clinic, FEES is generally performed first and is conducted in a team comprising an attending physician and an speech and language pathologist (SLP). Based on the respective findings, further instrumental diagnostics (VFSS, high-resolution manometry, etc.) are then considered. Instrumental dysphagia diagnostics also need to consider non-neurogenic dysphagia and its causes. Upon completion of the instrumental dysphagia evaluation, the swallowing impairment should be assigned to a neurological syndrome, and a tentative diagnosis should be made (Sect. 3.1.6). 4th Step: Additional Diagnostics Depending on the results of the previous three steps, specifically selected additional examinations should be carried out and help to establish a definitive diagnosis. The following additional examinations may be useful either individually or in combination: laboratory tests, a brain MRI, lumbar puncture, electromyography, electroneurography, sensory- and motor-evoked potentials, an MRI of the cervical spine, a whole-body muscle MRI, or a muscle biopsy. Table 4.6 lists neurological disorders that may lead to isolated neurogenic dysphagia and provides information regarding corresponding additional diagnostics. In some cases, when rapid management is required because the first three steps do not yield the desired information or due to the acute onset of dysphagia, the following diagnostics should be carried out quickly to identify relevant neurological disorders that require acute care: (1) a brain MRI including a DWI sequence and high-resolution imaging of the brainstem if acute stroke is suspected; (2) a lumbar puncture if brainstem encephalitis is considered, a special form of Guillain–Barré syndrome, or meningitis neoplastica come into consideration; and (3) a FEES Tensilon® test if a myasthenic syndrome is thought to be possible.

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Table 4.6  Neurological diseases featuring dysphagia as possible main symptom, and important additional diagnostics Neurological disease Brainstem infarction Listeria brainstem encephalitis Paraneoplastic brainstem encephalitis Brainstem tumor Meningeosis neoplastica Basal meningitis Special forms of Guillain– Barré syndrome Post-polio syndrome Pseudobulbar paralysis Bulbar-onset amyotrophic lateral sclerosis Presbyphagia Skull base tumors Arnold–Chiari malformation, type I Neuroleptic-induced dysphagia Polymyositis Inclusion body myositis Myasthenia gravis Lambert–Eaton myasthenic syndrome Botulism Tetanus Oculopharyngeal muscular dystrophy Myotonic dystrophy, type I Operations Psychogenic dysphagia

Critical additional diagnostics Brain MRI incl. DWI sequence Brain MRI, lumbar puncture Brain MRI, anti-neuronal antibodies (Hu, Ta, Ma, Ri), CV2/ anti-CRMP5, anti-amphiphysin, ANNA-3 Brain MRI, lumbar puncture with cytopathological examination, brain biopsy Brain MRI, lumbar puncture with cytopathological examination Lumbar puncture Lumbar puncture, ganglioside antibodies (GD1a, GM1b, GW1b, GT1a) Electromyography Brain MRI Electroneurography and electromyography Exclusion diagnostics Brain MRI Brain MRI Medication history, exclusion diagnostics of other extrapyramidal motor diseases (if necessary) Serum creatinine kinase, electromyography, muscle biopsy Electromyography, muscle biopsy EMG with low-frequency repetitive stimulation (3 Hz), Tensilon® test, anti-AChR, anti-MuSK, Thorax CT EMG with high-frequency repetitive stimulation (10–50 Hz), antibodies against voltage-gated calcium channels History, toxin detection in body liquids History, EMG, toxin detection in body liquids Family history, genetics (PABPN1 gene) Family history, EMG (myotonic discharges), genetics (CTG expansion in myotonin-protein kinase gene) History Exclusion diagnostics, psychiatric and psychosomatic evaluation

Figure 4.12 summarizes a structured algorithm for the diagnosis of neurogenic dysphagia that is suitable for neurological acute care clinics. In this algorithm, FEES represents the key instrumental examination method. The diagnostic procedure differs depending on whether or not a neurological disease has already been diagnosed. 1. In the context of a known neurological disease, the presence of disease-specific risk factors (predictors) for dysphagia is first evaluated. For example, in the case

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Patient with known neurological disorder?

Yes

No - Typical symptoms present? - Neurological exam: additional symptoms present?

- Disease-specific risk factors: positive? - Disease-specific tests/questionaires: positive?

Yes

No

FEES - Flexible endoscopic evaluation of swallowing: pathological?

Yes

Targeted diagnostic: positive?

Yes

Yes

Yes

FEES: Dysphagia pattern compatible with specific neurogenic dysphagia?

FEES: Dysphagia pattern compatible with specific neurological disorder?

Unspecific diagnostics: positive?

Yes Specific treatment

No

No Indication of neurogenic dysphagia

Yes

Specific treatment

No

No

Yes

No

No

No - Reevalution: VFSS, Manometrie - Comorbidities? - Non-neurological etiologies?

Fig. 4.12  Structured algorithm for diagnosis of neurogenic dysphagia

of an acute stroke, a lesion of the dorsolateral medulla oblongata or a high initial score on the NIH-SS (>10) is often associated with severe dysphagia (Sect. 4.1). In addition, disease-specific tests or questionnaires can be used, such as a water test for aspiration screening in acute stroke or specific swallowing-disorder ­questionnaires in patients suffering from Parkinson’s disease (Sect. 4.3.1). If these diagnostic steps indicate the presence of dysphagia, FEES is performed to gather a detailed analysis of the disorder, and the further procedure is determined based on the respective findings. 2. If no neurological disease is known so far, the further diagnostic workup is guided by the presence of additional neurological symptoms or clinical key features in the patient’s history that enable a specific diagnosis. For example, if the patient presents with exercise-related fatigue of the swallowing muscles, a ­diagnosis of myasthenia gravis comes into consideration (Sect. 4.8.1). If cranial nerve palsy is found in the clinical examination, a diagnosis of polyneuritis (Sect. 4.7) or basal meningitis (Sect. 4.4) should be taken into account. Once the diagnosis has been confirmed, FEES may also be required in order to initiate targeted behavioral and/or drug/surgical therapies. If no specific additional symptoms are found, FEES should be used to analyze the pattern of swallowing impairment and to initiate appropriate diagnostic procedures to help clarify the

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underlying etiology of the dysphagia. For example, bilateral flaccid pharyngeal paresis with a hypertonic upper esophageal sphincter is indicative of myositis (Sect. 4.9.1). In the case of a non-specific pattern, untargeted diagnostics should be used and should always include a brain MRI with high-­resolution imaging of the brainstem, a lumbar puncture, and a FEES Tensilon® test. The additional instrumental diagnostics should include neurophysiological examinations (electromyography and electroneurography) and possibly also a whole-body muscle MRI.

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Tsao GJ, Tsang MW, Mobley BC, et al. Foramen magnum meningioma: dysphagia of atypical etiology. J Gen Intern Med. 2008;23:206–9. Tung JD, Oh SR, Gruber AB, et  al. The man who could not see what he could not eat. Surv Ophthalmol. 2011;56(5):461–5. Turley R, Cohen S. Impact of voice and swallowing problems in the elderly. Otolaryngol Head Neck Surg. 2009;140:33–6. Uldry PA, Kuntzer T, Bogousslavsky J, et al. Early symptoms and outcome of Listeria monocytogenes rhombencephalitis: 14 adult cases. J Neurol. 1993;240:235–42. Vaiman M, Shoval G, Gavriel H. The electrodiagnostic examination of psychogenic swallowing disorders. Eur Arch Otorhinolaryngol. 2008;265:663–8. van de Loo S, Somasundaram S, Wagner M, et al. Dysphagia in symptomatic palatal tremor. Mov Disord. 2010;25:1304–5. van Hooren MR, Baijens LW, Vos R, et al. Voice- and swallow-related quality of life in idiopathic Parkinson’s disease. Laryngoscope. 2016;126(2):408–14. Vanderveldt HS, Young MF. The evaluation of dysphagia after anterior cervical spine surgery: a case report. Dysphagia. 2003;18:301–4. Vanier MT. Niemann-Pick disease type C. Orphanet J Rare Dis. 2010;5:16. Verma A, Bradley WG, Adesina AM, et al. Inclusion body myositis with cricopharyngeus muscle involvement and severe dysphagia. Muscle Nerve. 1991;14:470–3. Vernet M.  Syndrome du trou dechire posterieur (paralysie des IX, X, XI). Rev Neurol (Paris). 1918;34:117–48. Vigderman AM, Chavin JM, Kososky C, et al. Aphagia due to pharyngeal constrictor paresis from acute lateral medullary infarction. J Neurol Sci. 1998;155:208–10. Vigliani MC, Novero D, Cerrato P, et  al. Double step paraneoplastic brainstem encephalitis: a clinicopathological study. J Neurol Neurosurg Psychiatry. 2009;80:693–5. Vogel AP, Brown SE, Folker JE, Corben LA, Delatycki MB. Dysphagia and swallowing-related quality of life in Friedreich ataxia. J Neurol. 2014;261(2):392–9. Wada A, Kawakami M, Liu M, et al. Development of a new scale for dysphagia in patients with progressive neuromuscular diseases: the Neuromuscular Disease Swallowing Status Scale (NdSSS). J Neurol. 2015;262(10):2225–31. Waespe W, Niesper J, Imhof HG, et al. Lower cranial nerve palsies due to internal carotid dissection. Stroke. 1988;19:1561–4. Wallesch C, Unterberg A, Dietz V. Neurotraumatologie. Stuttgart: Thieme; 2005. Walsh R, Hill F, Breslin N, et al. Progressive dysphagia in limb-girdle muscular dystrophy type 2B. Muscle Nerve. 2011;43:761–4. Walterfang M, Chien YH, Imrie J, Rushton D, Schubiger D, Patterson MC. Dysphagia as a risk factor for mortality in Niemann-Pick disease type C: systematic literature review and evidence from studies with miglustat. Orphanet J Rare Dis. 2012;7:76. Wang Y, Zhang L, Zhang B, et  al. Comparative clinical characteristics of neuromyelitis optica spectrum disorders with and without medulla oblongata lesions. J Neurol. 2014;261(5): 954–62. Warnecke T, Teismann I, Meimann W, et  al. Assessment of aspiration risk in acute ischaemic stroke – evaluation of the simple swallowing provocation test. J Neurol Neurosurg Psychiatry. 2008a;79:312–4. Warnecke T, Teismann I, Zimmermann J, et al. Fiberoptic endoscopic evaluation of swallowing with simultaneous tensilon application in diagnosis and therapy of myasthenia gravis. J Neurol. 2008b;255:224–30. Warnecke T, Oelenberg S, Teismann I, et al. Dysphagia in X-linked bulbospinal muscular atrophy (Kennedy disease). Neuromuscul Disord. 2009a;19:704–8. Warnecke T, Ringelstein EB, Dziewas R.  Neurologische endoskopische Dysphagiediagnostik  – Untersuchungstechnik, Einsatzmöglichkeiten und typische Befunde. Klin Neurophysiol. 2009b;40:194–203. Warnecke T, Ritter MA, Kroger B, et al. Fiberoptic endoscopic Dysphagia severity scale predicts outcome after acute stroke. Cerebrovasc Dis. 2009c;28:283–9.

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5

Using FEES in the Treatment and Management of Neurogenic Dysphagia: General Principles and Methodologies

Contents 5.1  I ntroduction 5.2  F  EES as a Therapeutic Examination (in Comparison to VFSS) 5.2.1  Use of Behavioral Strategies During the Examination 5.2.2  Selecting the Appropriate Therapeutic Strategy 5.2.3  The Weak or Ineffective Swallow with Reduced Bolus Clearance 5.2.4  The Misdirected Swallow: Impaired Airway Protection Due to Incomplete Valving 5.2.5  The Delayed or Mistimed Swallow 5.2.6  Ice Chip Protocol 5.2.7  FEES as an Educational Tool to Increase Patient Compliance 5.2.8  FEES as Biofeedback Tool in Therapy 5.2.9  FEES as a Tool to Reevaluate Patients (Serial FEES) References

5.1

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Introduction

Conventional laryngoscopy is strictly a diagnostic procedure to establish a medical diagnosis. FEES has been described by Susan Langmore as a procedure using flexible laryngoscopy to evaluate and manage patients with oropharyngeal dysphagia. The topic of this chapter is the general use of FEES as a therapeutic examination in patients with neurogenic dysphagia and to compare it with the videofluoroscopic swallowing study (VFSS). When used for this purpose, usually by speech and language pathologists (SLPs) or by SLPs and neurologists working together as a team, endoscopy is applied as a tool to identify the presence and severity of dysphagia, to uncover the nature of the problem, and, finally, to guide dietary and behavioral treatment of the patient. FEES can also be used to guide surgical and medical treatment. This will be further addressed in Chap. 7 of this book. There are several ways how FEES can be used for guiding treatment: First, during the procedure, the examiner will trial dietary and behavioral interventions to © Springer Nature Switzerland AG 2021 T. Warnecke et al., Neurogenic Dysphagia, https://doi.org/10.1007/978-3-030-42140-3_5

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determine which interventions help the patient with neurogenic dysphagia to swallow more safely or more effectively. Second, during and after FEES examination, the recorded video is used to educate the patient, caregivers, and other involved staff about the specific problem. Recommendations and decisions about treatment often are made during the examination by consensus of the several people who are involved in the examination as well as the patient and family. During this initial procedure or in subsequent procedures, endoscopy may be used as a biofeedback tool to help the patient learn various behavioral strategies. After a period of treatment changes for other reasons, a repeat FEES examination can be done to reevaluate the dysphagia and further guide dietary and behavioral interventions. Treatment, management, and therapy are terms that sometimes are used interchangeably. In this chapter, treatment and management are used synonymously, but therapy is reserved for the day-to-day, hands-on sessions that are spent by a professional with a patient working on some behavioral strategy or exercise. Every patient needs to be managed, usually by a multidisciplinary group of professionals; however, every neurological patient cannot accept, cooperate with, or benefit from direct therapy. Management of patients with dysphagia encompasses direct therapy provided to patients, but it also includes education and training of other health care providers or family members to carry out a safe feeding and oral-care program. It includes dietary management and collaborative interdisciplinary efforts to prevent the medical complications of neurogenic dysphagia, including aspiration pneumonia, malnutrition (see Chap. 8), and dehydration. FEES is used to guide many aspects of patient management, including dietary decisions, feeding recommendations, management of secretions, and education of the patient, caretaker, and staff. In a recent multicenter registry study including 2401 patients with neurogenic dysphagia the use of FEES led to changes of treatment strategy in more than 50% of cases (Dziewas et al. 2019). Management of the neurological patient takes many factors into account besides the results of the swallowing examination. The patient’s mental status, medical condition, medical and swallowing prognosis, functional status, motivation and desire for therapy, availability for therapy, and many other factors also are considered in determining the best overall management plan. Therefore, the therapeutic interventions listed here as being indicated for specific swallowing deficits may not be appropriate for a given neurological patient. Clinical judgment and experience will be the ultimate guide.

5.2

 EES as a Therapeutic Examination (in Comparison F to VFSS)

FEES is a comprehensive examination with three purposes: to determine the severity of the swallowing problem, to determine the nature of the swallowing problem, and to explore and determine effective strategies and techniques that may help the problem. VFSS has the same three aims as FEES. However, when it comes to the therapeutic nature of the exams, some of the differences that give advantage to

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FEES are the fact that the examination is done in a clinic or bedside environment with the patient and family or staff members present, that the time devoted to therapy is not limited in FEES as opposed to minimizing radiation exposure time, and the fact that the patient is ingesting real food and liquid that is selected purposefully to test the effect of different postures, consistencies, etc. Other advantages include the ability to re-test the effect of an intervention on another day or several times, without exposing the patient to further radiation and to use the interactive nature of FEES to teach the patient about his/her problem, including the use of biofeedback. The two examinations (VFSS and FEES) display the anatomy of the oral and pharyngeal cavities very differently. This will sometimes dictate which examination is chosen. For example, if a cervical osteophyte is suspected, a fluoroscopy exam might be indicated to view the cervical spine. However, after osteophytes have been diagnosed (either from a VFSS or X-ray or CT scan), a FEES will guide therapy better because the exact location where the pharyngeal wall protrudes into the pharyngeal cavity can be seen directly. If the osteophyte impedes movement of the epiglottis and/or arytenoids, this can be viewed directly with FEES. The use of different postures or bolus consistencies to alter the bolus path and help the bolus flow to the esophageal inlet can then be tried with FEES, with excellent visualization of the effect on the altered anatomy. There are a multitude of other examples such as these.

5.2.1 Use of Behavioral Strategies During the Examination Chapter 3 included a detailed description of the standard FEES protocol. During a FEES procedure, whenever the patient begins to show signs of dysphagia, the examiner should shift roles, from being an observer to that of a detective. The examiner needs to question why the problem might be occurring, formulate a hypothesis about a solution to the problem, and then test the hypothesis with appropriate interventions. To do this successfully and expeditiously, the examiner needs to have a good knowledge of normal swallowing physiology (see Chap. 1) and to be able to recognize signs of characteristic abnormal features of neurogenic dysphagia (see Chap. 2). Then the examiner needs to reach for the “bag of tricks” that might help that particular problem. The rational and effective application of therapeutic interventions depends, first of all, on correctly identifying the physiologic swallowing impairment. Concerning FEES based treatment decisions, at least three distinctive patterns may be differentiated (see also phenotypic patterns of neurogenic dysphagia in Sect. 3.1.6): (1) the weak or ineffective swallow with reduced bolus clearance, (2) the misdirected swallow with impaired airway protection due to incomplete valving, and (3) the delayed or mistimed swallow. Neurogenic dysphagia is typically caused by a motor or sensory deficit or a variable combination of both. Physiologic parameters of motor and sensory control required for intact swallowing are (1) briskness of initiation of movement; (2) speed of movement; (3) precision, timing, and coordination of movement; (4) force or strength of movement; (5) amplitude of movement; (6) intact sensation and (7) functionally normal anatomy.

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5.2.2 Selecting the Appropriate Therapeutic Strategy For any given problem, several dietary or behavioral interventions may alter the bolus path, protect the airway, or improve bolus clearance. Their effect is not always predictable; if time allows, the examiner should try several different strategies. The particular interventions selected depend partly on the nature of the problem but also on what level of intervention is being considered. According to Huckabee and Pelletier (1999), strategies should be thought of as either rehabilitative or compensatory (see also Sect. 7.2.1). Therapeutic strategies that are rehabilitative are intended to restore or improve the actual swallowing physiology. An example is laryngeal adductor exercises to improve laryngeal valving. Other strategies are compensatory, meaning they are aimed at improving the ability to adapt and cope with the problem. An example is the chin-tuck posture, which may reduce the amount of bolus spillage into the hypopharynx before the swallow begins. Some strategies are combination of the two: An example is the maneuver known as the supraglottic swallow, which was designed to induce volitional airway protection before, during, and after the swallow. This maneuver is compensatory in nature, but it actually may have rehabilitative effects as well if it strengthens vocal fold adduction force. Finally, some compensatory interventions do not require changes in swallowing, but rather dietary alterations or changes in the amount or rate of bolus delivery. In general, rehabilitative strategies are reserved for patients with greater potential for swallow recovery and for patients who have the physical, cognitive, and psychological resources to perform, learn, retrain, and use the strategies independently. Compensatory strategies are aimed at patients with a temporary dysphagia, for example, patients following acute stroke, or a dysphagia that is not expected to improve, for example, patients with later-stage amyotrophic lateral sclerosis. Some compensatory strategies are complicated to learn, however, and so the physical, cognitive, and psychological status of the patient still must be considered. Sometimes a caregiver can be recruited to supervise or assist with some of these strategies. If a patient is not deemed capable of learning any behavioral strategy and help from caregivers is in question, the clinician may depend entirely on dietary interventions to address the problem.

5.2.3 T  he Weak or Ineffective Swallow with Reduced Bolus Clearance The first major pattern of dysphagia to be considered is the inability to clear the bolus completely through the pharynx. When inadequate bolus propulsion or bolus clearing occurs, the problem may lie with tongue propulsion, pharyngeal shortening, pharyngeal constrictor contraction, hyoid elevation, laryngeal elevation, or upper esophageal sphincter (UES) opening. If these movements are reduced in force or amplitude, they will not work effectively to clear the bolus through the pharynx. In most cases of neurogenic dysphagia, the problem is one of weakness, although reduced amplitude of movement can also be caused by stiffness, rigidity, or spasticity.

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If rehabilitative strategies are considered, the region or muscle group that has reduced force needs to be identified. VFSS is better at directly visualizing many of these movements during the swallow. FEES does not visualize as many structural movements during swallowing as does VFSS, but it is possible to identify the area of reduced force from observations made in the anatomic-physiological part of the exam (Part 1); even then, some structural movements are simply not visible. Pharyngeal contraction is probably the most readily visible movement, assessed in Part I of the standard FEES as the pharyngeal squeeze maneuver (Fuller et al. 2009). In addition, during the swallow, incomplete hyolaryngeal elevation can be inferred from reduced epiglottal inversion with a high degree of accuracy. Adequate tongue base retraction is difficult to assess but can be judged from some tasks included in part I of the FEES examination (see Sect. 3.1.3). Unilateral or asymmetric weakness of tongue, pharyngeal, or laryngeal structures can be detected very nicely with FEES during the Part 1 tasks or during swallowing. Another, very accessible strategy to determine where the region of reduced pressure lies is to look directly at the residue remaining after the swallow. The examiner can deduce which structural movements were impaired by identifying the location of residue left after the swallow. This deduction has been verified by studies that compared the location of residue with other measures of reduced force such as manometry or fluoroscopy (Dejaeger et  al. 1997; Olsson et  al. 1997; Perlman et al. 1992). Bolus clearance also can be reduced because of an anatomic or structural abnormality, whether a foreign body, missing structures, or structures altered by surgery or trauma. Structural aberrations may alter the path of the bolus and decrease clearance. In many anatomically based problems, endoscopy will reveal the problem. Additionally, foreign bodies, such as large bore feeding tubes, or feeding tubes that are placed such that they cross the midline of the larynx, are readily apparent with endoscopy, and their effect on bolus flow and movement of surrounding structures is well appreciated (Dziewas et al. 2008). Whereas assessment of structural movements or anatomical integrity is important for understanding the source of the problem, our best indication of the severity of the problem is to note the amount and location of residue left after the swallow. This is the clinician’s best marker for judging the significance of the problem and for monitoring the effect of therapeutic interventions. Both fluoroscopy and endoscopy can visualize residue, but endoscopy is better at judging amount of residue and localizing the residue. In attempts to identify the most effective intervention for an “ineffective swallow,” a reduction in amount of residue after using the strategy is the best evidence of a positive effect. The “weak or ineffective” swallow pattern with reduced bolus clearance can be addressed with rehabilitation or compensatory interventions. Exercises have been developed to help increase the force or strength of tongue, laryngeal, and pharyngeal movements (see Chap. 7). However, the reader is cautioned not to employ the exercises and maneuvers indiscriminately. They should be taught and recommended only when the patient can perform them correctly, when it is appropriate for the underlying problem, and when the condition is amenable to exercise. For example,

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although patients with motor neuron disease have weakness, intensive exercise is generally contraindicated in the later stages and should not be recommended. Similarly, patients with problems in the cervical spine may not be able to achieve some postures or perform some exercises effectively. In some medical conditions, the primary underlying problem may not be reduced muscle strength but rather decreased tissue compliance, increased tone, slowness of movement, or even delayed onset of movement. The type of exercise designed to improve one of these deficits might be quite different in these cases. Many of the exercises to treat the problem of an ineffective swallow can be taught quickly and effectively during a FEES examination because the patient can visualize performing them on the monitor and modify the performance under a biofeedback paradigm. Alternatively, a second endoscopy session may be scheduled to specifically identify, learn, and practice the exercises that seem to have the greatest potential. The tongue pull, tongue push, trill, gargle, “hawking” sound, grunt, and strained, loud high “ee” are movements that recruit base-of-tongue and pharyngeal muscles and can be visualized endoscopically. It is suggested that the examiner teaches the appropriate movement while viewing the monitor with the patient. If the patient performs it correctly, baseline movement can be noted and the specific goal (e.g., increased pharyngeal wall movement) can be illustrated. If greater movement occurs with increased effort, this can also be emphasized so that the patient will learn to perform the exercise correctly. The head-lifting exercise or Shaker exercise, which strengthens the suprahyoid and infrahyoid muscles (Shaker et  al. 1997), is highly recommended as a well-­ researched exercise (see Sect. 7.2.1). It has been shown to increase two important movements needed for swallowing, namely, laryngeal elevation and cricopharyngeal opening. Similarly the CTAR exercise has been shown to increase muscular effort of the suprahyoid muscles and can be used as an alternative to the Shaker exercise (Sze et al. 2016). Neither of these exercises are taught under fluoroscopy or endoscopy, of course; when implementing this exercise with a patient, it is recommended that several swallows be recorded before and after the exercise program. With endoscopy, progress would be marked by a reduction in the total amount of residue. Residue in the valleculae should be especially reduced if hyolaryngeal excursion is improved and residue in the piriforms should be reduced if the UES opens more widely. The Mendelsohn maneuver (Kahrilas et  al. 1991) is aimed at increasing hyolaryngeal elevation and thereby prolonging the UES opening. This maneuver can be taught and practiced under direct endoscopic visualization during the FEES exam or in a subsequent therapy session to determine whether has a positive effect on the swallow. When a person has good laryngeal elevation, the Mendelsohn maneuver will be seen as a sustained period of whiteout while the epiglottis remains retroflexed. The patient who needs this exercise will probably not be able to attain this target posture. There may be a prolonged period of “pinkout” during the time of sustained laryngeal elevation and the epiglottis may be seen only partly inverted. The clinician may need to show a video clip of the desired movements so that the patient can better understand what his/her goal is. This can be

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Fig. 5.1  Endoscopic view of an inverted epiglottis seen in the frame immediately after white-out ends in a patient who is successfully performing a Mendelsohn maneuver. With slightly less elevation, or in some anatomies, the epiglottis will not completely invert and the airspace will not completely close, producing pinkout, indicating that the airspace is still visible

judged endoscopically, as shown in Fig. 5.1. If executed successfully, it will lead to better bolus clearance and less residue after the swallow, especially in the valleculae. The “effortful” swallow (Kahrilas et al. 1993; Pouderoux and Kahrilas 1995) is aimed at increasing the force of tongue propulsion and contact against the posterior pharyngeal wall. The pharyngeal constrictors will also be recruited. When using endoscopy, the effortful swallow will need to be judged mainly by its effect on bolus clearance, throughout the pharynx. Increased tongue propulsion cannot be seen endoscopically during the swallow. However, pharyngeal squeeze should be increased and this may be seen. The effortful swallow should be accompanied by complete and slightly prolonged whiteout, indicating complete airspace closure. After the patient has learned the Shaker, Mendelsohn maneuver, or effortful swallow, direct visualization either by endoscopy or fluoroscopy is needed to determine whether it has had a positive effect on reducing the amount of residue. In a patient with an extremely weak swallow, the effect may not be immediate; however, because repeated practice with the maneuvers eventually may have a positive effect, the clinician may decide to undertake a therapy program using some of these in an “exercise” mode. In this venue, they should be practiced daily. The final category of interventions is compensatory strategies, including postures and behavioral strategies implemented by the patient and feeding strategies that may be introduced by the feeder. Postural changes all can be assessed successfully by using endoscopy or fluoroscopy, with endoscopy having the advantage of being able to see the change in anatomic configuration within the hypopharynx and the effect the altered posture will have on bolus flow. Figure 5.2 illustrates the effect of a head turn to the left. It is important to remember that even though postural changes are intended to have specific effects on bolus flow, the change the altered posture has on pharyngeal

230 5  Using FEES in the Treatment and Management of Neurogenic Dysphagia: General… Fig. 5.2  Effect of the head turn on the anatomy. A patient is turning his head to the left. This posture brings the larynx closer to the left pharyngeal wall and narrows that lateral channel

and laryngeal anatomy, and thereby on bolus flow, will be somewhat idiosyncratic and not always predictable. For example, turning the head to the weak side often is recommended for the swallow that is unilaterally weak, but sometimes this posture does not completely close off the affected lateral channel and pyriform, or it results in bolus spillage into the larynx from the unaffected side. A period of trial and error is recommended to find the most consistently effective posture that will facilitate bolus clearing in the individual patient. Postural changes sometimes can have dramatic effects on the path taken by the bolus. Some common eating and swallowing strategies that may improve bolus clearance are using dry (clearing) swallows and alternating food and liquid swallows (i.e., the liquid “wash”). Again, both fluoroscopy and endoscopy generally assess the effect on bolus clearance by looking at amount of residue after the swallow when using the strategy. An added benefit of endoscopy is to use it as a biofeedback tool to increase a patient’s awareness of residue and to reinforce and habituate the use of secondary “clearing” swallows or liquid washes. Some compensatory strategies can be implemented externally by the feeder or supervisor if the patient is not an independent feeder. Alternating food and liquid and altering the bolus size (larger may be better), the rate of delivery (probably slower rate), and the type of utensil used to ingest the food or liquid may have an effect on bolus clearance. Alterations in bolus consistency also may affect bolus clearance, with thinner liquids and more cohesive food boluses generally cleared through the pharynx most easily. These variations may be tried when using either fluoroscopy or endoscopy, but the advantages of endoscopy are that many variations can be tried and real liquids and foods are used; so there is no need to guess which compensatory feeding strategies work best.

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5.2.4 T  he Misdirected Swallow: Impaired Airway Protection Due to Incomplete Valving During swallowing, two valves must close tightly: the velopharyngeal sphincter and the laryngeal vestibule. Endoscopy has a better view of velopharyngeal closure than fluoroscopy because it can see lateral pharyngeal wall movement as well as velar elevation, whereas fluoroscopy sees only velar elevation. Endoscopy is also the preferred tool for assessing laryngeal competence, but some of the structural movements must be evaluated during non-swallowing tasks in various phonatory and breath-holding tasks (see Sect. 3.1.3). Arytenoid and epiglottic movement are assessed during swallowing while vocal fold closure is assessed in Part 1 from breath-holding, cough, or throat clearing tasks. Although it cannot assess glottis closure adequately, fluoroscopy has a more complete view of arytenoid, and hyolaryngeal rise. It also visualizes the epiglottis throughout the swallow. If velopharyngeal competence is defective, the bolus will leak superiorly into the nares during the swallow. This is most likely to happen with liquids, and both endoscopy and fluoroscopy can witness this event. If laryngeal incompetence is a problem, the bolus will leak into the larynx and be aspirated. Fluoroscopy sees this event as it occurs, whereas endoscopy is restricted to a view of the penetrated or aspirated bolus after the swallow, when the larynx reopens. If velopharyngeal incompetence is a problem, a standard set of exercises can be used to strengthen the muscles that close the port. Biofeedback is sometimes an effective technique when working on velopharyngeal incompetence, simply because people generally are not aware of movement of this sphincter until their level of awareness is raised through kinesthetic and visual feedback. Endoscopy can be used as biofeedback simply by ensuring that the patient has a view of the monitor while performing the task. It is also the preferred tool for monitoring change over time in amplitude of movement. Nonrehabilitative, compensatory strategies to deal with velopharyngeal incompetence and the problem of nasal backflow generally include postural changes (such as chin back), identifying more successful bolus consistencies and liquid viscosities, or finding the optimal bolus size to minimize the problem. Both fluoroscopy and endoscopy can assess these effects, but a greater range of liquids and foods can be tried with endoscopy. If laryngeal competence is a problem, exercises that increase vocal fold adduction and hyolaryngeal excursion can be implemented. Some of the common exercises for vocal fold adduction are the Valsalva, pushing or pulling, lifting, or grunting. Exercises that increase arytenoid and epiglottic movement are the same as those that increase hyolaryngeal excursion. These were covered above, in reduced bolus clearance. One maneuver that is specifically aimed at the patient with incompetent airway closure is the supraglottic swallow. This maneuver, first developed by Logemann (1983) has components of compensation and of rehabilitation. The goal is to close the vocal folds before and during the swallow, thus protecting the airway from aspiration, even if the bolus has penetrated the laryngeal vestibule. It was originally

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developed for the patient following a supraglottic laryngectomy to achieve early airway closure to compensate for having a compromised and exposed larynx (aryepiglottic folds, epiglottis, and false vocal folds have often been resected). The original instructions for the supraglottic swallow were to (1) take a deep breath in and hold it, (2) put the food or liquid in your mouth, (3) swallow, (4) cough out, (5) swallow again. Over the years, this maneuver also has been useful with other types of patients who have unilateral or generalized laryngeal weakness. In these cases, the maneuver focuses the patient’s efforts on producing maximal airway closure at the level of the vocal folds. In the case of a neurologically impaired or extremely debilitated patient, clinicians often modify the original instructions to accommodate their limited capabilities. For example, the patient may be instructed to “(1) put the food or liquid in your mouth, (2) hold your breath, (3) swallow it all at once, (4) exhale or cough as you end the swallow”. Although this shortened version of the original supraglottic swallow does not afford all the protection of the original maneuver, it is more feasible for many patients to learn and habitually use. Sometimes the instructions are modified further, depending on the patient’s ability to perform the sequence of steps. When the patient is instructed to “hold the breath tightly,” maximal airway protection occurs. Not only will the true vocal folds adduct, but with a strong enough larynx, the false vocal folds will contact, and the arytenoids will tilt forward, sometimes touching the petiole of the epiglottis (Martin et al. 1993; Logemann 1998). This variation of the maneuver is called the super supraglottic swallow (see Figure 7.1). The great advantage of this maneuver for swallowing safety is that tight airway closure at the level of the vocal folds is more likely to be maintained into and through the swallow thus producing sustained airway protection. The reader should recall that the normal order of airway closure for a swallow is (1) arytenoids move medially and forward to cover the glottis; (2) epiglottis retroflexes, (3) vocal folds adduct. In a “light breath-hold,” vocal fold adduction may relax briefly as the person transitions from “breath-hold” to “swallow,” whereas the “tight breath-hold” is more likely to produce continual vocal fold adduction into the swallow, without a break in airway closure. Therefore, if the patient is able to perform a tight breath-hold maneuver, this will ensure the best possible protection against aspiration. If there has been any penetration of material into the laryngeal vestibule, it is also important for the person to end the swallow with a strong exhale or light cough to expel this penetrated material and prevent it from falling below the vocal folds as they re-open. A vital component of this maneuver is closure of the airway as the patient holds the breath. As noted by Martin et al. (1993) and by Mendelsohn and Martin (1993), many persons will hold their breath without adducting their vocal folds; so it cannot be assumed that airway protection is achieved if the person holds the breath. Similarly, the tight breath-hold versus the light breath-hold may not produce the predicted movements in some patients. The only way to know whether the maneuver is being performed successfully is to visualize the vocal folds directly. Hence, these same authors recommended that endoscopy be used to teach the supraglottic swallow. When teaching the patient a breath-hold maneuver, the clinician should

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Fig. 5.3  Increasing degrees of airway protection seen in a normal person who is holding his breath (a) with little effort, (b) with normal effort, and (c) with excessive effort

use endoscopy in a biofeedback mode and turn the patient to face the monitor. Many patients need time to learn and stabilize the association of “breath-hold” with vocal fold adduction. It is recommended that endoscopy be used as the biofeedback tool to teach the maneuver and that a follow-up session be given to ensure that the posture has stabilized. Figure 5.3 shows three patterns of normal closure for breath-hold. Compensatory postural strategies for laryngeal incompetence often include postural changes, especially head turn to bring the vocal folds into closer approximation. A common dictum heard by clinicians is to, “turn the head to the weaker side,” especially if one side is known to be weaker. The effect of a head turn on bolus flow is not entirely predictable, however, because the anatomic alteration resulting from this postural change varies with the individual patient. Sometimes it helps to turn the head to the stronger side, and sometimes a head turn does not help at all because it redirects the bolus into the vestibule more easily. The effect cannot be predicted and must be tried with the individual patient to determine whether adopting this posture should be recommended. Finally, chin tuck may

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help reduce aspiration because it may bring the tongue base closer to the posterior pharyngeal wall and reduce the size of the laryngeal vestibule (Welch et al. 1993). Other compensatory techniques include modification of bolus volume (generally smaller), rate of delivery (sometimes consecutive swallows of liquid are actually better), and delivery method (e.g., straw versus spoon versus cup). A change in bolus consistency also may help the problem, with thicker liquids sometimes being safer than thin liquids because they flow more slowly, giving the patient more time to close off the airway. As with fluoroscopy, endoscopy can judge the effects on alternations made to the bolus, but the advantage is that real foods and liquids are used.

5.2.5 The Delayed or Mistimed Swallow The third swallowing problem commonly observed in patients with neurogenic dysphagia is mistiming of bolus propulsion and the pharyngeal response to initiate the swallow. More commonly, it is viewed as a delayed pharyngeal response. The underlying cause of this pattern is a breakdown somewhere in the complex neural circuitry that receives and processes sensory information, sends the command to swallow to the lower motor neuron pools, and transmits the motor signals to muscles that contract to produce the swallow. Both fluoroscopy and endoscopy see the common result of the delayed or mistimed swallow initiation, namely, the bolus spilling into the pharynx before the pharyngeal response is ready to initiate the swallow. Therapeutic strategies to deal with this problem include both compensatory and rehabilitative ones. A compensatory swallow strategy that is sometimes effective is the use of thickened liquids which flow more slowly, giving the patient more time to “start” the swallow. The chin-tuck posture may help to keep material in the mouth and reduce the tendency for bolus leakage into the pharynx until the patient is able to swallow. A category of interventions that are intended to be rehabilitative but, in fact, are mostly compensatory involve “prepping” the sensory system for a swallow by delivering thermal stimulation or delivering food and liquid boluses that carry more salient sensory cues, including cold temperature, sour taste, or food that needs to be masticated. All these “sensory stimulation” techniques have been found to only have a short-term effect (sometimes lasting only a few seconds), and thus are not generally recommended unless as a compensatory technique. The more sophisticated stimulation techniques such as pharyngeal stimulation and cortical stimulation have yielded more promise. These are summarized in Sect. 7.4 along with the evidence for their efficacy. Both endoscopy and fluoroscopy can judge the effects of all these stimulation techniques by looking for a quicker pharyngeal response and less spillage. The ability to use real foods and liquids for alterations in bolus consistency is a distinct advantage of endoscopy. In addition, the use of endoscopy as a biofeedback tool is a significant advantage over fluoroscopy or a noninstrumental evaluation when guiding treatment.

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Another intervention for this problem that has components of compensation and rehabilitation is the super supraglottic swallow. This technique was described above as a strategy for closing the airway tightly at the level of the vocal folds and maintaining this tight airway closure throughout the swallow. This will prevent aspiration during the swallow. In the case of a patient who spills liquid before the swallow begins and the bolus spills into the laryngeal vestibule and leads to penetration or aspiration, the use of a super supraglottic swallow will prevent aspiration before the swallow because the vocal folds will be tightly closed for a volitional, early breath-­ hold. Importantly, we must remember that the airway will still be open if the swallow response has not begun and thus, the only way to prevent aspiration is to teach a tight breath-hold. Whereas both fluoroscopy and endoscopy can identify aspiration that may occur before the swallow, endoscopy also can identify whether the patient was performing the maneuver correctly and actively closing off the airway before the swallow response. Another similar strategy that may be helpful is a maneuver we have called the “controlled swallow.” This strategy is a form of “skill training.” When well learned, it brings a safe swallow sequence to the level of consciousness. The first step is to consciously hold the bolus in the mouth and not let any spill into the throat. When first taught, the bolus (usually liquid) should be kept in the mouth for many seconds (10–30 s) to make the patient acutely aware of the location of the bolus. Biofeedback via endoscopy is important to know whether the bolus is, indeed, being contained in the mouth and is not leaking into the pharynx. The second step is to swallow the liquid bolus all at once. The patient is not given the “command to swallow” but rather told to swallow the entire bolus “when ready.” After the patient has learned to keep the bolus in the oral cavity until he/she is ready to swallow, the time for “bolus hold” is shortened progressively until it is only held for 1  s. At this point, the swallow appears normal. It becomes habituated over time and is easy to perform. Use of this swallow maneuver can reduce spillage dramatically and produce a more effective swallow in many patients.

5.2.6 Ice Chip Protocol One great advantage of a FEES examination is that very severe patients can benefit from the exam. Some patients who have been nil per oral decrease their frequency of spontaneous swallows over time, especially if they are tracheotomized and fed via a feeding tube. A finding of excess secretions in the larynx is highly predictive of a severe dysphagia and/or aspiration. However, clinicians should not refrain from treating these patients and “wait” until they swallow better. The ice chip protocol was developed for patients such as this. The rationale is to stimulate the swallow with a salient bolus in hopes of re-starting or re-invigorating the neural pathways that initiate swallowing. First described by Langmore in 1996 (Langmore 1996) as well as in her textbook (Langmore 2001) and presented in greater detail in a recent publication (Pisegna and Langmore 2018) it simply entails assessing anatomy and physiology as much as possible (Part 1), and then, if the patient has difficulty swallowing spontaneously, the examiner gives him an ice chip or two (about 2 ml), asks

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him to move the ice chips around in his mouth, and then “swallow them all at once” (Part 2). An ice chip bolus has advantages over other liquids or food. First, it is easier to control than water, which is more likely to spill into the pharynx before the patient has begun to swallow. It stimulates the oral preparatory phase when the patient masticates it or simply moves the ice chips from side to side. The oral preparatory phase, in turn, stimulates the oral propulsive stage which is part of the initiation of the swallow. Ice chips are a salient bolus (cold, smooth, familiar taste) which should stimulate swallowing and finally, it is a very safe bolus if aspirated. Sometimes, a patient needs three or four ice chips trials before the swallow mechanism “wakes up” and the swallow is triggered more easily. After each swallow, the status of secretions is assessed. If the swallows helped to reduce the secretions, it is a good prognostic sign. Recommendations from the ice chip protocol exam vary of course, However, if ice chips stimulate more frequent swallowing, and if the swallows help to clear secretions, this may be enough reason to recommend their use. Often ice chips are viewed as a transitional bolus, between the nil per oral stage and an oral diet (food and liquid). A common recommendation is to give the patient ice chips for the next few days to wake up the system and help strengthen the swallow. Then, a FEES reevaluation is warranted (Langmore 2017). Sometimes the recommendation is simply to practice swallowing, using ice chips. Other times, exercises, maneuvers, and postures are practiced, using ice chips as the bolus. If the patient has intact laryngeal sensation and a good cough, there will likely be no significant and lasting aspiration.

5.2.7 F  EES as an Educational Tool to Increase Patient Compliance In the clinical setting, it is of utmost importance to educate the patient and caregivers about the results of the FEES examination, to communicate the findings and interpretation of the examination to the referral source, to confer with other specialists who have expertise in areas relevant to patient management, and to make recommendations regarding treatment or management. The recommended treatment plan should take into consideration the nature of the problem, its prognosis, the anticipated response to treatment, the needs and wishes of the patient and caregivers, and the needs of the referring physician and other health care providers. One of the low moments of any clinician’s day is to realize that a thorough, insightful evaluation and tediously executed treatment plan has been foiled by a patient who chooses to ignore the recommendations or by a caretaker who thinks she or he knows better. Unfortunately, this happens frequently (DePippo et al. 1994). There are some key differences between a fluoroscopy, a clinical bedside, and a FEES examination that are relevant to this dilemma. First, the clinician examination is done without the advantage of directly seeing what is going on in the throat. If the patient does not cough during aspiration, many people will not believe any warnings that he or she is in danger. The fluoroscopy examination does witness this event

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directly and can be used to try to convince an unwilling patient or caretaker that there is a dysphagia and aspiration has occurred. Sometimes, however, the patient believes that he or she did aspirate barium during the study, but not while eating dinner at home. FEES does not have that problem. In fact, with the patient, family, nurse, or physician in the room, an event of aspiration is discussed at that moment, not 20 min later. If anyone seems unconvinced, it can be replicated and discussed again. When the patient declares that the food is “all gone,” and yet there is residue in the throat on the monitor for all to see, this can be pointed out at that moment. After several of these enlightening moments, the discordance between the patient’s complaints and the objectively viewed events is realized. On the other hand, if the patient’s complaints are not visualized, the examiner can probe further until they are revealed, thus satisfying everyone. The image on fluoroscopy is beautiful, but the structures within the larynx are not well visualized. Endoscopy provides the perfect picture for pointing out where the food should and should not go. Anyone can understand this concept without needing to learn the technical names for the structures in view. Finally, a FEES examination lends itself to a “group process” in which therapeutic options can be taught, openly discussed, debated, and tried. This process usually continues about which treatment options will be followed. When the decision-­ making is communal and a contract has been agreed to, the compliance rate soars.

5.2.8 FEES as Biofeedback Tool in Therapy Finally, endoscopy has one advantage over fluoroscopy and many other instrumental techniques, that is, its ability to be used in treatment as a biofeedback tool. FEES can take advantage of biofeedback as the patient pairs his kinesthetic awareness to the visual signal seen on the monitor. Biofeedback has been shown to be one of the most effective modes to learn or improve a motor skill. It helps to speed up learning by reducing uncertainty of performance. To use endoscopy in this manner, the patient simply needs to face the monitor with the endoscope in place. In fact, most FEES examinations should be done with this setup. After the clinician points out some of the key structures, the goals of the session will dictate the course. If a maneuver or posture or other intervention is to be implemented, the clinician will instruct the patient and then have him or her practice. The patient will learn to correlate how he or she is swallowing with what is seen on the monitor. Biofeedback is one of the most effective ways to learn a motor task because of the instantaneous nature of the information fed back to the learner. Conceptualization of the problem can be minimized with little need to discuss what is happening. Some forethought must be involved, however, for it to succeed. The clinician must have the objectives of the lesson clearly in mind. It is important to point out certain salient events to the patient and to instruct the patient regarding the desired behavior to be achieved. Whenever the patient improves, the clinician must be ready to reinforce this behavior. The desired behavior will not likely be learned in a short

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time (although this does sometimes occur). Instead, there will probably be a period during which the patient’s behavior successively approaches the desired goal. Few problems require more than a few lessons, however, and this technique is usually rewarding. Specific parameters may improve when using FEES as a biofeedback tool: –– Increased awareness of residue and habituation of dry or clearing swallows –– Increased control over spillage, with the goal of eliminating spillage before the swallow is initiated (controlled swallow) –– Increased awareness of aspiration or penetration, with habituation of throat clearing and coughing when it does occur –– Improved vocal cord adduction during breath-holding: more complete adduction, brisker onset of adduction, and maintenance of adduction over several seconds –– Consistent laryngeal closure before the swallow is initiated (no spillage prior to swallow initiation; controlled swallow) –– Improved velopharyngeal closure during phonation, with carryover to swallowing –– Improved base-of-tongue retraction after biofeedback and exercise (tongue-pull exercise) –– Improved pharyngeal lateral-wall medialization after biofeedback and exercise (pharyngeal squeeze) –– Habitual use of a posture that facilitates better swallowing Two publications where visual biofeedback was provided via FEES to dysphagic patients learning various swallowing strategies were Denk and Kaider (1997) with head and neck cancer patients and Manor et al. (2013) with Parkinson’s patients. In both cases, the patients trained swallow strategies with FEES biofeedback, learned the strategies sooner, and had better swallowing performance than the patients who did not receive biofeedback. Figure  5.4 shows a biofeedback treatment session Fig. 5.4  A patient with dysphagia in a treatment session using endoscopy in a biofeedback mode

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using endoscopy. The patient is feeding herself and both she and the clinician are watching the monitor.

5.2.9 FEES as a Tool to Reevaluate Patients (Serial FEES) Few inpatients or rehabilitation patients need only one FEES examination. If there is dysphagia, it is usually on a progressive or recovering course, and reevaluations are needed to monitor the patient’s status and to help to guide treatment. FEES is a patient-friendly, cost-effective tool for reevaluations. Even when a fluoroscopy examination is given to the patient initially, FEES is usually an acceptable examination for reevaluations. Patients can be retested at the convenience of the clinician and as soon as the medical and swallowing status warrants a reevaluation. It is always more expedient to test a patient the day the examination is warranted rather than to wait in status quo for several days for a fluoroscopy slot to open. The reevaluation can be brief and strictly focused on the clinical question that needs to be answered. Some common questions that may warrant a reevaluation include the following: –– –– –– –– –– ––

Can the patient now begin to eat by mouth? Can the patient now take (solid food) (thin liquids) orally? Does the patient still need to take thickened liquids? Does the patient still need to use the strategy that he or she has been using? With a new medical event, has the dysphagia changed? After several months, is the progressive course of this dysphagia worse, and how should the treatment change? –– Is the dysphagia severe enough to account for the new onset of pneumonia? When a patient can be reevaluated with the certainty and a wealth of information that an instrumental examination can provide as soon as the patient’s condition warrants an examination, the patient can be moved through the course of treatment as fast as possible (Leder 1998). Using the pattern of dysfunction as the basis for selecting an appropriate intervention, the clinician may apply FEES in several ways for treatment and management of neurogenic dysphagia. First, during the FEES examination, the clinician assesses the effect of the proposed intervention and uses this information to plan a therapy program. During the examination and in subsequent sessions, the video image is used to educate patients and caregivers and to improve compliance with the proposed recommendations. Endoscopy plays a part in therapy itself, being an excellent biofeedback tool. The FEES ice chip protocol will help to treat patients who are very ill (see Sect. 5.2.6) or are immunocompromised or have very poor pulmonary clearance or have not been eaten by mouth for several weeks. Finally, the clinician will want to use FEES for repeat examinations as needed to maximize the progress of the patient as he or she relearns effective swallowing or learns to compensate for the problem.

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References Dejaeger E, Pelemans W, Ponette E, Joosten E. Mechanisms involved in postdeglutition retention in the elderly. Dysphagia. 1997;12(2):63–7. Denk DM, Kaider A. Videoendoscopic biofeedback: a simple method to improve the efficacy of swallowing rehabilitation of patients after head and neck surgery. ORL J Otorhinolaryngol Relat Spec. 1997;59:100–5. DePippo KL, Holas MA, Reding MJ, Mandel FS, Lesser ML. Dysphagia therapy following stroke: a controlled trial. Neurology. 1994;44(9):1655–60. Dziewas R, auf dem Brinke M, Birkmann U, Bräuer G, Busch K, Cerra F, Damm-Lunau R, Dunkel J, Fellgiebel A, Garms E, Glahn J, Hagen S, Held S, Helfer C, Hiller M, Horn-Schenk C, Kley C, Lange N, Lapa S, Ledl C, Lindner-Pfleghar B, Mertl-Rötzer M, Müller M, Neugebauer H, Özsucu D, Ohms M, Perniß M, Pfeilschifter W, Plass T, Roth C, Roukens R, Schmidt-Wilcke T, Schumann B, Schwarze J, Schweikert K, Stege H, Theuerkauf D, Thomas RS, Vahle U, Voigt N, Weber H, Werner CJ, Wirth R, Wittich I, Woldag H, Warnecke T. Safety and clinical impact of FEES – results of the FEES-registry. Neurol Res Pract. 2019;1:16. Dziewas R, Warnecke T, Hamacher C, Oelenberg S, Teismann I, Kraemer C et al. Do nasogastric tubes worsen dysphagia in patients with acute stroke? BMC neurology. 2008;8:28. Huckabee ML, Pelletier CA. Management of adult neurogenic dysphagia. San Diego, CA: Singular Publishing Group; 1999. Kahrilas PJ, Logemann JA, Krugler C, et al. Volitional augmentation of upper esophageal sphincter opening during swallowing. Am J Phys. 1991;260:G450–6. Kahrilas PJ, Lin S, Logemann JA, Ergun GA, Facchini F.  Deglutitive tongue action: volume accommodation and bolus propulsion. Gastroenterology. 1993;104(1):152–62. Langmore SE. Dysphagia in neurologic patients in the intensive care unit. Semin Neurol. 1996;16:329–40. Langmore SE. Endoscopic evaluation and treatment of swallowing disorders. New York: Thieme; 2001. Langmore SE. History of fiberoptic endoscopic evaluation of swallowing for evaluation and management of pharyngeal dysphagia: changes over the years. Dysphagia. 2017;32(1):27–38. Leder SB. Serial fiberoptic endoscopic swallowing evaluations in the management of patients with dysphagia. Arch Phys Med Rehabil. 1998;79:1264–9. Logemann JA. Evaluation and treatment of swallowing disorders. San Diego: College-Hill Press; 1983. Logemann JA. Evaluation and treatment of swallowing disorders. 2nd ed. Austin: Pro-Ed; 1998. Manor Y, Mootanah R, Freud D, Giladi N, Cohen JT.  Video-assisted swallowing therapy for patients with Parkinson’s disease. Parkinsonism Relat Disord. 2013;19(2):207–11. Martin BJ, Logemann JA, Shaker R, Dodds WJ. Normal laryngeal valving patterns during three breath-hold maneuvers: a pilot investigation. Dysphagia. 1993;8(1):11–20. Mendelsohn MS, Martin RE. Airway protection during breath-holding. Ann Otol Rhinol Laryngol. 1993;102(12):941–4. Olsson R, Castell J, Johnston B, Ekberg O, Castell DO. Combined videomanometric identification of abnormalities related to pharyngeal retention. Acad Radiol. 1997;4(5):349–54. Perlman AL, Grayhack JP, Booth BM. The relationship of vallecular residue to oral involvement, reduced hyoid elevation, and epiglottic function. J Speech Hear Res. 1992;35(4):734–41. Pisegna JM, Langmore SE. The ice chip protocol: a description of the protocol and case reports. Perspectives of the ASHA Special Interest Groups. 2018;3(13):28–46. https://doi.org/10.1044/persp3.SIG13.28. Pouderoux P, Kahrilas PJ. Deglutitive tongue force modulation by volition, volume, and viscosity in humans. Gastroenterology. 1995;108(5):1418–26. Scott C. Fuller, Rebecca Leonard, Shervin Aminpour, Peter C. Belafsky. Validation of the pharyngeal squeeze maneuver. Otolaryngology–Head and Neck Surgery. 2009;140 (3):391–394. Shaker R, Kern M, Bardan E, Taylor A, Stewart ET, Hoffmann RG, Arndorfer RC, Hofmann C, Bonnevier J. Augmentation of deglutitive upper esophageal sphincter opening in the elderly by exercise. Am J Phys. 1997 Jun;272(6 Pt 1):G1518–22. Sze WP, Yoon WL, Escoffier N, Richard Liow SJ.  Evaluating the training effects of two swallowing rehabilitation therapies using surface electromyography- Chin tuck against resistance (CTAR) exercise and the shaker exercise. Dysphagia. 2016;31:195–205. Welch MV, Logemann JA, Rademaker AW, Kahrilas PJ.  Changes in pharyngeal dimensions effected by chin tuck. Arch Phys Med Rehabil. 1993;74(2):178–81.

6

Using FEES in the Stroke Unit and the Intensive Care Unit

Contents 6.1  Stroke Unit 6.1.1  Dysphagia Management in the Stroke Unit 6.1.2  Classification and Management of Post-Stroke Dysphagia 6.2  Intensive Care Unit 6.2.1  Epidemiology and Complications of Critical Illness Dysphagia 6.2.2  Etiology and Pathophysiology of Critical Illness Dysphagia 6.2.3  Applications of FEES in the ICU References

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Swallowing disorders play a special role in both the stroke unit and the neurological intensive care unit due to their extraordinary incidence, the acuteness of their occurrence, their related complications, and the different therapeutic options for treating them. When planning the diagnostic algorithm, it is important to keep in mind that the Videofluoroscopic Swallowing Study (VFSS) is applicable only in a limited number of often seriously ill patients (Langmore 1996) as this technique requires that patients have to be transported to the radiological unit, must remain in an upright position and need to be able to cooperate during the procedure. In contrast, in this clinical context, Flexible Endoscopic Evaluation of Swallowing (FEES) has the advantage that it can be performed at the bedside as well as on uncooperative and not fully mobilized patients (Langmore 1996). In this chapter, specific applications of FEES in the stroke unit and the neurological intensive care unit are explained, typical problems are addressed, and the possibilities and limitations of standardized diagnostic and therapeutic procedures are described.

Electronic Supplementary Material The online version of this chapter (https://doi. org/10.1007/978-3-030-42140-3_6) contains supplementary material, which is available to authorized users. © Springer Nature Switzerland AG 2021 T. Warnecke et al., Neurogenic Dysphagia, https://doi.org/10.1007/978-3-030-42140-3_6

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6  Using FEES in the Stroke Unit and the Intensive Care Unit

Stroke Unit

This section demonstrates how FEES can be usefully integrated into the overall concept of dysphagia management in the stroke unit. Subsequently, an endoscopy-­ based dysphagia score developed specifically for this context is presented.

6.1.1 Dysphagia Management in the Stroke Unit As a first diagnostic step, a simple aspiration screening should be performed on all stroke patients. For this purpose, a large number of protocols have been proposed over the past three decades that mainly differ in the volume of examined liquid (Gordon et al. 1987; Wade and Hewer 1987; Barer 1989; DePippo et al. 1992; Kidd et al. 1993; Odderson et al. 1995; Hinds and Wiles 1998; Daniels et al. 2000, 2016; Martino et al. 2009; Suiter et al. 2014). A water test is useful and is recommended by different guidelines (for example the S3 Guidelines of the German Society for Nutritional Medicine; Wirth et al. 2013) and is also implemented in comprehensive algorithms for the initial management of post-stroke dysphagia. The procedure developed by Perry (Fig. 6.1), starts with an examination of the state of consciousness, axial stability, oral-motor function and saliva management. Afterward, three small liquid boli (teaspoonfuls) are administered before the patient is instructed to swallow half a glass of water (Perry 2001a, b). At any time during the test, clinical evidence of aspiration—including an altered voice or coughing—require that the test be aborted (Fig.  6.1). Any liquid swallows are omitted if the patient cannot swallow his own saliva. According to this algorithm, for patients who successfully complete the final step of drinking water from the cup without clinical signs of aspiration, a soft-solid diet with continuous supervision during eating should be initiated. Alternatively, the Yale protocol—which was developed and validated by Leder et al.—can be recommended (Suiter et al. 2014; Warner et al. 2014). This screening begins with a cursory orofacial examination and a brief mental testing. Afterward, the patient completes a 90-ml water swallow test. Another option is the “Rapid Aspiration Screening for Suspected Stroke” (RASSS by Daniels et  al.) which—in addition to a 90-ml water swallow test—takes the variables “dysarthria” and “age above 70” into account (Daniels et al. 2016; Anderson et al. 2016) and— like the Yale protocol—can be reliably applied by specialized nurses. The fundamental importance of simple aspiration screening in patients who have had an acute stroke has been highlighted in recent years by various methodologically heterogeneous studies. For example, Odderson et al. (1995) showed that implementing aspiration screening led to a decrease in pneumonia rates thereafter. In several prospective observational studies failing an aspiration screening was associated with an increased incidence of pneumonia (Sellars et  al. 2007; Lakshminarayan et al. 2010), whereas performing an aspiration screening was generally associated with a reduction in infectious complications (Evans et al. 2001; Lakshminarayan et al. 2010; Middleton et al. 2011). In a prospective multicenter observational study (n = 2532), Hinchey et  al. compared the incidence of

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243

Can the patient be sat up and remain awake and alert for at least 15 minutes ? no yes

Keep nil by mouth and refer to SLP

Sit patient up. Check the follwing questions. Can the patient cough when asked to? Is the patient able to maintain some control of his saliva? Is the patient able to lick top and bottom lip? Is the patient able to breathe freely? 1 or more answers „no“ yes

Keep nil by mouth and refer to SLP

Does the patient have a ‘wet’ or hoarse‐sounding voice? yes no

Keep nil by mouth and refer to SLP

Give a teaspoone of water (up to 3 times). If normal, give half a glass of water. Check the following criteria after each task • Absent swallow • Coughing, choking, breathlessness (immediate or delayed) • Water leaking out of the mouth • Altered voice quality (‘wet’ or hoarse‐sounding voice) 1 or more criteria „yes“ no

Keep nil by mouth and refer to SLP

Order diet as appropriate. Make sure the patient is sat up to eat and supervise patient eating test meal. Check the following criteria: • Prolonged chewing • Oral residues • Prolonged time to finish the meal (>15 minutes) • Patient avoiding certain food items • Cough while/after eating • Liquid swallows after each solid bolus • Overall bad impressions or concerns 1 or more criteria „yes“ no

Keep nil by mouth and refer to SLP

Normalize oral diet, watch out for deterioration

Fig. 6.1  Standardized aspiration screening and dysphagia management in acute stroke patients (modified with permission from Perry 2001a and Perry 2001b).

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6  Using FEES in the Stroke Unit and the Intensive Care Unit

post-­stroke pneumonia in hospitals that provided a formalized dysphagia screen versus the incidence from hospitals that did not provide a formalized screening. In their study, the use of a formal protocol decreased the risk of pneumonia by threefold. More recently, Titsworth et al. adopted a “prospective interrupted time-series trial” to evaluate the effect of implementing a dysphagia protocol with a nurseadministered bedside dysphagia screen and a rapid clinical swallow evaluation by a speech and language pathologists (SLP). Their main findings were that adherence to the dysphagia screening nearly doubled (from 39.3 to 74.2%) and that the incidence of pneumonia more than halved (from 6.5% to 2.8%) after the implementation of the protocol (Titsworth et al. 2013). Finally, Bray et al. analyzed data from 63,500 acute stroke patients (Bray et  al. 2017). Dysphagia screening was performed in a median of 2.9 h after admission, and the incidence of pneumonia was 8.7%. One of this study’s main findings was a nearly linear association between delays in dysphagia screening and the incidence of pneumonia. Patients with the longest delays in screening (fourth quartile; delay ≥345 min) had 36% higher odds of pneumonia compared with those in the first quartile (delay of 0–79 min). In a second, methodically similar study, this relationship between a delayed execution of aspiration screening and an increased risk of pneumonia was confirmed (Al-Khaled et al. 2016). Despite these convincing studies, the significance of aspiration screening—especially that of simple water swallow tests—has been called into question by repeated critical observations regarding the validity of this instrument. For example, two meta-analyses indicated that the sensitivity of water tests for detecting aspiration was well below 80% in almost all studies compared with VFSS or FEES (Ramsey et al. 2003; Bours et al. 2009). The water tests’ specificity and positive and negative predictive value were also judged to be inadequate from a clinical point of view (Ramsey et al. 2003; Bours et al. 2009). This interpretation was confirmed in a study that adopted a modified water test that used liquid X-ray contrast agents instead of water to directly detect aspiration in a chest radiograph following the swallow test. Despite this optimized approach compared with that of the simple water swallow test, the sensitivity and specificity for detecting aspiration were only 0.47 and 0.72 compared with VFSS (Ramsey et  al. 2006). The “Toronto Bedside Swallowing Screening Test” (TOR-BSST©)—which was published by Martino et al. (2009)— also assesses the swallowing function by means of a water swallow test combined with an evaluation of the motor function of the tongue. Using VFSS as gold standard, the first study reported a sensitivity of 91.3% and a negative predictive value of 93.3% for acute stroke (n = 103) and a sensitivity of 89.5% for patients in the rehabilitation phase (n = 208). However, the impact of these findings is diminished by the fact that that only about one-fifth of all enrolled patients underwent VFSS to determine sensitivity. The results should therefore be confirmed in a larger group of patients, particularly in acute stroke victims. The test is protected by copyright and may only be used after obtaining a fee-based license that includes online training. Apart from water-screening tests, which are the most commonly used methods to screen for dysphagia in acute stroke and which provide binary test results (i.e., pass or fail), there are also screening tests available that use more than one consistency

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for screening. These multi-consistency tests therefore allow for a graded stepwise rating of swallowing impairment and usually add dietary recommendations to their risk assessments. The Gugging Swallowing Screen (GUSS) sequentially evaluates the patient’s ability to swallow semi-solid, liquid, and solid boli of increasing volumes. The test is terminated if clinical aspiration signs are observed. Based on the results of this test, dysphagia is graded in one of four categories (severe, moderate, mild, or no dysphagia), and a special diet and additional strategies are recommended for each severity level (Trapl et al. 2007; Fig. 6.2). Compared with FEES as an objective assessment, the GUSS achieved a sensitivity of 100% and a specificity of both 50% and 69% (n = 20 and n = 30, respectively; Trapl et al. 2007). Remarkably, in a second study, the results of the original publication were replicated by another group. In the analysis of 100 acute stroke patients,

Vigilance (the patient must be alert for 15 minutes) Cough and/or throat clearing (voluntary cough, the

Yes 1 1

No 0 0

Saliva Swallow: Swallowing successful Drooling Voice change (hoarse, gurgly, coated, weak)

1 0 0

0 1 1

patient should cough or clear his/her throat twice)

SUM

(5) (1-4: investigate further 5: continue with part 2)

In the following order Deglutition Swallowing not possible Swallowing delayed (>2 sec., solid textures > 10 sec.) Swallowing successful

1=> Semisolid

2=> Liquid

3 Solid

0 1 2

0 1 2

0 1 2

0 1

0 1

0 1

Drooling Yes No

0 1

0 1

0 1

Voice change Yes No

0 1

0 1

0 1

Cough (involuntary) (before, during or after swallowing

–until 3 minutes later)

Yes No

SUM I

(5) (1-4: investigate further 5: Continue liquid)

SUM II(Indirect AND direct swallowing test)

(5)

(5)

(1-4: investigate further 5: Continue liquid)

(1-4: investigate further 5: Continue liquid)

(20)

Fig. 6.2  Gugging swallowing screen (reproduced with permission; Trapl et  al. 2007; www. dysphagie-trapl.at)

246

20

15-19

6  Using FEES in the Stroke Unit and the Intensive Care Unit Results Severity Code Semisolid/liquid and Slight/No dysphagia solid texture successful minimal risk of aspiration Semisolid and liquid Slight dysphagia with texture successful and low risk of aspiration solid unsuccessful

10-14

Semisolid swallow sucessful and liquids unsuccessful

0-9

Preliminary investigation unsuccessful or semisolid swallow unsuccessful

Recommendations • Normal diet • Regular liquids (first time under supervision of SLP or stroke nurse)

• Dysphagia diet (pureed and soft food) • Liquids very slowly—one sip at a time • Functional swallowing assessments such as FEES or VFSS • Refer to SLP

Moderate dysphagia with risk of aspiration

• Dysphagia diet beginning with: • Semisolid textures (baby food and additional parenteral feeding) • All liquids must be thickened • Pills must be crushed and mixed with thick liquid • No liquid medication • Further functional swallowing assessment (FEES, VFSS) • Refer to SLP Severe dysphagia with • No oral food a high risk of • Further functional swallowing asssessment aspiration (FEES, VFSS) • Refer to SLP

Fig. 6.2 (continued)

the sensitivity and specificity of the GUSS in detecting an increased risk of aspiration were 96.5% and 55.8%, respectively (Warnecke et  al. 2017). Thus, this test seems to detect post-stroke dysphagia with risk of aspiration more reliably than do the different variants of the simple water swallow test. A disadvantage of the GUSS is its relatively low specificity, which results in less frequent prescription of oral feeding than is possible and in more frequent tube feeding (Fig. 6.3) than is actually necessary. As shown in the confirmation study, the GUSS underestimated the swallowing ability especially in patients with severe strokes characterized by an NIH-SS ≥ 10 points (Table 6.1). In addition to water swallow tests and multi-consistency tests, the swallowing provocation test (SPT) represents a third alternative. The SPT exclusively examines the involuntary swallowing reflex and thereby focusses on the pharyngeal phase of deglutition (Teramoto et al. 1999; Teramoto and Fukuchi 2000). For testing, a thin catheter—such as an infant feeding probe (Dziewas et  al. 2001)—is inserted transnasally and placed in the oropharynx. Subsequently, a bolus of 0.4 ml of distilled water or sterile physiological saline solution is injected through the catheter and onto the back of the pharyngeal wall, which allows the reflexive swallow response to be assessed. The SPT is considered normal if the time from water injection to reflexive swallowing is less than or equal to 3 s. If the swallowing reflex is delayed for more than 3  s, the test results are considered abnormal, and the patient is deemed to be at risk of aspiration. Subsequent to

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Fig. 6.3  Results of swallow test by means of FEES and GUSS (based on Warnecke et al. 2017)

120 100

Percentage

Normal Diet 80

Dysphagia Diet

60

Parenteral or enteral supplementation Nothing per mouth

40 20 0

FEES

GUSS

Table 6.1  Diagnostic parameters of the Gugging Swallowing Screen in screening aspiration risk in patients with stroke according to National Institutes of Health Stroke Scale (NIH-SS) subgroup NIH-SS (n) 0–4 (16) 5–9 (20) 10–14 (29) ≥15 (35)

Sensitivity 71.4 (29.0–96.3) 100 (66.3–100) 100 (79.4–100) 100 (86.8–100)

Specificity 88.8 (51.7–99.7) 63.4 (30.7–89.0) 53.8 (25.1–80.7) 20.0 (2.52–55.6)

PPV 83.3 (35.8–99.5) 69.2 (38.5–90.9) 72.7 (49.7–89.7) 75.7 (57.7–88.9)

NPV 80.0 (44.3–97.4) 100 (59.0–100) 100 (59.0–100) 100 (15.8–100)

Results in percent (95% CI). GUSS Gugging Swallowing Screen, PPV positive predictive value, NPV negative predictive value (based on Warnecke et al. 2017)

smaller retrospective studies (Teramoto et al. 1999; Teramoto and Fukuchi 2000), the SPT was evaluated in a prospective study that recruited acute stroke patients (n = 100; Warnecke et al. 2008). Compared with FEES as an objective diagnostic tool, the SPT achieved a sensitivity of 74.1% and a specificity of 100%. False negative findings were found in patients who had a severely disturbed oral phase and showed pre-deglutitive penetration or aspiration as a result of pronounced premature spillage. The high specificity of the SPT may render it a useful supplement to the other screening tools.

Aspiration screening should be performed in all acute stroke patients. A multi-consistency test should be considered as alternative to water swallow tests. The swallowing provocation test is recommended as a supplement. Aspiration screening should be performed as soon as possible after a patient’s admission.

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In the next step, all patients with a pathological screening should undergo a more detailed assessment of their swallowing function. Due to the insufficient sensitivity of most published screening procedures or due to missing replication studies, stroke patients without pathological findings in the initial bedside testing should undergo a further swallowing assessment if other known clinical predictors of dysphagia are present. These predictors include an overall severe neurological deficit, severe dysarthria or aphasia, and pronounced facial palsy (Dziewas et al. 2004; Sellars et al. 2007; Falsetti et al. 2009). In addition, buccofacial apraxia is considered an independent risk factor for dysphagia in patients who have had a stroke confined to the left middle cerebral artery (Somasundaram et al. 2014). The first option for providing a more differentiated assessment of swallowing impairments is the clinical swallowing examination (CSE) conducted by an SLP. The CSE should be carried out according to a standardized protocol (Logemann et al. 1999; Bartolome 2013; or Mann 2002). Due to the limitations of this approach—particularly with regard to the detection of silent aspiration an instrumental evaluation of the swallow is often preferred over a CSE when it is available. The primary goal of the CSE is to determine the severity of dysphagia, while the instrumental dysphagia assessment can reveal more about the pattern of dysphagia (eg., Is there excess spillage? Is pharyngeal clearance reduced?). The instrumental exam of choice is FEES, for reasons described in chapter 3. It is important to emphasize that performing FEES in the stroke unit by a team of neurologists and an SLP during the acute phase of the stroke is a safe procedure (Warnecke et al. 2009b). In a group of 300 acute stroke patients who were examined on average within 1.9 days of the onset of stroke symptoms, there was no laryngospasm, vasovagal reaction, decreased consciousness, symptomatic bradykinesia or tachycardia, or epistaxis (nosebleeds) that required treatment. The incidence of self-limited epistaxis was 6% and was not related to (1) the type of stroke (ischemia vs. hemorrhage), (2) the acute treatment (thrombolysis vs. no thrombolysis), or (3) secondary prophylaxis (anticoagulation vs. antiplatelet). No increased rate of epistaxis was observed, even in patients who were examined by FEES within 24  h of the onset of thrombolysis (Table  6.2). Overall, however, the incidence of self-limited epistaxis was higher compared with FEES performed in Oto-Rhino-Laryngology patient cohorts (6% vs. 0.4%; Aviv et al. 2005). This discrepancy probably results from the different patient groups. In acute stroke patients, many factors may directly contribute to the higher rate of Table 6.2  Incidence of self-limited epistaxis in 300 acute stroke patients examined by FEES Patients A

B

Total Stroke Thrombolysis No Yes Yes + within 24 h Secondary prevention Anticoagulation Platelet inhibition Intracerebral hemorrhage

Epistaxis 18/300 (6.00%) 16/265 (6.04%) 11/168 (6.55%) 5/97 (5.15%) 2/32 (4.26%) 8/11 (7.21%) 8/154 (5.19%) 2/35 (5.17%)

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All stroke patients Aspiration screening

All patients presenting with one or more of the following: • pathological aspiration screen • severe neurological deficit (NIH-SS ≥ 10) • severe facial palsy • severe aphasia • severe dysarthria

• Water Swallow Test • Multiple Consistency Test • Swallowing ProvocationTest Dysphagia assessement • Clinical assessement of dysphagia • FEES

Fig. 6.4  Diagnostic algorithm for acute stroke-related dysphagia

epistaxis, including an increased vulnerability of the nasal mucosa due to preceding nasotracheal suctioning or the insertion of a nasogastric tube, patients’ inability to cooperate, their uncontrolled head movements during the examination, treatment with antiplatelets or anticoagulants, or arterial hypertension (Warnecke et al. 2009b). While the mean diastolic blood pressure remained constant throughout the FEES in the same group of 300 acute stroke patients, statistically significant—albeit clinically modest—changes in systolic blood pressure, heart rate, and oxygen saturation occurred (RR systolic: +3.4 mmHg; heart rate: +1.9 beats/min; oxygen saturation: 0.5%). No change in cardiovascular parameters in any patient resulted in a serious adverse event. The additional support of a nurse was required to successfully perform FEES in less than 10% of cases. More than 80% of patients judged the examination to be slightly or not at all uncomfortable (Warnecke et  al. 2009b). The diagnostic algorithm for aspiration screening, the clinical swallowing examination, and FEES are summarized in Fig. 6.4.

A clinical swallowing examination should be performed by an SLP in all patients who fail an aspiration screening as well as in patients with normal screening results (or on whom screening could not be performed) who present with known clinical predictors for post-stroke dysphagia (a severe neurological deficit, severe dysarthria or aphasia, severe facial paresis, buccofacial apraxia). The CSE yields limited information about the nature of the swallowing problem and thus, in most cases, should be supplemented by FEES.

6.1.2 Classification and Management of Post-Stroke Dysphagia Grading acute post-stroke dysphagia is necessary to initiate immediate protective and rehabilitative measures and to determine a baseline for follow-­up examinations (Trapl et al. 2007; Dziewas et al. 2008b). In addition to the GUSS, which was developed for screening purposes and presented above, the Fiberoptic Endoscopic Dysphagia Severity Scale (FEDSS) for acute stroke patients yields an

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6  Using FEES in the Stroke Unit and the Intensive Care Unit

FEDSS-PROTOCOL

MAIN FINDINGS

CLINICAL IMPLICATIONS

Saliva

Penetration/aspiration

No oral food, NGT, watch out for respiratory distress (Score 6)

Puree

Penetration/aspiration without or insufficient protective reflex

No oral food, NGT (Score 5)

Puree

Penetration with sufficient protective reflex

NGT, small amounts of puree during swallowing therapy (Score 4)

Liquid

Penetration/aspiration without or insufficient protective reflex

NGT, small amounts of puree during swallowing therapy (Score 4)

Liquid

Penetration with sufficient protective reflex

Pureed food, parenteral application of fluids (Score 3)

Soft solid food

Penetration/aspiration or massive residues in valleculae or pyriformes

Pureed food and fluids (Score 2)

Soft solid food

No penetration/aspiration and not more than moderate residues in valleculae or pyriformes

Soft solid food and fluids (Score 1)

Fig. 6.5  Fiberoptic endoscopic dysphagia severity scale (FEDSS) for acute stroke patients

endoscopy-based score. Based on a modified FEES protocol and taking the typical endoscopic findings of acute stroke patients into account, the FEDSS allows for a fast and focused yet differentiated endoscopic swallowing examination within the first days post stroke. The FEDSS classifies post-stroke dysphagia into six severity grades, which are linked to specific protective and/or rehabilitative measures that should be implemented during treatment in the stroke unit (Dziewas et al. 2008b). As shown in Fig.  6.5, the endoscopic examination begins with an (abbreviated) anatomic physiological evaluation and examines the patient’s handling of oropharyngeal secretions (left column above). Afterward, the patient first receives semisolid food (pudding; IDDSI level 4), then liquid (IDDSI 0), and finally, solid food (bread; IDDSI 6/7). In order to minimize the risk of aspiration during the examination, the endoscopy is stopped at each of the steps if one of the findings listed in the middle column is detected. Depending on the precise finding, post-stroke dysphagia is graded according to the six severity levels shown in the right-hand column, which, in turn, directly results in a clinical recommendation regarding the feeding strategy and airway safety. The inter-rater reliability of the FEDSS is substantial. Thus, in a study in which 25 video-documented endoscopic examinations of acute stroke patients were independently classified by three examiners using the FEDSS, a high level of agreement (kappa coefficient: 0.89) was documented (Dziewas et al. 2008b). A second study revealed that the FEDSS can reliably be used by clinicians who are inexperienced in this field after receiving a short and structured training. After a 30-min lecture

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Fiberoptic Endoscopic Dysphagia Severity Scale (FEDSS)

consisting of a demonstration of the characteristic endoscopic findings based on the FEDSS protocol, the participants were able to correctly evaluate an average of 90% of examinations (Warnecke et al. 2009c). In addition, the FEDSS is an important predictor of complications and functional outcome during the further course of the disease. To investigate the prognostic properties of the FEDSS, a prospective observational study was performed over a 12-month period and included 153 first-ever acute stroke patients. The severity of dysphagia was classified within 24 h of patient admission to the stroke unit via the FEDSS. The functional outcome was determined by the modified Rankin scale (mRS) after 3 months. Intercurrent complications included pneumonia and endotracheal intubation during acute care. Multivariate linear and logistic regression analyses were used to determine the association between the FEDSS and the patients’ functional outcomes as well as the complications mentioned. Analyses were corrected for the variables of gender, age, and the National Institutes of Health Stroke Scale (NIH-SS) on the day of admission (Warnecke et al. 2009a). In this study, a statistically significant correlation was found between the FEDSS and the mRS at 3 months that was independent of the other variables mentioned (Fig. 6.6). For each additional point in the FEDSS, there was more than a twofold increase in the probability of developing pneumonia in the acute stage post-stroke and a 50% increase in the risk of not becoming independent in daily life (defined as mRS 0–2) after 3 months (Warnecke et al. 2009a). From a clinical point of view, the FEDSS—and especially the endoscopic evidence of saliva aspiration—is a strong predictor of the need for later intubation. Thus, in 6

(n=8)

5

(n=12)

4

(n=15)

3

(n=20)

2

(n=25)

1

(n=73)

0%

10%

20%

30%

40%

50%

60%

70%

80%

90%

100%

Modified Rankin Scale (mRS) MRS 0

MRS 1

MRS 2

MRS 3

MRS 4

MRS 5

MRS 6

Fig. 6.6  Relationship between initial FEDSS and mRS after 90 days (reproduced with permission; Warnecke et al. 2009a). Linear correlation of FEDSS and mRS at 3 months, independent of gender, age, or NIH-SS at admission

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Warnecke et al.’s study referenced above, the probability of endotracheal intubation in the post-stroke acute stage increased by nearly 2.5 times with each additional point scored in the FEDSS (Warnecke et al. 2009a). In another observational study of 100 acute stroke patients, seven patients presented with severe dysphagia with the penetration or aspiration of saliva. Of these patients, five later required intubation. By contrast, intubation was required in five of the 93 patients with an FEDSS 10 (Dziewas et al. 2008b). While the FEDSS has been designed for the initial focused dysphagia assessment of acute stroke patients, dysphagic patients should be followed up with a subsequent FEES according to Langmore’s standard protocol (see chapter 3), Here, FEES is well-suited for closely monitoring the course of post-stroke dysphagia, the severity of which can change rapidly (despite often going unnoticed clinically), especially in the first few days to weeks after the onset of a brain injury. In addition FEES provides insights into the related pathophysiology of swallowing impairments which will help to individualize dysphagia treatment. An early recognition of improved swallowing function—which, in turn, may lead to a change in the patient’s diet—is equally supported by FEES, as is the timely detection of a critical deterioration of swallowing function, which then gives rise to an immediate initiation of appropriate protective measures (Leder 1998; Warnecke et al. 2006). From a clinical point of view, it is worth mentioning that a nasogastric feeding tube should not be removed to perform FEES in acute stroke patients. In a prospective study that included 25 acute stroke patients and used FEES both with and without feeding tubes in immediate succession, no significant differences in the frequency or extent of relevant pathological findings (pooling of secretions, premature spillage, residue, penetration, aspiration) between the two study conditions could be found. There was therefore no evidence that feeding tubes lead to a clinically relevant impairment of swallowing in acute stroke patients (Dziewas et al. 2008a). Whether the consistent use of FEES in the stroke unit has a measurable impact on relevant clinical endpoints—such as the incidence of pneumonia and global functional outcome—cannot currently be assessed conclusively due to the lack of pertinent studies. In a prospective randomized—albeit small—study (n = 126) comparing dysphagia assessment with either FEES or VFSS, pneumonia occurred less often in the subgroups of stroke patients who were managed with FEES than in those managed with VFSS, although this difference just failed to be significant (Aviv 2000). In addition, in a recent study that recruited stroke patients (n = 220) and adopted a pre-post-design, Bax et al. demonstrated that providing a FEES service on a stroke unit reduced the incidence of post-stroke pneumonia (from 12% to 7%), increased the use of instrumental dysphagia diagnostics (from 6% to 38%), decreased the latency from admission to instrumental diagnostics (from 10.5 days to 2.3 days), and increased the proportion of patients who left the hospital on a regular diet (from 49% to 62%; Bax et al. 2014). However, because this study involved retrospective data collection with a historical control group, the validity of the results is limited.

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253

FEES is a reliable, safe, easy-to-learn tool for dysphagia assessment in acute stroke patients that can be used repeatedly during the course of the disease. The FEDSS allows for a clinically meaningful, multi-level grading of stroke-related dysphagia during the acute stage of the illness and is followedup by a FEES according to the standard protocol that is instrumental in individualizing the patients’ dysphagia treatment.

6.2

Intensive Care Unit

This section deals with the clinical significance of dysphagia in the field of (neuro-) intensive care. First, the incidence and pathophysiology of dysphagia are described; subsequently, a presentation of the possible application of FEES in this context is given.

6.2.1 E  pidemiology and Complications of Critical Illness Dysphagia Dysphagia is an extremely common symptom in intensive care medicine that can occur as a result of various disorders. Studies in medical and anesthesiological/surgical intensive care units have shown that 50–70% of all patients suffer from impaired deglutition (Ajemian et al. 2001; Skoretz et al. 2010). In a recent study on neurological intensive care patients, the incidence of dysphagia proved to be over 90% and persisted in half of the affected patients until their discharge from the hospital (Macht et al. 2013). Brodsky et  al. found persisting dysphagia in 25% of ARDS survivors, even after 6  months (Brodsky et  al. 2017). The finding that dysphagia in intensive care patients is most severe and is accompanied by silent aspiration in 10–20% of patients is of particular relevance (Ajemian et al. 2001; Barquist et al. 2001; El Solh et al. 2003). Regardless of the diagnostic spectrum analyzed, dysphagia in critically ill patients is a significant predictor of complications, especially of aspiration pneumonia and re-intubation, and is a key determinant of lengths of hospitalization and patients’ outcome (Macht et al. 2011).

6.2.2 Etiology and Pathophysiology of Critical Illness Dysphagia The causes of dysphagia in the critically ill can be divided into three etiological categories. Thus, dysphagia 1 . may be associated with the main diagnosis leading to ICU treatment, 2. may be due to pre-existing comorbidities, and 3. may be a consequence of the ICU treatment itself. In most patients, however, more than one etiology plays a role, which is particularly true for the neurologically ill.

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6  Using FEES in the Stroke Unit and the Intensive Care Unit

Ad (1) As shown in Fig. 6.7, various neurological disorders that typically require treatment in the ICU affect the swallowing network or the associated downstream nerves and muscles. For example, depending on their location, strokes and inflammatory diseases of the CNS can lead to a disturbance of the supramedullary or medullary control of swallowing. Guillain–Barré syndrome (GBS) as well as critical illness polyneuropathy (CIP) cause dysphagia by impairing motor- and sensory cranial nerve function. Finally, diseases of the swallowing musculature itself, such as inflammatory myositis or critical illness myopathy (CIM), in addition to neuromuscular transmission disorders lead to myogenic dysphagia. Ad (2) Apart from the main diagnosis (e.g., acute stroke, GBS, brainstem encephalitis; see (1)), pre-existing comorbidities also play a role in this context. A wide range of neurodegenerative (e.g., Parkinson’s disease, Alzheimer’s disease), neurovascular (stroke, subcortical arteriosclerotic encephalopathy), and neuromuscular disorders (Polymyositis, ALS) should be mentioned here. These disorders either are associated with pre-­existing dysphagia or—even if previously asymptomatic with regard to deglutition—increase the likelihood of a deterioration of the swallowing function during ICU treatment. Thus, although a given patient may be admitted to the ICU due to urosepsis or myocardial infarction, the further clinical course might deteriorate because decompensation of the swallowing network leads to complications.

Cortex

Stroke Encephalitis ADEM

Medulla oblongata swallowing centre

CIM Myasthenia Gravis Myositis

Cranial nerves

Afferents

V IX X

Sensory input

Brainstem swallowing centres

Organisation

Cranial nerves V, VII, IX, X, XII Spinal nerves C1-C3

Motor activity

Swallowing musculature CIP GBS

Sensory receptors in oropharynx, larynx and oesophagus

Fig. 6.7  Pathophysiology of dysphagia in (neuro) critical care, ADEM Acute demyelinating encephalomyelitis, CIM Critical illness myopathy, CIP Critical illness polyneuropathy, GBS Guillain-Barré syndrome

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255

Ad (3) ICU-related dysphagia may also be caused by the treatment itself and/or by additional environmental conditions. As shown in Fig. 6.8, six pathomechanisms can be differentiated (Macht et al. 2013). The endotracheal tube, the tracheal cannula, laryngeal masks, nasogastric tubes, and tracheal suction probes can lead to various injuries of the pharynx, larynx, or esophagus. In addition to mucosal erosions, there can be vocal cord lesions, arytenoid dislocations, tongue swelling, and compression-induced disorders of the recurrent laryngeal nerve and the lingual nerve. Second, intensive care patients often develop a weakness of the swallowing muscles. Alongside the above-mentioned CIP and CIM, which are sometimes associated with long-lasting dysphagia, inactivity atrophy of the swallowing muscles can also be observed in intensive care patients exposed to longterm ventilation. The third mechanism is the development of oropharyngeal and laryngeal sensory deficits. This condition may—among others—be the result of sensory nerve damage due to CIP or of a local mucosal edema followed by a disruption of the sensory feedback. Fourth, qualitative and quantitative disturbances of consciousness—either as an effect of sedative medication or due to delirium—can contribute to the development of dysphagia in intensive care patients. For example, a recent study found that patients who were not fully oriented had about a one-third greater risk of aspiration than did patients without an altered mental status (Leder and Suiter 2009). It should also be kept in mind that patients with reduced vigilance or an impaired ability to cooperate due to delirium are hardly able to participate in or benefit from swallowing therapy. Fifth, in addition to the above-mentioned disorders that lead to impaired oropharyngeal swallowing, gastroesophageal reflux is of great importance in critically ill patients. This condition is aggravated in the intensive care setting by the use of both sedative medication and tube feeding, during which the patient is kept in

Oropharyngeal and/or laryngeal trauma

Critical-Illness-Neuro-/ Myopathy

Gastropharyngeal reflux

Altered sensorium

Reduced pharyngeal/ laryngeal sensation

Poor coordination of breathing and swallowing

Fig. 6.8  Causes of dysphagia in intensive care patients. (Reproduced with permission from (Schwab et al. 2015). © 2015 Heike Blum)

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a supine position (Metheny et al. 2006). In addition to preventing the patient from receiving a sufficient supply of nutrients, reflux is particularly dangerous because it predisposes patients to tracheal aspiration. Finally, patients in the ICU often suffer from a dyssynchronization of breathing and swallowing. Under physiological conditions, swallowing and breathing are not independently controlled but rather closely coordinated at the level of the brainstem. Swallowing is regularly integrated into the expiration phase of the respiratory cycle (Boden et al. 2009). During swallowing and for a short time afterward, respiration stops (so-called swallowing apnea), after which the expiration ends before the next respiratory cycle begins with a subsequent inspiration. This additional protection against aspiration is considerably limited in patients with respiratory impairment and concomitant tachypnea since the duration of the swallowing apnea is reduced and the coordination of the respiratory cycle and swallowing is disturbed (Shaker et al. 1992; Gross et al. 2009). Dysphagia is a typical clinical symptom in intensive care units and is found in over half of all long-term ventilated patients. The most relevant etiologies include CIP and CIM, pre-existing neurogenic dysphagia, acute neurovascular or neuromuscular disorders associated with dysphagia as a major symptom, and tracheotomy-related pharyngeal sensory loss.

6.2.3 Applications of FEES in the ICU As outlined above, in the ICU dysphagia is characterized by a high prevalence and diverse etiologies. In this complex clinical context, the use of FEES enables a more precise diagnosis of swallowing impairments and aspiration (Donzelli et al. 2001; McGowan et  al. 2007). In order to avoid any additional aspiration in clinically unstable patients with suspected severe dysphagia, FEES in the ICU can be performed with a very conservative approach known as the Ice Chip Protocol (Langmore 1996, Pisegna and Langmore 2018). This examination begins with an anatomical and physiologic assessment of secretions, sensation, anatomy, and structural movement (see Sect. 5.2.6). Particular focus is the spontaneous swallow rate of the patient (norm = 2–4/min), the extent of pharyngolaryngeal saliva pooling, the patient's response to saliva penetration/aspiration and to touch with the tip of the endoscope, and the patient’s ability to swallow his own secretion (Murray et al. 1996; Langmore and Aviv 2001). Following these observations, the patient’s ability to swallow is evaluated, using ice chips as the first bolus to be swallowed. The rationale for this is that small amounts of water are considered the safest medium for aspiration because they are rapidly cleared by the lungs’ self-cleaning mechanisms and contain relatively few pathogenic microbes (Langmore 1996). An ice chip (i.e., frozen water) has the advantage of representing a solid bolus that can be better controlled by the tongue as compared with liquid water. It also creates a stronger sensory stimulus for triggering the swallowing reflex due to its cold temperature. The patient is given several trials of ice chips to see if this stimulus can waken the swallowing response; often the swallow will become more brisk over the trials. If it does improve over

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257

time, the protocol can move to other consistencies (puree, solid food, liquids); alternatively, if the swallow does not improve, and aspiration is frequent, the protocol may stop at this point (Langmore 1996; Pisegna and Langmore 2018). Diagnostic Algorithms for Intensive Care Dysphagia Management Similar to the situation in the stroke unit detailed above, FEES can be used in the intensive care unit to establish a precise diagnosis of dysphagia and to guide treatment. Specifically, FEES provides guidance with regard to (1) airway protection (intubation, tracheotomy), (2) nutritional management (oral feeding, nasogastric tube, PEG), and (3) rehabilitative treatment strategies. Hafner et al. (2008) reported on a total of 913 FEES procedures in 553 patients treated in different ICUs in a maximum-­care hospital over a 45-month period. As a result of an endoscopic swallowing evaluation, 6.3% of patients were tracheotomized for airway protection, 49.7% received a nasogastric tube, and 13.2% underwent PEG for artificial feeding. An oral diet could be started in 30.7% of patients. The following section offers suggestions for dysphagia management in non-­ intubated and tracheotomized ICU patients.

6.2.3.1 Non-intubated Patients In non-intubated ICU patients, dysphagia assessment provides important information for determining the appropriate feeding strategy and is also instrumental in guiding further protective and rehabilitative measures. Although there is currently no standardized algorithm that has been evaluated in prospective studies, the algorithm proposed in Fig. 6.9 takes the advantages and disadvantages of the various diagnostic modalities described above into consideration and implements existing knowledge to provide pragmatic recommendations. This proposal takes the limited validity of aspiration screening and the clinical swallowing examination into account and therefore suggests that FEES play a correspondingly central role. First, minimum basic requirements for an oral diet, such as a sufficient state of consciousness and trunk stability, are evaluated. If these conditions are satisfied, the presence of specific risk factors for dysphagia should be checked. As mentioned above, apart from the patient’s main diagnosis, relevant comorbidities also need to be considered here. Since dysphagia is at least in part a typical side effect of the ICU treatment itself (as described previously), the duration of intubation and artificial ventilation with a cut-off value of 24 h is introduced as an additional criterion. If none of these risk factors is present—such as in a patient with an uncomplicated surgery followed by a quick extubation—it is sufficient to carry out a simple bedside aspiration screening. If this test is normal, the patient may proceed directly to an oral diet. If indicators of dysphagia are present during any of the three steps described above, a clinical swallowing examination by an SLP and—ideally—a FEES should be performed. With the help of these diagnostic procedures a decision whether the patient can receive a normal oral diet, requires a modified diet, is in need of tube feeding, or should be considered as a candidate for intubation to secure the airway can be made.

pathological

Normal oral diet

Fig. 6.9  Dysphagia management in the intensive care unit

Normal oral diet

normal

Criteria ability to drink total amount loss of oral bolus changes of voice coughing during or up to 3 minutes after swallowing

Water-Swallowing-Test

no

no

NPO, Nasogastral tube & SLP therapy

SLP assessment & FEES

Adapted diet & SLP therapy

yes

pre-existing dysphagia pre-existing diseases associated with dysphagia acute disease associated with dysphagia intubation > 24 h

Risk factors?

yes

in cardio- and respiratory stable condition stable posture able to stay awake for a minimum of 15 minutes arbitrary coughing able to swallow own saliva

Requirements for an oral diet fullfilled?

Non-intubated ICU-patient

Intubation

258 6  Using FEES in the Stroke Unit and the Intensive Care Unit

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259

6.2.3.2 Tracheotomized Patients The tracheostomy, and particularly the minimally invasive dilatational approach, is now a standard procedure in most intensive care units. Therefore, in the majority of long-term ventilated patients this artificial airway is used today. After the patient has been successfully weaned from the respirator, the question arises as to whether the tracheal cannula can be removed. In light of the highly prevalent and often severe dysphagia in the critically ill, a standardized diagnostic procedure is also required here. In principle, the following three methods come into consideration: 1. A clinical swallowing examination is usually performed as the first diagnostic step on cannulated ICU patients who have been weaned from the ventilator. After careful suctioning, the cuff is first deflated, and a physiological airflow is thereby restored. In addition, if tolerated by the patient, the tracheal cannula is capped with a speaking valve. This procedure is followed by a standard swallowing examination that looks for clinical signs of penetration and aspiration of saliva and administered food. Consistent with the low reliability of clinical swallowing examinations in detecting these events in other patient cohorts—as has been demonstrated in numerous studies—Hales et al. (2008) found a sensitivity of only 66% (combined with a specificity of 91%) for this procedure compared with FEES in a prospective study of 25 tracheostomized ICU patients. Therefore, during the process of weaning a patient from a tracheotomy tube, the clinical swallowing examination needs to be augmented with more valide test procedures. 2. The so-called modified Evans blue dye test (mEBDT) is another clinical tool that has been put into practice (Peruzzi et  al. 2001). To carry out the mEBDT, the tracheotomy cannula is first unblocked and carefully suctioned. Subsequently, the patient receives small amounts of colored liquid and possibly other food consistencies per os. After swallowing, the tracheal cannula is suctioned again. If stained secretion is seen here, aspirated, there is proof previous of aspiration. Although this approach is commonly used in everyday clinical’s practice due to the low personnel and logistical effort required, its sensitivity has been shown to be insufficient in several studies. For example, in two small studies (Brady et al. (1999), n = 20; Donzelli et al. (2001), n = 14), false negative findings occurred in 50% of patients, in whom aspiration was demonstrated with VFSS and FEES, respectively. For the mEBDT, Peruzzi et al. (2001) found a sensitivity of 38% and a specificity of 100% in an etiologically heterogeneous cohort of 20 patients. These results were confirmed in a recent meta-analysis (Béchet et  al. 2016). Only Belafsky et al.’s (2003) study featured a sensitivity of 82% for clinical screening; however, the specificity dropped to 38% due to a modified test procedure in which subglottic suctioning was performed not only directly after the swallowing examination but also 30 and 60 min later. In light of these studies, the mEBDT should be classified as a screening instrument that can be used to guide further instrumental evaluations (see below). The exclusive use of the mEBDT to assess swallowing ability in tracheotomized patients is not recommended. 3. Due to the described limitations of the clinical procedures, the swallowing assessment should also include FEES in this context. In order to increase the

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reliability and reproducibility of the endoscopic examination, a standardized, step-by-step approach is available (SESETD-protocol; Standardized Endoscopic Swallowing Evaluation for Tracheostomy Decannulation in critically ill neurologic patients) (Warnecke et al. 2013, Warnecke et al. 2020). After deflating the tracheal cuff, pharyngeal and subglottic secretions are first cleared by careful suctioning. As shown in Fig. 6.10, the extent and localization of saliva pooling are assessed, and the spontaneous swallowing frequency is observed (Fig. 6.10). In order to gain the most accurate possible impression of a patient's secretion management and to precisely evaluate the amount of remaining pooled saliva and the resulting protective mechanisms, this examination step should take 2–4 min. In the event that massive pooling of saliva with silent penetration or aspiration is observed, the tracheotomy tube cannot be removed and should be blocked again. If there is no massive pooling of pharyngeal secretions but the spontaneous swallowing rate is less than 1/min or there is strong evidence of pronounced pharyngeal muscle weakness evidenced by a very weak or missing whiteout during the swallow, the tracheal cannula should also remain in situ. However, as in the following steps, it is possible to restore the physiological airflow via an intermittent deflation of the tracheal cannula’s cuff, which thereby helps to improve laryngeal sensory feedback. In the next step, laryngeal sensation is examined by lightly and briefly touching the arytenoids bilaterally. If no motor reaction can be provoked, a critical sensory disturbance must be assumed, and decannulation should therefore be postponed. If the patient coughs or swallows—or at least shows reflexive movements such as the adduction of the FEES-PROTOCOL

MAIN FINDINGS Massive pooling of saliva, silent penetration/aspiration of saliva

DECANNULATION?

1)

Secretions

2)

Spontaneous swallows

< 1 per minute missing “whiteout”

no

3)

Laryngeal sensibility/ cough

Anästhesia no effective cough

no

4)

Pureed consistency

Silent aspiration of complete bolus

no

5)

Fluids

Silent aspiration without triggering of swallowing reflex

no

6)

Transstomatal examination

no

Massive subglottic pooling of saliva, silent aspiration of complete bolus

no

No evidence of main findings

yes

Fig. 6.10  Endoscopic decannulation protocol

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arytenoids or a pharyngeal wall contraction—the swallowing function itself should be investigated in the next steps. For this purpose, the patient should first receive a semisolid food consistency, such as colored jelly. If the bolus is aspirated completely and without triggering any protective reflexes, the decannulation should be postponed. If the patient succeeds in at least partially swallowing the bolus, a teaspoon of fluid is subsequently tested. Again, complete bolus aspiration should preclude the removal of the tracheotomy tube. If, on the other hand, an at least partially efficient swallow is triggered, the tracheal cannula may be removed for the final examination step, which is the trans-stomatal examination. In this step, the endoscope is inserted through the tracheostoma into the trachea such that the examiner can look downward onto the bronchial system and upward onto the subglottic region (Fig. 6.11; Donzelli et al. 2001). From this position, intra-deglutitive aspiration that may have occurred during transnasal videoendoscopy at the time of whiteout and that may thus have escaped the examiner’s view can be directly detected (intra-deglutitive aspiration occurs when food boli enter the trachea through the glottis at the same time that the larynx is elevated and the pharyngeal constrictors are activated; Fig.  6.11). In addition, anatomical airway obstruction—such as a subglottic hematoma or fractured cartilage rings that protrude into the airway and present an obstacle to safe decannulation—can be detected. If this final examination step also fails to provide any evidence of salivary or massive food-bolus aspiration and no structural obstacles to decannulation have been detected, the tracheal cannula may be removed. The use of this algorithm in 100 tracheostomized neurological intensive care patients who had been weaned from the ventilator enabled more than half of them to be safely decannulated (Warnecke et al. 2013). In the further course of treatment, only one patient had to be recannulated. It is also noteworthy that a clinical swallowing examination—which took into account the parameters of “state of consciousness,” “ability to cooperate,” “saliva swallowing,” “cough reflex,” and “the amount of secretion suctioned through the tracheal cannula”—would have only allowed for the removal of the tracheal cannula in 27 patients (Warnecke et al. 2013). Regarding this decannulation algorithm, it is worth mentioning that in the original publication, all patients who fulfilled the criteria of Steps 1–3 also passed Steps 4 and 5, indicating that these steps did not provide any information with regard to the possibility of decannulating the patient. For this reason, in the clinical context, the FEES decannulation algorithm may be performed without Steps 4 or 5, as was the case in the PHAST-TRAC trial (Dziewas et al. 2018). Steps 4 and 5 of the decannulation algorithm do, however, provide important information for nutritional management after tube removal.

In the (neurological) intensive care unit, FEES enables a reliable assessment of dysphagia and provides guidance for the management of swallowing disorders. The clinically important and common question of whether a tracheotomized patient who has been safely weaned from the respirator should be decannulated can be reliably answered with the help of FEES.

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Tracheal cannula

a

b

c Fig. 6.11  Trans-stomatal swallowing endoscopy (© 2012/2017 Heike Blum). The photos on the right depict the respective endoscopic perspective. (a) Tracheal cannula in situ. (b) The tip of the endoscope is directed downward providing a view on the bronchial system. (c) The tip of the endoscope points upward and provides an overview of the subglottic region. Reproduced with permission

References

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Wade DT, Hewer RL. Motor loss and swallowing difficulty after stroke: frequency, recovery, and prognosis. Acta Neurol Scand. 1987;76:50–4. Warnecke T, Dziewas R, Oelenberg S, et al. Serial fiberoptic examination of swallowing in patients with acute stroke and dysphagia: case report and general considerations. J Stroke Cerebrovasc Dis. 2006;15:172–5. Warnecke T, Teismann I, Meimann W, et  al. Assessment of aspiration risk in acute ischaemic stroke – evaluation of the simple swallowing provocation test. J Neurol Neurosurg Psychiatry. 2008;79:312–4. Warnecke T, Ritter MA, Kroger B, et al. Fiberoptic endoscopic Dysphagia severity scale predicts outcome after acute stroke. Cerebrovasc Dis. 2009a;28:283–9. Warnecke T, Teismann I, Oelenberg S, et  al. The safety of fiberoptic endoscopic evaluation of swallowing in acute stroke patients. Stroke. 2009b;40:482–6. Warnecke T, Teismann I, Oelenberg S, et al. Towards a basic endoscopic evaluation of swallowing in acute stroke – identification of salient findings by the inexperienced examiner. BMC Med Educ. 2009c;9:13. Warnecke T, Suntrup S, Teismann IK, Hamacher C, Oelenberg S, Dziewas R.  Standardized endoscopic swallowing evaluation for tracheostomy decannulation in critically ill neurologic patients. Crit Care Med. 2013;41(7):1728–32. Warnecke T, Im S, Kaiser C, Hamacher C, Oelenberg S, Dziewas R.  Aspiration and dysphagia screening in acute stroke  - the Gugging Swallowing Screen revisited. Eur J Neurol. 2017;24(4):594–601. Warnecke T, Muhle P, Claus I, Schröder JB, Labeit B, Lapa S, Suntrup-Krueger S, Dziewas R. Interrater and test-retest reliability of the standardized endoscopic swallowing evaluation for tracheostomoy decannulation in critically ill neurologic patients. Neurol Res Pract. 2020;2:9. Warner HL, Suiter DM, Nystrom KV, Poskus K, Leder SB. Comparing accuracy of the Yale swallow protocol when administered by registered nurses and speech-language pathologists. J Clin Nurs. 2014;23(13-14):1908–15. Wirth R, Dziewas R, Jäger M, et al. Klinische Ernährung in der Neurologie – Teil des laufenden S3-Leitlinienprojekts Klinische Ernährung. Aktuel Ernahrungsmed. 2013;38(04):e49–89.

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Treatment of Neurogenic Dysphagia

Contents 7.1  E  vidence-Based Medicine 7.2  G  eneral Treatment Options 7.2.1  Behavioral Swallowing Therapy 7.2.2  Pharmacotherapy 7.2.3  Surgical Treatment Options 7.3  Disease-Specific Therapy 7.3.1  Stroke 7.3.2  Dementia 7.3.3  Parkinson’s Disease 7.3.4  Progressive Supranuclear Paralysis 7.3.5  Multiple System Atrophy 7.3.6  Dystonias 7.3.7  Wilson’s Disease 7.3.8  Huntington’s Disease 7.3.9  Multiple Sclerosis 7.3.10  Tetanus 7.3.11  Brain Tumors 7.3.12  Amyotrophic Lateral Sclerosis (ALS) 7.3.13  Spinobulbar Muscular Atrophy (Kennedy’s Disease) 7.3.14  Guillain–Barré syndrome 7.3.15  Myasthenia Gravis 7.3.16  Myopathies (Including Myositis) 7.3.17  Traumatic Brain Injury 7.3.18  Hereditary Ataxia 7.4  Neurostimulation 7.4.1  Transcranial Magnetic Stimulation 7.4.2  Transcranial Direct-Current Stimulation 7.4.3  Pharyngeal Electrical Stimulation 7.4.4  Neuromuscular Electrical Stimulation References

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Evidence-Based Medicine

Today, the principle of evidence-based medicine (EBM) has become particularly important for decisions regarding therapeutic options. According to Sackett et al. (1997) EBM is the conscientious, explicit, and reasonable use of the best available external scientific evidence in making decisions regarding individualized medical care for patients. The practice of EBM implies the integration of individual clinical expertise with the best available external evidence from systematic research. The Cochrane Library is an information portal that supports evidence-based medicine (http://www.thecochranelibrary.com). The Cochrane Collaboration, a worldwide association of physicians and scientists, publishes systematic reviews of medical therapies. The abstracts of these reviews can be viewed free of charge. The criteria of evidence-based medicine also need to be considered in the field of dysphagia treatment (Prosiegel et al. 2012). The scientific significance of clinical studies is assessed in EBM via evidence levels. Based on these levels of evidence, treatment recommendations are provided and weighted using predefined grading of recommendations. In accordance with the Guideline Manual issued by AWMF and the German Agency for Quality in Medicine (Ärztliche Zentralstelle für Qualitätssicherung; ÄZQ), the following definitions of levels of evidence and grades of recommendations are used in this chapter (Arbeitsgemeinschaft der Wissenschaftlichen Medizinischen Fachgesellschaften (AWMF) ÄZQÄ 2001): Evidence Levels

Ia. Evidence from a meta-analysis of at least three randomized controlled trials (RCTs) Ib. Evidence from at least one randomized controlled trial or a meta-­analysis of less than three RCTs IIa. Evidence from at least one methodically sound controlled study without randomization IIb. Evidence from at least one methodically sound quasi-experimental descriptive study III. Evidence from methodically sound non-experimental observational studies (e.g., comparative studies, correlation studies, and case studies) IV. Evidence from reports of expert committees or expert opinion and/or clinical experience of recognized authorities

Grades of Recommendation

A. At least one randomized controlled trial of generally good quality and consistency that is directly related to recommendation and has not been extrapolated (Evidence Classes Ia and Ib).

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B. Well-conducted clinical—but non-randomized clinical—trials directly related to recommendation (Evidence Classes II or III) or an extrapolation of Evidence Class I if there is no relation to a specific issue. C. Reports from experts, expert opinions, and/or clinical experience of recognized authorities (Evidence Class IV) or extrapolation from Evidence Classes IIa, IIb, or III. This classification indicates that directly applicable clinical trials of good quality were not available.

One of the major future challenges in the field of dysphagia research lies in conducting high-quality randomized controlled trials that evaluate the effectiveness of different procedures and interventions of swallowing therapy.

7.2

General Treatment Options

Speech and language pathologists (SLP) can resort to a variety of different methods (the generic term used in the following text is “behavioral swallowing therapy”) when treating neurogenic dysphagia with the primary goals of identifying a safe diet (minimizing risk of aspiration) and maintaining sufficient nutrition, hydration, and weight for the patient. Depending on the neurological condition causing dysphagia and the patient’s wishes, the most appropriate therapeutic components of the behavioral treatment approach can vary greatly between individual cases (Sect. 7.3). In addition, specific drugs and/or surgical procedures are available for certain forms of neurogenic dysphagia. In the case of etiologically unexplained dysphagia, the final therapeutic strategy is determined jointly by the SLP and the treating physician, and it is therefore of utmost clinical importance to carry out a comprehensive diagnostic workup, as is usually done with every unclear neurological syndrome (Sect. 4.1.13). Even if the cause of dysphagia cannot be initially determined, an etiological reevaluation should be considered in the further course of treatment. The optimal therapy of neurogenic dysphagia involves close interdisciplinary cooperation among neurologists, SLPs, nutrition experts, nursing staff, physiotherapists, occupational therapists, and social services as an essential prerequisite in both inpatient and outpatient settings (Prosiegel et al. 2012). The following sections of this chapter present an overview of the principles and procedures of the behavioral treatment options. Afterward, the current scientific evidence is outlined, and evidence-based recommendations for these behavioral treatment options of neurogenic dysphagia are provided. The remainder of this chapter describes the general outline of pharmacological and surgical therapies for neurogenic dysphagia. Section 7.3 presents studies in which the efficacy of behavioral procedures or pharmacological or surgical interventions have been studied specifically for individual neurological disorders (e.g., stroke or Parkinson’s disease). Finally, Section 7.4 provides an overview of neurostimulation procedures in the treatment of neurogenic dysphagia.

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7.2.1 Behavioral Swallowing Therapy In German-speaking countries, behavioral therapies such as Kay Coombes’ Facial-­ Oral Tract Therapy (F.O.T.T.®) and Castillo Morales’ orofacial regulation therapy (ORT) as well as the so-called functional dysphagia therapy (FDT) are often used. Berlin-­based SLP Ricki Nusser-Müller-Busch has contributed significantly to the widespread use of F.O.T.T.® in neurological diseases and authored a comprehensive work on this topic (Nusser-Müller-Busch 2010). F.O.T.T.® is based on the Bobath approach and can in principle be applied a in all neurological diseases in both the intensive care unit and the stroke unit as well as in inpatient and outpatient rehabilitation. An essential goal of F.O.T.T.®, which is a holistic treatment concept involving doctors, nurses, physiotherapists, and occupational therapists, is to facilitate patients’ communicative abilities, food intake, and swallowing. It may also be used with non-cooperative, semiconscious, or unconscious patients. FDT, which was mainly developed and researched by Munich-based SLP Gudrun Bartolome, differs from the other mentioned treatment methods in its functional and problem-oriented approach. FDT selects interventions according to the concrete pattern of neurogenic dysphagia that is present in a given patient. Furthermore, FDT aims to employ methods that have been shown to be effective in appropriate studies or are at least to be reasonable from a pathophysiological point of view. The term FDT is not commonly used in Anglo-American research (Bartolome and Schröter-Morasch 2013). In the USA, these more functional and holistic methods of swallowing therapy are not common. Most SLPs throughout the world do adhere to the following therapies, however. Behavioral swallowing therapy consists of restorative, compensatory, and adaptive techniques. 1. Restorative techniques are intended to restore impaired swallowing functions or to promote residual functions. This is done via pre-swallow stimulation (e.g., thermal stimuli), mobilization techniques (e.g., pressing the tongue against  a spatula), and specific motor exercises (e.g., the Shaker exercise (raising and lowering the head in a lying position at certain intervals) or the Masako maneuver (holding the tip of the tongue between the lips/teeth during swallowing)). Restorative methods include neuromuscular electrical stimulation (NMES). The swallowing muscles are synchronously contracted by stimulation of the intact peripheral nerves. Surface electrodes are placed externally on the base of the mouth and on the laryngeal area. A biphasic current is used for the stimulation (frequency: 80 Hz; Bartolome and Schröter-Morasch 2013). 2. Compensatory techniques are used during the swallow to enable effective and safe deglutition despite functional impairments. A distinction should be made between postural maneuvers and special swallowing techniques. The postural maneuvers include anteflexion of the head during swallowing (“chin-tuck maneuver”), which may be helpful in case of insufficient control of the oral bolus, reduced retraction of the base of the tongue, or a delayed swallow reflex. Table  7.1 describes various swallowing techniques (Table  7.1; Bartolome and Schröter-Morasch 2013).

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Figure 7.1 illustrates the key effects of different swallow maneuvers. (1) The effortful swallow consists of an increased activation of the swallowing muscles that leads to a rise in tongue pressure and related bolus propulsion force. (2) In super supraglottic swallowing, after a deep inhalation, the airway is closed to avoid aspiration and—in the case of penetration—can be transported out of the laryngeal vestibule by subsequent coughing. (3) The Mendelsohn maneuver helps lift the larynx and allows the bolus to slide more easily through the upper esophageal sphincter, which is opened longer and to a larger extent. 3. Adaptive methods include dietary modifications (e.g., mashed food, thickened liquids), the use of special drinking and eating aids, and assistance while eating (Bartolome and Schröter-Morasch 2013). The use of texture-modified foods and thickened liquids has become a cornerstone of clinical practice to manage dysphagia. The principle behind this approach lies in the assumption that modifying the properties of normal foods and liquids makes them safer and easier to swallow (Steele et al. 2015). For decades, there were no established and universally used terminology and definitions to describe the target consistency recommended for patients with dysphagia and to guide its preparation. Several countries have developed their own taxonomies or classification systems. Only recently the “International Dysphagia Diet Standardisation Initiative” (IDDSI) has been established, which pursues the goal of developing a global standardized terminology and definitions for texture-modified food and thickened liquids for individuals of all ages and in all care settings and cultures (Cichero et al. 2017), as shown in Fig. 7.2. Table 7.1  Special swallowing techniques for treatment of neurogenic dysphagia Swallowing technique “Effortful swallow”: improvement of tongue pressure and bolus transport Supraglottic swallow (SGS): voluntary glottic closure and cleaning of laryngeal vestibule for respiratory protection

Super supraglottic swallow (SSGS): like SGS but emphasizes the tight breath-hold Mendelsohn maneuver (MM): prolongation of laryngeal elevation, improved opening of upper esophageal sphincter

Implementation Instruction for patient: “Try to swallow as effortfully as possible with the full strength of your tongue and throat muscles” Instruction for patient 1.  “Inhale and hold your breath” 2.  “Now, swallow while holding your breath” 3.  “Cough immediately as you end the swallow, without breathing first” 4.  “Swallow again”(optional) Instruction as with SGSM, but breath should be “tightly” held

Instruction for patient: “please swallow but then continue to hold your larynx up for 2 s after swallowing” (patient can receive feedback by touching the larynx with the fingers)

Indication Weak pharyngeal contraction, reduced retraction of base of tongue Delayed swallow reflex with pre-deglutitive aspiration, incomplete laryngeal closure with intra-deglutitive aspiration; aspiration of residue after the swallow

Like SGS but improved protection of laryngeal vestibule Impaired opening of upper esophageal sphincter with post-deglutitive aspiration, reduced hyolaryngeal excursion

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a

b

c

b

c

b

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Fig. 7.1  Special swallowing techniques (© 2017 Heike Blum). Reproduced with permission

The method chosen for the behavioral swallowing therapy in an individual patient depends greatly on the nature of the underlying disease. It is particularly important to differentiate between acute neurological disorders (e.g., a stroke or traumatic brain injury) and chronic progressive neurological disorders (e.g., amyotrophic lateral sclerosis or Parkinson’s disease). In the former disease group, the primary goal in most cases is to correct an impaired swallowing

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Fig. 7.2  IDDSI diet levels (Cichero et al. 2017) FOODS S AN TR

REGULAR

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function, and restorative procedures are thus primarily used in these cases. In the latter disease group, functional improvement of the swallow is less likely achievable by sensorimotor restorative training. In these cases, compensatory and adaptive methods are hence more frequently adopted to preserve functional swallowing and oral nutrition as long as possible despite the progression of neurogenic dysphagia (Bartolome and Schröter-Morasch 2013). In a systematic review that analyzed the evidence available until November 2008, Speyer et al. (2010) concluded that there had only been a relatively small number of meaningful evidence-based studies on the effectiveness of behavioral swallowing therapy. A total of ten high-quality randomized and controlled studies as well as 49 methodologically sound but non-randomized studies could be identified. However, many of these studies included not only patients with neurogenic dysphagia but also or even exclusively patients with dysphagia resulting from ENT (ear, nose, and throat) diseases. Conclusions for the treatment of neurogenic dysphagia can only be drawn from such studies with great caution. There were no data from Evidence Class Ia for any of the behavioral interventions (i.e., a meta-analysis of at least three randomized controlled trials). In a non-systematic, narrative review by Susan Langmore and Jessica Pisegna from 2015, the authors stated: With the field of speech pathology growing and many clinicians creating new treatments for their patients, it is easy to fall into the trap of using a homegrown or popular rehabilitative treatment. However, while it is tempting to use anecdotes, clinical experience and popularized methods, clinicians must remember that the best treatment is one that has not only been tried, but tested. (Langmore and Pisegna 2015, p. 1)

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Compared with the evidence available until November 2008, the situation slightly improved until 2015. Based on the existing literature and following Langmore and Pisegna’s conclusions, there is sufficient evidence for the clinical effectiveness of the following procedures: • Shaker exercise (head-lift exercises while lying) for patients with various dysphagia etiologies, including stroke-related dysphagia • Expiratory muscle strength training for Parkinson-related dysphagia • Mendelsohn maneuver (to some extent) for stroke-related dysphagia However, there is still insufficient evidence for the procedures of the effortful swallow, the Masako maneuver, super supraglottic swallow, tongue strengthening, and Lee Silverman Voice Treatment (Langmore and Pisegna 2015). Finally, the authors wish to emphasize the following facts: The current lack of efficacy for many of the exercises being taught and prescribed to patients with dysphagia should not imply that these should NOT be prescribed. It is simply a reminder that they have not yet been proven to help strengthen swallowing. Further, well-­ designed studies would be extremely helpful to guide clinicians who work with patients with dysphagia. (Langmore and Pisegna 2015, p. 7)

When evaluating the effectiveness of different swallowing interventions, most of the available studies used either FEES or VFSS as a gold standard. Otherwise, clinical dysphagia scores or nutritional parameters served as endpoints. In recent studies, quality of life has also been taken into consideration; however, many studies have methodological shortcomings. In addition, the results of individual studies cannot be generalized or compared with the results of other publications due to the large heterogeneity of the study populations, the therapeutic approaches, and the examination methods (Speyer et al. 2010). The following high-quality (i.e., randomized controlled) trials are available for the non-disease-specific treatment of neurogenic dysphagia or individual neurogenic dysphagia symptoms (evidence class in parentheses): I. Restorative Methods Shaker et al. (2002) investigated the effectiveness of head-lifting exercises (Shaker exercise) in 27 dysphagic patients with an impaired opening of the upper esophageal sphincter. In these patients, dysphagia had been caused by various neurological diseases as well as previous radiotherapy and cardiovascular diseases. There were significant improvements in the anterior-posterior diameter of the upper esophageal sphincter and in the laryngeal elevation in patients treated with the Shaker exercise compared with patients having performed a sham treatment. In addition, a reduction of residue and aspiration was shown (Ib). II. Adaptive Methods: Groher (1987) studied 46 patients with chronic pseudobulbar dysphagia who had been fed with pureed food and liquids prior to the start of the study and who had suffered at least one episode of aspiration pneumonia before. One group of patients (n = 23) continued to receive liquids without restriction, while the other intervention

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group (n = 23) was given thickened liquids. At 6 months, pneumonia occurred significantly less frequently in the intervention group (28 vs. 5; Ib). However, this same author led a study in 1995 where they looked at 212 nursing home residents who were suspected of having feeding or swallowing disorders. Their evaluations showed that only 31% of these residents did indeed have dysphagia, and 91% of the patients with dysphagia were on a diet level below a diet they could safely tolerate. Their diet was upgraded (including the use of thin liquids for many patients) and the patients were followed for 1  month without pneumonia (Groher and McKaig 1995) III. Combination of Various Methods • Hwang et al. (2007) performed a study on 33 ventilated intensive care patients beginning on the second day after their intubation. One group of patients (n = 18) received standard of care, while the other group (n = 15) was treated with a combination of thermal-tactile stimulation, oral stimulation, digital manipulation, and neck mobility exercises as preventive swallowing therapy. After extubation, the treatment group showed better oral and oropharyngeal transit time and oropharyngeal swallowing efficiency than the control patients. There were no significant differences in the percentages of aspiration or swallowing volumes between the groups (Ib). • Robbins et al. (2008) included a total of 515 patients with neurodegenerative diseases in a randomized clinical trial (dementia: n = 260; Parkinson’s disease: n = 154; dementia + Parkinson’s disease: n = 101). Three therapeutic strategies for avoiding aspiration were compared: the chin-tuck maneuver (n = 259), the use of thickened liquid (nectar-like consistency; n = 133), and the use of a different thickened liquid (honey-like consistency). The cumulative pneumonia incidence rate was 11% at 3 months, which was lower than anticipated before the start of the study. However, at the time of primary endpoint assessment, no strategy proved superior in preventing pneumonia (Ib). The following findings regarding the effectiveness of behavioral swallowing therapy in neurogenic dysphagia can be obtained from various other methodologically sound yet non-randomized studies (evidence classes are given in parentheses). Studies conducted exclusively on patients with structural dysphagia due to ENT diseases or ENT surgery are not included here: I Restorative Methods • A single tactile-thermal stimulation of the anterior palatine arches led to an (immediate but only short-term) improved triggering of the swallow reflex and to an improvement in the total bolus transit time in a VFSS study in patients with various neurological diseases (n = 25; IIb; Lazzara et al. 1986). • In addition to conventional swallowing therapy, a surface electromyography biofeedback technique led to improvements in the physiology of swallowing and nutrition in a retrospective VFSS study (n = 10) in patients with chronic dysphagia due to brainstem lesions (strokes and brain tumors; III; Huckabee and Cannito 1999).

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II. Compensatory Methods • Effortful swallowing and the chin-tuck maneuver—but not supraglottic swallowing—reduced the depth of penetration into the larynx and pharyngeal residue in patients with cerebrovascular disease (and ENT tumors) in a videomanometry study (n = 8; IIa; Bulow et al. 2001). • The chin-tuck maneuver resulted in aspiration-free swallowing in 50% of dysphagic patients with pre-deglutitive aspiration as a result of various neurological conditions in a VFSS study (n = 30; IIb; Shanahan et al. 1993). • The chin-tuck maneuver was tested in a randomized crossover study on 47 patients with acquired brain lesions (31 stroke, 16 traumatic brain injury) and videofluoroscopically proven aspiration. During the chin-tuck maneuver, only 55% of patients managed a safe swallow without aspiration (40% avoided pre-­ deglutitive aspiration and 60% avoided intra-deglutitive aspiration). Initially, 51% of the patients displayed silent aspiration, and 48% of these patients continued to show aspiration during the chin-tuck maneuver (IIb; Terré and Mearin 2012). This study points out the need to test a postural maneuver before recommending it to determine if it achieves the desired outcome. • In a VFSS study, head rotation to the paretic side in patients with a unilateral pharyngeal paresis (n = 5) improved pharyngeal bolus transport along the unimpaired side (IIb; Logemann et al. 1989). III. Adaptive Methods • In a VFSS study (n = 31), pureed food consistencies reduced the incidence of aspiration compared with liquids in unilateral vocal fold paresis with aspiration and/or penetration, whereas pharyngeal residue increased (IIa; Bhattacharyya et al. 2003). • In a VFSS study (n = 92), a change in bolus viscosity from liquid to nectar-likeor pudding-like consistencies improved swallowing effectiveness and safety (less penetration and aspiration) both for non-progressive brain diseases and for neurodegenerative diseases (IIa; Clave et al. 2006). • Jelly-like bolus consistencies were swallowed without aspiration in almost all cases in a VFSS study of patients with Parkinson’s disease (n = 25) and in patients with cerebellar ataxia (n = 23) who aspirated on liquids (IIb; Nagaya et al. 2004). • Systematic reviews between 2013 and 2016 examined the effect of liquid thickening on the physiology of impaired swallow response (Andersen et al. 2013; Steele et al. 2015; Newman et al. 2016). According to these studies, liquid thickening reduced penetration and aspiration in patients with oropharyngeal ­dysphagia of different etiologies. The thicker the liquid (from thin to nectar-like and honey-like to even “spoon-thick”), the safer the swallow. However, with increasing levels of viscosity, the risk of oral and pharyngeal residue also increased (Ia). • In another systematic review and meta-analysis of pneumonia associated with thin liquid vs thickened liquid intake in patient who aspirate (Kaneoka et  al. 2017), the authors found no significant difference in incidence of pneumonia in

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patients who aspirated thin liquids but used safety strategies (e.g., chin tuck) compared to patients who only drank thick liquids. IV. Combination of Various Methods • In a VFSS study, sour boli improved the initiation of oral swallowing in stroke patients (n = 19) and in patients with other neurological disorders (n = 8). In contrast to the non-stroke patient group, stroke patients also displayed decreased pharyngeal delay and oral transit time, improved swallowing efficiency, and less aspiration. Increasing the bolus viscosity in both study groups resulted in an increase in oral residue and swallowing frequency as well as a decrease in oral and pharyngeal transit time (IIa; Logemann et al. 1995). • In a large VFSS study (n = 711) involving patients with Parkinson’s disease (n = 228), dementia (n = 351), and Parkinson’s disease + dementia (n = 132), honey-­ like- and nectar-like consistencies resulted in less aspiration than did liquid in combination with the chin-tuck maneuver. The group of Parkinson patients benefited significantly more often than did the other two groups of patients. However, in about half of all patients, no improvement of swallowing safety or efficacy was detectable with either intervention. Patients with severe dementia benefited the least from the treatment (IIa; Logemann et al. 2008). • Functional dysphagia therapy (FDT) allowed 55% of tube-fed neurologically ill patients with severe dysphagia (n = 208) to be upgraded to an unrestricted oral diet (III). Swallowing function was evaluated by means of VFSS and/or FEES (Prosiegel et al. 2002). • Functional dysphagia therapy (FDT) resulted in an improvement in the nutritional status of dysphagic patients with posterior cranial fossa tumors, cerebellar hemorrhages, Wallenberg syndrome, Avellis syndrome, and unilateral vagus nerve paresis (n = 43; III; Prosiegel et al. 2005). • A combination of restorative (direct) as well as compensatory and adaptive (indirect) methods improved swallowing function as assessed by clinical ­parameters in 90% of patients (n = 28) who suffered from cricopharyngeal dysfunction due to various neurological disorders (III; Bartolome and SchröterMorasch 2013). • A combination of restorative as well as compensatory and adaptive methods improved the nutritional status and the reliability of nutritional intake in 84% of patients (n = 66) who suffered from dysphagia due to various neurological disorders (III; Neumann 1993). • In 67% of 58 dysphagic and n.p.o. patients suffering from various neurological conditions, a combination of restorative and compensatory methods enabled oral food intake (III; Neumann et al. 1995). V. Facial-Oral Tract Therapy (F.O.T.T.®): • The Facial-Oral Tract Therapy (F.O.T.T.®) increased the swallowing frequency in the acute phase and improved patients’ ability to swallow and protect the respiratory tract in dysphagic patients with a traumatic brain injury and an intra-

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cerebral hemorrhage (n  =  10). Swallowing function was evaluated clinically (swallowing frequency) and by means of FEES (III; Seidl et al. 2007). To summarize the evidence described in detail above, the following recommendations for the general (disease-independent) behavioral swallowing therapy of neurogenic dysphagia can be derived (level of recommendation in parentheses):

• Head-lift exercises should be used (Shaker exercise) to treat impaired opening of the upper esophageal sphincter or reduced hyolaryngeal excursion (A) (While Antunes and Lunet (2012) concluded in a systematic review from 2012 that the available data on the Shaker exercise is promising yet still insufficient to allow classification as an evidence-based procedure, in their narrative review from 2015, Langmore and Pisegna (2015) classified the available evidence—especially for post-stroke dysphagia and ENT tumors—as sufficient for a recommendation). • The chin-tuck maneuver can be used to avoid pre- and intra-deglutitive aspiration (B). • Head rotation to the paretic side may be helpful in case of unilateral pharyngeal paresis (B). • Effortful swallowing may be recommended to reduce pharyngeal residue (B). • Supraglottic swallowing can be used for protection against pre-, intra-, and post-deglutitive aspiration, but there are no data on its long-term effects (C). • For patients with liquid aspiration, semi-solid food consistencies and thickened liquids may be used to allow aspiration-free swallowing (B) (It should be noted that the use of thickened liquids often results in an inadequate liquid intake (Speyer et al. 2010). Patients dislike this consistency because it alters flavor, creates an artificial feeling in the mouth, and does not quench thirst (Lim et al. 2016). A systematic review concluded that the use of thickened liquids is associated with a decline in quality of life (Swan et al. 2015). In addition, the fact that the thickening of liquids increases the risk of post-deglutitive oral and pharyngeal residue and—according to current data—does not reduce the incidence of aspiration pneumonia has to be taken into account (see above)). • Functional dysphagia therapy (FDT) can generally be recommended for the treatment of neurogenic dysphagia (B). • Facial-Oral Tract Therapy (F.O.T.T.®) can generally be recommended for the treatment of neurogenic dysphagia (C). • Expiratory muscle strength training (EMST) can be used to treat neurogenic dysphagia of various etiologies (Sect. 7.3; B) (Positive evidence is available for patients with Parkinson’s disease, amyotrophic lateral sclerosis, subacute stroke, and presbyphagia. In contrast, no effect of EMST was seen in patients with Huntington’s disease (Sect. 7.3). EMST should be used predominantly within randomized controlled trials (Laciuga et al. 2014)).

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Due to very ambiguous study results, neuromuscular electrostimulation (NMES) of the swallowing muscle is currently not generally recommended as a complementary method to behavioral swallowing therapy for the treatment of neurogenic dysphagia (Sect. 7.4.4; Logemann 2007). In addition, tactile-thermal stimulation of the palatal arches is not recommended because it only has a short-term effect of about 10–30 s as determined from multiple studies (see above). In order to select the most suitable combination of the available therapeutic components, the pathomechanism of the respective type of neurogenic dysphagia needs to be analyzed as precisely as possible. The clinical swallowing examination alone often provides only insufficient information. Instrumental dysphagia diagnostics are thus indispensable in most cases not only for diagnostic reasons but also for therapeutic ones (Logemann et al. 2008). In this context, the two most important instrumental methods for designing a treatment plan and evaluating the effectiveness of the applied therapy are VFSS and FEES.  Both methods are very well-suited to directly visualizing the impact of the different behavioral interventions. FEES has the advantage of time to train and judge an effect. It can also be used to help implement biofeedback procedures in the treatment process. By using synchronous endoscopic visualization of the swallow and maneuvers applied, the patient may gain a better understanding of the nature of the swallowing disorder and potential treatment effects. In addition, behavioral interventions can be easily trained with the patient during a FEES session by jointly observing the endoscopic view on the monitor while practicing (Langmore 2001a, b). In both, an observational study on patients with dysphagia due to ENT tumors and a randomized controlled trial on patients with Parkinson’s disease, additional biofeedback therapy with FEES was shown to effectively reduce aspiration and/or residue (III; Denk and Kaider 1997; Ib; Manor et al. 2013). When selecting suitable behavioral interventions, it is essential to consider the causative neurological disease as well as its dysphagia phenotype. In the vast majority of cases, FEES and/or VFSS are indispensable in providing an adequate analysis of the dysphagia pattern as well as in evaluating treatment effects.

7.2.2 Pharmacotherapy Regarding the pharmacological treatment options for neurogenic dysphagia, disease-­specific drug treatment can be differentiated from non-specific treatment strategies. 1. Disease-specific drug treatment strategies are used when neurogenic dysphagia—as a symptom of a particular neurological disease—is responsive to the specific pharmacotherapy of the disease. Examples include the treatment of myasthenic dysphagia with acetylcholinesterase inhibitors, the treatment of polymyositis-related dysphagia with corticosteroids, and the treatment of Parkinson-­related dysphagia with dopaminergic medication (Sect. 7.3).

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2. In contrast, general drug treatment strategies can in principle be used in all forms of neurogenic dysphagia because they have a non-specific effect on swallowing function, regardless of the pathophysiology of the underlying neurological disease. The following active ingredients may belong to this group: • Amantadine: prophylaxis of aspiration pneumonia; mechanism of action not fully explored, proof of effectiveness thus far only for stroke patients (Sect. 7.3.1). • Levodopa: reduction of the latency of the swallow reflex, effectiveness shown thus far in elderly patients (mean age: 78) with lacunar basal ganglia infarctions and a history of aspiration pneumonia in a randomized double-­ blind controlled trial with crossover design (Ib; Kobayashi et  al. 1996). Whether the administration of levodopa also reduces aspiration pneumonia was not investigated in this study (Sect. 7.3.1). • Inhibitors of angiotensin-converting enzyme (ACE inhibitors): promote protective cough/swallowing and (inconsistent data for) prophylaxis of aspiration pneumonia by inhibiting degradation of Substance P (which stimulates cough- and swallow reflex), proof of effectiveness thus far only for Asian stroke patients (Sect. 7.3.1). While a systematic review demonstrated a reduced risk of pneumonia with ACE-inhibitor therapy (Caldeira et al. 2012), a recent randomized controlled trial in elderly dysphagic tube-fed stroke patients failed to reduce pneumonia with ACE-inhibitor therapy (Caldeira et al. 2012; Lee et al. 2015). • Capsaicin (ingredient of chili peppers): TRPV1 agonist (TRPV1 = transient receptor potential cation channel, subtype 1; formerly vanilloid receptor 1 (VR1) or capsaicin receptor; expressed in nerve endings of ­superior laryngeal nerve and glossopharyngeal nerve). Capsaicin shortens the latency of the swallow reflex and accelerates closure of the laryngeal vestibule. By inhibiting the degradation of Substance P, capsaicin promotes protective coughing/ swallowing and is thereby believed to protect patients from aspiration pneumonia. In a randomized placebo-controlled study, elderly patients (mean age: 81.9) who received capsaicin for 4 weeks before each meal showed a significant improvement of both the swallow and cough reflex as compared with an age-matched control group (Ib). Since this study did not have clinical endpoints, a potential link of these physiological effects to a reduction in adverse clinical outcomes could not be assessed (Ebihara et al. 2005). In a randomized controlled trial in elderly patients with oropharyngeal dysphagia (n = 38; age: >70), a comparable positive effect on the safety of swallowing (improvement on the penetration/aspiration scale) was observed over a 10-day regimen of capsaicin therapy (Ortega et al. 2016). • Piperine (ingredient of black pepper): dual TRPV1/TRPA1 agonist (TRPA1 = transient receptor potential ankyrin 1). In a double-blind interventional controlled study, 40 dysphagic patients (mean age: 75.8; heterogeneous study population: stroke, neurodegenerative diseases, presbyphagia) showed

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a reduction in penetration and an accelerated closure of the laryngeal vestibule after receiving piperine (Rofes et al. 2014). • Botulinum toxin: Injecting botulinum toxin into the musculature leads to an inhibition of the release of acetylcholine at the neuromuscular junction and thereby to a relaxation or paralysis of the respective muscle. In neurogenic dysphagia associated with an impaired opening of the upper esophageal sphincter, injections of botulinum toxin into the cricopharyngeal muscle may cause upper esophageal sphincter relaxation with resulting improved pharyngeal bolus clearance. These injections can be performed either externally (transcutaneous) with or without electromyographic control or internally under visual observation via endoscopy. The effect occurs after 5–10  days and lasts for about 3 months. As a side effect, this treatment can result in a worsening of dysphagia; moreover, vocal fold paresis can occur. Several case reports and case series on this treatment have been published for various neurological disorders, including Parkinson’s disease, multiple sclerosis, tetanus, and oculopharyngeal muscular dystrophy (Sect. 7.3). Randomized controlled trials do not yet exist, as noted in a 2014 Cochrane Review (Regan et  al. 2014). The injection of the botulinum toxin into the swallowing muscles should only be performed by experienced doctors. The injections should be accompanied by behavioral swallowing therapy that is also directed at UES opening. This treatment may also be used prior to cricopharyngeal myotomy to test the potential effectiveness of this surgical procedure (Blitzer and Brin 1997). The following recommendations summarize general pharmacological treatment options for patients with neurogenic dysphagia according to present knowledge: • Amantadine, levodopa, ACE inhibitors, capsaicin, and piperine may have the potential to reduce the frequency of aspiration pneumonia in patients with neurogenic dysphagia. However, a general recommendation for the use of these drugs in the treatment of neurogenic dysphagia cannot currently be given. Amantadine can only be recommended for acute stroke patients with dysphagia being at increased risk of aspiration pneumonia (B). • Injections of botulinum toxin into the upper esophageal sphincter may be performed by experienced physicians to treat cricopharyngeal dysfunction as an alternative to myotomy (C). • Injections of botulinum toxin into the upper esophageal sphincter may be used prior to irreversible cricopharyngeal myotomy (C). • All pharmacological approaches to treat neurogenic dysphagia should be accompanied by long-term behavioral swallowing therapy to achieve the best possible therapeutic effect (A). Finally, pharmacological treatment options are also available for various symptoms associated with dysphagia:

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• Hypersalivation or sialorrhea: Sialorrhea is often the result of reduced spontaneous swallowing and/or neurogenic dysphagia. In addition, drugs used in neurology may cause hypersalivation as a side effect and include pyridostigmine (inhibition of acetylcholinesterase) or clozapine (atypical neuroleptic). To treat hypersalivation, the following pharmaceuticals can be used: amitriptyline (antidepressant with an anticholinergic component), a transdermal scopolamine patch (anticholinergic agent; duration of action: 72 h), a subcutaneous injection of glycopyrronium bromide (anticholinergic agent; only minimal penetration into the central nervous system), and injections of botulinum toxin into the salivary glands (parotid gland and possibly submandibular gland; onset of action after 2–3 days; duration of action: 2–6 months). • Xerostomia (dry mouth): Dry mouth—which often spreads from the oral cavity to the pharynx and esophagus—may interfere with bolus transport and lead to retention along the swallowing tract. Xerostomia can occur as a side effect of medication, including anticholinergics such as biperiden or antidepressants with an active anticholinergic component. In addition, autoimmune disorders affecting the salivary glands (particularly Sjögren syndrome or scleroderma) may result in the socalled sicca symptoms. To treat these conditions, parasympathomimetics such as pilocarpine can be used (pilocarpine hydrochloride tablets; prerequisite: reduced but not completely extinguished saliva production). Neurological disorders are usually not the primary cause of xerostomia (Ney et al. 2009). • Singultus (hiccup): Chronic singultus occurs as an idiopathic or symptomatic form (e.g., due to brainstem lesions). In many cases, it can be successfully treated with a combination of domperidone, a proton pump inhibitor (PPI), and baclofen (IIb; Petroianu et al. 1997). Gabapentin may be effective alone or in baclofen-­ resistant cases either as a substitute for baclofen or as an add-on therapy (III; Petroianu et al. 2000). Blocking the phrenic nerve with a local anesthetic cannot be recommended (Petroianu 1998). • Reflux disease: Gastroesophageal reflux may worsen oropharyngeal dysphagia and should therefore be treated with a proton pump inhibitor in respective patients. Reflux disease may also be the sole cause of dysphagia and in some cases represents a differential diagnosis of neurogenic dysphagia. In addition to classic gastroesophageal reflux, pharyngolaryngeal reflux may also occur and can be assumed if signs of “posterior laryngitis” are found in FEES (erythema and edema of the mucosa on the arytenoid cartilage; Ford 2005). Patients with dysphagia who had been diagnosed with pharyngolaryngeal reflux as the underlying cause displayed a sensory deficit (a so-called posterior inter-arytenoid neuropathy) in a FEESST study (Aviv et  al. 2000; Botoman 2002). Patients with pharyngolaryngeal reflux should be referred to an otorhinolaryngologist and a gastroenterologist for further diagnostics and treatment (Ford 2005). Swallowing Pills in Patients with Neurogenic Dysphagia Thus far, there have been few data on pill swallowing in various forms of neurogenic dysphagia. The extent to which pill swallowing is adversely affected by

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neurogenic dysphagia and how pills/capsules should be optimally designed (e.g., in terms of their size, shape, and surface) to allow them to be safely swallowed remain insufficiently investigated. In a recent survey that recruited patients without neurogenic dysphagia, 54% of respondents reported that they had been prescribed pills or capsules that were too difficult for them to swallow at least once. In up to 4% of the interviewed patients, therapy could not be continued because the pills/capsules could not be swallowed at all. Patients generally preferred medium-sized pills/capsules with a smooth surface (Fields et  al. 2015). In a German survey, 37.4% of respondents said they had had difficulty swallowing their pills/capsules. Of these, 58.8% had modified their pills/capsules in such a way that their potential safety and effectiveness may have been compromised. 9.4% of patients did not continue the therapy. Patients with dysphagia had a 7.9fold increased risk of having problems swallowing their pills (Schiele et al. 2013). Certain swallowing techniques may facilitate the swallowing of pills/capsules (the “pop-bottle method”/“chin-tuck maneuver”; Schiele et al. 2014). In clinical practice (particularly in the geriatric patient population), pills are often crushed, and capsules are opened to facilitate their ingestion. However, this “off label” preparation may distort pharmacodynamics and cause damage to the gastrointestinal tract (Logrippo et al. 2017). One-quarter of all patients with Parkinson’s disease or atypical Parkinson syndromes suffer subjectively from impaired pill swallowing. The difficulty in swallowing pills increases with disease progression and likely contributes to sub-optimal compliance with treatment (Kalf et al. 2011). Schiele et al. (2015) investigated pill swallowing in 52 patients with stroke-related dysphagia in a methodically sound study (mean age: 81; 67.3% women; average time after stroke: 2.4 weeks). Pill swallowing was evaluated with FEES. Four placebos (round, oval, and oblong pills/capsules) each were tested with thickened liquid and milk. Between 40.4% and 43.5% of patients had severe difficulties swallowing the pills. These swallow trials were associated with a worsening of penetration/aspiration and an increase in residue. There was no significant difference between the different placebo types tested. Overall, pill/capsule swallowing with thickened water was safer than swallowing with milk. Compared with FEES, neither patients’ self-assessment nor conventional clinical swallow tests were able to detect difficulties with pill swallowing (Schiele et al. 2015). In patients kept nil per os because of severe dysphagia, drugs should not be given orally until their oral intake has been specifically tested and approved with an instrumental method, such as FEES (Leder and Lerner 2013; Schiele et al. 2015). Finally, in addition to finding the appropriate medium for the pill to be swallowed, the use of an effortful swallow or Mendelsohn maneuver may help the pill traverse the pharynx and reach the UES.

7.2.3 Surgical Treatment Options Cricopharyngeal myotomy can be useful as surgical procedure in the treatment of dysphagia due to impaired opening of the upper esophageal sphincter. The respective muscles (the cricopharyngeal muscle, the lower inferior constrictor pharyngeal

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muscle, and the upper striated esophageal muscle) are longitudinally dissected via an anterior-lateral access path (cutting length: ca. 5 cm). The mortality rate of the procedure is listed in the literature at around 1%, and the complication rate is about 6%. The most important but rare complications are paralysis of the N. recurrens and the formation of a pharyngeal/esophageal fistula. In case of pre-existing unilateral damage of the N. recurrens, the procedure must always be performed on the paretic side in order to avoid bilateral damage to this nerve (Kelly 2000; Prosiegel 2008). Thus far, no randomized controlled trials on cricopharyngeal myotomy in neurogenic dysphagia due to UES dysfunction have been performed. Only uncontrolled case studies have been published and suggest a positive effect in 60–80% of patients. However, the actual benefit is likely to be controversial due to the different indications, outcome parameters, and follow-up periods featured in these case studies as well as due to an assumed publication bias that makes cases of unsuccessful surgery less likely to be published (Singh and Hamdy 2005). In general, prior to performing this type of surgery, the following criteria should be checked and fulfilled: I. Unsuccessful and sufficiently long (about 1 year) behavioral swallowing therapy (especially the Shaker exercise or the Mendelsohn maneuver and/ or the Masako maneuver) II. Videomanometric detection of an opening and relaxation disturbance of the upper esophageal sphincter III. Sufficient hyo-laryngeal elevation present in VFSS IV. No refractory reflux disease In summary, the indication for cricopharyngeal myotomy is difficult and should be made only by an interdisciplinary team of specialists. In the authors’ clinic, the indication is based on an extensive inpatient evaluation using FEES, VFSS, manometry, and gastroenterological as well as surgical consultation. Patients with inclusion body myositis have a particularly good response to cricopharyngeal myotomy according to the published case studies (Sect. 7.3.12; Oh et  al. 2007, 2008). Balloon dilatation of the upper esophageal sphincter may occasionally be considered in interdisciplinary consensus as an alternative to cricopharyngeal myotomy and as a temporary treatment in cases where recovery of the UES may occur. Balloon dilatation was compared with laser myotomy in a randomized controlled pilot study from Sweden. Four dysphagic patients with cricopharyngeal dysfunction were treated in both groups, and the effectiveness of the therapy was measured by videomanometry. The mean pre-operative sagittal diameter of the upper esophageal sphincter was 5.6 mm and rose to 8.4 mm after 6 months. The subjective swallowing difficulties evaluated by a questionnaire decreased, but there were no significant differences in outcomes between the two regimens (Arenaz Búa et al. 2015).

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• Cricopharyngeal myotomy of the upper esophageal sphincter may be recommended for the treatment of primary opening disorders after an appropriate interdisciplinary diagnostic workup (see above; C). • In cases of pre-existing unilateral laryngeal paresis of the N. recurrens, cricopharyngeal myotomy should always be performed on the paretic side to avoid bilateral nerve damage (B)

Neurostimulation procedures aimed at improving swallowing function in patients with neurogenic dysphagia are presented separately in Sect. 7.4.

7.3

Disease-Specific Therapy

This section presents disease-specific therapies for neurogenic dysphagia. Since there is a lack of available clinical data from randomized controlled studies for many neurological conditions, evidence-based recommendations are often not possible. An unmet need for future clinical research is therefore to investigate the efficacy of the various therapeutic methods for specific neurological conditions in randomized controlled trials. This section deals only with neurological diseases for which either scientifically sound studies or meta-analyses devoted to specific treatment modalities of neurogenic dysphagia are available.

7.3.1 Stroke Pharmacological Therapy Dopaminergic agents: Dopamine is one of the most important neurotransmitters of the human CNS and plays a significant role in the nigrostriatal (extrapyramidal motor) system. The impairment of dopamine metabolism as a result of neurodegenerative diseases (e.g., Parkinson’s disease or in strokes involving the basal ganglia) can lead to impaired swallowing. A transgenic mouse model characterized by a lack of D1 receptors typically exhibits impaired food intake in addition to movement disorders (Xu et al. 1994). • Kobayashi et al. (1996) investigated the effect of levodopa on the swallow reflex in a randomized controlled double-blind crossover study of 20 control subjects and 27 dysphagic chronic stroke patients who had previously experienced pneumonia. In the group of patients with a history of pneumonia, levodopa led to a more rapid triggering of the swallow reflex, whereas no levodopa-dependent effects were observed in the control group (Ib). • In a prospective randomized controlled trial, the authors studied the effects of cabergoline (0.25 mg/day; n = 13) and amantadine (50 mg/day; n = 14) or placebo (n = 12) on the incidence of silent nocturnal aspiration in a group of Asian

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patients with chronic stroke (Arai et al. 2003a). Following a 12-week course of treatment, aspiration frequency was significantly reduced in both therapy groups compared with the placebo group (cabergoline: from 100% to 23.1%; amantadine: from 100% to 28.6%; placebo: from 100% to 91.7%; Ib). • Nakagawa et  al. (1999) treated 163 chronic Asian stroke patients with either 100 mg of amantadine (n = 83) or placebo (n = 80) as part of a randomized controlled trial. The primary endpoint of the study was the occurence of pneumonia, and the observation period lasted 3 years. The primary endpoint was reached by 28% of the placebo group and by 6% of the treatment group. This difference was significant (Ib). Although summarized studies provide evidence supporting the use of dopaminergic drugs in dysphagic stroke patients, the fact that a clinically relevant endpoint (pneumonia) was only chosen in one of the cited studies should be considered a limiting factor. In addition, the results were reported in a very brief form, which makes it difficult to assess the scientific quality of the trials and— most importantly—possible side effects. Larger studies are needed to reliably assess the clinical significance of this pharmacological treatment. Capsaicin: Capsaicin stimulates TRPV1 receptors expressed at free nerve endings of the superior laryngeal and glossopharyngeal nerve and leads to an enhancement of the cough- and swallow reflex in animal studies and may be mediated by Substance P (Bergren 1988). • In a proof-of-concept study, the latency of the swallow reflex evaluated with the swallow provocation test (SPT) was chosen as the primary endpoint (Ebihara et al. 1993). Both the patient group (n = 20; chronic stroke or vascular dementia) and the age-matched healthy control group were exposed to water containing increasing concentrations of capsaicin (10–12–10–9  mmol/l) in a placebo-­ controlled design. The authors found a dose-dependent improvement of the pathological swallow reflex latency in the patient group (Ib). • A second study examined the influence of prolonged capsaicin administration on the latency of the swallow reflex (Ebihara et al. 2005). 64 elderly patients with dementia and/or chronic stroke received either a capsaicin tablet (1.5 μg) or placebo for 4 weeks prior to each meal. The main result of the study was a ­significant reduction of the swallow reflex latency and a reduction of the coughing threshold in the treatment group compared with the placebo group (Ib).

Capsaicin appears to be a low-risk approach to stimulating the cough and swallow reflex in dysphagic stroke patients. It should be noted that there have been no studies to date with relevant clinical endpoints (e.g., the incidence of pneumonia); thus, additional randomized controlled trials are needed to assess the potential role of capsaicin in the treatment of stroke-related dysphagia.

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ACE inhibitors: ACE inhibitors are used as a standard therapy for the treatment of arterial hypertension and heart failure. Their mechanism of action is the inhibition of the conversion of angiotensin I to angiotensin II. In addition, ACE inhibitors reduce the degradation of bradykinin and Substance P. Since Substance P reduces thresholds of both the cough- and the swallow reflex in animal studies, administering ACE inhibitors can be considered to strengthen protective reflexes. • Nakayama et al. (1998) studied the influence of ACE-inhibitor therapy on the latency of the swallow reflex in 22 elderly patients with a history of aspiration pneumonia. In a placebo-controlled crossover design, the authors found a significant shortening of the swallow response with ACE-inhibitor therapy in comparison with placebo (2.7 vs. 6.3 s), whereas no therapy-dependent changes could be found in the control subjects (Ib). • A second study chose the spontaneous swallowing frequency independent of food intake as target parameter (He et al. 2004). In a group of elderly patients with a previous episode of aspiration pneumonia (n = 22), the spontaneous swallowing frequency was significantly lower than in an age-matched control group (5.3/h vs. 18.3/h). A subgroup of patients with a previous episode of pneumonia was subsequently treated with ACE inhibitor for 2 weeks, whereupon the spontaneous swallowing frequency significantly increased (13.7/h; IIb). • In a prospective observational study, the impact of ACE-inhibitor therapy on silent nocturnal aspiration was investigated in a group of stroke patients (n = 16; Arai et al. 1998a). A reduction of aspiration was seen in ten of the 16 patients, which was also associated with an increase in Substance P levels in eight patients. On the other hand, there was also an increase in Substance P levels in three of the six patients without an improvement in nocturnal aspiration (IIb). • Another study also examined the relationship between ACE-inhibitor therapy and Substance P levels. Arai et al. (2003b) treated 60 chronic stroke patients with nocturnal aspiration in a randomized trial with either an ACE inhibitor or a placebo. A significant reduction in the proportion of aspiration was found in the treatment group compared with the control subjects (73.8% vs. 8.3%). Substance P levels increased significantly with ACE-inhibitor therapy and differed between patients who had experienced an improvement in aspiration and those who had not. The control group showed no change in Substance P levels (Ib). • By far the largest study on this topic was conducted by Ohkubo et al. (2004). Following the secondary prevention trial PROGRESS, which examined the effect of the ACE inhibitor perindopril on the incidence rate of stroke recurrence, the authors compared pneumonia rates in the study group (n = 3,051) and the placebo group (n = 3054) with a median follow-up of 3.9 years. Treatment with the ACE inhibitor revealed a non-significant relative risk reduction of 19% in comparison with placebo for the entire study population (117 vs. 144 cases of pneumonia; p = 0.09). However, in the subgroup of Asian study participants (n = 2352), a significant 47% reduction in pneumonia rates associated with ACE-­ inhibitor therapy was found (Ib).

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• In addition, five non-randomized Asian studies also found a significant reduction in pneumonia in patients on ACE-inhibitor therapy (IIa; Arai et  al. 1998a, b; Sekizawa et  al. 1998; Okaishi et  al. 1999; Arai et  al. 2005; Harada and Sekizawa 2006). • Consequently, a meta-analysis from 2012 revealed that patients (particularly those from Asia) who had had a stroke had a lower risk of pneumonia with ACE-­ inhibitor therapy (Caldeira et al. 2012). • On the other hand, a multicenter randomized controlled trial in which dysphagic stroke patients who had been put on artificial feeding for more than 2  weeks received either 2.5 mg of lisinopril or a placebo, had to be prematurely discontinued due to an increase in mortality in the intervention group. Furthermore, the incidence of pneumonia was the same in both groups (Lee et al. 2015). Numerous small pilot studies, several larger non-randomized studies, and a meta-analysis suggest that ACE inhibitors can reduce the risk of pneumonia in stroke patients by improving both the cough- and swallow reflex. These findings could not be confirmed in a methodologically sound randomized controlled trial. In addition, there was a different effect in Asian and Caucasian patients. Due to the inconsistent study situation, ACE inhibitors cannot currently be recommended for the prevention of aspiration and related pneumonia in Caucasian stroke patients with dysphagia, but may have an effect in Asian patients.  Oral decontamination: The aspiration of bacterially contaminated saliva has been identified as a major cause of pneumonia in stroke patients. While the physiological oral flora mainly consist of facultatively pathogenic gram-positive bacilli (e.g., alphahemolytic streptococci), gram-negative bacteria (e.g., E. coli, Klebsiella, Proteus, and Enterobacter) are also found in stroke patients and other critically ill patients (Millns et al. 2003). Intensive care medicine has been discussing selective oral and gastrointestinal decontamination as a therapeutic option for the prevention of endogenous infections for many years, and this treatment is commonly used in many sites today (Silvestri et al. 2007). • Gosney et al. (2006) studied the impact of selective oral decontamination in acute stroke patients in an oligo-centric randomized placebo-controlled study. Patients were treated intraorally four times daily for at least 2 weeks with 500 mg of Orabase gel (n = 103) consisting of 2% w/v colistin, 2% w/v polymyxin E, and 2% w/v amphotericin B, or with a placebo (n = 100). This treatment resulted in a reduction of oral gram-negative bacteria compared with placebo. The overall pneumonia rate was low (4%) in the entire study cohort, but there was a significant difference between the groups (study drug: 1%; placebo: 7%; p < 0.05). The mortality rate was unaffected by the treatment and was about 10% within the first 3 months after stroke (Ib). • In a controlled, non-randomized study from Denmark, a combination of the Gugging Swallowing Screen (GUSS) with intensified oral hygiene resulted in a

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reduction of pneumonia in acute stroke patients with moderate to severe dysphagia (Sørensen et al. 2013; IIa). The results of these studies should be interpreted as a first indication of the effectiveness of oral decontamination in acute stroke. In addition to recruiting a larger number of patients, follow-up studies should focus primarily on dysphagic stroke patients since the most likely outcome-relevant therapeutic effects are expected to be shown in this cohort. Brain-Stimulation Methods In recent years, various methods of brain stimulation have reached a methodological level that makes their application in the clinical context of stroke-related dysphagia increasingly practicable (Sect. 7.4). Gow et al. (2004) showed that repetitive transcranial magnetic stimulation (rTMS) in healthy individuals leads to an increased excitability of the pharyngeal motor cortex. A similar effect could be demonstrated for transcranial direct-current stimulation (tDCS; Jefferson et al. 2009a, b). While rTMS and tDCS directly stimulate the cortex, pharyngeal electrostimulation (PES) indirectly induces cortical modulation. As early as in 1998, Hamdy and co-workers demonstrated that PES leads to an increase in the motor representation of the pharyngeal musculature (Hamdy et al. 1998b). • In a randomized placebo-controlled trial, Khedr et  al. (2009) investigated the effect of 5-day rTMS treatment in 26 (14 real-rTMS, 12 sham stimulation) patients with infarctions confined to the middle cerebral artery. In comparison with the sham group, rTMS over the affected hemisphere led to a significant improvement in the clinical dysphagia score, which remained detectable during a follow-up of 2 months (Ib). • In a second study of the same group, rTMS was used in a placebo-controlled design in 22 patients with brainstem infarctions (Khedr and Abo-Elfetoh 2010). The 5-day bilateral stimulation caused a significant improvement in clinically assessed dysphagia severity (Ib) over the 2-month follow-up period compared with sham stimulation. • In a randomized, placebo-controlled, double-blind study of patients with post-­ stroke dysphagia (n = 40), Du et al. (2016) demonstrated that 5-day rTMS at both low- (1 Hz) and high-frequency (3 Hz) resulted in a clinical improvement of swallowing function that also remained detectable at a follow-up of 3  months. However, there was no instrumental dysphagia assessment (Du et al. 2016; Ib). • Kumar et al. (2011b) included 14 patients with supratentorial stroke in a placebo-­ controlled trial. The patients received either tDCS or sham stimulation over the healthy hemisphere for 5 days. Immediately after the last stimulation, the study group showed a significant improvement in clinically determined dysphagia severity in comparison with the sham group (Ib).

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• Three meta-analyses evaluating the effect of direct, non-invasive brain stimulation in patients with post-stroke dysphagia found that both rTMS and tDCS led to a lasting improvement in swallowing performance compared with sham stimulation. However, the patient populations in the studies were small (Yang et al. 2015; Doeltgen et al. 2015; Pisegna et al. 2016; Ia). In one of these meta-­analyses, the stimulation of the unaffected hemisphere displayed a significantly stronger effect than did ipsilesional stimulation (Pisegna et al. 2016). • Hamdy’s group included 28 patients with supratentorial cerebral infarctions in a randomized controlled study that examined the effect of PES treatment on three consecutive days (Jayasekeran et  al. 2010). The severity of dysphagia was assessed clinically and videofluoroscopically at baseline as well as 14 days after stimulation. While patients in the intervention group showed a significant improvement in post-stroke dysphagia, the severity of swallowing impairment remained unaffected in the control group. The hospital stay of the stimulated patients was significantly shorter than that of the sham group (Ib). Definitive conclusions about the effect of PES could not be obtained from another randomized controlled trial (n = 36) due to sub-optimal patient recruitment (Vasant et al. 2016; Ib). • The effect of PES on stroke-related dysphagia was evaluated in a meta-analysis that included data from 73 patients and three small randomized controlled trials. In the PES group, there was a significant reduction in the penetration–aspiration scale (PAS) measured by VFSS as well as in the dysphagia severity rating scale (DSRS) compared with the control group (Scutt et al. 2015; Ia). • Unfortunately, these promising results could not be confirmed in the international multicenter randomized controlled STEPS study, which is the largest PES study to date. 162 dysphagic patients with ischemic or hemorrhagic stroke (mean age: 74; 58% men; 89% stroke; mean PAS score: 4.8) were included and received either PES or placebo on three consecutive days. The primary outcome was PAS at 2 weeks post-treatment measured by VFSS. There was no significant difference between the intervention- and control groups (3.7 vs. 3.6 points). The secondary outcome parameters (including the dysphagia severity rating scale and quality of life at 6 and 12 weeks) also showed no significant differences. There were no serious treatment-related adverse events throughout the trial (Bath et al. 2016; Ib). • In a single-center randomized controlled trial (n = 30), tracheostomized stroke patients with severe dysphagia that precluded decannulation received either PES or placebo treatment (2:1 randomization) on three consecutive days. The primary outcome was readiness for decannulation 24–72  h after treatment, which was assessed using a FEES based standardized protocol. In the treatment group, significantly more patients were decannulated immediately after the intervention (75% vs. 20%; Suntrup et al. 2015b). This possible target group for PES is cur-

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rently being examined in the ongoing PHAST-TRAC study (Dziewas et  al. 2016; Ib). Brain-stimulation techniques for the treatment of post-stroke dysphagia are being investigated in an increasing number of randomized controlled trials. However, the study populations are heterogeneous, especially with regard to the inclusion criteria and the outcome parameters. There is an urgent need for large multicenter trials that use established instrumental dysphagia assessments and clinically relevant endpoints to assess the effect of neurostimulation interventions. Positive results from randomized controlled trials are available for repetitive transcranial magnetic stimulation (rTMS) and transcranial directcurrent stimulation (tDCS). However, the included patient numbers are too small to make a final conclusion. The data on the effect of pharyngeal electrical stimulation (PES) remain contradictory thus far with the exception of the target group of tracheostomized stroke patients where results have been promising. Behavioral Swallowing Therapy Behavioral swallowing therapy is the oldest and most commonly used approach for treating post-stroke dysphagia. This section presents the current state of knowledge based on Speyer et al.’s review (Speyer et al. 2010) and is supplemented by more recent articles. I. Adaptive Methods • Logemann et al. (1995) investigated the effect of a sour bolus on different characteristics of swallowing in a small group of dysphagic stroke patients (n = 19). As shown by VFSS, this intervention significantly accelerated the oral bolus propulsion and shortened the latency of the swallow reflex compared with a normal bolus (IIa). However, the effect was short-lived to the immediate next swallow only. • In a different study on a small group of dysphagic stroke patients (n = 12), Hamdy et al. (2003) found that cool and sour boli led to a decrease in bolus volume and to a deceleration of swallowing (IIa). The authors used the so-called timed test of swallowing by Hughes and Wiles, in which subjects are asked to drink a predefined amount of liquid as quickly and safely as possible (Hughes and Wiles 1996). II. Neuromuscular Electrical Stimulation • A small oligo-centric randomized trial studied the effect of neuromuscular electrical stimulation (NMES) carried out with VitalStim® (see above; Bulow et al. 2008). 25 stroke patients received either 60-min daily NMES or traditional dysphagia therapy for 3 weeks. At the end of the study, there was no difference between the two modalities regarding different clinical and videofluoroscopic parameters (Ib).

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• In a randomized study design, Permsirivanich et al. (2009) evaluated NMES vs. clinical dysphagia therapy in 23 stroke patients. After an average of 18 sessions over a period of 2–4 weeks, both groups showed a clinically relevant improvement of swallowing function that was significantly more pronounced in patients treated with NMES (Ib). • Xia et al. (2011) randomized 120 dysphagic stroke patients into three different treatment groups: (1) conventional dysphagia therapy using adaptive, compensatory, and restitutive elements as required, (2) treatment only with NMES by means of VitalStim®, and (3) a combination of conventional therapy and NMES. The treatment was performed twice daily for 30 min five times per week for 4 weeks. Subsequently, all three treatment groups showed improvements in both clinical and videofluoroscopic parameters, but these improvements were significantly greater in the group that received the combination therapy than in the two groups that were provided only one treatment option (Ib). • In a non-randomized study, the effect of NMES on swallowing function in chronic stroke patients who had had dysphagia for an average of 4 months was compared with the effect of the Masako maneuver (n = 47). Outcome was assessed by VFSS. An improvement in swallowing function was found after the 4-week therapy in both treatment groups, and there were no significant differences in the effect size between the two treatments (Byeon 2016b; IIa). • A meta-analysis by Chen et al. (2016) investigated the effect of NMES on post-­ stroke dysphagia. Only a few high-quality studies could be included. The main finding was that in addition to regular behavioral swallowing therapy, treatment with NMES may be more effective in the short-term than behavioral treatment alone. However, long-term data are missing. An advantage of stand-alone NMES over traditional treatment strategies was not found (Chen et al. 2016). III. Tactile-Thermal Stimulation of the Palatal Arches • More than 20 years ago, Rosenbek et al. (1991) investigated thermal-tactile stimulation (TTS) in a small group (n = 7) of stroke patients. In this first study, a 2-week treatment had no clear effect on different videofluoroscopic parameters (IIb). • In a second study, 22 stroke patients were treated with TTS in a crossover design (Rosenbek et al. 1996). After the stimulation, both the transitional period between the oral and pharyngeal phases and the total duration of swallowing (IIa) were shortened. • In a third study, Rosenbek et al. (1998) investigated different intensities of TTS in a randomized design (n = 45). Patients received 150, 300, 450, or 600 stimulations per week during a 2-week treatment period. There were no significant differences between the groups regarding different videofluoroscopic parameters (Ib). • A randomized study compared a 4-week therapy with TTS combined with NMES with TTS alone (Lim et  al. 2009). Patients in the combined treatment group (n = 16) displayed a significant improvement of various videofluoroscopic parameters—such as pharyngeal transit time and the penetration–aspiration score (PAS)—compared with the TTS group (n = 12; Ib).

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• Power et al. (2006) performed a small randomized study on electric palatal arch stimulation in 16 stroke patients. Compared with sham stimulation, several videofluoroscopic parameters—such as the oral and pharyngeal transit time as well as the opening time of the upper esophageal sphincter—remained unaffected in this study (Ib). In conclusion, thermal-tactile stimulation is not recommended because the effects have only been shown to be immediate (within the next few seconds) and not longlasting. IV. Shaker Exercise • In a small randomized study, Don Kim et al. (2015) compared the effectiveness of the Shaker exercise with a neck-flexion exercise based on the principles of proprioceptive neuromuscular facilitation. 13 patients with chronic stroke-related dysphagia were treated in each group. VFSS was used to evaluate the therapeutic effect. Both methods achieved a comparable improvement in swallowing function after 6 weeks that included a reduction in the amount of residue and aspiration as well as improved laryngeal elevation (Ib). V. EMG Biofeedback • In an observational study, Crary et al. (2004) investigated the effect of a systematic dysphagia treatment program, one component of which was EMG biofeedback (Crary et al. 2004). 25 stroke patients received an average of twelve 50-min therapy sessions. By the end of this training program, clinically determined dysphagia severity had improved in 92% of patients (III). • Bogaardt et  al. (2009b) used EMG biofeedback to help train the Mendelsohn maneuver in an observational study. Eleven patients with chronic dysphagia after stroke received approximately seven therapeutic sessions over a period of 70 days on average and were also required to perform the treatment independently at home several times per day. All patients experienced a clinically relevant improvement of dysphagia during the course of the study (III). VI. Tongue-Pressure Resistance Training • Steele et  al. (2016) compared the effect of two protocols for tongue-pressure resistance training (duration: 8–12 weeks) in a small randomized study (n = 14; mean age: 71; mean time since stroke: 70 days). The therapeutic effect was measured by VFSS. There was no significant difference between the two protocols. After the treatments, an improvement in tongue strength and liquid residue was seen in both groups. There was no improvement in the penetration–aspiration scale (Steele et al. 2016; Ib). VII. Mendelsohn Maneuver • In a prospective crossover study, McCullough et al. (2012) evaluated the effect of the Mendelsohn maneuver (in combination with EMG biofeedback) on VFSS parameters in patients with chronic post-stroke dysphagia (n = 18). After 2 weeks of therapy, superior and anterior motion of the hyoid bone and the opening of the UES improved as compared with baseline (McCullough et al. 2012; McCullough and Kim 2013; IIa).

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VIII. Comprehensive Therapy Programs • In a randomized study, Lin et al. (2003) investigated the impact of a systematic exercise program compared with no treatment in 49 stroke patients. The dysphagia therapy included adaptive methods, stimulation techniques, and compensatory strategies and lasted 8  weeks. Thereafter, the treatment group showed significant improvements in various clinical swallowing variables and also presented with significant weight gain compared with patients in the control group (Ib). • An observational study by Elmstahl et al. (1999) investigated the impact of dysphagia therapy on the nutritional status. 38 stroke patients received comprehensive dysphagia therapy for about 2 months, which included food modification, interventions to optimize body posture during eating, TTS, and swallowing maneuvers. 61% of patients showed an improvement in different videofluoroscopic parameters. This group also showed a significant improvement in laboratory nutritional parameters, whereas the group of patients who did not benefit from this treatment in terms of swallowing also experienced a worsening of these laboratory parameters and lost weight (III). • Takahata et al. (2011) evaluated the effect of systematic oral care and dysphagia therapy in 129 patients with hemorrhagic stroke in a retrospective cohort study. The primary endpoint of the study was the time until the patients could consume an oral diet. A historical patient cohort treated before the introduction of the new treatment regimen in the same institution was chosen as a control group (n = 90). The proportion of patients on an oral diet 3  months post-stroke was significantly higher under the new regimen than in the historical control group (86.8% vs. 67.8%), and the rate of pneumonia was also significantly reduced with the optimized intervention (20.9% vs. 35, 6%; IIb). • The largest-ever study focusing on the behavioral swallowing therapy of stroke patients was conducted by Carnaby et  al. (2006). In a multicenter design, the authors randomized 306 patients with acute dysphagic stroke in a control group that received behavioral treatment according to the local standard of care at the given study site or in two therapy groups that received either standardized low-­frequency or standardized high-frequency behavioral swallowing therapy. The standard of care consisted of supervised eating as well as provisions to facilitate safe swallowing (patient positioning, instructions to eat slowly, etc.). Low-­frequency dysphagia treatment was given three times per week for up to 1 month and included the teaching of compensatory strategies and food adaptation. High-­frequency dysphagia therapy was performed five times per week for up to 1 month. The primary endpoint of the study was defined as the proportion of patients on a normal diet at 6 months post-stroke. Although the primary endpoint of the study was narrowly missed (56% of the control group and 67% of the two therapy groups reached the primary endpoint), standardized dysphagia therapy displayed a trend toward reducing mortality and the need for transferal to long-­term care, a significant

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reduction of dysphagia-related complications and bronchopneumonia, as well as a significant increase in the proportion of patients who recovered a functional swallow (Ib). IX. Expiratory Muscle Strength Training (EMST) • A randomized placebo-controlled study examined the effect of 4-week expiratory muscle strength training (EMST) on chronic post-stroke dysphagia (n = 27). Compared with placebo, after EMST therapy, a significant improvement could be demonstrated in EMG activity of the suprahyoid muscles, the severity of liquid penetration/aspiration as measured by VFSS, and the Functional Oral Intake Scale (FOIS). The degree of penetration/aspiration for semi-solid consistencies remained unchanged (Park et al. 2016b; Ib).

Although many studies have been devoted to an extraordinarily wide range of behavioral techniques and maneuvers over the past 25 years, most of them have been limited in their significance by an overly small sample size, a retrospective design, the lack of a control group, or the choice of clinically less meaningful endpoints. Only the milestone study by Carnaby et al. (2006) is characterized by a high study quality. Although this study did not reach its primary endpoint, the effects shown on several clinically meaningful secondary endpoints are notable and strengthen the recommendation of initiating consistent behavioral swallowing therapy immediately after stroke (A). In addition, the data provide preliminary evidence for the effectiveness of specific therapeutic approaches, including tactile-thermal palatal arch stimulation, the use of EMG biofeedback, the Mendelsohn maneuver, the Shaker exercise, and EMST. However, prior to a final assessment and recommendation, additional, ideally multicenter randomized controlled studies are required

7.3.2 Dementia Behavioral Swallowing Therapy Meaningful randomized controlled studies that investigate the efficacy of swallowing therapies specific to the various types of dementia are not yet available, as illustrated by two systematic reviews (Alagiakrishnan et al. 2013; Boccardi et al. 2016). Two large multicenter studies included mixed populations of dementia patients (Alzheimer’s dementia (AD), vascular dementia (VD), and etiologically unclear or mixed forms of dementia; age range: 50–95 years): • In a controlled non-randomized study recruiting 351 dysphagic patients with dementia who had been demonstrated to be aspirating on thin liquids, Logemann et  al. (2008) revealed that nectar-like and honey-like liquids were less often aspirated in VFSS compared with the chin-tuck maneuver (with liquid). Patients with the most

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severe cognitive impairment benefited the least from the interventions. Overall, the percentage of reduction in aspiration was significantly lower in the dementia patient group than in a group of Parkinson patients who were also studied (IIa). • In a randomized controlled study of 260 dysphagic dementia patients who had been aspirating on thin liquids in VFSS, Robbins et al. (2008) found no significant differences in pneumonia rates after 3 months of using one of these therapeutic interventions: chin-tuck maneuver,  drinking only nectar-like liquid, or drinking only honey-like liquid. The cumulative pneumonia incidence was 11% which was lower than expected at the beginning of the study (Ib). • A systematic review addressed the question of the role of PEG feeding in patients with advanced dementia and dysphagia who were at risk of aspiration. Overall, there was no evidence for an improved long-term survival with artificial enteral nutrition via PEG in this review (Goldberg and Altman 2014). Pharmacotherapy • In one case report, a significant improvement in swallowing function was reported in an 81-year-old dysphagic patient with AD after initiating treatment with transdermal rivastigmine (rivastigmine is an acetylcholinesterase inhibitor). Clinically, an accelerated onset of the pharyngeal swallow was observed. An improved oral diet and increased oral intake resulted in a substantial weight gain; however, an instrumental dysphagia evaluation was not performed. The authors concluded that the cholinergic deficit associated with AD may have affected the initially delayed onset of the swallow reflex (Uwano et  al. 2012). A larger controlled FEES or VFSS study on the effect of transdermal rivastigmine on swallowing function in AD patients would certainly be a worthwhile sequel to this case report. Thickened liquids can be used to improve swallowing safety in the case of dementia-related neurogenic dysphagia with liquid aspiration as the main symptom. The effect is smallest in patients with severe dementia (B).

7.3.3 Parkinson’s Disease The evidence for various strategies to treat PD-related dysphagia has been investigated in recent years in several systematic and narrative reviews (Smith et al. 2012; Ciucci et al. 2013; van Hooren et al. 2014; Bloem et al. 2015; Suttrup and Warnecke 2016a, b). The consensus among these reviews is that large randomized controlled trials have not yet been performed to allow for meaningful evidence-based recommendations. According to current data, expiratory muscle strength training (EMST) and video-assisted swallowing therapy (VAST) are the most promising treatment options in combination with dopaminergic drug optimization (see below). Pharmacotherapy Several studies have investigated the effect of dopaminergic medication on swallowing function in PD patients and found inconsistent results. In an early review,

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Pfeiffer (2003) concluded that 33–50% of the dysphagic PD patients included in these studies responded to the administration of levodopa or apomorphine with varying degrees of improvement of their neurogenic swallowing dysfunction. The following studies on this topic are available: • Bushmann et al. (1989) investigated the impact of levodopa on swallowing function in 20 PD patients (mean age: 65.7; disease duration: 1–17  years; mean Hoehn and Yahr stage: 2.25). The dopaminergic medication was discontinued overnight for at least 8 h. In the off-state condition, patients were then given their regular dose of levodopa (100–500 mg). VFSS was performed in both the offand on-state, with five out of 15 dysphagic patients showing an improvement in swallowing. The following parameters responded particularly well to levodopa administration: residue in the valleculae, residue on the pharyngeal walls, and pharyngeal transit time for solid food boli (IIb). • Tison et  al. (1996) conducted a VFSS study on eight PD patients (mean age: 66.75; disease duration: 2–22  years; mean Hoehn and Yahr stage: 3.1; motor fluctuations in six patients) with swallowing disorders (subjective and/or with evidence of aspiration). After a 12-h overnight discontinuation of dopaminergic medication, the patients were given a subcutaneous apomorphine injection (0.05  mg/kg) the following morning. Swallowing function was evaluated by means of self-assessment, clinical examination of oral motor function, and VFSS in the off- and on-states. The following parameters were improved by apomorphine injections in some of the patients: oral motor function, residue in the valleculae, laryngeal penetration, and pharyngeal transit time. No improvement in swallowing function was detectable after apomorphine injection in three patients (IIb). • Robertson and Hammerstad (1996) studied the function of the masticatory muscles in eight PD patients (mean age: 53.7  years) in the off- and on-state and compared the results with those of a group of eleven control subjects. The dopaminergic medication was discontinued for the first study in the off-state for 10–12 h. The PD patients then received their regular morning dose of levodopa, and after 1  h, the second study was performed in the on-state. The chewing movements were measured via magnetometer and with EMG of the masticatory muscles. In the off-state, a deterioration of almost all measured parameters was found, including a lower amplitude and a slowing of chewing movements. In the on-state, specific parameters of the chewing motions improved, particularly the vertical amplitude and the duration of closure during rhythmic chewing movements (IIa). • Hunter et al. (1997) carried out a study on 15 dysphagic PD patients (mean age: 71 years; disease duration: 7–15 years; motor fluctuations in all patients). The dopaminergic medication was discontinued for at least 8 h overnight. At the first examination, patients were given 250 mg of levodopa after a 4-h fasting phase; at the second examination 1 week later, patients received a subcutaneous apomorphine injection (individual response dose of 1.5–6  mg of apomorphine). VFSS examinations were performed in the off- and on-state, with patients receiving liquid, semi-solid, and solid boli. The following parameters were signifi-

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cantly influenced by levodopa: fewer swallows were needed for complete pharyngeal bolus transfer (solid consistency), a shorter duration of the oral preparatory phase (liquid- and semi-solid consistencies), and a longer duration of the oral phase (solid consistency). The following parameters were significantly influenced by apomorphine: a decrease in residue in the valleculae (solid consistency) and a shorter duration of the pharyngeal transit time (semi-solid consistency; IIb). • Monte et al. (2005) compared swallowing function in 15 PD patients with dyskinesia (at least 25% of the day) and twelve PD patients without dyskinesia (mean age of all patients: 61.9; mean disease duration: 7.7 years; mean Hoehn and Yahr stage: 2.3). The dyskinetic PD patients received a significantly higher average dose of levodopa (977.2  mg/day vs. 513.8  mg/day). VFSS examinations were performed in both patient groups in the on-state. The group of non-­dyskinetic patients showed significantly more pharyngeal retention and had worse swallowing efficiency. In contrast, patients with a higher dose of levodopa showed a tendency to have a shortened oral transit time. In summary, the results were interpreted as an indication for an improvement in swallowing function caused by dyskinesia and/or higher doses of levodopa (IIa). • In an uncontrolled non-randomized observational study, 45 out of 75 (60%) advanced-stage PD patients on intestinal  levodopa/carbidopa infusion therapy (Duodopa® pump) subjectively experienced an improvement of their swallowing impairment. However, since no objective dysphagia assessment was performed, the significance of this finding with regard to the effect of intestinal levodopa/ carbidopa infusion on swallowing is very limited (III; Devos 2009). • In a narrative review, Melo and Monteiro (2013) concluded that based on the available data, there is no evidence for a positive effect of levodopa on swallowing function in PD patients (Melo and Monteiro 2013). In a narrative review published at the same time, Sutton (2013) came to a slightly different conclusion based on the same data. First, he pointed to methodological shortcomings in a meta-analysis published by Menezes and Melo in 2009, which concluded that levodopa does not improve swallowing function in PD patients (Menezes and Melo 2009). Afterward, Sutton re-evaluated the source data with regard to the risk of aspiration and came to the conclusion that levodopa therapy is associated with a lower, albeit not a statistically significant, risk of aspiration. Sutton cited the increase in the survival rate of PD patients after the introduction of levodopa therapy compared with the pre-levodopa era as a valid argument for a positive effect of levodopa on deglutition. As aspiration pneumonia is a frequent cause of death in PD and life expectancy has improved significantly since levodopa has been available, improved swallowing with a lower risk of aspiration could play a role here (Sutton 2013). Two further contributions to the discussion dealt with swallowing function in Parkinson patients in the off- and on-state following this controversy. Nóbrega et al. (2014) stressed that it is essential that dysphagic PD patients eat their meals in the on-state, which is when hand function is best and thus enables cutlery to be used more easily and more food to be taken into the mouth. In addition, in the on state compensatory swallowing maneuvers would be

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easier for patients to perform (Nóbrega et al. 2014). Warnecke et al. (2014) also reported an dysphagic patient with advanced Parkinson’s disease who showed significantly improved on-state swallowing in the FEES levodopa test compared with the off-state. In this PD patient, the initiation of intestinal levodopa/carbidopa infusion therapy (Duodopa® pump) led to a long lasting improvement of Parkinson-related dysphagia (Warnecke et al. 2014). In a pilot study, the authors investigated the response of neurogenic dysphagia to levodopa in five advanced-stage PD patients (age: 66–86; mean disease duration: 16.6  years; motor fluctuations in all patients). For this purpose, the FEES levodopa test (Sect. 3.1.4) was used (levodopa dosage: 200–400  mg). An improvement of all endoscopic parameters of swallowing function (and especially of residue and penetration) could be demonstrated in two of the five PD patients (IIb; Warnecke et al. 2010b: Suttrup et al. 2011). In a more recent study, the FEES levodopa test was used to evaluate the effect of levodopa on swallowing function in patients with advanced PD and motor fluctuations (n = 15; mean age: 71.9; disease duration: 14.3 years). In seven patients, the on-state was associated with a significant improvement of swallowing (>30%) compared with the off-state. The FEES parameters that improved most in these patients were premature spillage of liquids and residue of semi-solid and solid consistencies (IIb; Warnecke et al. 2016). In an uncontrolled retrospective Japanese open-label study, Hirano et al. (2015) reported the effect of the transdermal dopamine agonist rotigotine on swallowing function in six PD patients (w/m: 2/4; mean age: 75; disease duration: 1–5 years) who had had dysphagia symptoms from an early stage of the disease. Patients were evaluated by VFSS with a rotigotine patch at a low dose of 2 mg/24h both before as well as 1–2  weeks after initiating this treatment. Videofluoroscopic findings in all six patients revealed a significant improvement of dysphagia in both the oral and pharyngeal phases after the initiation of dopaminergic treatment. The pharyngeal transit time shortened from 1.07 ± 0.38 s to 0.84 ± 0.22 s. The subjective symptoms of dysphagia even disappeared completely (III; Hirano et al. 2015). An unexpected finding of this study was that 2 mg of rotigotine had such a strong effect on swallowing function. This dose was lower than the rotigotine dosages commonly used in Europe and the USA. The authors discussed the possibly that ethnic elements—particularly body weight and skin permeability—may have played a role (Hirano et  al. 2015). To assess the true effect of transdermal rotigotine on PD-related dysphagia, randomized controlled trials involving PD patients are required, ideally across all stages of the disease. In a prospective population-based observational study, 171 initially untreated PD patients were examined in Norway at the time of diagnosis and after 12 months. The frequency and severity of PD-related dysphagia was assessed using a questionnaire (the new version of the UPDRS). At 12  months, dopaminergically treated patients had a tendency to display an improvement of swallowing function, which was correlated with higher levodopa-equivalent doses. It was concluded that dopaminergic medication should always be optimized in PD patients with dysphagia (III; Müller et al. 2013).

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Summing up the results of these studies, some endoscopic and videofluoroscopic parameters of oropharyngeal swallowing appear to respond well to dopaminergic medication (at least in some early  stage as well as advanced stage PD patients), whereas other parameters are more difficult or impossible to influence via dopaminergic medication. Oropharyngeal swallowing parameters that may have good levodopa responsiveness include (1) pharyngeal residue (especially in the valleculae), (2) penetration, and (3) oral and pharyngeal transit times. Parkinson-related esophageal dysmotility may also be positively influenced by dopaminergic medication (Kempster et al. 1989). Overall, based on the results of these studies, increased or optimized dosages of dopaminergic medication should always be considered in individual cases of PD-related dysphagia (Monte et al. 2005). Therapy monitoring should be performed by means of instrumental dysphagia assessment (VFSS and/or FEES). Before making any changes to individual treatment protocols, the potential response of PD-related swallowing impairment to levodopa may be quantified via the FEES levodopa test (Warnecke et al. 2010a, 2016). In a case report by Fonda et al. (1995), the authors were able to use VFSS to show that swallowing function improved subjectively and objectively by shifting only the levodopa doses to just 1 h before meals in a dysphagic PD patient. It is generally recommended to take levodopa either half an hour before or more than 1 h after eating. Patients may be able to swallow the levodopa tablet together with a soft biscuit. In the case of PD-related dysphagia, it is necessary to examine whether an improvement in swallowing function can be achieved by increasing or optimizing the dopaminergic medication on a case-by-case basis (B). Deep Brain Stimulation The effects of deep brain stimulation (DBS) on swallowing function in PD patients have not yet been conclusively clarified. In a systematic review, Troche et al. analyzed several studies that focused on the stimulation of the subthalamic nucleus (STN). Nine experimental studies were identified in which swallowing function in PD patients was compared in on- and off-DBS and in pre- and postDBS. These studies included four VFSS studies and two FEES studies. The systematic review concluded that DBS did not result in either a clinically relevant improvement or a worsening of swallowing function in these studies (Troche et al. 2013). In a VFSS study, DBS in PD patients without dysphagia (n = 18) was found to result in subclinical modulation of the pharyngeal phase of swallowing—particularly with changes in movement timing—but without altering the oral phase (Lengerer et al. 2012). In a retrospective study comparing STN stimulation with stimulation of the globus pallidus internus (GPi), a slight worsening in mean values of the PAS score with respect to alterations of swallowing function was seen only in the STN stimulation group (Troche et al. 2014a). However, prospective comparative studies are lacking. Low-frequency 60 Hz stimulation of the STN may lead to an improved swallowing function in dysphagic PD patients and reduce aspiration (Xie et al. 2015). In a randomized crossover study,

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16 PD patients with STN stimulation were examined on- and off-stimulation with esophageal high-resolution manometry. This study found a subclinical improvement of esophageal motility and lower esophageal sphincter opening (Derrey et al. 2015). Model for Neuropathophysiology of PD-Related Oropharyngeal Dysphagia In the following section, a pathophysiological model of PD-related oropharyngeal dysphagia derived from the results of previous studies is presented and may explain why the swallowing disorder has at least partial levodopa responsiveness in some PD patients despite having no effect in others. At least three different pathomechanisms are likely to play an important role in the development of PD-related oropharyngeal dysphagia (Suttrup and Warnecke 2016a, b): 1. Lewy bodies—first described by Fritz Jacob Heinrich Lewy in the early twentieth century and named after him—have been found to be a characteristic neuropathological feature of PD (Lewy 1912). Lewy bodies are intraneuronal eosinophilic inclusion bodies that contain alpha-synuclein and other inadequately degraded proteins. Based on the anatomical localization of the Lewy bodies during the course of PD, Braak et al. (2003) developed the concept of different stages in the development of PD-related pathology (six stages in total). According to this concept, PD begins in the posterolateral glossopharyngeal and vagal areas in the medulla oblongata and the olfactory bulb. From there, the pathological process spreads via the brainstem into the midbrain—including the substantia nigra (SN)—and then propagates into neocortical brain areas. During this process, various non-dopaminergic swallowing-relevant areas in the brainstem and cortex are involved (Sect. 1.3). If such areas—particularly the medullary swallowing centers—are affected to a significant extent non-dopaminergic dysphagia symptoms (unresponsiv to levodopa treatment) are prone to occur (Hunter et al. 1997). 2. Neurogenic dysphagia can also be caused by a dopamine deficiency in the striatum. The importance of the basal ganglia in the control of swallowing was demonstrated by Suzuki et al. (2003) in an fMRI study examining healthy volunteers. During swallowing, the study participants demonstrated a bilateral activation of the putamen and the globus pallidus. In addition, positive effects of levodopa, cabergoline, and amantadine on swallowing function were found in stroke patients (including an earlier onset of the pharyngeal-stage swallowing; Sect. 7.3.1). Dysphagia associated with a dopaminergic deficit potentially responds to dopaminergic medication, which may explain the positive effects of levodopa, apomorphine, and rotigotine on swallowing function in some PD patients, as demonstrated in the studies mentioned above. 3. A decreased release of Substance P in the course of PD may play a significant role as a third pathomechanism. Since Substance P stimulates the cough- and swallow reflex in healthy individuals, its reduced release in advanced stages of PD—which has been demonstrated in the saliva of PD patients—may be primarily responsible

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for the development of sensory dysfunction and lead to silent aspiration (Ebihara et al. 2003). Table 7.2 provides an overview of various specific dysphagia symptoms of PD and their possible pathomechanisms. Against the background of this multifactorial neuropathophysiological model, the question of whether PD-related dysphagia responds to dopaminergic medication in a given case depends on what role deposits of Lewy bodies in non-dopaminergic swallowing-related CNS areas as well as the reduced Substance P concentration have on the development of the respective swallowing disorder. The more significant these non-dopaminergic ­pathomechanisms are, the lower the likelihood that oropharyngeal dysphagia will be significantly improved by dopaminergic treatment. Behavioral Swallowing Therapy The following section presents the results of methodologically sound studies on the effectiveness of behavioral swallowing therapy for PD: • In a controlled non-randomized study recruiting 228 dysphagic PD patients with thin liquid aspiration in VFSS, Logemann et al. (2008) were able to demonstrate that nectar-like- and honey-like liquids reduced the risk of aspiration compared with using the chin-tuck maneuver (with unthickened liquid). However, the patients themselves indicated a preference for the chin-tuck maneuver and an aversion to thickened liquids (IIa). • In a randomized controlled study that recruited 154 dysphagic PD patients with liquid aspiration documented by VFSS, Robbins et al. (2008) found no significant differences in the incidence of pneumonia after 3 months with respect to the study interventions, which consisted of either the chin-tuck maneuver or liquid thickening to create a nectar-like consistency or a honey-like consistency (Ib). • The effect of the chin-tuck maneuver on swallowing function in dysphagic PD patients was evaluated in a controlled study that examined three groups that were Table 7.2  PD-related oropharyngeal dysphagia symptoms and postulated pathomechanisms Symptom Prolonged oral transit time Premature spillage Delayed swallow reflex Prolonged pharyngeal transit time Penetration Aspiration Residue in valleculae Residue in piriform sinus Dysfunction of upper esophageal sphincter Insufficient cough reflex

Pathomechanisms Dopaminergic + non-dopaminergic (especially Lewy bodies in swallowing cortex?) Dopaminergic + non-dopaminergic (Lewy bodies in swallowing cortex?) Dopaminergic + decreased Substance P concentration Dopaminergic + non-dopaminergic (Lewy bodies in brainstem?) Dopaminergic + non-dopaminergic Dopaminergic + non-dopaminergic Primarily dopaminergic Dopaminergic + non-dopaminergic Primarily non-dopaminergic (Lewy bodies in swallowing centers of medulla oblongata?) Decreased substance P concentration

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re-examined after a 4-week period: The first group performed the chin-tuck maneuver (n = 11), the second group received no intervention (n = 14), and the third group was informed regularly about eating strategies (n = 7). The effects were measured with FEES, a clinical swallowing study including the Functional Oral Intake Scale (FOIS), and the SWAL-QOL. While FEES revealed no significant post-intervention differences between the groups, the first group—which had practiced the chin-tuck maneuver—performed better at follow-up with regards to FOIS and the clinical swallow examination (IIa; Ayres et al. 2017). In a randomized controlled trial, ten PD patients received a one-time swallowing training that included tongue mobility- and resistance exercises, exercises to improve vocal fold adduction, the Mendelsohn maneuver, and head, neck, and trunc mobility exercises. A significant reduction in pre-swallow time was detected via surface electromyography of the submental musculature, which was performed before and after the training (IIa; Nagaya et al. 2000). In an uncontrolled prospective study recruiting 15 dysphagic PD patients (m/w: 10/5; mean age 59.2), the effect of 5-week behavioral swallowing therapy targeting the strength and movement-range of oropharyngolaryngeal structures, respiratory- and swallowing coordination, and airway management was assessed by VFSS. After the study intervention, improvements in oral bolus control, improvement of piece-meal deglutition, and a reduction of residue on the tongue as well as in the valleculae and piriform sinus were detected. No therapeutic effect was found in patients with repetitive pumping movements of the tongue or in patients without teeth (IIb; Argolo et al. 2013). In an uncontrolled prospective study, El Sharkawi et al. (2002) investigated the effect of Lee Silverman Voice Treatment (LSVT®)—which was originally developed for the treatment of Parkinson-related dysarthria—on swallowing function in eight patients with PD (age: 48–77; Hoehn and Yahr stage: 2–4). VFSS was performed before and after the completion of the LSVT®. After the study intervention, a substantial improvement of all pre-existing oral- and pharyngeal-­stage dysfunctions was detectable. In particular, oral transit time, oral residue, and oropharyngeal swallowing efficiency improved for all consistencies and volumes (IIb). In an uncontrolled prospective study, Pitts et al. (2009) investigated the efficacy of a 4-week EMST intervention on swallowing function in ten dysphagic PD patients (age range: 62–80; Hoehn and Yahr stage: 2 or 3) who had shown penetration or aspiration of liquid boli in VFSS. After completing the training, an improvement in the PAS was demonstrated in eight PD patients (IIb). Troche et al. (2010) conducted a randomized controlled study of 60 dysphagic PD patients (mean age: ~68; Hoehn and Yahr stage: 2–4) with the same 4-week EMST intervention. Dysphagia severity was rated as mild to moderate. VFSS was performed before and after training in the on-state. Compared with sham, EMST resulted in a significant reduction in the mean PAS score. In addition, improved laryngeal elevation (secondary outcome parameter) was demonstrated (Ib).

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• In a subsequent follow-up study, ten PD patients from the former treatment group were re-examined after a 3-month period without training. While the maximum expiratory pressure—which had improved by 19% after the 4-week treatment phase—declined by 2% (yet still showed a 17% improvement), no significant worsening of swallowing function after treatment discontinuation was found in VFSS. However, there were differences depending on the individual initial dysphagia characteristics. Patients who had initially presented with the most severely impaired swallowing worsened again. In contrast, there was no significant change in the therapeutic effect after 3  months in patients with moderately impaired swallowing at study inclusion. The patients with a mildly reduced swallowing function even showed a further slight improvement with regard to swallowing safety measured with the PAS (IIb; Troche et al. 2014b). • In a small randomized controlled trial, the effect of EMST alone (n = 18) on swallowing function in dysphagic PD patients was compared with EMST in combination with various postural interventions (n = 15). Dysphagia was evaluated with VFSS.  An improvement in swallowing function was seen in both groups after 4 weeks of treatment, and the group of patients receiving the combination therapy showed a significantly greater benefit (Ib; Byeon 2016a). • In a non-randomized controlled VFSS pilot study, Baijens et al. (2012) investigated the effect of a single dose of neuromuscular electrical stimulation (NMES) on swallowing function in ten dysphagic PD patients and compared these results with those of ten age- and sex-matched normal subjects. Changes in swallowing physiology as seen in VFSS were modest and potentially caused by a placebo effect (IIa; Baijens et al. 2012). • In a randomized controlled study, Heijnen et al. (2012) investigated the effect of NMES on the quality of life (including SWAL-QOL) of 85 dysphagic PD patients. Three treatment groups were separated: The control group received traditional speech therapy (n = 28), and the other two groups received additional NMES—one group as motor stimulation (n = 27) and the other group as sensory stimulation (n = 30). The effect on the quality of life was evaluated immediately after the 3- to 5-week treatment phase and after 3 months. There was an improvement in the quality of life in all three therapy groups; however, an added benefit of NMES could not be demonstrated (Ib; Heijnen et al. 2012). • In a randomized controlled study, Baijens et  al. (2013) also investigated the effect of neuromuscular electrical stimulation (NMES) on swallowing function in 90 dysphagic PD patients separated into three treatment groups (n = 30 each): One group received only behavioral swallowing therapy, and the other two groups received additional NMES—one group as motor stimulation and the other group as sensory stimulation. Therapy was provided daily for 15 days, with therapy breaks over the weekends. The efficacy of the interventions was assessed using FEES and VFSS. Improvements in swallowing function were found in all study groups after 15 days, but no additional effect of NMES could be demonstrated (Ia; Baijens et al. 2013). • In a randomized controlled study, Manor et al. (2013) investigated the effect of video-assisted swallowing therapy (VAST) that employed FEES to provide biofeedback to patients. 21 PD patients without cognitive impairment (mean age:

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68.8; average Hoehn & Yahr stage: 2.2) were randomized to receive either VAST or conventional behavioral swallowing therapy. Both groups received five half-­ hour treatment sessions within 2 weeks. Four weeks later, sixth half-hour sessions were scheduled. In addition, a homework program was completed. The therapy consisted of swallowing exercises and compensatory procedures, which had been shown to be effective in the initial FEES. The key difference between both groups was that patients in the VAST group were shown additional FEES videos in a specific sequence that displayed an unimpaired swallow, their own impaired swallow, and their own swallow using an effective compensatory procedure. Immediately after the end of the treatment, FEES revealed a reduction of food residue in the pharynx in both groups, though this reduction was significantly greater in the VAST group. The most commonly used swallowing technique was repeated effortful swallowing. In addition, there were significant improvements in the VAST group compared with the control group in five areas of dysphagia-­associated quality of life 6 months after the end of treatment (as measured by the dysphagia-specific SWAL-QOL; Ib; Manor et al. 2013). Overall, the results of these studies on PD-related dysphagia are difficult to compare since patient populations varied across studies, heterogeneous treatment methods were tested, and very different outcome parameters were employed. It can therefore be concluded that large randomized controlled trials of multidimensional outcome evaluations (quality of life, nutritional examination, clinical testing of oral motor functions, and FEES and/or VFSS) should be performed to investigate the efficacy of different therapeutic strategies with regard to behavioral interventions in PD-related dysphagia (Baijens and Speyer 2009). The following recommendations can be derived from the studies published so far: • In many patients with PD-related dysphagia, thickened liquids are more effective than the chin-tuck maneuver in avoiding liquid aspiration. However, if patients prefer the chin-tuck maneuver due to an aversion to thickened liquids, a reduction in liquid aspiration can also be achieved in individual cases. In any case, the efficiency of the chosen method should be confirmed via instrumental testing (i.e., FEES or VFSS; B) and the overall risk for pneumonia should be taken into consideration. In particular when it comes to long-term interventions, the possible impact on the quality of life needs to be taken into consideration. • Effortful swallowing can be used to reduce pharyngeal residue in PD-­ related dysphagia (A). • FEES used to provide biofeedback in behavioral swallowing interventions of PD-related dysphagia may improve swallowing (A). • Lee Silverman Voice Treatment (LSVT®) may be recommended for the treatment of PD-related dysphagia; however, randomized controlled trials are not yet available (B). • Four weeks of expiratory muscle strength training (EMST) may result in decreased penetration and aspiration in mild to moderate PD-related

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d­ ysphagia. There is no proof of the efficiency of this method for severe PD-­related dysphagia (A). • Neuromuscular electrical stimulation (NMES) has no added benefit in behavioral swallowing interventions targeting PD-related dysphagia and should therefore not currently be used in everyday clinical practice for this indication (A). • Due to insufficient data, injections of botulinum toxin into the cricopharyngeal muscles are currently not recommended for PD-related dysphagia with hyperactivity of the upper esophageal sphincter (see below; C) The German Neurological Society’s (DGN) S3 guideline “Idiopathic Parkinson’s Disease”—which was published in 2016—offers the following recommendations for the treatment of PD-related dysphagia: • PD patients with dysphagia should receive behavioral swallowing treatment. • Behavioral interventions should be selected according to the individual pattern of swallowing impairment. The efficacy of the chosen treatment should be evaluated prior to and during treatment with FEES or VFSS. • In PD patients with bradykinetic dysphagia, optimizing dopaminergic medication can also improve swallowing. Injection of Botulinum Toxin Restivo et al. (2002) published a case series of four PD patients suffering from dysphagia with hyperactivity of the cricopharyngeal muscle. Guided by EMG, all four patients received botulinum toxin A injections (Dysport, 30 units) into both sides of this muscle. After 48 h swallowing function improved significantly in all patients. There were regular follow-up examinations using EMG and VFSS.  The positive therapeutic effect with a normalization of swallowing lasted for at least 20 weeks. During this time, the patients gained 5–8 kg of weight (III). However, these results have not yet been reproduced in a larger group of patients. Given that this therapy may also result in a worsening of dysphagia, more data is clearly required. Accordingly, in a recent review, the data available for treating PD-related dysphagia with injections of botulinum toxin were also considered insufficient (Mills et al. 2015). On the other hand, there is sound evidence available for treating PD-associated sialorrhea with injections of botulinum toxin (Mills et al. 2015): • Mancini et al. (2003) conducted a double-blind randomized placebo-controlled study on 14 PD patients and six MSA patients. Guided by ultrasound, botulinum toxin A (Dysport; 225 units per ml) was injected into the parotid gland (0.65 ml each) and the submandibular gland (0.35  ml each). As a result, a significant reduction in salivation was achieved after 1  week compared with the placebo group (Ib). • Ondo et al. (2004) conducted a double-blind randomized placebo-controlled trial on 16 PD patients using injections of botulinum toxin B (Myobloc; 1,000 units each injected bilaterally into the parotid gland and 250 units each injected bilat-

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erally into the submandibular gland). After 1  month, patients treated with the study drug noticed a significant reduction in salivation (Ib) compared with the placebo group. Lagalla et  al. (2006) included 32 PD patients in a double-blind randomized placebo-­controlled study. The intervention group received injections of botulinum toxin A (BOTOX®; 50 units each injected into the parotid gland) and showed significant salivary reduction after 1 month compared with the placebo group (Ib). Lagalla et al. (2009) conducted a double-blind placebo-controlled randomized trial on 36 advanced-stage PD patients. The intervention group received injections of botulinum toxin B (NeuroBloc; 4000 units each injected into the parotid gland), and salivation was significantly reduced after 1 month compared with the placebo group (Ib). Nobrega et al. (2009) investigated the effect of ultrasound-guided injections of botulinum toxin A (Dysport; 250 units each injected into the parotid gland) on swallowing function in 16 PD patients with sialorrhea. VFSS was completed 1 month before and after the injections. There was no worsening of the oropharyngeal swallowing function detected in this patient cohort (IIb). In a multicenter randomized controlled trial, Chinnapongse et al. (2012) investigated the effects and side effects of three increasing doses of botulinum toxin B (Myobloc; 1500, 2500, or 3500 units injected into the submandibular gland and parotid gland) on 54 PD patients with sialorrhea. After 4 weeks, there was a significant reduction in sialorrhea compared with placebo in all dosage groups. The effect increased with higher doses. Serious adverse reactions did not occur. Dry mouth was the most common side effect in the study-drug groups. Subjective dysphagia symptoms did not occur in the study-drug groups (Chinnapongse et al. 2012). Jost et al. (2019) randomized 184 patients with either PD, atypical parkinsonism, stroke, or traumatic brain injury to receive incobotulinum toxin A 75 or 100 U or placebo distributed in bilateral parotid and submandibular glands in a single injection cycle. Compared with the placebo, both treatment groups showed significant improvement of (subjectively rated) drooling (Jost et al. 2019). Parkinson-related sialorrhea can be effectively treated with injections of botulinum toxin A or B into the parotid and the submandibular gland (A).

Another treatment option for parkinsonian-related sialorrhea may be the anticholinergic drug glycopyrrolate, which—unlike other anticholinergics—does not cross the blood–brain barrier and therefore does not have central anticholinergic side effects, such as cognitive impairment. Arbouw et al. (2010) conducted a 4-week double-blind randomized crossover study that included 23 PD patients. One mg of glycopyrrolate was administered orally three times per day as an active ingredient. With glycopyrrolate,

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there was more often a clinically significant reduction in salivation as compared with the placebo during the 1-week trial episode, and no significant side effects occurred with this dosage. However, long-term data are not yet available (Ib). In addition, chewing gum may also lead to an improvement of PD-related sialorrhea. Thus, South et al. (2010) investigated the effect of 5 min of gum chewing on the swallowing frequency of 20 PD patients (age: 58–75; Hoehn and Yahr stage: 2–4) with no clinically relevant dysphagia. During gum chewing, the average swallowing frequency increased (from 3.1 swallows per 5 min to 14.95 swallows per 5 min), and the average latency between two swallows decreased (from 131.8 s to 24.1 s). The increase in swallowing frequency and the corresponding reduction of swallowing latency persisted immediately after the intervention. Whether or not salivation could actually be reduced was not explicitly investigated in this study (III).

7.3.4 Progressive Supranuclear Paralysis Pharmacotherapy Parkinsonian symptoms do not respond to dopaminergic medication in most PSP patients. However, according to one review, a moderate and often-transient yet positive levodopa effect on motor symptoms was observed in about one-third of cases (Constantinescu et al. 2007). In a recent study, Warnecke et al. (2010a) investigated the levodopa responsiveness of neurogenic dysphagia in seven PSP patients. The FEES levodopa test was used (Sect. 3.1.4), and levodopa doses between 200 and 400 mg were administered. Levodopa-responsive dysphagia could be detected in two PSP patients, and there were improvements in all major parameters of swallowing function. After increasing the daily dose of levodopa, both patients improved their oral diet (III). PSP patients with a positive FEES levodopa test had a shorter disease duration (2.0 years vs. 5.4 years) and a lower UPDRS III (26.5 vs. 52 points). In a recent case series, a clinical improvement in swallowing function in three dysphagic PSP patients was reported after increasing the daily dose of levodopa (from 600 to 1200 mg/day). A positive effect on the oral phase of swallowing—which was impaired in all patients by oral dystonia and oral apraxia—was observed clinically. An instrumental dysphagia evaluation was not performed (Varanese et al. 2014). Treating dysphagic PSP patients with levodopa to improve their swallowing function is justified, especially in the early stages of the disease. Adding amantadine to levodopa may be particularly beneficial. According to available data, a sufficiently high daily dose of levodopa must be administered (at least 600 mg/day). The therapy should always be monitored by FEES or VFSS. In a controlled double-blind crossover study, the effect of physostigmine on swallowing function in PSP patients (n = 8; mean age: 64) was clinically and sonographically evaluated. Physostigmine—a central inhibitor of acetylcholinesterase—was administered 6 times per day at a dose of 0.5–2 mg for a total duration of 10 days. A

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significant improvement in patients’ swallowing function could not be demonstrated (Frattali et al. 1999). PSP-related dysphagia may be treated with levodopa therapy in some early-stage patients (C). Behavioral Swallowing Therapy Methodologically sound studies on the efficacy of the various behavioral methods for the treatment of PSP-related dysphagia do not yet exist. However, certain procedures were also examined in the FEES- and VFSS studies on individual PSP patients, as presented in Sect. 4.3.1. Depending on the predominant pattern of swallowing impairment, the most effective strategies for improving swallowing were (1) the chin-tuck maneuver in the event of premature spillage, (2) effortful swallowing to treat residue, and (3) dietary modifications (especially switching to soft or semi-­ solid food consistencies) to address penetration/aspiration. When considering behavioral swallowing therapy in PSP patients, the association of dysphagia with neurocognitive symptoms should always be taken into account. For example, postural changes and swallowing maneuvers may be unsuitable for PSP patients with dementia if adherence is poor. More frequent but shorter therapy sessions may be useful in case of memory/executive dysfunction (Warnecke and Dziewas 2015). In PSP patients with severe dysphagia and aspiration of all food consistencies without response to pharmacological treatment, artificial enteral nutrition via a PEG may be indicated (Litvan et al. 1997; Warnecke et al. 2010a).

Depending on the pattern of impaired deglutition, the chin-tuck maneuver, effortful swallowing, and soft and semi-solid food consistencies may be particularly suitable for patients with PSP-related dysphagia (C).

7.3.5 Multiple System Atrophy Specific therapeutic procedures do not yet exist for multiple system atrophy (MSA)related dysphagia. Because MSA patients often have impaired vocal fold mobility (including paradoxical vocal fold movement) or laryngeal dystonia with impaired breathing and stridor, dysphagia therapy for MSA patients always needs to take the coordination between swallowing and breathing into account. In endoscopically verified vocal fold paresis and/or arytenoid tremors, cardiorespiratory polysomnography should be performed to detect sleep-disordered breathing and—if necessary—to initiate continuous positive airway pressure (CPAP) therapy (Ozawa et al. 2010; Videnovic 2017). Ultimately, disturbed vocal fold mobility or stridor may also require a tracheostomy (Giannini et al. 2016).

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In a Japanese observational study, tracheotomy was compared with surgical laryngeal closure in 18 MSA patients (ages: 52–76; female/male: 5/13) for the treatment of respiratory disorders and dysphagia. Swallowing function was assessed by VFSS or FEES (penetration–aspiration scale). While the majority of MSA patients with a postoperative tracheostomy displayed a worsening of swallowing, MSA patients with laryngeal closure were able to maintain complete or at least partial oral intake of solid- and liquid consistencies. From these data, the authors conclude that laryngeal closure is the better option in dysphagic MSA patients who are willing to accept voice loss but wish to continue oral nutrition (III; Ueha et al. 2016).

7.3.6 Dystonias Deep Brain Stimulation According to a recent review, dystonia-related dysarthria and dysphagia (measured with the corresponding items of the Burke–Fahn–Marsden Dystonia Rating Scale; BFMDRS) are somewhat less responsive to deep brain stimulation in the internal globus pallidus (GPi) than are other dystonia symptoms (Tagliati et  al. 2011). However, there are no studies in which the effect of deep brain stimulation on swallowing function in dystonia patients has been examined by FEES or VFSS. Pharmacotherapy Based on case reports and small case series, some suggestions with regard to pharmacological treatment options can be cautiously derived: • Pharyngeal dystonic dysphagia associated with oromandibular dystonia: tetrabenazine (Suttrup et al. 2014) • Focal dystonia of the hyoid musculature: injections of botulinum toxin (but with significant side effects, especially dysarthria and dysphagia; Norby et al. 2015) • Dysphagia caused by paroxysmal kinesigenic dyskinesia: carbamazepine (Kumar et al. 2011a; Rizek et al. 2015)

7.3.7 Wilson’s Disease Lee et al. (2012b) reported on a 33-year-old South Korean patient with Wilson’s disease who had been suffering from dysphagia for 7 years and experienced a worsening of swallowing function during the previous 2–3 months. Wilson’s disease had been diagnosed 13 years earlier. After 10 sessions of neuromuscular electrical stimulation (NMES; 1 h/day), VFSS revealed reduced pharyngeal residue (Lee et al. 2012b).

7.3.8 Huntington’s Disease Behavioral Swallowing Therapy In a non-randomized uncontrolled observational study that included twelve dysphagic patients with Huntington’s disease (HD), behavioral swallowing therapy was

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successfully used to upgrade three-quarters of patients from a modified to a normal oral diet. This improvement in swallowing persisted for up to 3 years (III; Leopold and Kagel 1985). Thus far, however, there have been no randomized controlled studies on the effect of behavioral swallowing therapy on Huntington-related dysphagia. Therefore, no specific evidence-based recommendations for the treatment of Huntington-related dysphagia can be provided at this time (Heemskerk and Roos 2011; Wirth et al. 2013). In a randomized controlled trial, Reyes et al. (2015) investigated the effect of a 4-month EMST training on swallowing function in patients with Huntington’s disease (n = 18). The outcome parameters included a water swallow test and a quality-­ of-­life questionnaire (SWAL-QOL). After both 2 and 4  months, no significant improvements in swallowing function could be demonstrated in relation to the study intervention (n = 9; Ib; Reyes et al. 2015).

There are currently no evidence-based recommendations for specific behavioral swallowing interventions in Huntington-related dysphagia. Based on current data, EMST training is not effective in this clinical context (A). The S3 guideline “Clinical Nutrition in Neurology” also contains a separate chapter on Huntington’s disease, which—despite the lack of evidence and clinical experience—recommended behavioral swallowing therapy (grade B) in this context based on a consensus conference decision (Wirth et al. 2013). In general, restorative techniques can be used in the early stages of HD to maintain motor function for as long as possible. Relaxing stimuli can reduce oral hyperkinesia. In more advanced stages of the disease, the focus of dysphagia therapy lies on compensatory and adaptive procedures. Suitable eating and drinking aids—such as non-slip pads or cups with handles on both sides—should enable patients to maintain their independence while eating for as long as possible. If independent eating is no longer possible, patients are recommended to eat meals with the assistance of an attendant who provides verbal instructions, if needed. Particular attention must be paid to proper eating habits as Huntington patients are at an increased risk of aspiration due to fast eating and swallowing of overly large boli (Bartolome et al. 2013). In dysphagia therapy, the nutritional status of Huntington patients must always be taken into account, and specific nutritional interventions may have to be initiated. Depending on the stage of the disease, a daily energy intake of approximately 2500–4000 kcal may be required in HD to maintain an adequate body weight. PEG should be considered if the required caloric intake can no longer be maintained and/ or there is neurogenic dysphagia with an increased risk of aspiration. Artificial feeding may also be required as an adjunct to an oral diet in order to administer additional liquids for patients with swallowing disorders or—in case of very severe dysphagia—as the only source of nutrition. Nutrition via artificial feeding is not recommended in the end stages of Huntington’s disease; however, this decision should be made on a case-by-case basis (Wirth et al. 2013).

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7.3.9 Multiple Sclerosis In a systematic review published in 2016, data on the treatment of multiple sclerosis (MS)-related dysphagia were systematically analyzed for the first time (Alali et al. 2016). Five studies were found that met predefined inclusion criteria, three of which evaluated methods of neurostimulation (neuromuscular electrical stimulation, vagal stimulation, and pharyngeal electrical stimulation), whereas the two other studies evaluated injections of botulinum toxin. However, one of the two studies on botulinum toxin included only 2 MS patients out of a cohort of 34 patients suffering from different neurological conditions. There were no high-­quality studies on behavioral swallowing therapy in MS patients. All five studies included in the analysis reported positive effects, and the effect size was greater for the neurostimulation procedures than for the injection of botulinum toxin. Overall, there is still a lack of evidence for the recommendation of certain procedures in the treatment of MS-related dysphagia (Alali et al. 2016). Behavioral Swallowing Therapy There is no particular behavioral intervention that specifically applies to MS-related dysphagia. All methods can in principle be used depending on the individual pattern of swallowing impairment (Prosiegel et al. 2004). In addition to dysphagia, a severe cerebellar tremor can significantly affect food intake in MS patients. In this case, tools should be used that enable independent eating, ideally in conjunction with occupational therapeutic interventions (Bartolome et al. 2013). Pharmacotherapy Restivo et al. (2011) treated 14 MS patients with severe oropharyngeal dysphagia with injections of botulinum toxin A in a non-randomized observational study. All patients displayed hyperactivity of the upper esophageal sphincter. Guided by EMG, botulinum toxin A (Allergan, 10 units per side) was injected transcutaneously into the cricopharyngeal muscle. Follow-up examinations of swallowing function were performed using EMG and VFSS. Swallowing function improved significantly in all MS patients, and the mean PAS score decreased from 6.8 to 1.4 after 1 week. On average, the therapeutic effect lasted for 14.6 weeks. These results have not yet been reproduced in a larger cohort of patients with a randomized controlled design. Given that this kind of treatment may also cause side effects leading to a deterioration of swallowing function, further studies are clearly required. Neurostimulation Methods • In a randomized controlled pilot study (n = 20; 14 with relapsing-remitting MS; 6 with secondary chronic progressive MS; w/m: 13/7; mean age: 39.7; mean EDSS: 5.7; mean disease duration: 9.8 years), Restivo et al. (2013a) investigated the effect of pharyngeal electrostimulation (PES) on MS-related dysphagia in patients with moderate dysphagia (22.0 months). MS patients received either a 5-Hz stimulation for 10 min daily over a period of five consecutive days (n = 10; mean stimulation intensity: 14.2  mA) or a placebo stimulation (n = 10).

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Swallowing function was evaluated by VFSS and EMG. All included patients had infratentorial MS lesions, and 16 of 20 patients showed strategic lesions of the dorsolateral medulla oblongata. As shown by VFSS, dysphagia was characterized by disturbed pharyngeal bolus clearance and an impaired opening of the upper esophageal sphincter. Immediately after stimulation as well as both 2 and 4 weeks after the stimulation, there was a significant reduction in the PAS in the treatment group (from 6.4 to 3.1, 3.3, and 4.0, respectively), whereas there were no changes in the placebo group. All secondary outcome measures (EMG parameters) also improved significantly in the PES group and did not show changes in the control group (Restivo et al. 2013a). • In an uncontrolled FEES study, Bogaardt et al. (2009a) investigated the effect of NMES on swallowing function in 25 dysphagic MS patients (mean age: 53.1; mean disease duration: 16.5 years). FEES was not possible in eight patients, and the authors cited hypersensitivity and/or severe head tremor as reasons. The other 17 MS patients received one FEES each both 1 week before and 1 week after treatment. There was a significant decrease in pharyngeal saliva accumulation after treatment in six MS patients, and there was a significant decrease in aspiration during liquid swallowing in nine MS patients. Relevant side effects did not occur (III; Bogaardt et al. 2009a). • In a small case series, Marrosu et al. (2007) investigated the effect of vagus nerve stimulation on cerebellar tremor and dysphagia in three MS patients (mean age: 32; relapsing MS) after the neurosurgical implantation of a corresponding vagus nerve stimulator. All three patients were wheelchair-bound and needed assistance with eating (EDSS: 8.5). Clinically, patients had problems with both liquids and solid food. Swallowing function was evaluated with the 50-ml water test. After 2–3 months, there was an improvement in fragmented swallowing and the swallowing of liquids. No significant improvement could be observed for solid food consistencies. The effect persisted over a follow-up period of 26 months (III; Marrosu et al. 2007). Currently, there are no specific behavioral swallowing interventions for MS-related dysphagia.

Pharyngeal electrical stimulation can reduce penetration and aspiration (A) in MS-related dysphagia characterized by incomplete pharyngeal bolus clearance and an impaired opening of the upper esophageal sphincter due to brainstem lesions and especially due to lesions of the medulla oblongata.

7.3.10 Tetanus Pharmacotherapy In one case report, two dysphagic tetanus patients suffering from cricopharyngeal dysfunction were treated during the acute stage of the disease with injections of

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botulinum toxin A (Dysport, 30 units per muscle), which was injected transcutaneously into the cricopharyngeal muscle guided by EMG. 48  h after the injection, swallowing function improved such that the nasogastric tubes could be removed. Follow-up examinations of swallowing function with VFSS and EMG at 1, 2, and 4 weeks revealed a normal swallowing function, and the tonic hyperactivity in the cricopharyngeal muscle remained low. Patients had gained 3–6 kg in body weight by the final follow-up examination. Further injections of botulinum toxin A were not required (Restivo et al. 2006).

7.3.11 Brain Tumors Behavioral Swallowing Therapy In a retrospective study, the effect of behavioral swallowing therapy during inpatient rehabilitation in 24 dysphagic brain tumor patients was compared with that of an age-matched group of dysphagic stroke patients. Both groups showed a similar improvement of swallowing function (III). Based on these results, the authors suggested that there should be no “therapeutic nihilism” in dysphagic brain tumor patients and that rehabilitation should involve swallowing therapy that is similar in type and intensity to that of stroke patients (Wesling et al. 2003). Patients with brain-tumor-related dysphagia should receive a similar behavioral swallowing therapy during rehabilitation as is commonly provided for dysphagic stroke patients (C).

7.3.12 Amyotrophic Lateral Sclerosis (ALS) Pharmacotherapy To initiate adequate pharmacotherapy for ALS-related dysphagia, it is important to distinguish between predominantly central pseudobulbar dysphagia and predominantly peripheral bulbar dysphagia. Central pseudobulbar dysphagia (degeneration of the 1st motoneuron) is mainly characterized by slowed movements due to disease-­related spasticity and a disturbed coordination of the swallowing act. Antispasmodics—such as baclofen—may improve this symptom. In contrast, the peripheral bulbar form (degeneration of the 2nd motor neuron) is characterized by muscular atrophy and subsequent paresis of the swallowing muscles. In addition, neuromuscular transmission may be disturbed, leading to fatigable weakness of the swallowing muscles (similar to myasthenia). In such cases, a trial with pyridostigmine can be considered, beginning with 30 mg and then slowly increasing the dosage. When trying this pharmacological intervention, it is necessary to watch out for an increase in salivation as a side effect of treatment, which may require a combination with the anticholinergic drug ipratropium bromide. However, none of these therapeutic strategies has been studied in a randomized controlled trial (Kraft et al. 2010). According to the authors’ experience, treatment

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with pyridostigmine may indeed result in endoscopically verifiable improved swallowing in some dysphagic ALS patients, although this effect does not come close to what is usually seen in myasthenic dysphagia. The pharmacotherapy of sialorrhea is also used as a prophylaxis of pneumonia in dysphagic ALS patients. For this purpose, the German Neurological Society’s (DGN) guidelines recommend the following strategies, all of which have been poorly investigated: Scopoderm patches (every 1–3 days), amitriptyline (25–50 mg up to 3x daily), 1% atropine drops taken sublingually (1–2 drops up to 3× daily; https://dgn.org/wp-content/uploads/2012/12/030001_DGN_LL_ALS.pdf). As a further treatment option for cases in which anticholinergics are insufficient, botulinum toxin injections into the parotid and the submandibular glands are recommended. Several systematic reviews that evaluate the treatment of ALS-­related sialorrhea with botulinum toxin injections have been published in recent years (Young et al. 2011; Stokholm et al. 2013; Squires et al. 2014; Ng et al. 2017). As a result, according to current data, botulinum toxin injection in ALS patients is safe and effectively reduces sialorrhea. However, evidence from large randomized controlled trials remains limited. Overall, data are better for botulinum toxin B than for botulinum toxin A (Squires et al. 2014) because a methodologically sound randomized controlled trial has only been conducted in this clinical scenario for botulinum toxin B (albeit with a small study population): • Jackson et  al. (2009) included 20 ALS patients with sialorrhea in their study. Patients had either failed to respond to at least two anticholinergics or had not tolerated anticholinergic therapy because of its side effects. Guided by ultrasound, patients in the treatment group received 500 units of botulinum toxin B in the parotid gland and 750 units in the submandibular gland under electromyographic control. Significantly more patients in the treatment group showed a reduction in salivation after 2 and 4 weeks than did patients in the placebo group. Even after 3 months, half of all patients in the treatment group noticed less salivation. Relevant side effects—such as a worsening of dysphagia or of the patient’s vital capacity—did not occur (Ib).

ALS-related sialorrhea can be effectively treated with injections of botulinum toxin into the parotid and submandibular glands (A). • However, a 64-year-old woman who had been diagnosed with bulbar ALS 6 months earlier experienced an acute worsening of bulbar symptoms (including anarthria and severe dysphagia) 4 days after injections of botulinum toxin into the salivary glands, whereupon enteral nutrition via a PEG was required (III; Meijer et al. 2008). In an observational study, Restivo et al. examined the effect of injections of botulinum toxin into the upper esophageal sphincter (UES) in ALS patients with dysphagia characterized by esophageal hyperactivity. In each case, VFSS was

316

7  Treatment of Neurogenic Dysphagia

carried out before as well as 2, 4, and 20 weeks after the injections. The PAS was used as the main outcome parameter. ALS patients with and without involvement of the second motor neuron of bulbar muscles were differentiated. Affection of the second motor neuron was assumed when pathological spontaneous activity could be detected in EMG recordings of the suprahyoid/submental musculature and/or the pharyngeal musculature. A significant reduction in the PAS at 2 and 4 weeks was found in the group of patients without involvement of bulbar motoneurons. Additionally, no therapeutic effect could be observed in any patient with an additional disturbance of the oral phase of swallowing independent of whether the patient did or did not present with bulbar involvement. Based on these results, it can be concluded that injections of botulinum toxin are only effective for dysphagia treatment in ALS patients if there is isolated hyperactivity in the UES (III; Restivo et al. 2013b). Multicenter randomized controlled trials are required to assess the true benefits of injections of botulinum toxin into the UES in ALS-related dysphagia. Behavioral Swallowing Therapy Controlled studies on the effectiveness of the various methods of behavioral swallowing therapy on ALS-related dysphagia do not yet exist (Palovcak et al. 2007). In general, restorative procedures are indicated only during the initial stage of the disease or when the disease progresses very slowly. Over-exertion should be avoided in all cases because it can result in an exhaustion of swallowing muscles and further worsen swallowing function. In advanced stages of ALS, only compensatory strategies and adaptive methods should be used (Kuhnlein et  al. 2008; Bartolome et al. 2013). • In a FEES study by Leder et al. (2004), the following recommendations were made depending on the endoscopic findings: If premature spillage is the main problem, liquids should be thickened, and only small food boli should be swallowed. In the event of pharyngeal residue, repetitive clearing swallows or an additional liquid bolus is recommended to clean the hypopharynx (III). • In a non-randomized uncontrolled study that included 81 ALS patients, the effect of compensatory methods on ALS-related dysphagia was investigated using videomanometry. 24 patients displayed aspiration. 13 patients treated with the chin-­ tuck maneuver and six treated with head rotation regained a safe swallow without aspiration. Five patients did not benefit from either of these two compensatory procedures (III; Solazzo et al. 2011). • In an uncontrolled experimental study, the effect of 5-week EMST (50% of maximum expiratory pressure) on the respiratory and swallowing function of 15 ALS patients (mean age: 62.1; mean disease duration: 16.3 months; male/female: 7/8) was examined. The primary outcome parameter was maximum expiratory pressure, and secondary outcome parameters included VFSS parameters of swallowing function as well as quantification of the voluntary cough via spirometry. The implementation of EMST training proved to be safe and effective in this small

7.3  Disease-Specific Therapy

317

group of patients. After EMST training, improvements in maximum expiratory pressure and maximum hyoid movement during swallowing were seen. There were no changes in the PAS score (IIb; Plowman et al. 2016). In the early stages, when dysphagia is mild or moderate, selective exercises and skill training such as controlling spillage at the onset of the swallow, may enable the patient to safely swallow thin liquids for a period of time. EMST has been shown in a 5-week intervention trial to improve hyoid movement in ALS-related dysphagia (C).

Compensatory strategies may be effective in many ALS patients, especially in the mid to late stages. The chin-tuck maneuver, head rotation, frequent repeated swallowing, an additional liquid bolus, and thickened liquids may be particularly suitable for ALS-related dysphagia depending on the pattern of swallowing impairment (C). To date, no controlled trials have been performed to determine the optimal time of PEG implantation in ALS- patients. The German Neurological Society’s (DGN) guidelines cite psychological stress, weight loss, dehydration, and the risk of aspiration as indications for this procedure. The American Academy of Neurology also recommends PEG to be placed before forced vital capacity (FVC) declined below 50% (Miller et al. 2009). The decision to use PEG for ALS patients should not be solely dependent on swallowing function because the risk of complications increases with decreasing respiratory function. In case of reduced vital capacity to minutes until test on state is present

Liquid Swallow 4 Swallow 5 Swallow 6 White bread Swallow 7 Swallow 8 Swallow 9

Calculating off state dysphagia sum score

Step 7 Final evaluation

Comparing off state'and on state sum scores

Calculating on state dysphagia sum score

1 Positive: On state score more than 30% lower than of state score = L-dopa responsive dysphagia 2 Negative: On state score higher or not more than 30% lower than off state score = L-dopa unresponsive dysphagia

Off state FEES Bolus consistency

I Liquid: II Pudding: III Bread: 1. 2. 3.

Premature spillage 0, the bolus is behind the tongue 1, the bolus is at the base of tongue or valleculae 2, the bolus moves to lateral channels or the tip of the epiglottis 3, the bolus is in the piriforms or touches the laryngeal rim 4, the bolus falls into the laryngeal vestibule Penetration-aspiration events 0, No penetration -aspiration event 1, Penetration with protective reflex 2, Penetration without protective reflex 3, Aspiration with protective reflex 4, Aspiration without protective reflex Residue 0, No residues 1, Coating, no pooling 2, Mild pooling, less than half of the cavities 3, Moderate pooling, fills the cavities 4, Severe pooling, overflows the cavities Off state sum score:

/108

1. 2. 3.

1. 2. 3.

Appendix. Scales and Scores

385

On state FEES Bolus consistency

I Liquid: 1. 2. 3.

II Pudding: III Bread: 1. 2. 3.

Premature spillage 0, the bolus is behind the tongue 1, the bolus is at the base of tongue or valleculae 2, the bolus moves to lateral channels or the tip of the epiglottis 3, the bolus is in the piriforms or touches the laryngeal rim 4, the bolus falls into the laryngeal vestibule Penetration-aspiration events 0, No penetration -aspiration event 1, Penetration with protective reflex 2, Penetration without protective reflex 3, Aspiration with protective reflex 4, Aspiration without protective reflex Residue 0, No residues 1, Coating, no pooling 2, Mild pooling, less than half of the cavities 3, Moderate pooling, fills the cavities 4, Severe pooling, overflows the cavities On state sum score:_______ /108

Final evaluation

FEES-Levodopa-Test

Results

Off state sum score

On state sum score

Percentage improvement On vs. Off

more than 30% less than 30%

Interpretation

positive negative

1. 2. 3.

Appendix. Scales and Scores

386

 EES Tensilon Test (Tensilon = Edrophonium Chloride), from F Warnecke et al., J Neurol. 2008;255:224–30, with permission FEES with simultaneous Tensilon application

pureed food

FEES following a standard protocol

penetration or aspiration

improvement

Result of FEES-Tensilon-Test

positive

pureed food no improvement

negative

no penetration and aspiration

soft solid food + thin liquids

moderate or severe pathological findings

food consistency with the most severe pathological finding

improvement

positive

negative no improvement

no or mild pathological findings Fatigable swallowing test (FST)

thirty consecutive small pieces of white bread

pathological

normal

thirty consecutive small pieces of white bread

improvement

no improvement

positive

negative

negative

Appendix. Scales and Scores

 urray Secretion Rating Scale (Short version), from Murray et al., M Dysphagia 1996; 11: 99–103, with permission 0. Normal (moist) 1. Pooling in valleculae/pyriforms 2. Pooling in laryngeal vestibule transiently 3. Pooling in laryngeal vestibule consistently

387

Appendix. Scales and Scores

388

 urray Secretion Rating Scale (Long Version), from Murray et al. M Dysphagia 1996; 11: 99–103, with permission Murray Secretion Rating Scale (Long version)

0. Most normal rating. No visible secretions anywhere in the hypopharynx or some transient

bubbles visible in the valleculae and pyriform sinuses. These secretions were not bilateral or deeply pooled

1. Any secretions evident upon entry or following a dry swallow in the channels surrounding the laryngeal vestibule that were bilaterally represented or deeply pooled. This rating would include cases where there is a transition in the accumulation of secretions during the observation segment. A subject could start with no visible secretions but accumulate secretions in an amount great enough to be bilaterally represented or deeply pooled. Likewise, a subject would be rated as a "1" if initially presenting with deeply pooled bilateral secretions and ending the observation segment with no visible secretions

2. Any secretions that changed from a "1" rating to a "3" rating during the observation period 3. Most severe rating. Any secretions seen in the area defined as the laryngeal vestibule (Fig. I). Pulmonary secretions were included if they were not cleared

Appendix. Scales and Scores

389

 enetration-Aspiration Scale (PAS), from Rosenbek et al., P Dysphagia 1996; 11: 93–98, with permission Penetration-Aspiration Scale 1 2 3 4 5 6 7 8

Material does not enter the airway. Material enters the airway, remains above the vocal folds, and is ejected from the airway. Material enters the airway, remains above the vocal folds, and is not ejected from the airway. Material enters the airway, contacts the vocal folds, and is ejected from the airway. Material enters the airway, contacts the vocal folds, and is not ejected from the airway. Material enters the airway, passes below the vocal folds, and is ejected into the larynx or out of the airway. Material enters the airway, passes below the vocal folds, and is not ejected from the trachea despite effort. Material enters the airway, passes below the vocal folds, and no effort is made to eject.

390

Appendix. Scales and Scores

 unctional Oral Intake Scale (FOIS), from Crary et al., Arch Phys F Med Rehabil 2005; 86: 1516–1520, with permission The Functional Oral Intake Scale (FOIS) TUBE DEPENDENT (levels 1–3) 1 No oral intake 2 Tube dependent with minimal/inconsistent oral intake 3 Tube supplements with consistent oral intake TOTAL ORAL INTAKE (levels 4–7) 4 Total oral intake of a single consistency 5 Total oral intake of multiple consistencies requiring special preparation 6 Total oral intake with no special preparation, but must avoid specific foods or liquid items 7 Total oral intake with no restrictions

Appendix. Scales and Scores

391

 ysphagia Outcome and Severity Scale (DOSS), from O’Neil et al. D Dysphagia 1999; 14: 139–145, with permission Full per-oral nutrition (P.O): Normal diet Level 7: Normal in all situations • Normal diet • No strategies or extra time needed Level 6: Within functional limits/ modified independence • Normal diet, functional swallow • Patient may have mild oral or pharyngeal delay,retention or trace epiglottal under- coating but independently and sponta-neously compensates/clears • May need extra time for meal • Have no aspiration or penetration across consistencies Full P.O: Modified diet and/or independence Level 5: Mild dysphagia: Distant supervision, may need one diet consistency restricted May exhibit one or more of the following • Aspiration of thin liquids only but with strong reflexive cough to clear completely • Airway penetration midway to cords with one or more consistency or to cords with one consistency but clears spontaneously • Retention in pharynx that is cleared spontaneously • Mild oral dysphagia with reduced mastication and/or oral retention that is cleared spontaneously

Nonoral nutrition necessary Level 2: Moderately severe dysphagia: Maximum assistance or use of strategies with partial P.O only (tolerates at least one consistency safely with total use of strategies)

May exhibit one or more of the following • Severe retention in pharynx, unable to clear or needs multiple cues • Severe oral stage bolus loss or retention, unable to clear or needs multiple cues

Level 4: Mild-moderate dysphagia: Intermittent supervision/cueing,one or two consistencies restricted May exhibit one or more of the following • Retention in pharynx cleared with cue • Retention in the oral cavity that is cleared with cue • Aspiration with one consistency, with weak or no reflexive cough or airway penetration to the level of the vocal cords with cough with two consistencies or airway penetration to the level of the vocal cords without cough with one consistency Level3: Moderate dysphagia: Total assist, supervision, orstrategies, two or more diet consistencies restricted May exhibit one or more of the following • Moderate retention in pharynx, cleared with cue • Moderate retention in oral cavity, cleared with cue • Airway penetration to the level of the vocal cords without cough with two or more consistencies or aspiration with two consistencies, with weak or no reflexive cough or aspiration with one consistency, no cough and airway penetration to cords withone, no cough

• Aspiration with two or more consistencies, no reflexive cough, weak volitional cough or aspiration with one or more consis-tency, no cough and airway penetration to cords with one or more consistency, no cough Level 1: Severe dysphagia: NPO: Unable to tolerate any P.O. safety May exhibit one or more of the following

• Severe retention in pharynx, unable to • clear Severe oral stage bolus loss or retention, unable to clear • Silent aspiration with two or more consistencies, nonfunctional volitional cough or unable to achieve swallow

Appendix. Scales and Scores

392

 tandardized Endoscopic Swallowing Evaluation S for Tracheostomy Decannulation in Critically Ill Neurologic Patients (SESETD Protocol), from Warnecke et al., Crit Care Med, 2013; 41(7): 1728–1732, with permission FEES-PROTOCOL

MAIN FINDINGS Massive pooling of saliva, silent penetration/aspiration of saliva

DECANNULATION?

1)

Secretions

2)

Spontaneous swallows

< 1 per minute missing “whiteout”

no

3)

Laryngeal sensibility/ cough

Anästhesia no effective cough

no

4)

Pureed consistency

Silent aspiration of complete bolus

no

5)

Fluids

Silent aspiration without triggering of swallowing reflex

no

6)

Transstomatal examination

no

Massive subglottic pooling of saliva, silent aspiration of complete bolus

no

No evidence of main findings

yes

Index

A ACE inhibitors, 280, 281, 287, 288 Act of swallowing effortful, 229, 271, 274, 276, 278, 283, 305, 309, 336 supraglottic (SGS), 226, 231, 232, 235, 271, 278 Agnosia, orotactile, 124 Airflow method, 63, 128 Amantadine, 280, 281, 285, 286, 301, 308 Amitriptyline, 282, 315 Amyloidosis, 163 Amyotrophic lateral sclerosis (ALS), 20, 22–24, 42, 76, 92, 136, 156–161, 163, 173, 190, 197, 200, 226, 254, 272, 278, 314–318, 362 Anamnesis, 40 Anatomic-physiologic assessment, 159, 227 Anesthesia, 29, 30, 60, 90, 93 Ansa cervicalis, 4 Anti-IgLON5 syndrome, 194 Apomorphine, 67, 297, 298, 301 Apraxia, 137, 138, 153, 308 buccofacial, 248, 249 Arnold–Chiari malformation, 197, 200 Arthritis, rheumatoid, 195 Arytenoid cartilage, 62, 63, 128, 260, 282 Arytenoid tremors, 135, 137, 309 Aspiration, 9, 10, 17, 30, 40, 42, 43, 45, 46, 48, 50, 60, 61, 63, 64, 66, 69–73, 75, 77–79, 81, 84, 86, 87, 93, 97–99, 111, 114, 115, 118–120, 123, 125, 127, 129, 130, 133, 134, 136–139, 141, 143, 144, 147, 148, 151, 153, 157–160, 162, 166, 168, 169, 171, 175, 176, 179, 181–183, 185, 189–191, 193, 195, 231, 234–236, 238, 242, 244–247, 250, 251, 253, 255,

© Springer Nature Switzerland AG 2021 T. Warnecke et al., Neurogenic Dysphagia, https://doi.org/10.1007/978-3-030-42140-3

256, 259, 261, 269, 271, 274, 276, 278–280, 283, 285, 287, 288, 293, 295–298, 300, 302, 303, 305, 309, 311, 316, 321, 323, 326, 332, 356, 358–360, 362, 363 pneumonia, 11, 116, 125, 133, 135–137, 139, 142, 143, 147, 156, 167, 173, 177, 182, 185, 187–189, 224, 253, 274, 278, 280, 281, 287, 298, 353, 360, 362 screening, 43–50, 127, 199, 242, 244, 247, 249, 257 Ataxia, hereditary, 187–188, 197, 324 Atropine, 315 B Baclofen, 282, 314 Basal ganglia, 13, 14, 18, 113, 146, 280, 285, 301 Base-of-tongue, 187–188, 228, 238 Becker muscular dystrophy (BMD), 172 Bedside screening, 43 Besinger score, 167 Bilateral anterior opercular syndrome, 113, 150 Biofeedback, 95, 295, 323 Blepharospasm, 141, 142 Blue dye test, 44, 48 Body mass index (BMI), 42, 126, 355 Bogenhausener Dysphagia Score (BODS), 50 The Bosten Residue and Clearance Scale (BRASC), 74 Botulinum toxin, 171, 281, 282, 306, 307, 310, 312, 314–316, 321, 323 Brain metastases, 153–154 Brain tumors, 153–154, 196, 275, 314

393

394 C Cabergoline, 285, 286, 301 Capsaicin, 48, 280, 281, 286 Carotid endarterectomy (CEA), 193 Central pattern generator (CPG), 11, 13, 161 Cerebellar degeneration, subacute, 155, 197, 199, 278, 333 Cerebellum, 13, 146, 189, 190 Cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalopathy (CADASIL), 119 Cerebral microangiopathy, 119 Chameleon tongue, 139 Chicago classification, 91–93, 131, 181 Chin-tuck maneuver, 79, 270, 275–278, 283, 295, 296, 302, 303, 305, 309, 316, 317 Chronic obstructive pulmonary disease (COPD), 195 Cingulate cortex, 13, 14, 27 Clinical assessment of hyoid movement, 49, 50 Close view, 62 CNS listeriosis, 150 Collet–Sicard syndrome (CSS), 113, 154 Computer tomography (CT), 83, 97–99 Contrast agents, 82–83, 96, 97, 244 Cortex, primary sensorimotor, 13, 14, 16, 18, 24, 25, 27, 28, 31, 118 Cortical middle cerebral artery, 112 Cortical plasticity, 18–34, 330, 332 Corticobasal degeneration (CBD), 132 Corticobasal syndrome (CBS), 132, 133, 137, 138 Cough reflex test (CRT), 48 Cricopharyngeal bar, 175 Critical illness myopathy (CIM), 165, 254–256 Critical illness polyneuropathy (CIP), 94, 165–167, 254–256 Cuneus, 13 D Decannulation, 166, 171, 260, 261, 290, 318, 334 Decontamination, oral, 288, 289 Dehydration, 11, 111, 116, 224, 317, 362 Dementia Alzheimer’s disease, 117–118 frontotemporal dementia, 119–120 frontotemporal lobar degeneration, 196 Lewy bodies, 120–121 vascular, 119

Index Dermatomyositis (DM), 92, 155, 156, 172 Diagnostics, gold standard, 43, 50, 57, 59, 81, 99, 126, 158, 244, 274, 322 Diaschisis, 18 Diffuse idiopathische skeletal hyperostosis (DISH), 84, 191 Digastric muscle, 4, 96, 335 Digital spot imaging (DSI), 82 Distribution neurons, 12 Dopamine, 285, 299, 301 Dorsal swallowing group (DSG), 11–13, 66, 81 Dorsolateral medulla oblongata, 76, 111, 113, 114, 201, 313 Dysferlinopathy, 172 Dysphagia ALS-related, 157–161, 163, 314–317 botulism-related, 171, 197, 200 bradykinetic, 128, 137, 143, 144 bulbar, 155–157, 160, 161, 172, 173, 190, 314 CBD-related, 132 chronic myasthenes, 319 classification, 157 definition, 8 documentation, 78 dyskinetic, 143, 144 dystonic, 140, 141, 310 fatigable, 67, 76, 168–171, 314 functional, 27, 28, 185, 277, 278 GBS-related, 164 Huntington-related, 139, 311 LEMS-related, 171 limit, 44, 94, 95, 116 MG-related, 170, 319 MSA-related, 135, 136, 309 MS-related, 147, 312, 313 myopathy-related, 172 myositis-related, 173, 323 neuroleptic-induced, 76, 143, 144, 196, 200 position, 190 post-polio-related, 151 postural, 141 PSP-related, 134, 135, 309 psychogenic, 185–187, 197, 200 stroke-related, 9, 18, 39, 50, 111, 114, 115, 283, 289, 290, 293 summary assessment, 78, 79 TBI-related, 183, 185 tetanus-related, 152 Dysphagia score, 242, 274, 289 Dysphagia Limit Test, 44 Dystonia cervical, 140, 141 oromandibular, 140–142, 310

Index Dystrophy, myotonic, 76, 172, 180–182, 197, 200 E Eating and drinking aids, 116, 123, 311, 321, 358 Electroencephalography (EEG), 13 Electromyography (EMG), 94, 95, 99, 118, 131, 141, 142, 148, 149, 152, 160, 163, 170, 174, 182, 187, 193, 199, 200, 202, 275, 293, 295, 297, 303, 306, 312–314, 316, 321, 336 Electrostimulation, 289, 335, 336 neuromuskular (NMES), 270, 279, 291, 292, 304, 306, 310, 312, 313, 330, 335–336 EMG biofeedback (EMGBF), 64, 95, 99, 187, 224, 225, 228, 230, 231, 233–235, 237–239, 275, 279, 293, 295, 304, 305, 323 Endoscopic-neurological, 75 Epidemiology, 8, 253 Epiglottal tremor, 144 Epiglottis, 2, 4, 62, 63, 65, 66, 70, 74, 87, 145, 163, 169, 181, 225, 228, 229, 231, 232 Esophageal phase, 1, 3, 4, 8, 14, 79, 82, 88, 99, 130, 138, 146, 163, 169, 172, 187 Esophageal spasm, 131, 187 diffuse (DES), 130, 131, 134, 140 Esophageal sphincter impaired opening, 75, 76, 87, 99, 172, 176, 185, 196, 271, 274, 281, 283, 313 opening, 4, 8, 20, 86, 87, 91, 112–115, 130, 131, 136, 141, 152, 160, 174, 177, 179, 181, 226, 228, 271, 281, 284, 285, 293, 301, 318, 322, 323, 330, 358 upper (UES), 2–4, 8, 20, 29, 75, 76, 84, 86–88, 91–94, 99, 112–115, 129–131, 134, 136, 142, 148, 152, 160, 169, 172, 174–179, 181, 182, 185, 195, 196, 202, 226, 271, 274, 278, 281, 283–285, 293, 302, 306, 312, 313, 315, 318, 322, 323, 330, 336 Evans blue dye test, 259 Evidence-based medicine (EBM), 39, 50, 268–269 levels of evidence, 268 strength of recommendations, 295 Examination clinical neurological, 168, 199 trans-stomatal, 261 unit, 58, 59

395 Expiratory muscle strength training (EMST), 274, 278, 295, 296, 303–305, 311, 316, 317 F Facial nerve, 4, 164 Facial-Oral Tract Therapy (F.O.T.T.®), 270, 277 Fasciculations, 20, 49, 71, 156, 159 Fatigable swallow test (FST), 67, 168, 171 Flexible endoscopic dysphagia severity scale (FEDSS), 64, 78, 249–253 Flexible endoscopic evaluation of swallowing (FEES), 40, 45, 47, 48, 50, 56, 59 certificate, 57, 80 curriculum, 80, 81 fatigable swallow test, 67 instructor status, 57 levodopa test, 66, 67, 79, 299, 300, 308 Tensilon® test, 67, 68, 168, 169, 171, 199, 200, 202 Flexible endoscopic evaluation of swallowing with sensory testing (FEESST), 123, 159, 194, 282 Friedreich’s ataxia (FA), 188 Frontal operculum, 13, 16, 118 Functional dysphagia therapy (FDT), 270, 277, 278, 330 Functional magnetic resonance imaging (fMRI), 13 G Generator neurons, 12 Geniohyoid muscle, 4, 95, 96 Glasgow Coma Scale (GCS), 183, 185 Globus hystericus, 186, 187 Globus pharyngis, 9, 186, 187 Gugging Swallowing Screen (GUSS), 44, 245, 288 Guillain–Barré syndrome (GBS), 76, 164, 165, 254, 318, 319 H Harris–Benedict equation, 356 Head rotation, 316, 317 to the paretic side, 276, 278, 284, 285 Heart surgery, 194 Hemispheric specialization, 14–18 Herpes encephalitis, 150 Hiccups, 149, 150, 282 High-frequency cinematography, 82

396 High-resolution manometry (HRM), 90–93, 115, 131, 174, 195 Home position, 62 Huntington’s disease (HD), 42, 76, 92, 138–140, 196, 278, 310–311 Hyoid-laryngeal movement, 115 Hypersalivation, 9, 146, 282 Hypoglossal nerve, 4, 119, 154, 184, 193, 194 Hypopharynx, 2, 9, 62, 63, 66, 67, 70, 72, 115, 120, 158, 159, 175, 191, 195, 226, 229, 316, 323, 331 initial observation without swallowing, 63, 84 sensitivity testing, 59, 99 I Ice chip, 235–236, 239, 256, 318 IgLON5 syndrome, 194–195 Inclusion body myositis (IBM), 76, 172, 174, 175, 200, 284, 321–323 Inferior pharyngeal constrictor muscle, 8, 152 Insular cortex, 13, 14, 16, 27, 113, 186 Intensive care unit (ICU), 165, 166, 168, 253–261 International Dysphagia Diet Standardisation Initiative (IDDSI), 271 Intubation, 41, 60, 111, 164, 165, 194, 195, 251, 252, 257, 275 K Kearns–Sayre syndrome (KSS), 178, 179 Kennedy’s disease (KD), 20, 79, 162–163, 197, 318 L Lambert–Eaton myasthenic syndrome (LEMS), 155, 156, 170, 171 Larynx, 2, 4, 8, 29, 62, 65, 71, 73, 84, 86, 96, 98, 136, 184, 190, 227, 230–232, 235, 237, 255, 261, 271, 276, 335 Leakage, 72, 87, 117, 234 Leaking, 50 Lee Silverman Voice Treatment (LSVT®), 303, 305 Levodopa, 280, 281, 285, 297–301, 308, 309 Lewy bodies, 120–121, 301, 302 Lidocaine, 60, 61 Lipid storage disease, 188 Logemann standard, 81, 84 Long-term ventilation, 165, 166, 255, 256, 259

Index M Magnetoencephalography (MEG), 13, 16, 20, 22, 24, 25, 27, 28, 31, 186, 329, 332 Malnutrition, 11, 111, 116, 123, 125, 139, 157, 224, 354–364 Masako maneuver, 270, 274, 284, 292 Medulla oblongata, 11–13, 111, 113, 114, 116, 149, 155, 301, 302, 313 Medulla oblongata infarction, 76, 111, 114 Meige syndrome, 141, 142 Meningeosis, 154, 197, 200 Meningitis meningococcal, 150 pneumococcal, 150 Miller Fisher syndrome (MFS), 164 Modified barium swallow (MBS), 81 Modifizierter Evan’s Blue Dye Test (MODS), 44 Motor neuron diseases (MNDs), 20, 228 Multiple-consistency test, 47, 245–247 Multiple sclerosis (MS), 147–149, 196, 197, 281, 312–313, 334 Multiple system atrophy (MSA), 67, 76, 132, 135–137, 188, 306, 309–310 Munich Dysphagia Test (MDT), 126 Münster Dysphagia Score (MDS), 64, 66 Muscle propulsions, 175 pharyngeal, 175, 176 Muscular dystrophy Duchenne muscular dystrophy, 172, 197 facioscapulohumeral, 179–180, 197 limb-girdle dystrophy, 173 oculopharyngeal, 172, 176–177, 197, 200, 281, 320–322 Myasthenia gravis (MG), 26, 67, 76, 156, 167–170, 197, 200, 201, 319–320 Myasthenic crisis (MC), 167, 319 Mylohyoid muscle omohyoid muscle, 4 palatopharyngeus muscle, 4 pterygopharyngeus muscle, 4 sternothyroid muscle, 4 stylohyoid muscle, 4 stylopharyngeus muscle, 4 thyrohyoid muscle, 4 Myoclonus palatal, 190–191 pharyngolaryngeal, 190, 191 velopharyngolaryngeal, 71 Myopathies, 8, 41, 172–182, 197, 320–323 oculopharyngodistal (OPDM), 177, 197 Myositis, 26, 172–176, 197, 202, 254, 323

Index Myotomy, cricopharyngeal, 99, 281, 283–285, 317, 318, 320–323 Myotonia, oropharyngeal, 182 Myotonic dystrophies, 197 Myotonic response, 182 N Nasopharynx, 2, 4 Necrotizing myositis (NM), 172, 173 Neuroacanthocytosis syndromes (NAS), 140 Neuroborreliosis, 150 Neurodegeneration with brain iron accumulation (NBIA), 140 Neurointensive care unit, 60, 99, 241, 261 Neuromyelitis optica (NMO), 149 Neuromyotonia (NMT), 155 Neuropathies, 190, 193 Niemann–Pick disease (NPD), 188–189, 197 Nucleus ambiguus (NA), 11, 12, 114 solitary nucleus (SN), 11, 12 Nutrition, 83, 121 enteral, 296, 315, 333, 357, 362–364 parenteral, 193, 363, 364 Nutritional management, 257, 261, 354 Nutritional requirements, 356, 358 Nutritional therapy, 356–362 O Obesity, 191 Obesity paradox, 354 Obstructive sleep apnea syndrome (OSAS), 195 Odynophagia, 9, 193 Older, 74 Ophthalmoplegia plus, 178 Oral onset time, 85 Oral phase, 1, 3, 10, 13, 15, 17, 18, 20, 28, 50, 65, 72, 84, 87, 94, 112, 113, 115, 118, 121, 124, 130, 138, 139, 141, 148, 168, 189, 247, 298, 300, 308, 316, 318, 328 muscle groups, 94 Oral-phase dysphagia, 160, 328 Oral preparatory phase (OPP), 1, 3, 10, 13, 15, 17, 18, 72, 119, 139, 236, 298 Oral-tactile agnosia, 118 Oral transit time (OTT), 87, 146, 277, 298, 302, 303 Oropharynx, 2, 31, 65, 160, 195, 246, 323 Osteophytes, 84, 225 Overlap-myositis, 172 Oxygen desaturation, 45

397 P Palatine arches, 275 thermal stimulation, 31, 234, 275, 279, 292, 335, 336 Pantothenate kinase-associated neurodegeneration (PKAN), 140 Parahippocampal, 13 Paraneoplastic syndromes, 154–156, 173 Parietal association cortex, 13 Parkinsonism atypical, 124, 132, 283, 307 idiopathic, 124 Parkinson’s disease, 124–126, 131, 137, 276 Penetration, 9, 10, 17, 28, 43, 46, 48, 50, 60, 61, 63, 64, 66, 69, 70, 72, 73, 75, 77, 78, 85–87, 97, 111, 112, 114, 118, 119, 121, 123–125, 129, 133, 138, 144, 145, 147, 148, 152, 153, 158, 162, 166, 169, 173, 175, 181, 182, 184, 190, 194, 195, 232, 235, 238, 247, 252, 256, 259, 260, 271, 276, 281–283, 295, 297, 299, 300, 302, 303, 305, 309, 313, 323 Penetration–aspiration scale (PAS), 61, 73, 78, 148, 159, 280, 290, 292, 293, 300, 303, 304, 310, 312, 313, 316, 317, 333, 334 Percutaneous endoscopic gastrostomy (PEG), 117, 319, 362 Phagophobia, 186, 187 Pharmacotherapy, 279–283, 296, 310, 312–315, 319–321 Pharyngeal electrical stimulation (PES), 32, 33, 330–335 Pharyngeal manometry, 93, 160, 175 Pharyngeal phase, 1–4, 10, 14, 15, 17, 18, 20, 25, 40, 57, 64, 65, 72, 84, 87, 88, 94, 112, 113, 118, 119, 121, 124, 131, 136, 138, 139, 142, 143, 148, 149, 151, 158, 160, 163, 165, 166, 168, 169, 172, 174, 176, 188, 189, 246, 292, 299, 300, 328 muscle groups, 2, 4 Pharyngeal squeeze maneuver, 70, 114, 154, 175, 227 Pharyngeal transit time (PTT), 85, 87, 174, 176 Piriform sinus, 2, 62, 66, 71, 72, 74–76, 85–87, 111, 113, 114, 116, 128, 129, 133, 134, 136, 138, 141, 144, 148, 151–153, 158, 159, 161, 169, 171–173, 177, 181, 194, 196, 302, 303, 323 Pneumonia, 11, 18, 111, 116, 121, 123, 125, 133, 147, 180, 184, 239, 242, 244, 251, 252, 274–276, 280, 285–289, 294, 296, 302, 305, 315, 333

398 Progressive supranuclear palsy (PSP), 67, 76, 79, 132–135, 137, 162, 196, 308–309 Q Quality of life, 11, 42, 116, 117, 123, 125, 126, 157, 176, 274, 278, 290, 304, 305, 311, 360 R Rapid assessment of aspiration risk, 43, 48, 49 Recurrent laryngeal nerve (RLN), 71, 184, 185, 191, 193, 255 Reflexive swallow response, 50 Repetitive transcranial magnetic stimulation (rTMS), 289–291, 325–330, 332 Residues, 9, 10, 46, 50, 66, 67, 72, 74–76, 78, 79, 85–87, 113, 114, 118–121, 123, 124, 128–130, 134, 138, 143, 144, 146, 148, 151–153, 158–161, 163, 168, 169, 171–173, 175–177, 179, 181, 194, 195, 227–230, 237, 252, 271, 274, 276–279, 283, 293, 297, 298, 300, 302, 303, 305, 310, 311, 316, 320, 323, 326, 357 Residues, 28, 163, 182, 196 Retentions, 9, 72, 182, 282, 298 Rhombencephalitis, 150, 155, 156, 196 Risus sardonicus, 152, 197 S Saliva, 1, 2, 9, 13, 14, 29, 33, 46, 47, 50, 63, 64, 68, 97, 99, 111, 112, 116, 129, 132, 133, 143, 171, 181, 242, 251, 252, 256, 259–261, 282, 288, 301, 313, 332, 359, 360 Saliva pooling, 68, 256, 260 Sarcopenia, 121, 354, 355 Scleroderma, 195, 282 Scopoderm patches, 315 Semisolid bolus swallow test, 44 Sensitivity testing, 49, 95, 244 Shaker exercise, 228, 270, 274, 278, 284, 293, 295, 318 Sialorrhea, 9, 125, 126, 128–130, 132, 146, 282, 306–308, 315 Parkinson-related, 307 Sip feed nutrition, 361, 362 Sjögren syndrome (SjS), 195, 282 Skull base tumors, 197, 200 Soft palate paresis, 71, 171 Spinal and bulbar muscular atrophy (SBMA), 20, 24, 162–163

Index Spinal cord injury, 184, 185 Spinocerebellar ataxia (SCA), 187, 188 Spondylophytes, 191, 192 Spontaneous swallowing frequency, 282 Standard FEES protocol, 59–64, 68, 78, 225, 250 Standardized swallowing assessment (SSA), 46, 47 Stress test, 84, 94 Stridor, 135, 309 inspiratioinal, 135 Stroke, 9, 17, 18, 20, 32, 42, 43, 45, 47, 50, 56, 60, 64, 66, 69, 76, 78, 80, 110–116, 121, 127, 153, 154, 184, 194, 196, 199, 201, 226, 242, 244–247, 249–254, 269, 272, 275–277, 280, 281, 283, 285–295, 301, 307, 314, 326, 329–336, 353–355, 362, 363 Stroke units (SUs), 56, 57, 60, 64, 66, 99, 241–257, 259–261, 270 Subglottic region, 9, 261, 262 Substance P, 31, 33, 280, 286, 287, 301, 302, 332 Supplementary motor areas (SMA), 13, 23, 25–28 Swallow provocation test (SPT), 44, 286 Swallowing, 1, 4, 8, 11–34, 39–41, 43, 44, 46 apraxia, 87, 118, 124, 186 bradykinetic, 137 centers, 11–14, 23, 25, 26, 28, 153, 182, 301, 302, 329 dystonia, 142, 143 endoscopy, 159, 262 examination, 39, 40, 43, 49–50, 138, 139, 164, 183, 224, 248–250, 257, 259, 261, 279 frequency, 132, 260, 277, 278, 308, 334 pills, 282, 283 supramedullary network, 8, 12, 14, 15, 18, 25, 28, 29, 31, 118, 135, 254, 329, 330 Swallowing provocation test (SPT), 47, 48, 72, 246, 247 Swallowing quality of life (SWAL-QOL) questionnaire, 42, 126, 127, 162, 176, 195, 303–305, 311 Swallowing reflex, 9–11, 14, 31, 49, 134, 139, 141, 145, 148, 171, 246, 256 Swallowing therapy adaptive methods, 271, 273, 274, 276, 277, 291, 294, 316 compensatory methods, 276, 277, 316 Systemic lupus erythematosus (SLE), 195

Index

399

T Tactile-thermal palatal arch stimulation, 279, 292, 295, 335 Test of oral bolus control, 133 Test of oral containment, 72 Tetanus, 151–153, 197, 200, 281, 313–314 Tongue paresis, 193 repetitive pump movements, 130 Tongue-pressure resistance training, 293 Toronto bedside swallowing screening test (TOR-BSST©), 244 Tracheotomy, 41, 60, 150, 165, 256, 257, 259–261, 310, 318 Training curriculum, 56, 57, 80–81 Transcranial direct-current stimulation (tDCS), 289–291, 326–330 Transnasal endoscopy, 261 Trigeminal nerve, 4, 119 Trismus, 152, 197 Type II glycogenosis, 172

Velum, 2, 4, 31, 62, 87, 159 Ventral swallowing group (VSG), 11–13, 114 Vestibular folds, 144 Video-assisted swallowing therapy (VAST), 296, 304 Videofluoroscopy (VFS), 43, 45, 82, 98, 99, 130, 131, 224, 333 Vocal folds, 2, 9, 62, 63, 71–73, 129, 139, 231–233, 235, 255, 303, 309 chorea, 139 paresis, 135–137, 193, 195, 276, 281, 309 Volume-viscosity swallow test (VVST), 44, 46, 158

V Vagus nerve, 4, 71, 119, 193, 277, 313 Valleculae, 2, 62, 66, 72, 74–76, 79, 85–87, 111, 114, 128–130, 133, 134, 138, 141, 142, 144, 151–153, 158, 159, 161, 163, 169, 171, 172, 177, 179–181, 194, 228, 229, 297, 298, 300, 302, 303 Valleculae/piriform sinus, 120 Vasculitis, 119 Velolingual closure, 169 Velopharyngeal closure (VPC), 2, 61, 63, 86, 231, 238

X Xerostomia, 121, 282, 359

W Wallenberg’s syndrome, 196, 277 Water test, 44, 127, 244 Weight loss, 116, 126, 134, 139–143, 154, 157, 185, 186, 191, 317, 321, 354, 356

Y The Yale Pharyngeal Residue Severity Rating Scale, 74 Yale protocol, 242 Z Zenker’s diverticulum, 8, 9