Pediatric Swallowing and Feeding: Assessment and Management, Third Edition [Third ed.] 1944883517, 9781944883515

Table of contents :
Foreword
Preface
About the Editors
Contributors
1. Overview of Diagnosis and Treatment
2. Anatomy, Embryology, Physiology, and Normal Development
3. Neurodevelopmental Assessment of Swallowing and Feeding
4. The Upper Airway and Swallowing
5. Pediatric Gastroenterology
6. Pediatric Nutrition
7. Clinical Swallowing and Feeding Assessment
8. Instrumental Evaluation of Swallowing
9. Management of Swallowing and Feeding Disorders
10. Pulmonary Manifestations and Management Considerations for Aspiration
11. Drooling and Saliva/Secretion Management
12. Clinical Genetics: Evaluation and Management of Patients With Craniofacial Anomalies Associated With Feeding Disorders
13. Behavioral Feeding Disorders: Etiologies, Manifestations, and Management
Index

Citation preview

Pediatric Swallowing and Feeding Assessment and Management Third Edition

Pediatric Swallowing and Feeding Assessment and Management Third Edition

Joan C. Arvedson, PhD Linda Brodsky, MD Maureen A. Lefton-Greif, PhD

5521 Ruffin Road San Diego, CA 92123 e-mail: [email protected] Website: https://www.pluralpublishing.com Copyright © 2020 by Plural Publishing, Inc. Typeset in 10.5/13 Minion Pro by Flanagan’s Publishing Services, Inc. Printed in the United States of America by McNaughton & Gunn, Inc. All rights, including that of translation, reserved. No part of this publication may be reproduced, stored in a retrieval system, or transmitted in any form or by any means, electronic, mechanical, recording, or otherwise, including photocopying, recording, taping, Web distribution, or information storage and retrieval systems without the prior written consent of the publisher. For permission to use material from this text, contact us by Telephone:  (866) 758-7251 Fax:  (888) 758-7255 e-mail: [email protected] Every attempt has been made to contact the copyright holders for material originally printed in another source. If any have been inadvertently overlooked, the publishers will gladly make the necessary arrangements at the first opportunity. Disclaimer: Please note that ancillary content (such as documents, audio, and video, etc.) may not be included as published in the original print version of this book. Library of Congress Cataloging-in-Publication Data Names: Arvedson, Joan C., author, editor. | Brodsky, Linda, editor. | Lefton-Greif, Maureen A., author, editor. Title: Pediatric swallowing and feeding : assessment and management / Joan C. Arvedson, Linda Brodsky, Maureen A. Lefton-Greif. Description: Third edition. | San Diego, CA : Plural Publishing, [2020] | Includes bibliographical references and index. Identifiers: LCCN 2019013064| ISBN 9781944883515 (alk. paper) | ISBN 1944883517 (alk. paper) Subjects: | MESH: Feeding and Eating Disorders of Childhood | Deglutition Disorders | Feeding Behavior—physiology | Deglutition—physiology | Infant | Child Classification: LCC RJ463.I54 | NLM WM 175 | DDC 618.92/31—dc23 LC record available at https://lccn.loc.gov/2019013064

Contents Foreword vii Preface ix xi About the Editors Contributors xiii



1 Overview of Diagnosis and Treatment



2 Anatomy, Embryology, Physiology, and Normal Development

11



3 Neurodevelopmental Assessment of Swallowing and Feeding

75



4 The Upper Airway and Swallowing

149



5 Pediatric Gastroenterology

191



6 Pediatric Nutrition

237



7 Clinical Swallowing and Feeding Assessment

261



8 Instrumental Evaluation of Swallowing

331



9 Management of Swallowing and Feeding Disorders

369

Joan C. Arvedson and Maureen A. Lefton-Greif Joan C. Arvedson and Maureen A. Lefton-Greif Brian Rogers and Shannon M. Theis

Robert Chun and Margaret L. Skinner Ellen L. Blank

Mary Beth Feuling and Praveen S. Goday Joan C. Arvedson, Maureen A. Lefton-Greif, and Donna J. Reigstad Maureen A. Lefton-Greif, Joan C. Arvedson, Robert Chun, and David C. Gregg Joan C. Arvedson, Maureen A. Lefton-Greif, and Donna J. Reigstad

10 Pulmonary Manifestations and Management Considerations for Aspiration

1

453

J. Michael Collaco and Sharon A. McGrath-Morrow

v

vi  Pediatric Swallowing and Feeding: Assessment and Management

11 Drooling and Saliva/Secretion Management

479

12 Clinical Genetics:  Evaluation and Management of Patients With Craniofacial Anomalies Associated With Feeding Disorders

517

13 Behavioral Feeding Disorders:  Etiologies, Manifestations, and Management

551

Joan C. Arvedson and Maureen A. Lefton-Greif

Julie E. Hoover-Fong and Natalie M. Beck

Meghan A. Wall and Alan H. Silverman

Index 577

Foreword It has been 25 years since the first edition of this landmark publication Pediatric Swallowing and Feeding: Assessment and Management was published. The second, updated edition was published in 2002. Now, in 2020, we have the third edition of this fundamental text concerning the understanding and care of pediatric swallowing and feeding. The editors, one of whom unfortunately was deceased before publication, have recognized the advances and changes in the understanding of the information now available for the care of pediatric swallowing and feeding challenges. They have recruited an outstanding group of contributors for this newest edition and there are numerous critically important updates and additions. The editors have included the World Health Organization’s International Classification of Functioning, Disability, and Health as the functional basis for all areas of the book. This text is important as there are an increased number of children with complex medical and

health care conditions who are at risk for feeding and swallowing disorders. This third edition stresses the need for a team approach and it also documents the use of “virtual” teams. This is evidenced through the chapter contributors who are professionals in their respective fields. Chapter 10 is especially important now as it documents the pulmonary manifestations and considerations concerning aspiration in pediatric patients. Chapter 12 addresses the genetics underlying many of these conditions, which was information that was unavailable in the first two editions. Pediatric Swallowing and Feeding: Assessment and Management, Third Edition is the fundamental holistic source for all health care professionals who provide care for children with swallowing and feeding problems throughout the world. The previous editions have been, and now this updated third edition continues to be the standard for information concerning diagnosis and care of these children. Robert J. Ruben, MD, FAAP, FACS Distinguished University Professor Departments of Otorhinolaryngology—   Head and Neck Surgery and Pediatrics Albert Einstein College of Medicine Montefiore Medical Center Bronx, New York

vii

Preface This third edition of Pediatric Swallowing and Feeding: Assessment and Management, now co-edited with Maureen A. LeftonGreif, PhD, is published at a time when recognition of the complexities of infants and children with swallowing and feeding disorders is increasing. Recent advances in genetics and epigenetics and the neurophysiologic underpinnings of feeding and swallowing development and their disorders have contributed to the appreciation of the complicated inter-relationships among structures, functions, and the environment throughout childhood. This body of information has advanced this field since publication of the first two editions of this book in 1993 and 2002. Consequently, this third edition is long overdue. It includes significant updates and considerable new information, making it a “new” edition rather than a simply revised edition. We trust that this edition meets the challenges of balancing updates with new information, while adhering to the salient and immutable basic concepts that underlie this area of practice. Notably, breathing and eating are basic to survival. Their disruptions can lead to significant compromises in nutrition and growth, respiratory health, development and academic skills, and overall general health and well-being. With medical advances and the increases in the survival and life expectancy of medically fragile children, more attention has been given to the multidisciplinary needs of these children. Nonetheless, high-quality evidence to support the care of these children

and the development of consensus-driven guidelines have not kept pace with the recognition of the needs of these children. The World Health Organization’s emphasis on “function” and “participation” serve as essential steps in the development of meaningful evaluations and effective interventions, and mandates that professionals set high priorities on interactions between caregivers and children, and the need for non-stressful feedings from preterm infants through teenage years and into adulthood. Focusing on only “oral skills” or “safe swallowing” is not enough. This edition builds on the first two in which Dr. Linda Brodsky contributed her extraordinary medical knowledge and leadership in many ways. She is missed not only for her role in this book, but for her contributions to research and patient care in pediatric otolaryngology. We have built on her knowledge and passion for children and their families. We acknowledge the many people who made this edition possible. First, we offer a special thank you to all the authors who shared their extensive knowledge and experience in their specialty areas and for their generous time commitments given their busy clinical and research schedules. We thank Beth Ansel, PhD, and Jeanne Pinto, MA, for their superb editing, suggestions, and attention to detail. The editors at Plural Publishing have paid attention to the many details necessary to bring this book to publication, and we thank them for their patience and expertise. We are grateful ix

x  Pediatric Swallowing and Feeding: Assessment and Management

for the families who gave permission for their children to be photographed adding examples of the real purposes for all of us— enhancing the lives of children with swallowing and feeding disorders. Most of all we thank all the families and caregivers who have trusted us with the care of their children. We are in awe of

their courage, inspired by their strength, grateful for their contributions to the care of future generations of children with swallowing and feeding disorders, and delight in the joy they have brought to us. Finally, we thank our families, to whom this book is dedicated.

About the Editors Joan C. Arvedson, PhD, is a speech-language pathologist, with Specialty in Pediatric Feeding and Swallowing Disorders at the Children’s Hospital of Wisconsin-Milwaukee and a clinical professor in the Department of Pediatrics, Medical College of Wisconsin. She is recognized internationally for her clinical work in pediatric swallowing and feeding disorders, lecturing/ teaching, and scientific publications. The first two editions of this book were published while she was at the Children’s Hospital of Buffalo/Kaleida Health in Buffalo, NY. She and Dr. Lefton-Greif co-authored Pediatric Videofluoroscopic Swallow Studies: A  Professional Manual with Caregiver Guidelines. Dr. Arvedson developed an online course, Interpretation of videofluoroscopic swallow studies of infants and children: A study guide to improve diagnostic skills and treatment planning. She also developed independent study videoconferences for the American Speech-Language-Hearing Association’s professional development initiatives. Dr. Arvedson is a founding member of the Board of Certified Specialists in Swallowing and Swallowing Disorders. She is a Fellow of ASHA and was awarded Honors of the Association in 2016. Dr. Arvedson is a member of the editorial board of Dysphagia. She is past-president of the New York State Speech-Language-Hearing Association and the Society for Ear, Nose, and Throat Advances in Children.

xi

xii  Pediatric Swallowing and Feeding: Assessment and Management

Linda Brodsky, MD (1952–2014), an internationally recognized pediatric otolaryngologist, was Chief of Pediatric Otolaryngology at the Children’s Hospital of Buffalo/Kaleida Health in Buffalo, New York; Professor at the State University of New York at Buffalo Medical School; Director of the Children Hospital’s Center for Pediatric Otolaryngology and Communication Disorders. Dr. Brodsky was co-editor of the first two editions of Pediatric Swallowing and Feeding: Assessment and Management with Dr. Arvedson. In 2014, preliminary discussions were underway for this third edition. She’s authored more than 100 scientific papers and 27 book chapters and served on the editorial boards of several medical journals. She was listed in the Best Doctors in America series and Who’s Who in Science and Engineering. Dr. Brodsky was presented with the Sylvan Stool award for excellence in teaching by the Society for Ear, Nose, and Throat Advances in Children. She was a strong advocate for mentorship of young women in medicine. Her devotion to her patients and tenacity in advocating for their care was legendary. Dr. Brodsky is missed by her family, colleagues, and patients. Maureen A. Lefton-Greif, PhD, is Professor in the Departments of Pediatrics, Otolaryngology— Head and Neck Surgery, and Physical Medicine and Rehabilitation at Johns Hopkins Medical Institutions. She is an internationally recognized speech-language pathologist for her clinical expertise and research on swallowing and its development and disorders in children of all ages. Her work focuses on optimizing pediatric swallowing evaluations to facilitate the prompt initiation of treatment and lessen the consequences associated with dysphagia. Dr. Lefton-Greif is the recipient of grants and support from National Institutes of Health—Deafness and Other Communication Disorders, Ataxia-Telangiectasia Children’s Project, and the Muscular Dystrophy Association. She and Dr. Arvedson co-authored the book, Pediatric Videofluoroscopic Swallowing Studies: A Professional Manual with Caregiver Guidelines. More recently, she and Dr. Bonnie Martin-Harris developed the BaByVFSSImP©. She is a Fellow of ASHA and a founding member and the first vice-president of the Board of Certified Specialists in Swallowing and Swallowing Disorders. Dr. Lefton-Greif serves on the editorial advisory boards of Dysphagia and the Canadian Journal of Speech-Language Pathology.

Contributors Joan C. Arvedson, PhD, CCC-SLP, BCS-S Board Certified Specialist in Swallowing and Swallowing Disorders Program Coordinator, Feeding and Swallowing Services Children’s Hospital of Wisconsin-Milwaukee Milwaukee, Wisconsin Chapters 1, 2, 7, 8, 9, and 11 Natalie M. Beck, MGC, CGC Genetic Counselor Johns Hopkins McKusick-Nathans Institute of Genetic Medicine Baltimore, Maryland Chapter 12 Ellen L. Blank, MD, MA Retired Pediatric Gastroenterologist Children’s Hospital of Wisconsin Associate Adjunct Professor of Pediatrics-Bioethics Medical College of Wisconsin Milwaukee, Wisconsin Chapter 5 Robert Chun, MD Associate Professor Division of Pediatric Otolaryngology Department of Otolaryngology Medical College of Wisconsin Milwaukee, Wisconsin Chapters 4 and 8 J. Michael Collaco, MD, MS, MBA, MPH, PhD Associate Professor

Johns Hopkins University School of Medicine Eudowood Division of Pediatric Respiratory Sciences Baltimore, Maryland Chapter 10 Mary Beth Feuling, MS, RD, CSP, CD Advanced Practice Dietitian Clinical Nutrition Children’s Hospital of Wisconsin Milwaukee, Wisconsin Chapter 6 Praveen S. Goday, MBBS, CNSC, FAAP Professor of Pediatrics Division of Pediatric Gastroenterology and Nutrition Medical College of Wisconsin Milwaukee, Wisconsin Chapter 6 David C. Gregg, MD Medical Direction Pediatric Imaging Associate Professor of Radiology Medical College of Wisconsin Children’s Hospital of Wisconsin Milwaukee, Wisconsin Chapter 8 Julie E. Hoover-Fong, MD, PhD Associate Professor McKusick-Nathans Institute of Genetic Medicine Greenberg Center for Skeletal Dysplasias Johns Hopkins University Baltimore, Maryland Chapter 12 xiii

xiv  Pediatric Swallowing and Feeding: Assessment and Management

Maureen A. Lefton-Greif, PhD, CCC-SLP, BCS-S Professor of Pediatrics, Otolaryngology— Head and Neck Surgery, and Physical Medicine and Rehabilitation Eudowood Division of Pediatric Respiratory Sciences Johns Hopkins University School of Medicine Baltimore, Maryland Chapters 1, 2, 7, 8, 9, and 11 Sharon A. McGrath-Morrow, MD, MBA Professor of Pediatrics Division of Pediatric Pulmonary Johns Hopkins School of Medicine Baltimore, Maryland Chapter 10

Alan H. Silverman, PhD Pediatric Psychologist Professor of Pediatrics Medical College of Wisconsin Milwaukee, Wisconsin Chapter 13 Margaret L. Skinner, MD Assistant Professor, Pediatric Otolaryngology and Pediatrics Director, Multidisciplinary Pediatric Aerodigestive Center Johns Hopkins University School of Medicine Baltimore, Maryland Chapter 4

Donna J. Reigstad, MS, OTR/L Senior Occupational Therapist Feeding Disorders Program Kennedy Krieger Institute Baltimore, Maryland Chapters 7 and 9

Shannon M. Theis, PhD, CCC-SLP Assistant Professor Department of Pediatrics Department of Otolaryngology—Head and Neck Surgery School of Medicine Oregon Health and Science University Adjunct Faculty, Portland State University Portland, Oregon Chapter 3

Brian Rogers, MD Professor of Pediatrics Institute on Development and Disability Department of Pediatrics Oregon Health and Science University Portland, Oregon Chapter 3

Meghan A. Wall, PhD, BCBA Child and Adolescent Psychologist Assistant Clinical Professor of Psychiatry Children’s Hospital of Wisconsin Medical College of Wisconsin Milwaukee, Wisconsin Chapter 13

To Linda Brodsky for all she has contributed in the past and how she continues to influence professionals who follow in her footsteps. We miss you. To my family: Sons and daughters-in-law Stephen and Tara, Mark and Julie, along with grandsons Matthew, Jonathan, and Jason. You are all very special to me. To my husband Geoffrey, daughters and sons-in-law Jennifer and Daniel, Alissa and Daniel, and grandchildren Madelyn, Alexander, Emily, and Cooper. I love you and am grateful to share my life with you.

1

Overview of Diagnosis and Treatment

Joan C. Arvedson and Maureen A. Lefton-Greif

Introduction During the years since the second edition of this book, there has been an exponential increase in basic and clinical research related to swallowing and feeding in infants and children. The complexities of interacting systems continue to present challenges to clinicians and to parents. All involved in the care of children strive to help them to be healthy and to grow appropriately, while ensuring that eating and drinking are pleasurable with no stress to children or their caregivers. Factors that have not changed relate to basic physiologic functions. Breathing and eating are the most basic physiologic functions defining the beginning of life for newborn infants outside of the womb. Breathing is reflexive, life sustaining, and occurs in response to the transition from the fluid environment of the womb to the postnatal air environment. Eating is partly instinctual and partly a learned response. Eating requires the ingestion of nutrients provided by an outside source. In the newborn infant, sucking and swallowing require a complex series of events and coordination of the neurologic, respiratory, and gastrointestinal (GI) systems. Normal GI function must occur in

digestion of foods to provide nutrients. All of these functions are mediated by the integrity of physical and emotional maturation. The act of feeding is a dyadic process that requires interaction between the feeder, usually the mother, and the infant. From the beginning, feeding should be parent led with emphasis on quality of feeding, and not on volume, which often results in stressful feedings and a potentially reduced volume of intake and refusals. The pleasure of eating extends beyond the feeling of satiety to the pleasure gained through food ingested by the infant and provided by the mother, who is most often the primary caregiver. This interactive primary relationship is the first for every neonate. It serves as a foundation for normal development, somatic growth, communication skills, and psychosocial well-being. Thus, feeding of the newborn infant, young child, and rapidly growing teen is an activity with far-reaching consequences. When feeding is disrupted, the sequelae can include malnutrition, behavioral abnormalities, and severe distress for family and child alike. Interruption of growth and development sometimes cannot be reversed if it occurs at a critical time during the early months and years of a child’s life (Chapter 3). Lifelong disabilities may result. 1

2  Pediatric Swallowing and Feeding: Assessment and Management

Prevalence Currently, more than 100,000 newborn infants are given diagnoses of feeding problems after being discharged from acute care hospitals, and more than one-half million children (3–17 years) in the United States are diagnosed with dysphagia annually (Bhattacharyya, 2015; CDC/NCHS National Hospital Discharge Survey, 2010). The number of children with swallowing and feeding disorders has been increasing in part due to recent medical and technological advances, which have improved the survival of many infants and children who previously would not have survived. The range and complexity of their problems will continue to challenge the health care, educational, and habilitation/rehabilitation systems because many of these children are now living longer, remaining healthier, and having greater expectations for leading full and productive lives. Approximately 40% of children born preterm have swallowing/feeding disorders. Globally, an estimated 15 million infants are born preterm (less than 37 weeks’ gestation), and the number is increasing (World Health Organization [WHO], 2017). Although many children and their families have benefited greatly, the increasing number of children born prematurely at low birth weight (less than 2,500 g), very low birth weight (less than 1,500 g), and extremely low birth weight (less than 600 g) are frequently confronted with multiple complex medical problems. In comparison to full-term infants, late preterm infants (34-0/7 to 36-6/7 weeks gestation) are at increased risk for respiratory and neurologic complications that may produce or exacerbate feeding difficulties (Engle, Tomashek, & Wallman, 2007; Mally, Bailey, & Hendricks-Munoz, 2010). Other

infants with genetic, cardiac, and gastrointestinal abnormalities are faced with complex medical and in some instances surgical problems. Early recognition and intervention have been invaluable despite the cognitive disabilities, cerebral palsy, chronic pulmonary problems, structural deficits, and neurologic impairments that infants endure. Swallowing and feeding problems compound most of these conditions.

Developmental Considerations After the establishment of adequate respiration and physiologic stability, the highest priority for caregivers is to meet the nutritional needs of their newborn infants. To achieve this goal successfully, infants and children of all ages require a well-functioning oral sensorimotor and swallowing mechanism, overall adequate health (including respiratory, gastrointestinal, and neurologic), appropriate nutrition, central nervous system integration, and adequate musculoskeletal tone. In addition, the emergence of communication, an often-overlooked process, is closely aligned with successful swallowing and feeding, particularly in young children (Malas, Trudeau, Chagnon, & McFarland, 2015). Normal feeding patterns are reflected in the early developmental pathways that sequentially and rapidly emerge during the first several months and years of life. Communication is one of the most important of those pathways. The interrelationship between feeding, shared by all biologic creatures, and language-based, verbal communication, unique to humans, cannot be overemphasized. The comparative anatomy of the upper aerodigestive tract and its impli-

1. OVERVIEW OF Diagnosis and Treatment   3

cation for the development of human communication has been established (e.g., Laitman & Reidenberg, 1993, 2013; LaMantia et al., 2016; Lieberman, McCarthy, Hiiemae, & Palmer 2001; Madriples & Laitman, 1987). Children who are born prematurely with very low birth weight or neurologic impairment are commonly found to have swallowing and feeding problems. Other highrisk children are those experiencing birth trauma, prenatal and perinatal asphyxia, and a multitude of genetic syndromes with accompanying structural and neurologic impairment (Chapters 3 and 12). The presence of cardiac, pulmonary, and GI disease

often creates additional difficulty in sorting out primary and secondary etiologies. Diagnosis and management in these patients present even greater challenges (Table 1–1). The ability to feed an infant successfully and thereby nurture an infant is imprinted early on the maternal–infant relationship. Normal oral sensorimotor development includes the establishment of (a) stability and mobility of the ingestive system, (b) rhythmicity, (c) sensation, and (d) oral-motor efficiency and economy (Gisel, Birnbaum, & Schwartz, 1998). Optimally, maternal, as well as paternal, and infant bonding begins at the outset by providing nutrition with

Table 1–1.  Major Diagnostic Categories Associated With Swallowing and Feeding Disorders in Infants and Children Neurologic

Encephalopathies (e.g., cerebral palsy, perinatal asphyxia) Traumatic brain injury Neoplasms Intellectual disability Developmental delay

Anatomic and structural

Congenital (e.g., tracheoesophageal fistula and esophageal atresia, cleft palate) Acquired (e.g., tracheostomy, vocal fold paralysis or paresis)

Genetic

Chromosomal (e.g., Down syndrome) Syndromic (e.g., Pierre Robin sequence, Treacher Collins syndrome, CHARGE syndrome) Inborn errors of metabolism

Secondary to systemic illness

Respiratory (e.g., bronchopulmonary dysplasia, chronic lung disease of prematurity, bronchopulmonary dysplasia) Gastrointestinal (e.g., inflammatory conditions, GI dysmotility, constipation) Congenital cardiac anomalies

Psychosocial and behavioral

Oral deprivation Secondary to unresolved or resolved medical condition Iatrogenic

4  Pediatric Swallowing and Feeding: Assessment and Management

visual and auditory stimulation of loving and concerned parents. Thus, swallowing and feeding disorders likely have negative impact not only on the physical but also on the psychosocial well-being of the infant and child with caregivers.

Sensorimotor Function The epidemiology of oral sensorimotor dysfunction in the general population and in the population of children with neurologic impairments is not well defined. Precise incidence and prevalence data are difficult to ascertain. Cerebral palsy (CP) serves as an example of the range of estimates that continue to be similar from multiple sources that have reported approximately 20% to 85% of children with CP are believed to have swallowing difficulties at some time during their lives (Benfer, Weir, Bell, Ware, Davies, & Boyd, 2013; Parkes, Hill, Platt, & Donnelly, 2010). During the first year of life of all children with CP, 57% are estimated to have problems with sucking, 38% with swallowing, and 33% with malnutrition (Reilly, Skuse, & Poblete, 1996). As the severity of CP increases, not surprisingly the severity of the oral sensorimotor dysfunction increases. The most severely affected are children with spastic quadriparesis, 90% of whom have swallowing and feeding problems (Benfer et al., 2013; Paulson & VargusAdams, 2017; Stallings, Charney, Davies, & Cronk, 1993). During the first five years of life, the overall incidence of dysphagia decreases in children with CP and particularly in those with better baseline and improving gross motor function (Benfer, Weir, Bell, Ware, Davies, & Boyd, 2017 ). These findings suggest that gross motor skills and their improvement may herald those at risk for “persistent” dysphagia.

Team Approaches to Swallowing/ Feeding Disorders Feeding disorders that may or may not include swallowing deficits (dysphagia) manifest in many different ways. Resistance to accepting foods, lack of energy for the work of oral feeding, and oral sensorimotor disabilities broadly encompass most problems (Gisel et al., 1998; Kerzner, Milano, MacLean, Berall, Stuart, & Chatoor, 2015). Effective management of these medically complex children depends on the expertise of many specialists working independently and as a team (Chapter 9). A few examples follow, not intended to be an inclusive list, since different institutions and professionals within those institutions, carry out patient care in multiple ways. Some teams may specialize in specific underlying etiologies or presentations, for example, Aerodigestive Clinic, Foregut Clinic (focused specifically on children with tracheoesophageal fistula and esophageal atresia (TEF/EA), Tracheostomy/Ventilator Clinic, Craniofacial Team with a subspecialty clinic for those children with feeding disorders. Team approaches also may differ depending on availability of resources that may even include “virtual” teams. It is important that teams can offer coordinated consultation and problemsolving for co-occurring etiologies and interrelated problems. Essential components can be incorporated in all types of teams (Table 1–2). The family’s ability to synthesize and cope with multiple, sometimes disparate opinions must also be a top priority. Whenever possible, an interdisciplinary team model is encouraged. This approach refers to interaction of a group of professionals who meet in person with family allowing for optimal efficient communication. Regardless of the type of team, each

1. OVERVIEW OF Diagnosis and Treatment   5

Table 1–2.  Essential Components for Successful Feeding Teams • Collegial interaction among relevant specialists with active family involvement • Shared group philosophy for diagnostic approaches and treatment protocols • Team leadership with organization for evaluation and information sharing • Willingness to engage in creative problem-solving and research • Time commitment for the labor-intensive nature of such work

professional brings expertise that is useful in the solution of complex medical problems. A group philosophy for both evaluation and treatment engenders respect for other team members’ expertise. An organized structure with a clearly defined leader is important. Finally, a shared fund of knowledge is critical and results in creative problem-solving and fruitful research. In situations where interdisciplinary teams are not possible, professionals are urged to develop strategies that promote effective communication with parents and other primary caregivers. Team member roles are similar regardless of the specific type team, with all professionals providing services within their scope of practice and training. Most importantly, parents/caregivers are integral members of any team. Over the past 20 years, there has been increased recognition of the complex interface between feeding disorders and swallowing impairments in children. The term feeding disorder refers to inappropriate development of oral intake and its associated medical, nutritional, and psychosocial consequences. Swallowing impairments are more specific to the process of deglutition. Hence, all children with swallowing impairments have feeding disorders, but not all children with feeding disorders have swallowing impairments. Importantly, swallow-

ing impairments can lead to the development of feeding disorders. Different types of models and settings have emerged to accommodate assessment and treatment of specific patient populations. Some teams function primarily in an outpatient setting and serve as a transitional bridge between inpatient and outpatient settings. Names for such teams vary and may include the following: Feeding Clinic; Feeding Disorders Clinic; Nutrition Clinic; or Swallowing, Feeding, and Nutrition Clinic; and Feeding and Growing Clinic. Inpatient swallowing and feeding teams may be separate from outpatient teams that have different personnel. Some teams work across in- and outpatient settings for assessment and management of children with specific diagnoses or presentations. Such teams also vary and may include craniofacial and aerodigestive teams. The core team members usually include a physician and other health care providers as dictated by the needs of the patient population. The primary oral sensorimotor swallow therapist is most likely to be a speech-language pathologist, although in some instances an occupational therapist may be primary. All teams benefit from both when underlying knowledge and experience is extensive with infants and children demonstrating swallowing and feeding disorders.

6  Pediatric Swallowing and Feeding: Assessment and Management

Ethical and Legal Challenges Underlying Care for Children With Swallowing/ Feeding Disorders In addition to making evidence-based decisions, all team members must adhere to the moral and ethical principles within the framework of their professions as well as their scopes of practice (Arvedson & LeftonGreif, 2007; Horner, Modayil, Chapman, & Dinh, 2016). Ethics is a discipline that uses a systematic approach to examine morality with the intent of promoting the overall welfare of the community (Lefton-Greif & Arvedson, 1997). The four primary principles of ethical decision-making, respect for autonomy, beneficence, nonmaleficence, and justice, are reviewed in detail in Beauchamp and Childress (1994) and Purtilo (1988). Adherence to these four commitments is critical to decision making that goes beyond the realm of facts by rendering judgements. In addition, for pediatrics, decision making must take into account in “the child’s best interests.” Bioethics is the discipline that deals with ethical issues that arise with advances in medicine. Hence, bioethical dilemmas are not typically defined by professional codes of ethics and are often controversial. Bioethical questions may include issues that range from allocation of resources (e.g., expensive drugs used in rare diseases) to stem cell research. As medical advances continue, it is likely that all professions involved with children with dysphagia will be called on to address bioethical quandaries.

Special Considerations for School, Home, and Residential Settings Oral sensorimotor and swallowing specialists frequently function outside of a hospi-

tal setting and outpatient clinic. Assessment and treatment for children with complex feeding and other medical problems are common in a variety of educational (schoolbased) and residential (home-based) settings. Working knowledge of the challenges faced by infants and children with a wide variety of swallowing problems is mandatory. Families may be followed through a center or home-based educational program. These services have been mandated by federal legislation that guarantees a free and appropriate educational program for all handicapped children. The Education for All Handicapped Children Act (1975–1990) was revised in 1990 and became known as Individuals with Disabilities Education Act (IDEA–Public Law No. 94-142). This law was established to guarantee that all students with disabilities are provided with the same access to public education as students without disabilities. “IDEA is composed of four parts, the main two being part A and part B. Part A covers the general provisions of the law, Part B covers assistance for education of all children with disabilities, Part C covers infants and toddlers with disabilities, which includes children from birth to age three years, and Part D is the national support programs administered at the federal level. Each part of the law has remained largely the same since the original enactment in 1975 Individuals with Disabilities Education Act (2017, November 13).” Section 504 of the Rehabilitation Act of 1973, as amended (Section 504), clarified information about the Americans with Disabilities Act (ADA, 2008) in the areas of public elementary and secondary education (U.S. Department of Education, 2015). The ADA (2008) broadened the interpretation of disability, which clearly includes eating. Schools are bound by IDEA and 504 because of their responsibility to provide a free and appropriate public education (FAPE).

1. OVERVIEW OF Diagnosis and Treatment   7

Challenges in Caring for Children With Swallowing/ Feeding Disorders A comprehensive approach to children with swallowing and oral sensorimotor function problems can be hampered by the lack of a shared fund of knowledge. A clearly defined set of terms related to this rapidly expanding field is necessary. Several terms will be defined here with others defined as they are encountered throughout the book. Deglutition1 is the act of swallowing and is just one process in the broader context of feeding. Swallowing refers to the entire act of deglutition from placement of food and liquid into the mouth until they enter the upper esophagus. Sucking, chewing, and swallowing are three physiologically distinct processes occurring during deglutition (Kennedy & Kent, 1985). Estimates of the frequency of swallowing have ranged from 600 to 1,000 times per day (Lear, Flanagan, & Moorrees, 1965). The highest frequency is during food intake, and the lowest is during sleep. Aside from providing nourishment and hydration, swallowing accomplishes other purposes, such as the removal of saliva and mucous secretions from the oral, nasal, and pharyngeal cavities. A decrease in swallowing frequency may be coupled with oral sensorimotor dysfunction and thereby may result in severe drooling (Chapter 11). Feeding is a broad term to encompass the process for getting food/liquid into the mouth (https://en.oxforddictionaries.com/ definition/deglutition). Once food and liquid enter the mouth, the process continues with bolus formation as the initial process to include sucking and chewing (depending on the composition of the food or liquid) that leads to moving food/liquid through

the mouth, into the pharynx for initiation of swallowing. Dysphagia is a swallowing deficit (https://en.oxforddictionaries.com/defi​ nition/dysphagia). Oral sensorimotor function refers to all aspects of sensory and motor functions involving the structures in the oral cavity and pharynx related to swallowing from the lips until the onset (or initiation) of the pharyngeal phase of the swallow (Chapter  2). Finally, nutrition is the process by which all living organisms obtain the food and nourishment necessary to sustain life and support growth (https://en.oxforddiction​ aries​.com/definition/us/nutrition). Care for children with swallowing and feeding disorders requires a broad knowledge base that must be supplemented by a thoughtful and often creative problemsolving approach. The steps in this approach are universal to the diagnosis and treatment of any medical condition or illness. Their importance to the approach of a medically complex child cannot be overemphasized. Team care is most effective in developing alternate strategies when normal swallowing is absent and nutrition is severely compromised (Table 1–3).

Table 1–3.  Process Steps for Diagnosis and Treatment of Pediatric Swallowing and Feeding Disorders • Define problem feeding and swallowing • Identify etiology(ies) • Determine appropriate diagnostic tests • Plan approach to patient/family • Teach about problem, implement treatment • Monitor progress • Evaluate progress (outcomes focused)

The terms swallowing and deglutition have been used interchangeably. The term swallowing will be used throughout the text, unless distinguishing between these terms is relevant to the text.

1

8  Pediatric Swallowing and Feeding: Assessment and Management

Clinical and Research Updates for the Care of Children With Swallowing/ Feeding Disorders This third edition provides updated clinical and research findings that have direct impact on care for infants and children with swallowing and feeding disorders. Emphases continue to be placed on the critical importance of a fund of knowledge across multiple systems that are factors in children of all ages and all underlying etiologies. Clinical approaches are presented and discussed in ways that readers are expected to find useful in the evaluation and management of infants and children with oral sensorimotor dysfunction and swallowing problems. The next several chapters cover information that provides a basis for understanding the common problems associated with swallowing and feeding disorders. Knowledge of anatomy, embryology, physiology, and pathophysiology of the upper aerodigestive tract is fundamental for the understanding of infants and children with a wide range of swallowing and feeding disorders. The following chapters focus on neurodevelopment (normal and abnormal), airway, gastroenterology, and nutrition. These chapters are followed by a chapter on oral sensorimotor clinical feeding evaluation and a chapter on instrumental assessment with primary focus on videofluoroscopic swallow studies and fiberoptic endoscopic examination of swallowing. Significant clinical and research advances over the past 10 years are highlighted in these chapters as well as the chapter on decision making regarding management strategies and intervention. Chapters that follow cover specific topics including aspiration and saliva/secretion management. The chapter on cranio-

facial anomalies has an entirely new section focused on the genetic basis of conditions associated with swallowing/feeding problems in infants and children with craniofacial anomalies. The final chapter focuses on children with psychologic and behavioral problems, often accompanied by sensory factors, as major components in their feeding disorders. The importance of integrating these factors that include parent/child relationships cannot be overstated. Functional outcome is the goal for every child and family. Clinical case studies that are found at the end of most chapters provide concrete examples of teamwork with varied emphases that encompass the depth and breadth of pediatric feeding disorders. Evaluation and treatment approaches are included where supported by clinical experience and the scientific literature. Medical, psychosocial, and satisfaction outcomes are reported when available. Although there are some reports in recent years, the literature continues to be sparse in the areas of pediatric swallowing and feeding in normal development as well as disorders. Strong emphasis continues to be placed on the importance of making a diagnosis based on etiology of disease preceding treatment. All professionals involved in assessment and management of infants and children in both medical and educational settings must have appropriate knowledge and training to assess and treat infants and children with dysphagia and related conditions. All decision-making, communications, and interactions with families and other professionals must be carried out with adherence to the respective professional ethical codes of conduct. The overall importance of an appropriate fund of knowledge and shared experience employing team approaches is emphasized throughout this third edition as in the earlier editions of this book.

1. OVERVIEW OF Diagnosis and Treatment   9

References Arvedson, J. C., & Lefton-Greif, M. A. (2007). Ethical and legal challenges in feeding and swallowing intervention for infants and children. Seminars in Speech and Language, 28(3), 232–238. Beauchamp, T. L., & Childress, J. F. (1994). Principles of biomedical ethics. New York, NY: Oxford University Press. Benfer, K. A., Weir, K. A., Bell, K. L., Ware, R. S., Davies, P. S., & Boyd, R. N. (2013). Oropharyngeal dysphagia and gross motor skills in children with cerebral palsy. Pediatrics, 131(5), e1553–1562. doi:10.1542/peds​ .2012-3093 Benfer, K. A., Weir, K. A., Bell, K. L., Ware, R. S., Davies, P. S. W., & Boyd, R. N. (2017). Oropharyngeal dysphagia and cerebral palsy. Pediatrics, 140. doi:10.1542/peds.2017-0731 Bhattacharyya, N. (2015). The prevalence of pediatric voice and swallowing problems in the United States. Laryngoscope, 125(3), 746–750. CDC/NCHS National Hospital Discharge Survey, 2010. Retrieved from https://www.cdc​ .gov/nchs/data/nhds/8newsborns/2010new8​ _numbersick.pdf Deglutition. (n.d.). In Oxford University Press dictionary. Retrieved from https://en.oxford​ dictionaries.com/definition/deglutition Dysphagia. (n.d.). In Oxford University Press dictionary. Retrieved from https://en.oxford​ dictionaries.com/definition/dysphagia Engle, W. A., Tomashek, K. M., & Wallman, C. (2007). “Late-preterm” infants: A population at risk. Pediatrics, 120(6), 1390–1401. doi:10.1542/peds.2007-2952 Gisel, E. G., Birnbaum, R., & Schwartz, S. (1998). Feeding impairments in children: Diagnosis and effective intervention. International Journal of Orofacial Myology, 24, 27–33. Horner, J., Modayil, M., Chapman, L. R., & Dinh, A. (2016). Consent, refusal, and waivers in patient-centered dysphagia care: Using law, ethics, and evidence to guide clinical practice. American Journal of Speech-Language

Pathology, 25, 453–469. doi:10.1044/​2016_​ ajslp-15-0041 Individuals with Disabilities Education Act. (2017, November 13). Retrieved from https:// sites.ed.gov/idea/about-idea/ Kennedy, J. G., & Kent, R. D. (1985). Anatomy and physiology of deglutition and related functions. Seminars in Speech and Language, 6, 257–273. Kerzner, B., Milano, K., MacLean, W.C. Jr, Berall, G., Stuart, S., & Chatoor, I. (2015). A practical approach to classifying and managing feeding difficulties. Pediatrics, 135(2), 344–353. doi:10.1542/peds.2014-1630. Laitman, J., & Reidenberg, J. (1993). Specializations of the human upper respiratory and upper digestive systems as seen through comparative and developmental anatomy. Dysphagia, 8, 318–325. Laitman, J. T., & Reidenberg, J. S. (2013). The evolution and development of human swallowing: the most important function we least appreciate. Otolaryngology Clinics of North America, 46(6), 923–935. doi:10.1016/j.otc​ .2013.09.005 LaMantia, A. S., Moody, S. A., Maynard, T. M., Karpinski, B. A., Zohn, I. E., Mendelowitz, D., . . . Popratiloff, A. (2016). Hard to swallow: Developmental biological insights into pediatric dysphagia. Developmental Biology, 409(2), 329–342. doi:10.1016/j.ydbio.2015​ .09.024 Lear, C. S., Flanagan, J. B., Jr., & Moorrees, C. F. (1965). The frequency of deglutition in man. Archives of Oral Biology, 10, 83–100. Lefton-Greif, M. A., & Arvedson, J. C. (1997). Ethical considerations in pediatric dysphagia. Seminars in Speech and Language, 18(1), 79–86. Lieberman, D. E., McCarthy, R. C., Hiiemae, K. M., & Palmer, J. B. (2001). Ontogeny of postnatal hyoid and larynx descent in humans. Archives of Oral Biology, 46(2), 117–128. Madriples, U., & Laitman, J. (1987). Developmental change in the position of the fetal human larynx. American Journal of Physical Anthropology, 72, 463–472. Malas, K., Trudeau, N., Chagnon, M., & McFarland, D. H. (2015). Feeding-swallowing

10  Pediatric Swallowing and Feeding: Assessment and Management difficulties in children later diagnosed with language impairment. Developmental Medicine and Child Neurology, 57(9), 872–879. doi:10.1111/dmcn.12749 Mally, P. V., Bailey, S., & Hendricks-Munoz, K. D. (2010). Clinical issues in the management of late preterm infants. Current Problems in Pediatric and Adolescent Health Care, 40(9), 218–233. doi:10.1016/j.cppeds.2010.07.005 Nutrition. (n.d.). In Oxford University Press dictionary. Retrieved from https://en.oxford​dic​ tionaries.com/definition/nutrition Parkes, J., Hill, N., Platt, M. J., & Donnelly, C. (2010). Oromotor dysfunction and communication impairments in children with cerebral palsy: A register study. Developmental Medicine and Child Neurology, 52(12), 1113– 1119. doi:10.1111/j.1469-8749.2010.03765.x Paulson, A., & Vargus-Adams, J. (2017). Overview of four functional classification systems commonly used in cerebral palsy. Children (Basel), 4(4). doi:10.3390/children4040030

Purtilo, R. B. (1988). Ethical issues in teamwork: The context of rehabilitation. Archives of Physical Medicine and Rehabilitation, 69(5), 318–322. Reilly, S., Skuse, D., & Poblete, X. (1996). Prevalence of feeding problems and oral motor dysfunction in children with cerebral palsy: A community survey. Journal of Pediatrics, 129, 877–872. Stallings, V. A., Charney, E., Davies, J. C., & Cronk, C. E. (1993). Nutritional-related growth failure of children with quadriplegic cerebral palsy. Developmental Medicine and Child Neurology, 35, 126–138. U.S. Department of Education. (2015). Protecting students with disabilities. Retrieved from https://www2.ed.gov/about/offices/list/ocr/​ 504faq.html#skipnav2 World Health Organization (WHO). Preterm birth. Fact sheet. Retrieved from http://www​ .who.int/mediacentre/factsheets/fs363/en/ (updated November 2017).

2

Anatomy, Embryology, Physiology, and Normal Development

Joan C. Arvedson and Maureen A. Lefton-Greif

Summary The human upper aerodigestive tract is the most complex neuromuscular unit in the body. It is the intersection of the digestive, respiratory, and phonatory systems. Normal swallowing requires precise integration of the important functions of breathing, eating, and speaking. A thorough understanding of the anatomy, embryology, and physiology of these systems is necessary to appreciate the etiology, diagnosis, and treatment of swallowing and feeding disorders in infants and children. Attention to functional anatomy provides a basis for the discussion of clinically relevant embryologic development. The physiology of swallowing, with emphasis on neurophysiology, posture, and muscle tone, is presented in detail in this chapter. The challenges of developmental change beginning with premature infants and extending through adolescents are nowhere more apparent than for swallowing and feeding. Swallowing and feeding are explained in the context of normal oral sensorimotor

development of the infant and child. Special focus on the anatomy and physiology of the airway and gastrointestinal (GI) tract will help to enhance the reader’s understanding of the clinical manifestations, diagnosis, and treatment of swallowing and feeding problems in children.

Introduction Deglutition, more commonly referred to as swallowing,1 is defined as the semiauto­matic motor action of the muscles of the respiratory and GI tracts that propels food from the oral cavity into the stomach (Miller, 1986). Swallowing functions not only to transport food to the stomach, but also in clearing the mouth and pharynx of secretions, mucus, and regurgitated stomach contents. Thus, the function of swallowing is nutritive as well as protective of the lower airways. The act of swallowing is complex because respiration, swallowing, and phonation all occur at one anatomic location— the region of the pharynx and larynx. To

The common usage term, swallowing, is used throughout this textbook for ease of reading. Similarly, ingestion, the taking in of food, will be referred to as feeding or eating (as age appropriate) throughout.

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12  Pediatric Swallowing and Feeding: Assessment and Management

be successful, normal swallowing requires the coordination of 31 muscles, six cranial nerves, and multiple levels of the central nervous system (CNS), including the brain stem and cerebral cortex (Bosma, 1986). Thus, understanding the anatomy, embryology, physiology, and normal development of this functional neuromuscular unit is of paramount importance to the proper diagnosis and treatment of swallowing and feeding disorders in children.

Anatomy The upper aerodigestive tract consists of the nose, oral cavity, pharynx, larynx, and esophagus. The trachea, bronchi, and pulmonary parenchyma are considered the lower airways. The upper digestive tract

ends at the entrance to the stomach. Each area is discussed separately.

Nose The nose is important for respiration throughout life, but particularly in neonates (first 28 days of life) and young infants (up to 6 months), when preferential nasal breathing is present. The nose also cleans, warms, and humidifies inspired air. As the nasal passage continues posteriorly, it opens at the bilateral posterior nasal choanae into the nasopharynx, which is an important anatomic chamber that serves as a resonator for speech production. In addition, the nasopharynx is one of the two airway conduits into the hypopharynx (Figure 2–1). The lateral nasal walls are composed of three bones covered with a highly sensitive

INFANT Hard Palate

Soft Palate

Vallecula

Maxilla

Nasopharynx Tongue

Mandible

Hypopharynx Epiglottis

Hyoid Larynx

Esophagus

Trachea

Figure 2–1. Lateral view of the infant’s upper aerodigestive tract. Structures and boundaries of the oral cavity, pharynx, and larynx are noted. The soft palate is in close approximation to the valleculae. This anatomic proximity effectively separates the oral route for ingestion from the preferred nasal route for respiration.

2. Anatomy, Embryology, Physiology, and Normal Development   13

mucosa—the nasal turbinates. The nose is separated into two nasal cavities by the midline septum, which is cartilage anteriorly and bone posteriorly. Septal deviation in the newborn may occur from birth trauma and result in severe nasal obstruction leading to perinatal feeding difficulties (Emami, Brodsky, & Pizzuto, 1996). Other etiologies of nasal obstruction include, but are not limited to, choanal atresia, encephalocele, glioma, nasal dermoid, nasolacrimal duct cyst, pyriform aperture stenosis, and rhinitis (Gnagi & Schraff, 2013; see Chapter 4). Soft palate elevation and retraction seal off the nasal cavity from the oropharynx and the oral cavity.

Oral Cavity (Mouth) The oral cavity is involved in ingestion of food, vocalization, and oral respiration. Structures include lips, mandible, maxilla, floor of the mouth, cheeks, tongue, hard palate, soft palate, and anterior surfaces of the anterior tonsillar pillars. Older infants and children also have teeth for chewing. The lateral sulci are spaces between the mandible or maxilla and the cheeks. The anterior sulci are spaces between the mandible or maxilla and the lip muscles. The structures in the mouth are important for bolus formation and oral transit (described in detail in the following text). In infancy, the cheeks with fat pads or sucking pads are important for sucking. The tongue has attachments to the mandible, hyoid bone, and styloid process of the cranium by the extrinsic muscles of the tongue (genioglossus, hypoglossus, and styloglossus muscles) (Bosma, 1972). When anatomic defects of the lips, palate, maxilla, mandible, cheeks, or tongue are present, normal sucking and swallowing may be compromised (see Chapters 4 and 12). In children

with oral sensorimotor problems, food or liquid can be lodged in both the anterior and lateral sulci, making bolus preparation difficult. Muscles involved in bolus formation and oral transit include the digastric, palatoglossus, genioglossus, styloglossus, geniohyoid, mylohyoid, buccinators, and those muscles intrinsic to the tongue (no bony attachment, classified by orientation of the muscle fibers: longitudinal, vertical, and transverse). Cranial nerves involved include V, VII, IX, X, XI, and XII (Bosma, 1986; Derkay & Schechter, 1998; Perlman & Christensen, 1997).

Pharynx The pharynx consists of three anatomic areas (Figures 2–1 and 2–2): the nasopharynx, the oropharynx, and the hypopharynx. In the infant, the nasopharynx and hypopharynx blend into one structure, and thus there is no true oropharynx as seen in the older child. The nasopharynx begins at the nasal choanae and ends at the elevated soft palate. The eustachian tubes originate in the nasopharynx (Bosma, 1967). As growth and development occur, two important anatomic changes emerge: (a) the angle of the nasopharynx at the skull base becomes more acute and approaches 90°, and (b) the pharynx elongates so that an oropharynx is created. The faucial arches form a bridge between the mouth and the oropharynx. This junction and the tongue base form the anterior boundary of the oropharynx, which extends inferiorly to the epiglottis. The oropharynx includes the epiglottis and the valleculae. The valleculae are bilateral pockets formed by the base of the tongue and the epiglottis (Donner, Bosma, & Robertson, 1985). The hypopharynx (sometimes called the laryngeal pharynx) extends from the base of the

14  Pediatric Swallowing and Feeding: Assessment and Management

OLDER CHILD

Nasopharynx Tongue

Soft palate

Oropharynx

Vallecula

Hypopharynx Hyoid

Larynx

Epiglottis Trachea Esophagus

Figure 2–2. Lateral view of the older child’s upper aerodigestive tract. Note the wide distance between the soft palate and the larynx. The elongated pharynx is unique to humans and has allowed the development of human speech production.

epiglottis to the cricopharyngeal muscles in the upper esophageal sphincter. The anterior wall of the hypopharynx includes the laryngeal inlet and the cricoid cartilage. The pyriform sinuses are pockets lateral and just below the inlet to the larynx. The vertical enlargement of this space enables the development of human speech. Phonation of a wide variety of speech sounds can thus occur. However, this elongation challenges the timing and coordination needed for functional swallowing and breathing as a common and enlarged intersection of the respiratory and digestive tracts is created (Laitman & Reidenberg, 1993). The walls of the pharynx consist of three pairs of constrictor muscles—the superior, medial, and inferior constrictors. These

striated muscle fibers arise from a median raphe in the midline of the posterior pharyngeal wall. They extend laterally and attach to bony and soft tissue structures located anteriorly. Initiation of the pharyngeal swallow function is under voluntary neural control and becomes involuntary for completion of the pharyngeal swallow. This function is under the control of cranial nerves (CN) V, IX, and X that synapse in the swallowing center located in the medulla.

Nasopharynx The nasopharynx is a boxlike structure located at the base of the skull. It connects the nasal cavity above with the oropharynx below, and serves as a conduit for air,

2. Anatomy, Embryology, Physiology, and Normal Development   15

a drainage area for the nose and paranasal sinuses and eustachian tube/middle ear complex, and a resonator for speech production. The boundaries of the nasopharynx are the posterior nasal choanae (anteriorly), the soft palate (anterior-inferior), the skull base (posteriorly), and the hypopharynx in infants and oropharynx in children and adults (inferiorly). Tongue propulsion moves a bolus posteriorly and thus assists in the elevation of the soft palate and closes off the nasopharynx from the rest of the pharynx. Anatomic or functional defects of the soft palate may result in nasopharyngeal backflow/reflux during oral feedings (Chapters 4 and 12). The adenoid is a mass of lymphatic tissue located behind the nasal cavity, in the roof of the nasopharynx where the nose blends into the throat. The adenoid, unlike the palatine tonsils, has pseudostratified epithelium. The adenoid is part of the “Waldeyer ring” of lymphoid tissue, which includes the palatine tonsils and the lingual tonsils. During the first years of life, the adenoid increases in size. Involution begins at about age 8 years and extends through puberty. Excessive enlargement of the adenoid may cause nasal obstruction and feeding difficulties, even in older children.

Oropharynx The oropharynx is the posterior extension of the oral cavity. The oropharynx begins at the posterior surface of the anterior tonsillar pillars and extends to the posterior pharyngeal wall. The palatine tonsils are attached to the lateral pharyngeal walls between the

anterior and posterior tonsillar pillars. The superior boundary of the oropharynx is parallel to the pharyngeal aspect of the soft palate in a line extending back to the posterior pharyngeal wall. The inferior boundary of the oropharynx is at the base of the tongue and includes the epiglottis and valleculae. The valleculae are wedge-shaped spaces at the base of the tongue and the epiglottis. The lingual tonsil is along the tongue base. When the lingual tonsil becomes enlarged, it can encroach on the valleculae and cause significant airway, feeding, and swallowing problems. Enlargement may be seen when severe gastroesophageal reflux disease (GERD)/extra-esophageal reflux disease (EERD)2 is present. The lateral and posterior walls of the oropharynx are formed by the middle and part of the inferior pharyngeal constrictor muscles. The greater cornua of the hyoid bone are included in the lateral pharyngeal walls (Donner et al., 1985). The body of the hyoid bone, located in the deep musculature of the neck, attaches to the base of the tongue. The base of the tongue and the larynx descend inferiorly during the first 4 years of life. By age 4, the base of the tongue is anatomically separated from the larynx in the vertical plane and thus becomes the anterior border of the oropharynx (Caruso & Sauerland, 1990). Because the infant’s larynx is high in the neck, almost “tucked under” the base of the tongue, no true oropharynx exists (see Figures 2–1 and 2–2). Thus, in neonates and young infants, a single conduit for breathing is created from the nasopharynx to the hypopharynx that allows them to coordinate sucking, swallowing, and breathing.

Gastroesophageal reflux disease (GERD) refers to the abnormal regurgitation of acid into the esophagus causing symptoms. When acid and other stomach contents emerge from the esophagus into the pharynx, larynx, mouth, and nasal cavities, the most commonly accepted term is extra-esophageal reflux disease (EERD) (Sasaki & Toohill, 2000).

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16  Pediatric Swallowing and Feeding: Assessment and Management

Hypopharynx The hypopharynx extends from the base of the epiglottis at the level of the hyoid bone down to the cricopharyngeus muscle. Anteriorly it ends at the laryngeal inlet above the true vocal folds at the level of the false vocal folds and includes the cricoid cartilage. Posteriorly, the hypopharynx ends at the level of the entrance to the esophagus, which is guarded by the cricopharyngeus muscle. This muscle has no median raphe, in contrast to the pharyngeal constrictors. Except

during swallowing, belching, or regurgitation, the cricopharyngeus is in a state of tonic contraction functioning as the pharyngoesophageal sphincter or upper esophageal sphincter (UES)3 (Caruso & Sauerland, 1990; Kahrilas et al., 1986). The fibers of the inferior constrictors attach to the sides of the thyroid cartilage. These spaces are known as the pyriform sinuses, and they extend down to the cricopharyngeus muscle (Figure 2–3). The oblique fibers of the inferior constrictor muscles end where the horizontal fibers of the cricopharyngeus muscle

Figure 2–3.  Posterior sketch of the upper aerodigestive tract (larynx and pharynx). Pathway for food bolus is around the larynx and down the channels made by the pyriform sinuses, which elongate during the act of swallowing. The bolus is moved through the upper esophageal sphincter (UES) partially via action of the hyolaryngeal complex decreasing tension on the open UES while the larynx is closed and protected high in the neck under the tongue base. Terminology is rapidly changing in this field. For purposes of this book, the more familiar term upper esophageal sphincter (UES) is used.

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2. Anatomy, Embryology, Physiology, and Normal Development   17

begin. The lateral and posterior walls of the hypopharynx are supported by the middle and inferior constrictors. The anterior boundary of the hypopharynx is the larynx.

Larynx The larynx is a complex structure that is the superior entrance to the trachea. The larynx consists primarily of cartilages, suspended by muscle and ligament attachments to the hyoid bone and cervical vertebrae. The cartilages include the epiglottis, thyroid, cricoid, and paired arytenoids, cuneiforms, and corniculates. Intrinsic muscles of the larynx form the vocal folds (true and false) that are integral to respiration and phonation. The thyrohyoid and thyrocricoid ligaments aid in laryngeal suspension and stability. In order of priority, the three functions of the human larynx are the protection of the lower airways, respiration, and phonation. The structures important in swallow production and in airway protection during swallowing are described in detail. Detailed anatomic description of the intrinsic muscles of the larynx (involved primarily with phonation) is beyond the scope of this chapter. The most important structures of the larynx that protect against aspiration are the paired arytenoid cartilages and the two pairs of vocal folds. In most humans, the epiglottis plays a role in airway protection. However, there are examples of children with congenitally absent epiglottis (Koempel & Holinger, 1998) and functional oral feeding. The epiglottis has a flattened lingual surface, which acts to direct food laterally into the recesses formed by the pyriform sinuses. The movement of food is directed away from the midline and the laryngeal inlet. The arytenoid cartilages and the aryepiglottic folds, reinforced by the smaller

cuneiform and corniculate cartilages, move medially to further buttress the larynx from penetration. The larynx is elevated anteriorly under the tongue and mandible by the hyolaryngeal complex (hyoid bone and attached musculature). The valvelike function provided by the paired false and true vocal folds is the next and most critical level of laryngeal structures involved in airway protection. The false vocal folds (ventricular folds) are primarily involved in regulating the expiration of air from the lower respiratory tract (Sasaki & Isaacson, 1988). In contrast, the true vocal folds do not resist expired air but can prevent inspired air (and foreign material) from entering the larynx. Thus, specific anatomic abnormalities at the laryngeal level must be precisely defined to avoid serious sequelae of an incompetent larynx.

Neuroanatomy of the Larynx Multilevel sphincteric closure of the upper airway is controlled by the recurrent laryngeal nerves. The aryepiglottic folds, made up of the superior part of the thyroarytenoid muscles, approximate to cover the superior inlet of the larynx. The anterior gap is protected by the posteriorly displaced epiglottis, the posterior gap closed by the arytenoid cartilages (Figure 2–4). The false vocal folds form the roof of the laryngeal ventricles and are the second level of protection within the larynx. The thyroarytenoid muscles aid in adduction of the false vocal folds. The third level of protection is the true vocal folds, with the inferior part of the thyroarytenoid muscles providing the bulk of these folds. The true vocal folds attach to the vocal processes of the arytenoid cartilages posteriorly, to the inside surface of the thyroid lamina laterally, and to the thyroid notch anteriorly. Muscular pull by the arytenoid cartilages controls movement of

18  Pediatric Swallowing and Feeding: Assessment and Management

Figure 2–4.  Superior view of the larynx showing the intrinsic structures of the larynx. The laryngeal ventricle is the space between the false and true vocal folds. Airway closure occurs from distal to proximal regions (i.e., first true vocal folds, next false vocal folds, and finally aryepiglottic folds).

the true vocal folds during both swallowing and phonation. Innervation of the protective laryngeal and respiratory functions is centrally located in the brain stem. This control relies on fine sensory and motor innervation to the region. Sensory innervation of the supraglottic and glottic areas is provided by the internal branch of the superior laryngeal nerve (SLN), a branch of the vagus nerve (CN X). The recurrent laryngeal nerve (RLN) (also from CN X) provides sensory innervation to the subglottic mucosa. The posterior part of the true vocal folds and the superior surface of the epiglottis appear to be the most densely innervated part of the larynx (Sasaki & Isaacson, 1988). Chemical and thermal receptors are also found in the supraglottic larynx and are sensitive to a variety of stimuli. In particular, receptors sensitive to water in infants and young children may explain the favorable response to cool mist in children with laryngotracheitis, also known as “croup.” The effect of the mist

slows the rate of respiration while increasing tidal volume, resulting in an overall positive effect on the respiratory status (Sasaki, Suzuki, Horiuchi, & Kirchner, 1979). Other sensory receptors of the larynx include joint, aortic, baroreceptors, and stretch receptors. These afferent impulses are interpreted at the brain-stem level in the tractus solitarius. The ipsilateral RLN (vagus—CN X) innervates all of the intrinsic muscles of the larynx except the cricothyroid muscles. The cricothyroid is innervated by the external branch of the SLN. Only the interarytenoid muscles receive bilateral innervation from the recurrent laryngeal nerves. All of the intrinsic muscles of the larynx are involved in adduction except the posterior cricoarytenoid muscles, the only abductors of the vocal folds. Control at the brain-stem level is within the nucleus ambiguus. Anatomic changes in the larynx are evident when SLN paralysis occurs. The lateral cricoarytenoid muscle, a laryngeal adductor, rotates the posterior laryngeal commis-

2. Anatomy, Embryology, Physiology, and Normal Development   19

sure to the paralyzed side. This results in a foreshortening of the vocal fold on the ipsilateral side, which gives an appearance of asymmetry or tilt to the larynx. In contrast, paralysis of the RLN results in a paramedian position of that vocal fold, caused by the unopposed adductor action of the ipsilateral cricothyroid muscle, innervated by an intact external branch of the SLN.

Esophagus The esophagus is a muscular tube lined with mucosa that propels food from the hypopharynx to the stomach. The cricopharyngeus is the major muscle of the upper esophageal sphincter (UES), also called the cricopharyngeal sphincter and pharyngoesophageal segment (PE segment) and forms the junction between the hypopharynx and the esophagus. The mucosa just above the cricopharyngeus muscle is thin and vulnerable to injury, such as perforation from foreign bodies (Caruso & Sauerland, 1990). The gastroesophageal or lower esophageal sphincter (LES) forms the junction between the esophagus and the stomach. The LES has transient relaxations in contrast to the UES which is in tonic contraction (discussed later in this chapter). These sphincters help keep the esophagus empty between swallows (Derkay & Schechter, 1998). The esophagus is in close proximity to other structures in the neck and thorax. In the neck, it lies anterior to the cervical vertebrae, posterior to the trachea, and between the carotid arteries. The recurrent laryngeal nerves are located on either side of the esophagus in the tracheoesophageal groove. Other important structures in the posterior mediastinum related to breathing, feeding, and swallowing are the left main-

stem bronchus, the aortic arch, the pericardium, and the nerves and blood vessels to the esophagus. The wall of the esophagus is composed of four layers: mucosa, submucosa, muscularis, and adventitia. The mucosa of the esophagus constitutes three layers of tissue: epithelium, lamina propria, and muscularis mucosae. The mucosa of the esophagus is stratified squamous, continuous with the epithelium in the pharynx. Intrinsic muscles of the esophagus are found in an outer longitudinal layer and an inner circular layer. The posterior and lateral portions of the longitudinal muscle encircle the inner muscle layer in a spiral pattern. The upper third of the esophagus is composed of striated muscle similar to the constrictors in the pharynx; the lower two-thirds is made up of smooth muscle fibers. The pharynx and proximal esophagus are the only regions in the body where striated muscle is not under voluntary neural control. Both sympathetic and parasympathetic fibers innervate the esophagus, although the cricopharyngeus muscle seems to be primarily under parasympathetic control via the vagus nerve (Derkay & Schechter, 1998). The vagal motor nerve fibers to striated muscles of the upper esophagus arise from the nucleus ambiguus in the brain stem and those to smooth muscles of originate in the dorsal motor nucleus, next to the nucleus ambiguus. This brief description of the esophagus does not begin to cover the complexities of neural innervation, muscle types and function, mucosal changes, connective tissue, and the extracellular matrix of the esophagus (see Perlman & Konrad Schulze-Delrieu, 1997, with additional references). Significant anatomic differences are found between the infant and older child/adult (see Figures 2–1 and 2–2). These differences are listed by anatomic location in Table 2–1.

20  Pediatric Swallowing and Feeding: Assessment and Management

Table 2–1. Anatomic Locations and Differences Between the Infant’s and Older Child’s Upper Aerodigestive Tracts Differences

Anatomic Location

Infant

Older Child

Oral cavity

Tongue fills mouth

Mouth is larger

Edentulous

Dentulous

Tongue rests between lips and sits against palate

Tongue rests on floor of mouth

Cheeks have sucking pads (fatty tissue within buccinators)

Tongue rests behind the teeth and is not against palate

Relatively small mandible

Buccinators are muscles for chewing only

Sulci important in sucking

Mandibular-maxillary relationship relatively normal Sulci have little functional benefit

Pharynx

Larynx

No definite/distinct oropharynx

Elongated pharynx, so distinct oropharynx exists

Obtuse angle at skull base in nasopharynx

90º angle at skull base

One-third adult size

Less than one-third true vocal fold of cartilage

Half true vocal fold of cartilage

Flat, wide epiglottis

Narrow, vertical epiglottis

By 2 years of age, approximates adult position re: cervical vertebrae

High in the neck, re: cervical vertebrae

Embryology Embryology is the branch of biology involving the study of prenatal development that includes the embryo and the fetus. The anatomy of the oral cavity, pharynx, larynx, and esophagus is the result of embryologic processes that begin at fertilization of the ovum and continue through infancy, childhood, and even into adulthood. In this section, the

development of the head and neck, respiratory system, digestive system, and pertinent parts of the CNS are described in some detail. However, this section is intended to provide a brief overview of the developmental processes. Salient features of the related cardiovascular and musculoskeletal systems are also reviewed. The interested student is referred to texts on embryology for further detail (e.g., Brookes & Zietman, 1998; Moore, Persaud, & Torchia, 2015;

2. Anatomy, Embryology, Physiology, and Normal Development   21

Schoenwolf, Bleyl, Brauer, Francis-West, & Philippa, 2015). Normal embryologic development related to oral sensorimotor function and swallowing is discussed later in this chapter, followed by a brief description of some of the congenital abnormalities that present with swallowing problems.

Embryonic Period (Weeks 1 to 8) Human prenatal development begins at fertilization with formation of a zygote. The zygote is a diploid cell containing 46 chromosomes with half from the mother and half from the father. Fertilization of the egg is completed within 24 hours of ovulation. Repeated mitotic divisions of the zygote result in a rapid increase in the number of cells. By the 3rd week, three germ layers (ectoderm, mesoderm, and endoderm) are formed from which all tissues and organs of the embryo develop. The ectoderm gives rise to the epidermis and the nervous system. The mesoderm gives rise to smooth muscle, connective tissue, and blood vessels. The endoderm gives rise to the epithelial linings of respiratory and digestive systems. During the 3rd week, the CNS and the cardiovascular system begin to form. The neural plate, which is the origin of the CNS, gives rise to the neural folds and the beginning of the neural tube. The neural crest consists of neuroectodermal cells that form a mass between the neural tube and the overlying surface ectoderm. The neural crest gives rise to the sensory ganglia of the cranial and spinal nerves, as well as to several skeletal and muscular components in the head and neck region. All major organ systems are formed during the 4th to 8th weeks of development. During the 4th week, the trilaminar embryonic disc forms into a C-shaped cylindrical

embryo, which later becomes the head, tail, and lateral folds. The dorsal part of the yolk sac becomes incorporated into the embryo and gives rise to the primitive gut (Moore et al., 2015). Infolding at the head region yields the oropharyngeal membrane. The heart is carried ventrally, and the developing brain is at the most cranial part of the embryo. By the end of the 8th week, the embryo begins to have a human appearance.

Fetal Period (Week 9 to Birth) The fetal period begins in the 9th week and is primarily marked by rapid body growth, with relatively slower head growth compared with the rest of the body. Differentiation of tissues and organs continues during this time. A brief description of major embryologic changes is followed by more detailed information regarding systems directly involved in swallowing.

9 to 12 Weeks At the beginning of the 9th week, the head makes up half the length of the fetus, measured from the crown to the rump (Caruso & Sauerland, 1990). At 9 weeks, the face is broad, with widely separated eyes, fused eyelids, and low-set ears. The legs are short with relatively small thighs. By the end of 12 weeks, the upper limbs will have almost reached the final relative lengths, although lower limbs are still slightly shorter than the final relative lengths.

13 to 16 Weeks By the 13th week, body length has more than doubled. Body growth occurs so rapidly that by the 16th week, the head is relatively small compared with the end of

22  Pediatric Swallowing and Feeding: Assessment and Management

the 12th week. Ossification of the skeleton begins during this period.

17 to 20 Weeks Somatic growth slows down, but length continues to increase. Fetal movements are beginning to be felt by the mother. Eyebrows and head hair become visible at 20 weeks.

21 to 25 Weeks Substantial weight gain occurs during this time. By 24 weeks, the lungs begin producing surfactant, which is a surface-active lipid that maintains the patency of the developing alveoli of the lungs. However, the respiratory system is still very immature and unable to sustain life independently. If born at this premature stage, however, surfactant replacement therapy has allowed some of these premature infants to survive.

26 to 29 Weeks The lungs are capable of air exchange, but with some difficulty. The CNS is beginning to mature, and rhythmic breathing movements are possible although not present in all infants. Control of body temperature begins. The eyes are open at the beginning of this period.

30 to 34 Weeks By 30 weeks, the pupillary light reflex of the eyes can be elicited. By 34 weeks, white fat in the body makes up about 8% of body weight. The presence of white fat is a developmental milestone for normal feeding potential because the infant then begins to show some nutritional reserves. Body temperature regulation is more stable by 34 to 35 weeks.

35 to 40 Weeks At 36 weeks, the circumferences of the head and the abdomen are approximately equal. After 36 weeks, the abdomen circumference may be greater than that of the head. Although at full term the head is much smaller relative to the rest of the body than it was during early fetal life, it is still reasonably large in relation to the size of their bodies. The expected time of birth is 38 weeks after fertilization (gestational age or postconceptual age) or 40 weeks after the last menstrual period. By full term, the amount of white body fat should be about 16% of body weight.

Head and Neck Development Branchial (Pharyngeal) Apparatus Development The head and neck are developed from the branchial apparatus, which consists of branchial arches, pharyngeal pouches, branchial grooves, and branchial membranes. Branchial arches are derived from the neural crest cells and begin to develop early in the 4th week, as the neural crest cells migrate into the future head and neck region. By the end of the 4th week, four pairs of branchial arches are visible (Figure 2–5). The fifth and sixth pairs are too small to be seen on the surface of the embryo. The branchial arches are separated by the branchial grooves, which are seen as prominent clefts in the embryo. The branchial arches contribute to formation of the face, neck, nasal cavities, mouth, larynx, and pharynx, with the muscular components forming striated muscles in the head and neck. Anatomic development of the thyroid and cricoid cartilages

2. Anatomy, Embryology, Physiology, and Normal Development   23

Otic vesicle Third branchial arch Second branchial arch (Hyoid) First branchial arch (Mandibular)

Optic vesicle

Heart prominence

Yolk stalk Body stalk

Figure 2–5. Human embryo at about 28 days showing early branchial (pharyngeal) apparatus relationships. Four pairs of branchial arches can be seen with their respective branchial grooves.

beginning at the 13th week (up to 27 weeks) reveals a correlation between laryngeal length and fetal crown-rump (C-R) with no differences between genders (GawlikowskaStoka et al., 2010). The width of both thyroid cartilage laminae was significantly larger in males than in females across 13 to 27 weeks (Gawlikowska-Stoka et al., 2010) with similar sexual dysmorphism noted for glottis opening in postmortem study (Fayoux, Marciniak, Deisme, & Storme, 2008). These authors suggest that findings may be useful in planning treatment of airway emergencies. The cranial nerve supply for each branchial arch, along with the skeletal structures

and muscles derived from the branchial arches are described in Table 2–2.

Facial Development The mandible is the first structure to form by the merging of the medial ends of the two mandibular prominences of the first branchial arch during the 4th week. Maxillary prominences of the first branchial arch grow medially toward each other, as do the medial nasal prominences soon thereafter. The auricles of the external ear begin to develop by the end of the 5th week. As the brain enlarges, a prominent forehead is noted, the eyes move medially, and the

Table 2–2. Cranial Nerves, Structures, and Muscles Derived From Branchial (Pharyngeal) Arch Components Arch

Cranial Nerves

Structures

Muscles

First (mandibular)

Trigeminal (V)

Mandible

Muscles of mastication

Maxilla

Mylohyoid and anterior belly of digastric

Malleus, incus

Tensor tympani

Zygomatic bone

Tensor veli palatini

Temporal bone (squamous portion) Second (hyoid)

Facial (VII)

Stapes

Muscles of facial expression

Styloid process

Stapedius

Hyoid bone

Stylohyoid

(Lesser cornu) (Upper body) Posterior belly of digastric Third

Glossopharyngeal (IX)

Hyoid bone

Stylopharyngeus

(Greater cornu) (Inferior body)

Hypoglossal (XII)

Posterior one-third of tongue Epiglottis

Fourth and sixth

Vagus (X)

Tongue

Palatoglossus

SLN

Laryngeal cartilages

Cricothyroid

RLN

Epiglottis (fourth)

Levator veli palatini Pharyngeal constrictors Intrinsic muscles of larynx Striated muscles of esophagus

Note. RLN = recurrent laryngeal nerve; SLN = superior laryngeal nerve. Source: Adapted from Structures derived from pharyngeal arch components. In K. L. Moore (Ed.), The developing human (10th ed., p. 160). Philadelphia, PA: Elsevier, 2015.

24

2. Anatomy, Embryology, Physiology, and Normal Development   25

external ears ascend. At 16 weeks, the eyes begin to migrate and are situated more anteriorly than laterally. The ears are closer to their final position at the sides of the head. The medial and lateral nasal prominences are formed by growth of the surrounding mesenchyme, which results in formation of primitive nasal sacs. The nasal cavity is separated from the oral cavity by the oronasal membrane (Figure 2–6), which ruptures at about 6 weeks. This rupture that forms the primitive choanae brings the nasal and oral cavities into direct communication. If the oronasal membrane does not rupture, a choanal atresia will make it impossible for an infant to suck, swallow, and breathe synchronously (Chapter 4). The posterior nasal choanae are located at the junction of the nasal cavity and the nasopharynx once the development of the palate is completed. Palatal development begins toward the end of the 5th week and is completed in the 12th week (Figure 2–7). Development occurs from anterior to posterior as mesenchymal masses merge toward the midline. The primary palate, or medial palatine

process, develops at the end of the 5th week and is fused by the end of the 6th week to become the premaxillary part of the maxilla. The primary palate gives rise to a very small part of the adult hard palate that is positioned just posterior (or caudal) to the incisive foramen of the skull. Subsequently, the secondary palate develops from two horizontal lateral palatine processes that fuse over the course of a few weeks from the incisive foramen posterior to the soft palate and uvula. The anterior hard palate (ossified) is fused by 9 weeks, and the muscular soft palate is completed by the 12th week. The nasal septum develops downward from the merged medial nasal prominences. During the 9th week, the fusion between the nasal septum and the palatine processes begins anteriorly and is completed at the posterior portion of the soft palate by the 12th week. This process occurs in conjunction with the fusion of the lateral palatine processes. The palatine processes fuse about a week later in female than in male fetuses, which may explain why isolated cleft palate is more common in female infants (Burdi,

Rupturing oronasal membrane Pharynx

Nasal cavity Primary palate

Tongue

Oral cavity Mandibular process

Figure 2–6.  Sagittal section showing oronasal membrane, which separates the nasal and oral cavities. At about 6 weeks, the oronasal membrane ruptures to form the primitive choanae. This brings the nasal and oral cavities into direct communication.

26  Pediatric Swallowing and Feeding: Assessment and Management

Philtrum Upper lip Choanae Nasal septum

Nostril Primary palate (Premaxilla) Lateral palatine process

Figure 2–7.  Palatal development from anterior to posterior. The lateral processes fuse to form most of the hard and soft palate, completed by 9 and 12 weeks, respectively.

1969). As the jaws and the neck develop, the tongue descends and occupies a relatively smaller space in the oral cavity. The tongue also develops from the third and fourth branchial arches.

Prenatal Sucking, Swallowing, and Breathing Development The pharyngeal swallow is one of the first motor responses in the pharynx. It has been reported between 10 and 14 weeks’ gestation (Humphry, 1970). Pharyngeal swallows have been observed in delivered fetuses at 12.5 weeks’ gestation (Humphry, 1970). Ultrasound studies reveal nonnutritive suckling/sucking and swallowing in most fetuses by 15 weeks’ gestation (Moore et al., 2015). Sucking, suckling, and sucking act are terms often used interchangeably in the literature to describe mouthing movements and ingestion of food by infants (Wolf & Glass, 1992). Suckling, the earliest intake pattern for liquids, is characterized by a definite backward and forward movement of the tongue, with the backward phase

more pronounced (Figure 2–8). In contrast, sucking begins to emerge at four months of age, and involves more of an up and down movement of the tongue and active use of the lips. A suckling response may be elicited at this stage as noted by the finding that stroking the lips yields suckling responses in spontaneously aborted fetuses. True suckling begins around the 18th to the 24th week. Self-oral-facial stimulation precedes suckling and swallowing with consistent swallowing seen by 22 to 24 weeks’ gestation (Miller, Sonies, & Macedonia, 2003). Tongue protrusion does not extend beyond the border of the lips (Morris & Klein, 1987). By the 34th week, most healthy fetuses, if born at that time, can suckle and swallow well enough to sustain nutritional needs via the oral route. Some infants appear coordinated enough to begin oral feedings by 32 to 33 weeks’ gestation (Cagan, 1995). Infants born late preterm (between 34 0/7 and 36 6/7 weeks of gestation), account for 70% of all preterm births (Davidoff et al., 2006; Dong & Yu, 2011; Loftin et al., 2010; Perugu, 2010). The incidence of late pre-

2. Anatomy, Embryology, Physiology, and Normal Development   27

Figure 2–8.  Suckling and sucking comparisons of tongue and mandibular action. Suckling is characterized by in–out tongue movements and some jaw opening and closing; sucking is characterized by up–down tongue movements and less vertical jaw action. Readers are reminded that terms may be used differently in the literature.

term births has increased markedly in the past two decades with increased prevalence of medical problems that are also noted in early term (37 to 38 weeks’ gestation) compared to infants born full term (39 to 41 weeks) (Brown, Speechley, Macnab, Natale, & Campbell, 2014; Hwang et al., 2013; Sahni & Polin, 2013). Feeding difficulties are reported with high frequency in infants who are bottle or breastfeeding (Dosani et al., 2017). There are limited data on feeding problems in late preterm infants (Bloomfield et al., 2018; DeMauro, Patel, MedoffCooper, Posencheg, & Abbasi, 2011). Gianni and colleagues (2015) note that nutritional support is likely to be needed for those late preterm infants with a birth weight less than or equal to 2000 g, gestational age of 34 weeks, and born small for gestational age, develop respiratory distress syndrome, and require a surgical procedure. Decreased rates of fetal suckling are associated with alimentary tract obstruction or neurologic damage, the latter of which manifests as intrauterine growth restriction (Derkay & Schechter, 1998). It is estimated that 450 ml of the total 850 ml of amniotic fluid produced daily is swallowed in utero (Bosma, 1986).

Ultrasound has shown that suckling motions increase in frequency in the later months of fetal life. The frequency of the suckling motions can be modified by taste. Taste buds are evident at 7 weeks’ gestation, with distinctively mature receptors noted at 12 weeks (Miller, 1982). Ultrasonography is shown to have a high degree of intra- and interobserver repeatability for analysis of sucking and swallowing movements (Levy et al., 2005).

Digestive System Development The endoderm of the primitive gut, which forms in the 4th week, gives rise to most of the epithelium and glands of the digestive tract. The muscles, connective tissue, and other layers comprising the wall of the digestive tract are derived from the splanchnic mesenchyme (loosely organized connective tissue) surrounding the endodermal primitive gut. The foregut, midgut, and hindgut make up the primitive gut. The derivatives of the foregut include the pharynx and its derivatives, respiratory system, esophagus, stomach, duodenum (up to the opening of the bile duct),

28  Pediatric Swallowing and Feeding: Assessment and Management

liver, pancreas, and the biliary apparatus (gallbladder and biliary duct system). The celiac artery supplies all derivatives except the pharynx, respiratory tract, and most of the esophagus. The esophagus elongates rapidly and reaches its final relative length by the 7th week. If it does not elongate sufficiently, part of the stomach may be displaced superiorly through the esophageal hiatus in the thorax, resulting in a congenital hiatal hernia (Moore et al., 2015). (See Chapter 5.) Although the upper third of the esophagus is made up of striated muscle and the lower two thirds of smooth or nonstriated muscle, there is a transition region between the cervical and thoracic levels where striated and smooth muscle fibers intermingle. Both types of muscle are innervated by branches of the vagus nerve (CN X). The esophagus and airways share common innervations with complex interrelationships of afferents and efferents having both sympathetic and parasympathetic responses, as reviewed by Jadcherla (2017).

Respiratory System Development The respiratory system begins to develop during the 4th week by formation of a median laryngotracheal groove in the caudal end of the ventral wall of the primitive pharynx. This laryngotracheal groove develops into a laryngotracheal diverticulum that then becomes separated from the primitive pharynx (cranial part of the foregut) by longitudinal tracheoesophageal folds. During the 4th and 5th weeks, these folds fuse and form the tracheoesophageal septum, which is a partition dividing the foregut into a ventral and a dorsal portion. The ventral portion is the laryngotracheal

tube that eventually becomes the larynx, trachea, bronchi, and lungs. The dorsal portion becomes the esophagus. It is clear from these early embryologic changes that the airway and digestive systems are inextricably related because they initially develop from the same embryonic structure.

Laryngeal Development The opening of the laryngotracheal tube into the pharynx becomes the primitive glottis. The laryngeal cartilages and muscles are derived from the 4th and 6th pairs of branchial arches (see Table 2–2). The epithelium of the mucous membrane lining of the larynx develops from the endoderm of the cranial end of the laryngotracheal tube. The mesenchyme proliferates rapidly at the cranial end of the laryngotracheal tube to produce paired arytenoid swellings at 5 weeks (Figure 2–9A). The primitive glottis (Figure 2–9B), a slitlike opening, is converted into a T-shaped opening as the arytenoid swellings grow toward the tongue (Figure 2–9C). This action reduces the developing laryngeal lumen again to a narrow slit. The laryngeal lumen is temporarily occluded by rapid proliferation of the laryngeal epithelium. By the 10th week, recanalization of the larynx occurs (Figure 2–9D). The epiglottis develops from the caudal part of the hypobranchial eminence. This eminence is produced by proliferation of mesenchyme in the ventral parts of the third and fourth branchial arches.

Tracheobronchial and Pulmonary Development The laryngotracheal tube distal to the larynx gives rise to the epithelium and glands

2. Anatomy, Embryology, Physiology, and Normal Development   29

A

5 Weeks

Epiglottis

B

6 Weeks

Arytenoid swelling

C

7 Weeks

Epiglottis Primitive glottis

Epiglottis Glottis

Arytenoid swelling

D

10 Weeks

Epiglottis

Glottis Cartilages

Figure 2–9.  Embryologic stages of laryngeal development. A. At 5 weeks, paired arytenoid swellings develop at cranial end of the laryngotracheal tube. B. At 6 weeks, the primitive glottis can be seen. C. At 7 weeks, T-shaped opening is evident in the glottis as arytenoid swellings grow toward the tongue. D. At 10 weeks, recanalization of the larynx occurs.

of the trachea and lungs. The tracheal cartilages, connective tissue, and muscles are derived from the surrounding splanchnic mesenchyme. The cartilage is in the form of C-shaped rings in the trachea and major bronchi. In more peripheral airways, the cartilage becomes more irregular and less prominent. The subglottic space is defined by the cricoid cartilage, the only cartilage that forms a complete ring. The respiratory system develops so that it is capable of immediate function by full-term gestation. The lungs must have sufficiently thin alveolocapillary membranes and an adequate amount of surfactant for normal respiration to occur.

Maturation of the lungs occurs in four periods (Moore et al., 2015): n Pseudoglandular period (6 to 16 weeks):

Resembles an exocrine gland and by 16 weeks all major elements have formed, except those involved with gas exchange. Respiration is not possible. n Canalicular period (16 to 26 weeks): Overlaps with previous period since cranial segments mature faster than caudal segments. Lung tissue becomes highly vascular by the end of this period. Fetuses born near the end of this period may survive if given intensive care, but survival is not always

30  Pediatric Swallowing and Feeding: Assessment and Management

possible due to respiratory and other systems still being relatively immature. n Terminal saccular period (26 weeks to birth): Many terminal saccules develop, and their epithelium becomes very thin. Capillaries bulge into developing alveoli. The blood–air barrier is established through intimate contact between epithelial and endothelial cells that permit adequate gas exchange for survival. Complex development of type I and II alveolar cells takes place. The type II cells secrete pulmonary surfactant, which is a monomolecular film, over the internal walls of the terminal saccules. That action lowers surface tension at the air–alveolar interface. Production of surfactant increases during the final stages of pregnancy, especially during the last two weeks. n Alveolar period (32 weeks to 8 years): Exactly when this period begins depends on the definition of the term alveolus. At 32 weeks, saccules are present and analogous to alveoli. However, characteristic mature alveoli do not form until after birth with about 95% of alveoli developing postnatally. During the first few months after birth, an exponential increase is seen in the surface of the air–blood barrier that is accomplished by multiplication of alveoli and capillaries. The lungs of full-term newborn infants contain about 50 million alveoli (one sixth of adult number), which make their lungs denser than adult lungs. By 2 years of age, most postnatal alveolar development is completed (Thurlbeck, 1982). The lungs are about half-filled with fluid at birth. Aeration of the lungs occurs from the rapid replacement of intra-alveolar fluid by air. The fluid is cleared by three routes: (a) through mouth and nose by pressure on the

fetal thorax during delivery, (b) into the pulmonary capillaries, and (c) into the lymphatics and pulmonary arteries and veins. Normal lung development depends on three factors: (a) adequate thoracic space for lung growth, (b) fetal breathing movements, and (c) adequate amniotic fluid volume (Moore et al., 2015).

Cardiovascular System Development The cardiovascular system is the first organ system to function in the embryo. By the end of the 3rd week, blood begins to circulate, and the first heartbeat occurs at 21 to 22 days. The heart develops from splanchnic mesenchyme as paired endocardial heart tubes form and fuse into a single heart tube, which is the primitive heart. From the 4th to the 7th week, the four chambers of the heart are formed. The critical period of heart development is from Day 20 to Day 50 after fertilization. The partitioning of the primitive heart results from complex processes, and defects of the cardiac septa are relatively common. Fetal blood is oxygenated in the placenta. The lungs are nonfunctional as organs of respiration during prenatal life. Adequate respiration in the newborn infant is dependent on normal circulatory changes occurring at birth. The modifications that establish postnatal circulatory patterns at birth are gradual and continue for the first several months of life. Congenital heart disease (CHD) is the most common cause of major congenital anomalies, occurring in an estimated 8 per 1,000 live births (van der Linde et al., 2011). Detection of fetal CHDs is possible as early as the 17th or 18th week of development. Although the underlying causes of CHD

2. Anatomy, Embryology, Physiology, and Normal Development   31

need further clarification, single-gene, chromosomal variations and exposure to teratogens have been associated with these problems. See Chapter 12.

Central Nervous System Development The CNS develops from the neural plate, which appears about the middle of the 3rd week and becomes the neural tube. The cranial end of the neural tube forms the brain, which consists of the forebrain, midbrain, and hindbrain. The forebrain is the basis for the cerebral hemispheres and the diencephalon. The midbrain becomes the adult midbrain. The hindbrain becomes the pons, cerebellum, and medulla oblongata. The spinal cord is formed from the rest of the neural tube. The ventricles of the brain and the central spinal canal are derived from the lumen of the neural tube. Proliferation of neuroepithelial cells causes the walls of the neural tube to thicken. These cells give rise to all nerve and macroglial cells in the CNS. Twelve pairs of cranial nerves are formed during the 5th and 6th weeks of development. They are classified into three groups according to their embryological origins: (a) somatic efferent cranial nerves—trochlear (CN IV), abducent (CN VI), hypoglossal (CNXII), and greater part of oculomotor (CN III); (b) nerves of pharyngeal arches— trigeminal (CN V), facial (CN VII), glossopharyngeal (IX), and vagus (CN X); and (c) special sensory nerves—olfactory (CN I), optic (CN II), and vestibulocochlear (CN VIII). Neural tube defects are described by Copp, Stanier, & Greene, 2013, but will not be discussed here. The cranial nerves of the branchial arches, described earlier, are particularly important for normal swallowing. The

CNS regulates the buccal, lingual, and pharyngeal movements necessary for sucking and swallowing. Four-dimensional ultrasound demonstrates that the fetal face is an important indicator of fetal brain function at 20 to 24 weeks of gestation, with a range of facial expressions to include mouthing, tongue expulsion, and features of emotionlike behaviors (AboEllail & Hata, 2017; Sato et al., 2014). Further description of CNS development is found in Chapter 3. The neural control of deglutition is discussed in more detail in the physiology section in this chapter (e.g., Costa, 2018).

Embryologic Abnormalities Affecting Swallowing and Feeding Congenital abnormalities or birth defects are structural abnormalities of any type present at birth. (See Chapter 12 for a review of the evaluation and management of patients with craniofacial anomalies associated with feeding disorders and an overview of clinically available tests.) Briefly, four clinically significant types are malformation, disruption, deformation, and dysplasia. Congenital abnormalities or malformations result from both genetic factors and environmental factors, with some malformations caused by these factors acting together. An accurate diagnosis is integral for patient care of children with underlying genetic conditions. Recent advances in sequencing, particularly whole-exome sequencing (WES), are identifying genetic basis of disease for 25% to 40% of patients. These percentages are anticipated to increase as these analyses become more common (Sawyer et al., 2016). CNS damage from congenital malformations is a major underlying cause of swallowing and feeding problems in infants. In

32  Pediatric Swallowing and Feeding: Assessment and Management

addition, upper airway anomalies or other anatomic defects may occur. It is estimated that 5% to 7% of human developmental abnormalities result from the in utero action of drugs, viruses, and other environmental factors (Persaud, Chudley, & Skalko, 1985). Exposure of the embryo to teratogens (agents that produce or raise the incidence of congenital malformations, such as drugs and viruses) have their effect during the stage of active differentiation of an organ or a tissue. The most critical period for brain development is from 3 to 16 weeks; however, disruptions in development can occur after this time period. The brain is differentiating and growing rapidly at birth and continues at least throughout the first 2 years of life. Three important principles must be considered regarding possible susceptibility to teratogens: (a) critical periods of development, (b) dosage of the drug or chemical, and (c) genotype (genetic constitution of the embryo) (Moore et al., 2015). Injuries early in gestation are generally more severe for two reasons. First, little or no barrier exists between blood and brain, so chemicals enter the brain easily. After birth, the blood–brain barrier is more effective. Second, a small injury in the early developing brain will be magnified by the effect on the total remaining sequence of development, which is dependent on the injured area (Lenn, 1991). Patterns of malformation occur in recognizable ways because the parts of the brain that arise from a region of early injury are malformed after the injury. Readers interested in brain development, early brain injuries, and neuroplasticity are encouraged to review the works by Anderson, Spencer-Smith, and Wood (2011); Johnston (2009); Kolb, Harker, and Gibb (2017); and Staudt (2010). Low birth weight and prematurity are other potential complicating factors. Survival is unlikely with a birth weight of less than 500 g and a gestational age of less than

22 to 23 weeks. By 28 weeks’ gestational age, survival is more common because significant development occurs in the respiratory system and CNS from 24 to 32 weeks. Detailed descriptions of conditions are beyond the scope of this chapter. Some information can be found in separate chapters with direct relevance to swallowing and feeding factors in infants and children. Readers are encouraged to keep aware of updated information available via online sites, including but not limited to PubMed (https://www.pubmed.gov) and Online Mendelian Inheritance in Man (https:// www​.omim.org/). Embryologic abnormalities can affect multiple systems (e.g., CNS, head and neck structures, respiratory tract, esophageal and rest of GI tract, and cardiopulmonary system).

Physiology of Swallowing The swallowing process depends on a highly complex and integrated sensorimotor system. Swallowing is considered one of the most complex functions because it includes several anatomic areas, has voluntary and involuntary components, and requires simultaneous inhibition of respiration. Neuromuscular coordination must engage the CNS, afferent sensory input, motor responses of voluntary and involuntary muscles, the brain stem, and the enteric nervous system (ENS). Hormonal factors also play a critical role that is poorly understood. The integration of several normal functions further complicates the act of swallowing. These include chewing and swallowing, respiration and chewing, and the pharyngeal phase of swallowing and respiration (Miller, 1999). These functions, along with the entire act of swallowing, are controlled by pattern generators in the brain stem that

2. Anatomy, Embryology, Physiology, and Normal Development   33

are modulated by the cerebral cortex as well as through sensory input (Miller, 1999). The historic interest in dysphagia has provided a rich and detailed understanding of the swallowing processes in adults, especially those with neurologic deficits and head/neck cancer. Although much of the information may be applicable to the older child, preterm infants, neonates, infants, and young children have additional factors of normal and abnormal development (see later text) to consider. For the student interested in the neurophysiology of swallowing, publications by Miller and coworkers are recommended (Miller, 1999; Miller, Bieger, & Conklin, 1997).

Swallow Components/Phases The swallowing process is commonly described in phases or stages. Although the functions needed to carry out the work of each phase of swallowing may overlap, for discussion purposes, swallowing is described in five phases: 1. oral preparatory (also known as bolus formation), 2. oral transit, 3. initiation of pharyngeal swallow, 4. pharyngeal, and 5. esophageal transit. The first two phases are under voluntary neural control. The pharyngeal phase has both voluntary and involuntary control. The esophageal phase is under involuntary control. The sequence of movements is diagrammed in Figure 2–10.

Oral Preparatory/Bolus Formation The oral preparatory phase is voluntary and requires a process for getting food and/or liquid into the mouth. Someone needs to

feed the infant or child when age or neurologic impairment precludes self-feeding. Once food is in the mouth, formation of a bolus begins. In a normal infant, bolus formation per se is minimal. This phase is characterized by latching to the nipple (breast or bottle). Once liquid is extracted from the nipple, the liquid is being transported posteriorly. When foods are added to the diet, duration of the oral preparatory phase varies considerably, depending on the texture of the food and the child’s oral skill level. As children begin to handle thicker, lumpier textures, bolus formation may last for several seconds. The more chewing that is required, the longer it takes for bolus preparation. Oral manipulation of liquid presented via cup varies significantly from one child to another, but usually liquid is held in the oral cavity for less than 2 s. Lip closure is needed once material is in the mouth so that no liquid or food will be dribbled down the chin. Some children may move liquid (and at times food) around in the mouth before they form a cohesive bolus. The material is then held between the elevated tongue and hard palate. The digastric, genioglossus, geniohyoid, and mylohyoid muscles aid in tongue elevation. The bolus is held in a median groove in the tongue created by the movement of the intrinsic muscles of the tongue, and the lateral borders of the tongue abut the hard palate (e.g., Derkay & Schechter, 1998). The buccinator muscles help to generate suction in neonates and hold food between the teeth in older infants and children. During this process, the soft palate is in a lowered position and resting against the tongue base. This position helps to prevent a bolus from entering the pharynx before the swallow is produced. Active lowering of the soft palate occurs by contraction of the palatoglossus muscle. The airway remains open and nasal breathing continues until a pharyngeal swallow is initiated.

34  Pediatric Swallowing and Feeding: Assessment and Management

Figure 2–10.  Oral, pharyngeal, and esophageal components/phases of normal swallow in a young child. A. Oral transit/phase showing formed bolus moving posteriorly through the oral cavity. B. Initiation of pharyngeal phase. C. Bolus moving through the pharynx with adequate airway protection. D. End of pharyngeal phase as upper esophageal sphincter (cricopharyngeus) opens. E. Esophageal transit with bolus in the cervical esophagus.

Oral Transit Oral transit is under voluntary neural control and begins with posterior propulsion of the food bolus by the tongue and ends with the initiation of a pharyngeal swallow. The voluntary actions in manipulating a bolus of food or liquid include elevation and posterior movement of the tongue, aided in part by the styloglossus muscle. Sequential contact of the tongue to the hard and soft palate occurs as the bolus is propelled into the pharynx. Elevation of the soft palate against the posterior pharyngeal wall seals the nasopharynx and prevents pharyngonasal backflow, more commonly described as nasopharyngeal reflux. Given the material moves from the pharynx into the nasal passage, it seems more accurate to use the term pharyngonasal backflow (or reflux).

Oral transit timing does not vary according to texture and is minimal in infants and less than 1 s in children.

Initiation of Pharyngeal Swallow The precise anatomic location for initiation of the pharyngeal swallow is variable with no published reports in children. Initiation may occur at the anterior tonsillar pillars, base of tongue, valleculae, or the pyriform sinuses (Derkay & Schechter, 1998). Asymptomatic adults are seen to initiate pharyngeal swallows with greater frequency in the valleculae, whereas symptomatic adults and elderly persons more often initiate pharyngeal swallows in the hypopharynx and pyriform sinuses (Zancan, Luchesi, Mituuti, & Furkim, 2017). Sensory input and feedback during bolus formation and oral transit are criti-

2. Anatomy, Embryology, Physiology, and Normal Development   35

cal to normal swallowing. The rich and diverse sensors include mechanoreceptors (touch, pressure), pain receptors, proprioceptive receptors (shape, location), chemical receptors, and special receptors for taste, smell, and temperature. Interestingly, water is perceived differently than other liquids, particularly in the oropharynx (Miller, 1999). Mechanoreceptors located in the tongue, teeth, soft palate, and hard palate help to modulate the muscles of mastication through brain-stem integrative pathways.

Pharyngeal Swallow Function The pharyngeal swallow function is critical because the potential for aspiration is greatest in this phase of the swallow. Sensory input proceeds into specific regions of the trigeminal nuclei (V) and the nucleus tractus solitarius (NTS) of the brain stem (Miller, 2008). Tongue base propulsion is an important basis for pharyngeal swallow initiation. The pharyngeal phase begins with the voluntary production of a swallow and the elevation of the soft palate to close off the nasopharynx. Pharyngeal constrictors contract to propel the bolus through the pharynx. Simultaneously, the larynx is closed to protect the airway. There is no interruption of the posterior bolus movement with normal swallowing. From a biomechanical perspective, the pharyngeal swallow function can be divided into six steps (Miller, 1999): 1. elevation and retraction of the soft palate that results in closure of the nasopharynx, 2. opening of the UES (relaxation and passive opening with anterior laryngeal movement), 3. laryngeal closure at the level of the laryngeal vestibule, 4. tongue loading or ramping,

5. tongue propulsion, and 6. pharyngeal clearance. It was thought that the mylohyoid muscle initiates this series of steps; however, the genioglossus may be the first tongue muscle to start the pharyngeal swallow (Miller, 1999). As the swallow occurs, the larynx engages several mechanisms to provide protection: 1. Respiration ceases. 2. Laryngeal elevation and anterior movement supported by the hyoid bone bring the larynx under the base of the tongue. Elevation contributes to closure of the airway entrance (minimal elevation occurs in young infants given the larynx is high in the neck). Forward movement contributes to opening of the upper esophageal sphincter (e.g., Logemann, 1998). 3. The epiglottis diverts food laterally into the pyriform sinuses, although not equally in all individuals. Pyriform sinuses then open into the esophageal inlet during simultaneous cricopharyngeal (UES) opening. 4. Aryepiglottic folds move in an anterior and medial direction to cover the glottis. 5. Closure of the larynx (false vocal folds and true vocal folds adduct) begins at the level of the vocal folds and progresses upward to the laryngeal vestibule (Ardran & Kemp, 1952, 1956). The most important protection is the complete and automatic closure of the larynx during swallowing. Vocal fold closure occurs when the larynx elevates to approximately 50% of its maximum elevation (Gilbert et al., 1996). Contrary to popular belief, the epiglottis is not absolutely essential for

36  Pediatric Swallowing and Feeding: Assessment and Management

glottic closure or for the prevention of aspiration; however, it does play an important and active role in most individuals. The epiglottis is brought down over the glottis during swallowing and deflects the bolus being swallowed material laterally and posteriorly toward the esophagus. High-speed cineradiography has been used to distinguish two steps in closure of the laryngeal vestibule (as opposed to the glottis) during swallowing. The first step observed was closure of the supraglottic space of the laryngeal vestibule. Apposition of the lateral walls seemed to be caused by contraction and thickening of the superior portion of the thyroarytenoid muscles (Ekberg, 1982). The second step was compression of the subepiglottic space from above as the posterior tongue movement brought the epiglottis down over the laryngeal vestibule. This sequence of events supported the observation that a peristalticlike motion can clear the vestibule of bolus material. Therefore, when the vestibule is open after a swallow, it is free from any residue of foreign particles. Normally an infant swallows about six times per minute while awake and six times per hour while asleep. In infants a safe swallow is aided by the cessation in breathing and sustained laryngeal closure. This mechanism is typically effective in protecting the larynx from aspiration. During the cessation of breathing, the swallowing rate increases, presumably to clear secretions from the airway before another breath is drawn (Loughlin & Lefton-Greif, 1994). The increase in survival of preterm infants has led to increased urgency for evidencebased knowledge of the physical and physiologic immaturity of these infants in order to understand the difficulties many infants have in feeding orally. This understanding is needed in order to facilitate safe and efficient oral feeding in these preterm infants

who swallow primarily during the cessation of breathing and subsequent inhalation, both of which increase the risk of oxygen desaturation and laryngeal penetration/ aspiration (Lau, 2016; Lau, Smith, & Schanler, 2003). Another major protective mechanism for the airway is the cough reflex (Thach, 2007). Cough is triggered by sensory receptors stimulated in the larynx and the subglottic space and transmitted to the brain stem by the vagus nerve (CN X). Immediately upon stimulation of these receptors, the glottis is closed and an explosive cough follows. Although limited data are available regarding coughing and airway clearance in infants and young children, mechanisms associated with cough, provocation, and resolution have been studied in premature infants with bronchopulmonary dysplasia (BPD). Coughing appears to have an upper aerodigestive origin, while clearing appears to be associated with peristaltic reflexes (Jadcherla, Hasenstab, Shaker, & Castile, 2015). Glottic closure reflex also aids in protecting the larynx from noxious stimuli. During swallowing, as the epiglottis moves posteriorly and inferiorly, contraction of intrinsic laryngeal muscles brings together the arytenoids, epiglottis, and the false and true vocal folds. Simultaneously, the larynx is elevated and pulled forward, away from the path of the bolus. Laryngeal function during swallow has been examined in healthy young adults via frame-by-frame analysis of concurrent transnasal videoendoscopy, videofluoroscopy, pharyngeal intraluminal manometry, and submental surface electromyography (Shaker, Dodds, Dantas, Hogan, & Arndorfer, 1990). Four sequential events associated with laryngeal closure were noted: (a) adduction of the true vocal folds associated with the horizontal approximation of arytenoid cartilages, (b) vertical approximation of the arytenoids

2. Anatomy, Embryology, Physiology, and Normal Development   37

to the base of the epiglottis, (c) laryngeal elevation, and (d) epiglottal descent. The onset of vocal fold adduction was the first event to occur in the oropharyngeal swallow sequence. Shaker and colleagues (1990) noted that the mere introduction of liquid into the mouth frequently caused the vocal folds to adduct partially, suggesting that there may be sensory afferent fibers within the oral cavity that stimulate the laryngeal closure protective mechanism. A simple oroglottal reflex or higher brain-stem function may be involved. Maximal vocal fold adduction preceded the appearance of the peristaltic wave in the oropharynx. The most striking finding by Shaker et al. (1990) was that true vocal fold closure was the first event to occur in the oropharyngeal swallow sequence and that it persisted throughout the sequence. The vocal fold closure results primarily from contraction of the intrinsic laryngeal adductor muscles, specifically the thyroarytenoids, lateral cricoarytenoids, interarytenoids, and cricothyroids. Previous studies (Barclay, 1930; Sasaki & Isaacson, 1988; Sasaki & Masafumi, 1976) showed that the false vocal folds closed during swallowing, but Shaker et al. (1990) found that the false vocal folds generally remained open. Infants and children demonstrate cessation of breathing with laryngeal closure that precedes posterior bolus propulsion (Derkay & Schechter, 1998; Loughlin & Lefton-Greif, 1994).

Esophageal Swallow Function Esophageal swallow function is characterized by an automatic peristaltic wave that carries the bolus to the stomach. The process of peristalsis moves the bolus through the esophagus and ends when the food passes through the gastroesophageal junction. The skeletal muscle in the cervical esophagus propels the food more quickly

than the smooth muscle in the thoracic esophagus. Primary peristalsis is triggered in the pharyngeal phase of swallowing and goes from the UES to the LES in one contraction. It is associated with cessation of breathing during swallowing (Jadcherla, 2016). Secondary peristalsis is triggered by esophageal provocation and is independent of swallowing sequences. The waves occur starting at the mid-esophagus and extend to the stomach. These events participate in propulsion of a bolus during swallowing and also during gastroesophageal reflux. The ENS, which was once dismissed as a simple collection of relay ganglia, is now recognized as a complex, integrative brain in its own right that is capable of controlling the GI function (e.g., Altaf & Sood, 2008; Kumral & Zfass, 2018; Lake & Heuckeroth, 2013). Its complexities are beyond the scope of this chapter. An esophageal phase promptly follows each separate pharyngeal swallow when there is a definite time delay between swallows. As long as the bolus remains in the striated segment, inhibition of the esophageal phase occurs. When the bolus is in the smooth muscle segment, delay in esophageal transit of the initial bolus will occur. An inactive, distended esophagus and continuous LES relaxation may result from rapid sequence swallowing seen during feeding and increase the risk of gastroesophageal reflux (GER). Some infants may have esophageal propulsion after four or more pharyngeal swallows. The esophageal peristalsis may be delayed until the end of an active burst of sucking. Swallow-induced peristalsis normally propagates at about 2 to 4 cm/s and traverses the entire body of the esophagus in 6 to 10 s in children (Arvedson & Lefton-Greif, 1998; Dodds, Hogan, Reid, & Stewart, 1973). Solids have been shown to increase the probability that a primary peristaltic wave

38  Pediatric Swallowing and Feeding: Assessment and Management

will progress through the entire esophagus (Miller, 1982). LES function is dependent on bolus size in adults with an increased opening diameter and prolongation of the interval of sphincter relaxation seen with larger bolus volumes (Kahrilas, Dodds, Dent, Logemann, & Shaker, 1988). Transient LES relaxations (TLESRs) are brief periods of relaxation that are unrelated to swallowing or esophageal peristalsis. These transient pressure drops have been attributed to relaxation of the smooth muscle of the LES, although direct measurements are difficult (Altaf & Sood, 2008). LES pressure is decreased by various pharmacologic and hormonal influences. Anticholinergics, theophylline, caffeine, nicotine, alcohol, dopaminergics, epinephrine, and prostaglandins lower LES pressure. GI hormones that lower LES pressure include glucagon, secretin, cholecystokinin, progesterone, and estrogen (Boeck, Buckley, & Schiff, 1997). Mechanisms involved in normal acid clearance include salivation, swallowing, and peristalsis. All may be significantly impaired in patients with swallowing disorders. The sequence of events for acid clearance is disrupted by drooling, decreased numbers of swallows, and abnormal peristalsis, all seen frequently in children with oral sensorimotor dysfunction. Delay in acid clearance sets the stage for a vicious cycle of reflux esophagitis. Normal function of the GI tract is necessary for “normal” feeding in infants and children. Esophageal motility and esophageal and gastric competence are necessary for a healthy upper digestive tract. Swallowing and feeding problems are caused by and contribute to the development of GI disease in children. (See Chapter 5.) Less obvious may be the role that proper intestinal absorption and lower GI tract motility play in the development of dysphagia. For

example, the cycle of dysphagia can result in decreased fluid intake. Reduced fluid intake leads to underhydration or dehydration. The chronically low fluid intake, when combined with relative immobility often seen in children with neurologic impairment, can lead to chronic constipation, resulting in significant irritability during or after feedings and in early satiety. Prevention of excessive gastric contents from returning to the esophagus and continuing upward beyond the esophagus, into the pharynx, larynx, nose, and oral cavity, is extremely important for the prevention and maintenance of normal swallowing in many infants and children. The physiology of sphincters, mucosal protection, and the role of swallowing in prevention of regurgitation of gastric contents are described briefly.

Lower Esophageal Sphincter (LES) The lower esophageal (or gastroesophageal) sphincter (LES) at the distal end of the esophagus normally prevents free reflux of gastric contents into the esophagus. A definite, anatomically defined sphincter, such as that which exists at the pylorus, has not yet been identified. However, a zone of increased intraluminal pressure in the most distal 1 to 3 cm of esophagus does exist. During swallowing, a momentary relaxation of the LES allows swallowed food to enter the stomach. The LES muscle is an extension of the esophageal circular muscle of the body of the esophagus. Although anatomically indistinguishable, the area of the LES muscle differs from the circular muscle of the body of the esophagus in that the LES demonstrates a greater responsiveness to cholinergic stimulation and more impressive length–tension characteristics. Pressure generated by the LES is important in maintaining sphinc-

2. Anatomy, Embryology, Physiology, and Normal Development   39

ter competence. Several ligaments connect the LES to the diaphragm and may aid in maintaining sphincter function. The closed lumen of the distal esophagus is collapsed into an H-shape and is surrounded by a collection of loose areolar tissue, providing many of the attributes of a choke valve. The angled entrance of the esophagus into the stomach aids LES competence. This angle produces function similar to that of a flap valve. Intraluminal gastric pressure, aided by the presence of gastric contents, may also apply pressure on the esophageal lumen and aid in sphincter competence. The normal location of the LES is partially in the abdomen. The pressure differential between the abdominal esophagus (high pressure) and thoracic esophagus (low pressure) helps to prevent the reflux of gastric contents into the esophagus. The stomach has a positive resting pressure of 6 to 10 mm Hg, and the thoracic esophagus has a resting pressure of −6 to +10 mm Hg. A pressure barrier of approximately 15 to 60 mm Hg must be generated to overcome the LES and for stomach contents to reach the esophagus. The important effects of abdominal pressure on the LES are illustrated by the existence of a hiatal hernia, which is a rare occurrence in infants. A laparoscopic approach to repair is feasible, even for neonates (Petrosyan et al., 2018). A hiatal hernia exists when the abdominal esophagus and part of the stomach rise up through the diaphragm into the chest cavity. The LES is then surrounded by negative intrathoracic pressure. The intra-abdominal esophageal pressure differential is gone, and the LES is surrounded by a negative (instead of positive) pressure. Free reflux of gastric contents into the esophagus occurs because of absence of this pressure differential (Heine & Mittal, 1991; Sondheimer, 1988). Several anatomic and physiologic mechanisms interact to contribute to the preven-

tion of reflux into the esophagus—sphincter pressure, the mucosal choke mechanism, a flap valve, intra-abdominal position, and the anchoring by phrenoesophageal ligaments, especially by the right crus of the diaphragm. The relative importance of each of these mechanisms is not clear at this time. However, it is believed that GERD/EERD is prevented by several mechanisms relative to the esophagus. At birth, the greater pressure in the esophagus is the principal mechanism of preventing reflux of stomach contents (Boix-Ochoa & Canals, 1976). In the first few weeks after a term birth, the LES at the gastroesophageal junction matures rapidly and contributes to the prevention of reflux. Esophageal bolus transport is recognized as an equally important component of infant oral feeding skills (Lau, 2016). Thereafter, the pattern of esophageal swallow peristalsis is essentially the same in infants, children, and adults.

Airway and Gastrointestinal Physiology Airway Physiology Proper oxygenation is essential for life and necessary for safe oral feeding. Coordination and regulation of breathing and eating matures during the first several weeks after birth. During nutritive sucking in the first week of life, normal preterm and full-term infants often experience decreases in minute ventilation, respiratory rate, and tidal volume (Durand et al., 1981; Guilleminault & Coons, 1984; Mathew, Clark, Pronske, Luna-Solazano, & Peterson, 1985; Miller & DiFiore, 1995; Shivpuri, Martin, Carlo, & Fanaroff, 1983; Wilson, Thach, Brouillette, & Abu, 1981). Shortly after birth, these physiologic aberrations disappear except

40  Pediatric Swallowing and Feeding: Assessment and Management

in children with neurologic compromise (Rosen, Glaze, & Frost, 1984). Normally throughout oral feeds, infants produce from one to three sucks before they initiate a pharyngeal swallow. A short breath hold may precede such a run. Although fullterm infants tolerate breath cessation reasonably well, preterm infants may not and therefore experience hypoxia more readily, especially if they have underlying lung disease such as BPD (Garg, Kurzner, Bautista, & Keens, 1988). Preterm infants may initiate a swallow during the period of breathing cessation and inhalation that increases the risk of oxygen desaturation and laryngeal penetration/aspiration (Amaizu, Shulman, Schanler, & Lau, 2008; Fucile, McFarland, Gisel, & Lau, 2012). Term infants typically swallow at respiratory phases that minimize risks of aspiration during respiratory pauses or when inspiratory airflow is minimized (e.g., during exhalation or at end of inspiration or exhalation) (Lau, 2016; Nishino, 2013). As the infant matures, suck and swallow occur in a 1:1 ratio, and the infant takes a breath after a burst of suck and swallow sequences (e.g., 10 to 30 sucks and swallows, then a breath). Mathew et al. (1985) found decreased minute ventilation secondary to a slower respiratory rate in 19 healthy term infants during continuous nutritive sucking. The mechanism of the decreased respiratory rate was thought to be from the inhibitory effects of liquid in the pharynx. Minute ventilation was found to decrease during continuous sucking, with return to baseline during rest (Shivpuri et al., 1983). Infant maturation leads to a reduction in the degree of hypoventilation. A normal pharyngeal swallow requires complete bolus transport through the pharynx and UES. This action must occur while the body ensures protection of the airway from aspiration of the swallowed material.

Posterior transport through the pharynx is achieved via coordinated posterior tongue propulsion, tongue base retraction, effective pharyngeal constriction, and UES opening by inhibition of tonic contraction (Cook et al., 1989; Dodds, 1989; Loughlin & LeftonGreif, 1994; Shapiro & Kelly, 1994). Safe transport through the upper esophagus is achieved through precise coordination between bolus transport and anterior superior elevation and closure of the laryngeal complex, which assist in airway protection (Derkay & Schechter, 1998; Loughlin & Lefton-Greif, 1994; Martin, Logemann, Shaker, & Dodds, 1994; Rogers, Arvedson, Msall, & Demerath, 1993; Shaker et al., 1990). During swallowing, normal persons occasionally show transient barium spillover into the laryngeal vestibule above the level of the true vocal folds. Aspiration does not occur when complete vocal fold closure is maintained throughout the swallow. That said, competent glottic closure does not mean that aspiration will not occur with the resumption of glottic opening for breathing. In the young infant, the airway may be compromised by neck flexion, intrinsic hypotonia of pharyngeal muscles, posterior displacement of the mandible, and hyoid bone compression. Airway patency is critical to the infant and is helped by appropriate midline neutral positioning and muscle tone. Elevation of the entire larynx occurs by shortening of the thyrohyoid and suprahyoid muscles. The arytenoids come together by contraction of the thyroarytenoids. The epiglottis closes off the vestibule by a vertical-to-horizontal movement achieved primarily by thyrohyoid shortening. These multiple levels of sphincteric action are capable of closing off the trachea completely from the pharynx and may prevent food or liquid from penetrating into the trachea during swallowing. As the bolus moves

2. Anatomy, Embryology, Physiology, and Normal Development   41

through the pharynx, it usually divides so that approximately half moves through the pyriform sinus at each side of the pharynx (see Figure 2–3). These two portions of the bolus rejoin just above the level of the opening into the esophagus. In some instances, a greater portion of the bolus is seen moving through one side of the pharynx and is not considered abnormal. The cricopharyngeus is closed during quiet respiration. During swallowing the UES opens as anterior–superior motion of the larynx occurs with contraction of the genioglossus and other muscles of the larynx (Derkay & Schechter, 1998; Shapiro & Kelly, 1994). The resting tonic contraction of the cricopharyngeus is initially inhibited by the swallowing center through CN X parasympathetic fibers (Derkay & Schechter; Doty, 1968). The closed UES assures that no air enters into the esophagus during inspiration. At the initiation of a pharyngeal swallow, inhibition of tonic contraction of the cricopharyngeus muscle allows a bolus of food or liquid to pass from the pharynx into the esophagus. The UES then closes immediately after the bolus passes through it. Elevated UES pressure at rest is necessary to protect the pharynx from reflux of esophageal or gastric contents. The innervation of the cricopharyngeus muscle is not well understood (Sasaki, 2000). Neural innervation occurs via recurrent laryngeal nerve and the superior laryngeal nerve (Prades et al., 2009). According to Schechter (1990), parasympathetic innervation enters the muscle via CN X, as the source of both contraction and relaxation. Schechter described relaxation beginning when the larynx moves anteriorly and superiorly by the genioglossus and suprahyoid muscles. The bolus is then carried into the esophagus by a series of contraction waves, a continuation of the pharyngeal stripping action.

Gastrointestinal (GI) Physiology The normal pattern of gastric motility and gastric emptying (GE) represents the end result of a variety of complex interactions. Stomach function is influenced by myenteric neural and hormonal factors. Food volume, physical state (solid or liquid), and specific food content all affect GE (Siegel & Lebenthal, 1981). For example, the stomach empties breast milk faster than formula milk (Cavell, 1979; Meyer, Foong, Thapar, Kritas, & Shah, 2015). Increased concentrations of carbohydrates and proteins slow GE. This effect appears to be mediated by osmoreceptors because GE is delayed when higher concentrations of glucose are present (Barker, Cochrans, Corbett, & Hunt, 1974; Cooke & Moulang, 1972). The ability of starches and most proteins to delay emptying as effectively as isocaloric solutions of glucose and amino acids implies that starches and proteins are broken down into component glucose and amino acids before affecting GE. Selective perfusion of the jejunum and duodenum with hyperosmotic solutions has localized osmoreceptors to the duodenum, because perfusion of the duodenum slows GE while perfusion of the jejunum does not (Meeroff, Go, & Phillips, 1975). Body position affects the rate of GE and therefore the amount of gastric residue. Premature infants are found to have similar lower levels of gastric residue in the right lateral and prone positions and higher levels of gastric residue in left lateral and supine positions. Yayan and colleagues (2018) found the gastric emptying rate to be highest in the right lateral position at 30, 60, and 180 min and in the prone position at 120 min (Yayan, Kucukoglu, Dag, & Karsavuran Boyraz, 2018).

42  Pediatric Swallowing and Feeding: Assessment and Management

Gastric emptying is responsive to fats. Long-chain fatty acids have a greater retarding effect on emptying than do mediumchain fatty acids when equal molar concentrations are compared (Siegel, Krantz, & Lebenthal, 1985). The “gold standard” for measuring gastric emptying is technetium scintigraphy, which requires radiation exposure. Development of the C-acetate breath test (C-ABT) standardized in healthy children for GE of liquids (Hauser et al., 2016a) and the C-octanoic acid breath test (C-OBT) for GE of solids (Hauser et al., 2016b). These techniques are determined to be reliable and well accepted by parents and children. The mechanisms by which small bowel receptors control emptying is not established. Both neural and hormonal mechanisms are possible. Experimental animal and human clinical studies have both indicated that when a small amount of acid is instilled in the distal esophagus, nearly all of the acid material is cleared following the initiation of a single swallow (Helm, Dodds, Pelc, Palmer, & Teeter, 1984). The low pH is not returned to normal until successive swallows occur, when saliva is delivered to the distal esophagus. Saliva clings to the esophageal mucosa and has an important role in mucosal protection. Saliva diverted by oral suction can prevent return to baseline esophageal pH. Awake adults with GERD/EERD have the same salivary volume and buffering capacity as those without reflux. During sleep, however, the mean resting salivary flow is very low in those who have GERD/EERD. Decreased swallowing frequency during sleep may also be responsible for prolongation of acid clearance time. Patients with oral sensorimotor disorders may be particularly prone to the development of esophagitis by the mechanisms

explained previously. Excessive drooling limits the amount of saliva to the esophagus. Decreased rates and effectiveness of swallowing impair esophageal clearance frequency. All of these situations may interrupt normal acid clearance and predispose to GERD/EERD. See Chapter 5.

Neural Control of Swallowing Neural control of swallowing has been studied with electromyography, through lesion studies of CNS pathways and peripheral nerves, by removal of specific muscles, and by electrical stimulation (Miller, 1986). The neural control of swallowing involves four major components (Dodds, 1989; Dodds, Stewart, & Logemann, 1990): n afferent sensory fibers contained in

cranial nerves,

n cerebral, midbrain, and cerebellar fibers

that synapse with the brain-stem swallowing centers, n the paired swallowing centers in the brain stem, and n efferent motor fibers contained in cranial nerves (Figure 2–11).

Swallowing can be evoked by many different central pathways, even after removal of the entire cortical and subcortical regions above the brain stem. This indicates that the cerebral cortex is not essential to the pharyngeal and esophageal phases (Miller, 1972), although the cerebral cortex appears to facilitate the oral phase and the initiation of the pharyngeal phase. Nonetheless, limited information is available regarding the cortical control of both swallowing and respiration (Martin & Sessle, 1993).

2. Anatomy, Embryology, Physiology, and Normal Development   43

Supranuclear Descending Pathways Cortical and Subcortical

Primary Afferents Cranial Nerves V, VII, IX, X

Fasciculus Solitarius Medulla Nucleus Tractus Solitarius and Ventral Medial Reticular Formation “Central Pattern Generator”

Primary Efferents Cranial Nerves V, VII, IX, X, XII

Motor Nuclei Cranial Nerves V, VII, IX, X, XII

Pons and Medulla

Figure 2–11. Major peripheral and central nervous system pathways for deglutition. Significant afferents that include cranial nerves and subcortical pathways send input through fasciculus solitarius to the nucleus tractus solitarius (NTS) and the ventral medial reticular formation (VMRF) (central pattern generator). Efferent nerves synapse with motor nuclei primarily of cranial nerves V, VII, IX, X, and XII.

Central Nervous System The relevance of the cerebral cortex to motor control may relate to dependence on the cortical region for the learning of motor responses. Bilateral movements of the face and tongue and repetitive jaw movements have been observed by stimulation of the prefrontal cortex with microelectrodes (Kubota, 1976). Stimulation with larger electrodes and more current over the same regions evokes swallowing (Miller & Bowman, 1977; Sumi, 1970). Although extensive research has been carried out over many years with important findings, the underlying neural mechanisms for both normal and disordered swallowing remain vague (Humbert & German, 2013).

These researchers suggest that principles of motor learning based on limb movements be used as a model system to provide a basis for deeper understanding of control of oropharyngeal function. Sensory input is stressed as necessary for accurate motor control. Sensory information is processed during planning, executing, and evaluating an action. Concepts of sensory feedback and predictions prior to confirmation seem especially significant for oropharyngeal swallowing (Humbert & German, 2013). These principles are applicable across the age span. However, the process of obtaining evidence in infants seems even more complicated. Thus, researchers and clinicians are always encouraged to consider the interrelationships of sensory and motor

44  Pediatric Swallowing and Feeding: Assessment and Management

learning. The term sensorimotor is useful in a generic sense. In neonates, consideration must be given to CNS, ENS, as well as neuromuscular effects on maturational delays, maldevelopment, maladaptation, and malfunction involving multiple systems (Jadcherla, 2016). Sensory (afferent) cranial nerve input to the brain-stem swallowing centers is provided mainly by the glossopharyngeal (CN IX) and vagus (CN X) nerves, with some contribution of the maxillary branch of the trigeminal (CN V2) and facial (CN VII— chorda tympani) nerves (Table 2–3). Stimuli that induce swallowing vary from one region to another. Taste stimulation alone is a weak stimulus for swallowing (Dodds, 1989), although the degree of sweetness of the fluid appears to be one type of sensory input for infants (Burke, 1977). Light touch is the most effective stimulus at the faucial pillars, heavy touch in the posterior pharynx, and water at the posterior larynx (Shinghai & Shimada, 1976; Storey, 1968). The faucial pillars, pharynx, and posterior larynx provide sensory stimuli needed to elicit a swallow (Miller, 1986; Steele & Miller, 2010). Peripheral nerve stimulation to the posterior tongue and the oropharyngeal region innervated by the pharyngeal branches of the glossopharyngeal nerve

(CN IX) or by two branches of the vagus nerve (CN X—superior laryngeal nerve and the recurrent laryngeal nerve) evokes swallowing. Sensory fibers of these two cranial nerves proceed centrally and synapse within the nucleus tractus solitarius (NTS). Microelectrode recordings indicate that stimulation of the sensory fibers evokes potentials within the NTS and in an adjacent region, the ventral medial reticular formation (VMRF) around the nucleus ambiguus, which is a vagal motor nucleus (Car & Roman, 1970; Jean, 1972; Miller, 1972, 1982). A small lesion within the dorsomedial region of the NTS prevents the sequence of esophageal contractions (Jean, 1972), and led Miller (1986) to suggest that the core central pathway, which controls the peristaltic activity of the esophagus, partially resides near or in the NTS. The brain stem contains the interneurons essential to the swallowing response. Each side of the brain stem has its own central pattern generator, which is a complete neural circuit capable of generating the pattern without peripheral feedback. Miller (1982) described two animal studies (Roman, 1966; Roman & Tieffenbach, 1972) establishing that once deglutition is elicited by stimulation of an afferent pathway, the motor sequence of peristalsis will proceed

Table 2–3.  Sensory (Afferent) Cranial Nerve Input for Swallowing Cranial Nerve

Function

Trigeminal (V2)

General sensation, anterior two-thirds of tongue, soft palate, nasopharynx, mouth

Facial (VII) (chorda tympani)

Taste, anterior two-thirds of tongue, touch sensation to lips

Glossopharyngeal (IX)

Taste and general sensation of posterior third tongue; sensation to tonsils, palate, soft palate

Vagus (X)–SLN

Pharynx, larynx, viscera, base of tongue

Note.  SLN = superior laryngeal nerve.

2. Anatomy, Embryology, Physiology, and Normal Development   45

in the pharynx and esophagus, even with esophageal transection or deviation of a bolus. In contrast, Miller suggested that peripheral feedback modifies the central pattern generator as noted by the decrease in the number of peristaltic waves by deviation of a bolus in the esophagus. These central pattern generators or swallowing centers (NTS, VMRF, and interneurons in the medulla) use many of the same cranial motor fibers and cervical muscles that are needed for coughing, gagging, and vomiting functions (McBride & Danner, 1987). These swallowing centers are not discrete focal areas but consist of ill-defined broad areas located lateral to the midline and ventral to the caudal portion of the fourth ventricle, incorporating the NTS and the VMRF. Sensory cranial nerve input to the swallowing centers provides taste and sensory information from the tongue and oral–pharyngeal mucosa, as well as proprioceptive information from the musculature involved. The swallowing centers also receive input from rostral brain-stem centers, cerebellum, basal ganglia, and higher cortical centers (McBride & Danner, 1987). Thus, bolus size, taste, temperature, location, and consistency have well-defined receptors and are sensed at many levels of the CNS. The sequential semiautomatic discharge of neurons to groups of muscles of the oropharyngeal, laryngeal, and esophageal regions is the most characteristic property of swallowing (Doty & Bosma, 1956). Motor neurons leave the swallow center to synapse in cranial nerve nuclei on the ipsilateral side. The lower motor neurons to the muscles for swallowing reside in cranial nerves V, VII, IX, X, and XII and the ansa cervicalis (C1–C3), which joins to run with the hypoglossal nerve (CN XII). The ansa cervicalis innervates some of the muscles in the neck responsible in part for laryngeal elevation.

The motor nerves and their respective muscle innervation are shown in Table 2–4. The swallowing centers ensure the accuracy of bilateral motor activity and proper sequencing of the muscles involved in swallowing. Prevention of competing muscle activities, for example, speech and respiration, allows completion of the complex motor act of deglutition without interruption (Kennedy & Kent, 1985). Two functionally distinct central pattern generators appear to be present for pharyngeal and esophageal swallowing function, with the relevant interneurons residing in different regions of the medulla. Stimulation of a peripheral nerve to evoke swallowing elicits activity in muscles ipsilateral to the input, except for the middle and inferior pharyngeal constrictor muscles, which are controlled by the contralateral brain stem (e.g., Aida et al., 2015). Animal studies have established that once swallowing is elicited by electrical stimulation of an afferent pathway or by volition, the motor sequence of peristalsis will proceed (Miller, 1982; Miller, Bieger, & Conklin, 1997). The fact that peristalsis occurs without peripheral feedback from an accompanying bolus indicates that the mammalian neural control of peristalsis is governed by a central pattern generator. Protection of the laryngeal opening from aspiration appears to be carried out more effectively with stimulation of those receptive fields innervated by the superior laryngeal nerve (SLN of CN X). The role of peripheral feedback is not clearly understood. Some authors suggest that there may be both facilitative and inhibitory inputs (Miller & Sherrington, 1916; Sumi, 1970). Miller (1982) suggested that peripheral feedback modifies the dominant central control of swallowing. Repetition rate of swallowing is modified by both the type of bolus and the presence of material within the pharynx, larynx,

46  Pediatric Swallowing and Feeding: Assessment and Management

Table 2–4. Anatomic Location and Motor (Efferent) Controls for Normal Swallow Anatomic Location

Innervation

Oral cavity Muscles of mastication

Trigeminal(V3) mandibular branch

Lip sphincter and face muscles

Facial (VII)

Tongue-intrinsic muscles

Hyoglossal (XII)

Extrinsic muscles

Ansa cervicalis (C1-C2)

Palatoglossus

Vagus (X)

Pharynx Stylopharyngeus

Glossopharyngeal (IX)

Palate, pharynx, and larynx

Vagus (X)

Tensor veli palatini

Trigeminal (V3)

Hyoid and laryngeal movement

X, IX, V3, VII, C1-C2

Esophagus

or esophagus. The intensity and duration of individual muscle activity in pharyngeal and esophageal sequences vary with the consistency of a bolus and ease of passage through the tract. The genioglossus and the geniohyoid muscles demonstrate a longer duration of discharge with a more dense consistency bolus (Hrychshyn & Basmajian, 1972). Topical anesthesia to the mucosal regions of soft palate, faucial pillars, tonsils, base of the tongue, and the pharynx causes an increase in the time required to evoke repeated swallows (Mansson & Sandberg, 1975). Electromyographic (EMG) studies have shown that esophageal muscle activity is of longer duration and higher amplitude with a bolus of water compared with a bolus of saliva (Miller, 1986). As the bolus proceeds through the esophagus, continuous sensory feedback occurs. Thus, primary and secondary peristalsis can be modulated as swallowing occurs. Furthermore, bolus movement

Vagus (X)

is affected by intrathoracic pressure associated with changes in respiration. Specifically, inspiration enhances movement and the positive pressure associated with expiration slows movement (Schechter, 1990). Swallowing may depend on a central patterned program (central pattern generator) that is modulated or reinforced by feedback from sensory input, but it is not dependent on this sensory input. Sensory feedback modification of oral and pharyngeal swallowing processes may occur as a preprogrammed modification governed by proprioreceptors in the tongue that sense the bolus size before initiation of a swallow. It is also possible that sensory feedback modification might occur online during the swallowing sequence. The neural control mechanism for esophageal peristalsis in smooth muscle differs significantly from that for esophageal striated muscle. It is generally agreed that

2. Anatomy, Embryology, Physiology, and Normal Development   47

peristalsis in esophageal striated muscle is determined by a descending sequence of efferent neural discharges, generated by the central swallow program (Diamant & El-Sharkawy, 1977). Esophageal smooth muscle appears to be innervated by at least two types of nerves (Dodds, Dent, Hogan, & Arndorfer, 1981), although the precise control mechanisms are controversial. It is not clear whether a neural control mechanism of esophageal peristalsis occurs as an “on” response elicited by cholinergic nerves, or an “off ” response mediated by nonadrenergic, noncholinergic nerves (Dodds, 1989). Nerve fibers that innervate esophageal smooth muscle originate in the dorsal motor nucleus rather than in the nucleus ambiguus and synapse in the esophageal intramural neural plexus, known as Auerbach’s plexus (Ingelfinger, 1958). General agreement exists that peristalsis in the esophagus, as well as in the pharynx, occurs as a rapid wave of relaxation followed by a slower wave contraction. The rapidly descending wave of inhibition relaxes the pharynx, UES, esophageal body, and LES in a sequence to allow the structures to accommodate an oncoming bolus advanced by the peristaltic contraction wave. The extrinsic component of the ENS consists of both parasympathetic and sympathetic divisions. This component is capable of modulating motility as well as other functions in the GI tract that are beyond the scope of this chapter (Altaf & Sood, 2008). Gravity assists peristalsis in persons who are in an upright position.

Taste and Smell Clinical concerns related to feeding problems in infants and young children usually revolve around the motor mechanisms and failure to handle changes in physical char-

acteristics of food, but the sense of taste and smell also have important roles in feeding. The addition of sucrose to fluid (water or formula) has been found to aid in eliciting suck-and-swallow patterns in infants (Weiffenbach & Thach, 1973) and to increase intake over a period of several weeks (Desor, Maller, & Turner, 1973; Foman, Ziegler, Nelson, & Edwards, 1983). Newborns are generally responsive to breast odors (Winberg & Porter, 1998) possibly facilitated by the high norepinephrine release and arousal of the locus coeruleus at birth. Two-day-old infants recognize their mother by the mother’s axillary odor, likely from influence of skin-to-skin contact (Marin, Rapisardi, & Tani, 2015). Food flavor preferences are shown to relate to sensitive periods during which infants seem most likely to form flavor preferences and aversions that may provide the foundation for lifelong food habits (Beauchamp & Mennella, 1998). Mennella and colleagues (2004) reported that variation in formula flavor affected acceptance by young infants. A hydrolysate formula is tolerated on first exposure to infants when introduced less than 4 months of age (e.g., Mennella & Beauchamp, 1996, 1998). Older infants strongly reject those formulas. These researchers suggest that there is a profound change at about 4 months of age in perception of those formulas and that early experience modifies later acceptance. Breastfeeding offers an advantage in initial acceptance of a food if the mothers eat the food regularly (Forestell & Mennella, 2007). Infant facial expression, although not a true objective measure, is a response that indicates food acceptance (Forestell & Mennella, 2017) and can be modified with changes in experiences over time. According to Forestell and Mennella (2017), infants who are breastfed by mothers eating varied

48  Pediatric Swallowing and Feeding: Assessment and Management

flavors, especially vegetables, tend to accept those foods more readily when they are ready for transition feeding. The increasing variety in taste and smell of foods offered to infants may be one of the prime factors in the success of transitional feeding (Bosma, 1986). The interactions of chemosensory cues and physical characteristics of food continue to be studied. This is an area of research that may aid in increased effectiveness of intervention with some types of feeding disorders.

Reflexes Related to Swallowing A number of reflexes relate to swallowing. Table 2–5 describes these reflexes in term infants, their stimuli, the cranial nerves involved, and the age of disappearance. Some of these reflexes are more directly related to the act of swallowing than others. They include the gag reflex, phasic bite reflex, transverse tongue response, tongue protrusion, and rooting response. The gag reflex consists of tongue protrusion, head and jaw protrusion, and pharyngeal contractions. A gag reflex is evident

by 26 to 27 weeks’ gestation and is usually strong in full-term infants. A hyperactive gag may be noted in some children with neurologic impairment and often obviously a sensory response. Some children gag at the sight or smell of food and others when food is in the oral cavity prior to posterior propulsion of a bolus. In some children, a gag may be difficult to elicit when profound motor dysfunction exists (Love & Webb, 1992). With ataxia, the gag may be hypoactive. The absence of a gag reflex has no relationship in and of itself to swallowing. Children may have safe swallowing, but no gag reflex. The gag reflex may diminish somewhat at about 6 months of age, which is usually marked by the onset of chewing and swallowing of solids. Phasic bite and tongue reflexes are present by 28 weeks’ gestation. The phasic bite reflex is the rhythmic closing and opening of the jaws in response to stimulation of the gums. Tongue protrusion is noted in a full-term infant in response to touching the anterior tongue. This tongue protrusion begins to diminish by 4 to 6 months of age, permitting introduction of solids and a spoon. The transverse tongue response is

Table 2–5. Infant Oral Reflexes Present at Term and Age They Disappear in Typical Infants Reflexes Present at Birth

Stimulus

Response

Cranial Nerve

Age Reflexes Disappear

Rooting

Touch to cheek or corner of the mouth

Turns head toward touch

V, VII, XI, XII

3–6 months

Tongue protrusion

Touch to tongue or lips

Tongue protrudes

XII

4–6 months

Tongue transverse

Touch to tongue

Lateral tongue motion

XII

6–9 months

Phasic bite

Pressure on gums

Rhythmic closing

V

9–12 months

Gag

Touch posterior tongue or pharynx

Contraction of palate and pharynx

IX, X

Persists

2. Anatomy, Embryology, Physiology, and Normal Development   49

movement of the tongue toward the side of stimulation when the lateral surface of the tongue has been touched. The rooting response, observed as the head turns toward the side of stimulation of the cheeks or the corner of the mouth, is noted by 32 weeks’ gestation. It strengthens gradually until term, when it becomes more difficult to prevent an alert, hungry infant from turning. Higher cortical pathways cause inhibition by 3 to 6 months of age, when the rooting reflex disappears. In addition, several reflexes are initiated in the fetus and newborn infant when hypochloremic or strongly acidic solutions (gastroesophageal reflux and particularly laryngopharyngeal reflux that occurs multiple times a day in all infants) contact the epithelium surrounding the entrance to the laryngeal airway (Praud, 2010; Thach, 2001). These reflexes are known as the laryngeal chemoreflex (LCR) and include startle, rapid swallowing, apnea, laryngeal constriction, hypertension, and bradycardia. Praud (2010) stated that the role of these upper airway reflexes is still debated with uncertainties persisting regarding treatment and prevention of potentially dramatic consequences.

Development of Feeding Skills Suckling and Sucking Underlying factors that are important to facilitate oral feeding of preterm and term infants at breast and with bottle/nipple include, but are not limited to, global neurologic, airway, and gastrointestinal systems (see other chapters for detailed information about these topics). Suckling and sucking are considered to be flexor skills.

Physiologic flexion (a characteristic of fullterm infants) is observed when the limbs are flexed, whether the infant is in prone or supine position. Some researchers differentiate suckling and sucking, while others use the term sucking for all. Thus, no prescriptive guidance can be given for use of terms, although differences that have been described will be shared. Readers have to make their own decisions until evidence-based reports support a rationale for terminology During the 1st month after term birth, infants maintain much of the physiologic flexion as a result of the crowded space in utero during the final weeks before birth. This overall body flexion contributes to successful oral feeding by allowing for attainment of appropriate positioning relatively easily. Two distinct patterns of the suck occur in infant development, suckling and sucking (Table 2–6 and see Figure 2–8). Suckling, the first pattern to develop, is acquired gradually in the second and third trimesters and involves definite backward and forward movements of the tongue (Bosma, 1986; Morris & Klein, 1987). Liquid is drawn into the mouth through a rhythmic licking (or stripping) type action of the tongue, combined with pronounced opening and closing of the jaw. Lips may be loosely approximated and flared around a nipple. The tongue moves forward for half the suckle pattern, but the backward motion is more pronounced. Tongue protrusion does not extend beyond the border of the lips. In contrast, sucking is the second pattern that develops at about 6 months. The body of the tongue raises and lowers with strong activity of its intrinsic muscles while the jaw makes a smaller vertical excursion. Firmer approximation of the lips that must be flared for efficient nipple-feeding along with the pattern of tongue motion allows for a negative pressure to build up in the

50  Pediatric Swallowing and Feeding: Assessment and Management

Table 2–6.  Suckling and Sucking Comparisons Characteristic

Suckling

Sucking

Tongue configuration

Flat, thin, cupped, or bowl shaped

Flat, thin, slightly cupped, or bowl shaped

Movement direction

In–out movement horizontal

Up–down movement vertical

Range of movement

Extension or protrusion no further out than middle of lip.

From mandible to the anterior hard palate

Lip approximation

Loose

Firm

Expected ages/times

Normal in early infancy

Normal later infancy, childhood, and adult

mouth. This combination of movements works to get liquid and soft food into the mouth. Strength of lip closure is a major factor in the shift of tongue patterns from primarily an in–out to primarily an up–down direction. The tongue has more room for movement because of the downward and forward growth of the oral cavity. The action is sometimes referred to as “pump sucking” because it resembles the action of a pump handle (Morris & Klein, 1987). Similarities and differences noted between suckle and suck patterns include the following: n Both patterns reveal a raising and

lowering of the jaw and tongue together to create the pressure required to express the liquid into the mouth. n Sides of the tongue move upward to form a central groove that helps in formation of the liquid bolus and to move the bolus posteriorly over the tongue. n The differences between suckling and sucking are noted primarily in the direction of tongue movement and in the degree of valving or closure of the lips (Morris & Klein, 1987).

n The developmental sequence from

suckling to sucking is a step in preparation for oral manipulation of thick liquids and advancement to spoonfeeding of soft food.

The term sucking tends to be the generic term and will be used to refer to the organized intake of a liquid or soft solid as described in previous paragraphs. Suckle will be used when emphasis is placed on a specific developmental sequence of mouth movements. Otherwise suck or sucking will be used to describe typical infants younger than 6 months of age and children with developmental skill levels at those estimated ranges in whom a mixture of suckle and suck may be seen. Patterns of sleeping and waking usually determine the time intervals between feedings during the first months of life. The process of feeding at fairly regular intervals is a major factor in establishing and maintaining quiet arousal episodes or homeostasis. Arousal helps prepare the infant for feeding. Initially, arousal is noted when gross motions of head, face, trunk, and extremities occur. Respiratory irregularities and an increased respiratory rate are also noted.

2. Anatomy, Embryology, Physiology, and Normal Development   51

Incidental phonation is common before crying. Crying may then become prominent when there are delays in initiation of the feeding process.

Nipple-Feeding: Breast and Bottle Breastfeeding The normal suck–swallow sequence during breastfeeding is similar to, but not the same as other nipple-feeding options (McBride & Danner, 1987; Sakalidis & Geddes, 2016). Detailed guidance to facilitate breastfeeding is beyond the scope of this chapter; however, multiple resources are available for parents and medical professionals (e.g., Casey, Fucile, & Dow, 2018). A brief discussion to emphasize some basic factors follows. Primary signs for a mother to make sure her infant is well latched include the following (Martin & Zaichkin, 2016): n a wide-open mouth with lips spread

(flared) around the breast,

n the infant’s mouth covering the entire

nipple and some of the areola, n a firm tug on the breast with every suck by the infant, n the infant suckles for more than three to four sucks in a row, and n the infant maintains latch to the nipple during pauses between bursts of sucks. The tip of the tongue stays behind the lower lip and over the lower gum, while the rest of the tongue cups around the areola of the breast. The mandible moves the tongue up, allowing the breast areola to be compressed against the infant’s alveolar ridge. Milk is then expressed into the oral cavity from the lactiferous ducts. While the

anterior portion of the tongue is raised, the posterior tongue is depressed and retracted. This forms a groove that channels the milk to the posterior oral cavity where receptors are stimulated to initiate a voluntary swallow. As the posterior tongue is depressed, the buccal mucosa, supported by the buccinator muscles and fat pads, moves inward slightly and then outward while the mandible and tongue are elevated during compression. This movement of the buccal mucosa allows for the maintenance of tongue approximation to the cheeks keeping milk within the tongue’s groove (Smith, Erenberg, Nowak, & Franken, 1985). The jaw is then lowered, allowing the lactiferous ducts to refill, and the sequence is repeated. A rhythm is created by this sequence of vertical jaw movement and posterior tongue depression and elevation. The suck–swallow sequence is repeated approximately once per second as long as milk is present and the infant is hungry. The infant may interrupt feeding for rest periods of various lengths. Feeders should not interrupt a feeding as long as an infant is coordinating sucking, swallowing, and breathing sequencing (see Chapter 9 for management guidance). Observe the infant for cues for interruptions that may be part of the total sequence (e.g., a few seconds after every 8 to 12 suck–swallow sequences) or at less predictable intervals. Although the vertical jaw movement is a normal part of the total sequence, excessive jaw excursion may interfere with effective sucking. Some infants use more of a biting action that is painful for mothers and results in inadequate intake. Most infants show a gradual decrease in consistency of the rhythmic pattern of sucking and swallowing with reduction in force of the suck as the feeding progresses. The duration of a breastfeeding session can

52  Pediatric Swallowing and Feeding: Assessment and Management

vary. After emptying each breast, infants may continue to suck for pleasure.

Bottle-Feeding In contrast, bottle-feeding infants can be observed more directly regarding the volume consumed in a given time period. Bubbles can be seen with every suck and swallow in some “standard” bottles, but not in some specialized bottles that have venting systems. Although each year brings new bottles and nipples, there is no perfect system. Individual differences are wide ranging.

Post-Feeding A variety of behaviors may be noted in the time immediately after feeding. Some infants continue to hold the nipple in the mouth and move it around with the tongue, but without real sucking movements. Others actively resist attempts to remove the nipple by clamping the jaws together or other types of struggle behavior. Newborn infants tend to go to sleep directly after feeding. Some infants give attention to the environment, making this period an appropriate time for communication. Vocalizations can be imitated by the feeder, who can also use this time for talking or singing to the infant in a gentle voice, with the infant held in a comfortable position allowing for eye contact and touch in ways that yield pleasurable interactions. These interactions are an integral part of early communication development, which is an ongoing process beginning in utero.

Transition Feeding In typical infants, the transitional feeding period usually begins at 4 to 6 months of age. The readiness for varied textures after

several months of suckle feeding is primarily related to changes in the CNS, along with some anatomic changes. Growth in the upper aerodigestive tract occurs, but with relatively minimal change in proportion or form. There is an increase in intraoral space as the mandible grows downward and forward. The oral cavity also elongates in the vertical dimension. The hyoid bone and larynx shift downward resulting in alterations to coordinate breathing and swallowing. Breathing and swallowing truly become reciprocal activities. The sucking pads are gradually absorbed over the first few months of life. Eruption of teeth may be the most notable change in the peripheral anatomic structures. Mandibular teeth usually erupt before the maxillary teeth, and girls’ teeth usually erupt sooner than boys’ teeth (Moore, Persaud, & Torchia, 2015). Deciduous teeth erupt between 6 and 24 months after birth, with all 20 deciduous teeth usually present by the end of the 2nd year in most healthy children. Mandibular incisors usually erupt 6 to 8 months after birth, but the process may be as late as 12 to 13 months in some normal children. Molars erupt from 12 to 24 months and the canines from 16 to 20 months. The erupted teeth are probably more important as sensory receptors than for motor purposes, because biting and chewing during the transitional period can be accomplished effectively with no teeth on the “molar tables.” Biting and chewing at this developmental stage are usually described as “munching.” The sensory inputs of teeth may be significant in the development of CNS control of the feeding process (Bosma, 1986). The resorption of the sucking pads, eruption of molars, and enlargement of the oral cavity all contribute to an increase in the buccal space. As this buccal space increases, food is manipulated between

2. Anatomy, Embryology, Physiology, and Normal Development   53

the tongue and the buccal wall. The crushing and grinding of food is assisted by the molars (when present) or that portion of the gums. Lateral tongue movements are basic to manipulation of food in the oral cavity as food is moved from midline to the lateral buccal walls. It is common for infants to approach their first spoon experiences with suckling movements of the tongue. The anteroposterior tongue movements result in some food being pushed out of the mouth. At times, these movements appear similar to tongue thrusting. Gradually the lateral tongue action becomes more consistent with the rotary jaw action required for efficient oral phase functioning. The tongue continues to be a primary contributor to normal oral feeding. Bosma (1986) suggested that smooth food that is homogeneous or with fine granular bits is mashed by tongue gestures focused on the midline of the tongue. As infants mature they advance to semifirm food that requires the tongue to move food to the lateral buccal area, where it is mashed by vertical motions of the tongue and jaw. These manipulations appear to be a prelude to chewing via molars. The motions of chewing occur with or without erupted molars in young children. Initial chewing gestures are simple vertical mandibular movements. Development of rotary jaw motion, jaw motion speed, and management on consistency upgrades are protracted during the first 2 years of life in typical children (Wilson & Green, 2009). As children continue to develop, the vertical movements become associated with alternating lateral motions characteristic of mature mastication. Mastication coordination is not observed by 30 months (Wilson & Green, 2009). Mature chewing is seen between 3 and 6 years of age (Vitti & Basmajian, 1975). Although the precise developmental stages have not yet been well delineated, normal infants and

young children demonstrate increasing competence in the oral manipulation and swallowing of varied food textures as they get older. As the ability to manipulate varied food textures increases, parallel gains occur in speech development as well as in trunk, head, and neck stability (see the following text). As the brain develops throughout the first several months of life, sensory inputs pertinent to feeding extend into the midbrain, cerebellum, thalamus, and cerebral cortex. These developmental processes permit the older infant and young child to gain competence in the evaluation of the physical character of food and ability to manipulate and swallow it. Children who are in this transition stage of feeding may still have inconsistent suckle patterns, especially when they are sleepy, distressed, or ill.

Termination of Nipple-Feeding Many factors are considered when one thinks about ending breast- or bottle-feeding. These include age, culture, and a maternal desire to maintain the bonding established with breast- or bottle-feeding. By approximately 12 months of age, most children have several teeth and appropriate CNS timing and coordination capabilities to manage cup drinking. Prolonged nipple-feeding has been identified as a cause of dental caries, particularly when sweetened liquid is taken immediately before a sleeping period or intermittently during sleeping periods. It appears that prolonged bottle-feeding with sweetened formula and juice has a greater effect as a cause of dental caries compared with breastfeeding (Kotlow, 1977). Breastfeeding infants also can get dental caries. Prolonged use of bottles, pacifiers, and “sippy-cups” has been associated with an increased incidence of otitis media (Niemela, Pihakari, Pokka, Uhari, & Uhari, 2000).

54  Pediatric Swallowing and Feeding: Assessment and Management

Normal/Typical Development of Swallowing and Feeding The evolution of feeding experiences is just one aspect of a more generalized development of the growing child. Oral sensorimotor skills improve within general neurodevelopment, acquisition of muscle control (posture and tone), and psycho­social development (e.g., Törölä et al., 2012). Cultural and social factors within a family also influence the feeding patterns. Culturally appropriate techniques are important for monitoring psychosocial development (Lansdown et al., 1996), as well as expected feeding milestones. Feeding is a complex developmental process in which the infant or child and caregivers all play active roles. The role of overall development, including posture and muscle tone and psycho­social development, is described in the next section. The milestones described reflect general concepts and should be considered within the specific cultural context of the family. Clinicians must make decisions with parents that incorporate family goals within their respective cultures.

Normal Development of Feeding Skills Acquisition of age-appropriate feeding skills is critical for the development of selfregulation in infants and young children. These early gains eventually lead to independent oral feeding. The development of socially acceptable feeding processes begins at birth and progresses throughout the first few years of childhood. Major strides in sensorimotor integration of swallowing and respiration, hand-eye coordination, normal posture and tone development, and appropriate psychosocial maturation are all acquired during the critical first 3 years of

life (e.g., Delaney & Arvedson, 2008). An appropriate nurturing environment is fundamental to the emergence of high-quality normal feeding and eating skills, to support physical development, to acquire cognitive and linguistic competence, and to secure strong emotional attachments with caregivers. These early skills lay the foundation for normal physical growth and emotional maturity extending through the adult years. Normal developmental, position and posture, and psychosocial milestones for selffeeding skills from birth to 36 months are shown in Tables 2–7 and 2–8.

Neonatal and Early Infancy Period (0 to 3 months) Infant feeding behavior begins with a hunger and satiety pattern interspersed with an irregular pattern of sleep and awake periods. During the first 2 to 3 months of life, a more regular pattern becomes established. The infant is taking first steps toward self-regulation. Coordination of breathing and eating takes time to regulate, although postswallow expiration is a robust feature of breathing– swallowing coordination from birth (Kelly, Huckabee, Jones, & Frampton, 2007). During the first week of life, normal preterm and full-term infants often experience decreases in minute ventilation, respiratory rate, tidal volume, and precise patterns of respiratoryswallow coupling change (Durand et al., 1981; Guilleminault & Coons, 1984; Kelly et al., 2007; Mathew et al., 1985; Shivpuri et al., 1983; Wilson et al., 1981). Shortly after birth, these physiologic alterations disappear, except in children who are neurologically compromised (Rosen et al., 1984). Between 6 and 12 months, further maturation of respiratory-swallow coupling occurs most likely due to neural and anatomical maturation (Kelly et al., 2007).

Table 2–7.  Development/Posture and Feeding/Oral Sensorimotor Milestones, Birth–36 Months Milestone Age/Stage

Development/Posture

Feeding/Oral Sensorimotor

0–1 month (Neonate)

Learning to control body against gravity

Suckle on nipple

Weight-bearing in prone (allows head, neck, and shoulders freedom of motion) Head moves side to side in supine position Head lag when pulled to sit

Nasal respirations Rooting reflex present During feeding, hands fisted/ flexed across chest Incomplete lip closure Unable to release nipple

Physiologic flexion Posture to maintain pharyngeal airway Strong grasp reflex 2 months (Infancy, 2–6 months)

Emergence of improving tone and symmetric purposeful movements Improving head control Exploring environment Shifting weight toward chest and moving arms forward in prone Visual tracking

Range of movement for jaw Suckling pattern (anteroposterior motion of tongue) Mouth opens in anticipation of food Lip closure improved Active lip movement with sucking

Sitting supported, head bobs Preparing background movement for future use (upper extremities coming off surface to function in space; weight shifting to pelvis, and lower extremities move more freely) Pelvis and lower extremities provide additional support for upper extremities 3 months

Lifting head to 90° in prone

Nipple feeds continue

Lifting chest off the floor in prone

Neck flexion widens pharyngeal airway

Weight-bearing on lower abdominal muscles and pelvis in prone Playing in space with flexion and extension of neck in supine

Midline orientation Liquids

Head participating in final half pull to sit with fixation on examiner Tolerating weight in supported standing Early reflexes begin to fade continues

55

Table 2–7.  continued Milestone Age/Stage

Development/Posture

Feeding/Oral Sensorimotor

4 months

Gaining balance between flexor and extensor development

Dissociating lip and tongue Lip pursing

Freeing arms for function in supine and supported sitting

Blowing bubbles with saliva

Controlling head in prone, sitting

Increased sound imitation (cooing and laughing emerge)

Controlling head in mid-line through pull to sit

Voluntary control of mouth

Head in midline in supported sitting Pivoting in prone Rolling from prone accidentally Rolling from supine actively Playing with knees in supine Tactile awareness in hands 5 months

Refining head and trunk control Moving constantly Rocking in prone Opening hands Playing with hands and feet in supine Putting hands in mouth Chin tuck to sit maneuver Rolling actively from prone to supine

Holding nipple with center portion of lips with balance and stability Tongue with small range of up–down movement Tongue reversal after spoon removed, ejecting food involuntarily Sucking pattern emerging (uses during spoon feeding) Liquids, eating pureed Gags on new textures

6 months

Moving in a variety of directions Pushing backward in prone Reaching for toys; transfers from one hand to another Shows visual interest in small objects Pulling up independently in pull to sit

Moving with a wide range of up–down, forward–back tongue and jaw movements Pushing semisolid foods by spoon out of mouth by tongue Teething

Elongating of muscles increasing as infant moves

Increased active oral exploration, with toys, other objects, and fingers

Increasing upward movement against gravity

Rooting reflex, automatic bite release are gone Diminished gag reflex

56

Table 2–7.  continued Milestone Age/Stage

Development/Posture

Feeding/Oral Sensorimotor

6 months

Displaying good spinal mobility and rib cage expansion (necessary for adequate respiratory coordination for phonation and swallowing)

Longer lip closure

Crawling on belly, creeping on all fours

Gag reflex becomes protective

Full trunk control

Mouth used for investigation of the environment

continued

7–9 months (late infancy)

Initiating movement from pelvis and upper extremities Changing position with lower extremities as a base of support for upper extremities Moving smoothly Development of extension, flexion, and rotation has expanded what infant can do in sitting Pull to stand/hold on Uses index finger to poke Increased active head and neck to lean forward 10–12 months

Full range of motion of upper extremities Changes position of lower extremities independent of upper body Stands independently Learning to walk (cruising) Pincer grasp (thumb and forefinger) Smooth release for large objects

Coordinated lip, tongue, and jaw movements in all positions Drooling only with teething Cup drinking, lower lip as stabilizer at 9 months Mouth closure around cup rim Moving lateral tongue to touch solids while upper lip cleans off spoon Variegated babbling (mixture of consonant and vowel combinations, e.g., “ma,” “da”) Self-finger-feeding Increasing coordinated jaw, tongue, and lip movements in all positions Weaning from nipple as cup drinking increases Easily closes lips on spoon and uses lips to remove food from spoon Controlled sustained bite on cracker Chews with up–down and diagonal rotary movements

13–18 months

Walking alone

Movement in lips

Using stairs

Fully coordinated phonating, swallowing, and breathing

Grasp and release with precision Scoops food to mouth

All textures taken Lateral tongue motion Straw drinking continues

57

58  Pediatric Swallowing and Feeding: Assessment and Management

Table 2–7.  continued Milestone Age/Stage

Development/Posture

Feeding/Oral Sensorimotor

19–24 months

Equilibrium improving

Swallows with lip closure Up–down tongue movements precise Self-feeding predominates Chewable foods Rotary chewing Independent food intake

24–36 months

Refinement of skills of first 24 months

Circulatory jaw rotations

Jumps in place

Lip closure with chewing

Pedals tricycle

One-handed cup holding and open cup drinking without spillage

Uses scissors

Fills spoon with use of fingers Solids Total self-feeding; uses fork

The overall body posture of a normal newborn is characterized by passive or physiologic flexion. Trunk is neutrally aligned and well supported for feeding, usually in a semireclined position. Head and neck play a primary role in feeding as they assume a neutral to slightly flexed position with stable support from the feeder (e.g., Wolf & Glass, 1992). Head and neck posture/position is an important factor in maintenance of the patency of the pharyngeal airway (Bosma, 1988), with implications for the process of craniocervical postural control. The rib cage is positioned high and elevated in relation to the trunk (Alexander, 1987). Postural control and normal sensorimotor development involve the infant’s progression from primitive mass patterns of movement to selective

movement against gravity (Caruso & Sauerland, 1990) and the development of stability and mobility. The most important example of postural stability in the newborn is the maintenance of the pharyngeal airway. The muscles of the pharynx adjust their contractions to maintain a constant diameter of the pharynx, so gravity does not pull the tongue back into the airway when an infant is in the supine position. Similarly, the pharynx does not collapse when the head is forward, although a chin “tuck” is not advocated for young infants. A chin tucked down toward the chest may result in upper airway collapse. The infant learns to control body against gravity with the head moving side-to-side when supine and weightbearing in prone to allow

Table 2–8.  Psychosocial Milestones, Birth–36 Months Stage

Psychosocial Milestones

0–3 months (homeostasis)

Cues for feeding: arousal, cry, rooting, sucking Caregiver response leads to self-regulation Quiets to voice Hunger–satiety pattern develops Interaction with primary caregiver becomes established with infant smile Pleasurable feeding experiences lead to greater environmental interaction

3–6 months (attachment)

“Falling in love” Increased reciprocity of positive infant–caregiver interactions Cues consistent Anticipates feeding Somatic functions stabilize Pauses may be socialization (not necessarily satiety or for burping) Laughing, smiling, alert, social Parents are preferred feeders Calls for attention (~6 months) Means–end:  repeats actions for toys, people, and things to evoke a response (6 months)

6–36 months (separation/ individuation)

Copies movements Responds to “no” Play activity to explore environment (7–9 mos.) Uses facial expressions for likes and dislikes Follows simple directions Begins independent problem solving Self-feeding emerging Meal times become more predictable Further experimentation with environment Speech emerging Speech very important Follows two-step commands Meals are increasingly linked to family schedule Rapid increase in language Independence complete

59

60  Pediatric Swallowing and Feeding: Assessment and Management

the head, neck, and shoulders increased freedom of movement. Thus, a base of stability allows for increased mobility. Neurodevelopmental milestones relevant to normal feeding at this stage include visual fixation and tracking and balanced flexor and extensor tone of neck and trunk. A variety of feeding positions may be used for infant breast- and bottle-feeding. Careful consideration must be given to the characteristics of each infant. In general, infants should be held in a fairly upright semiflexed posture during feeding with head higher than trunk for both breast- and bottlefeeding. Infant–caregiver interaction during feeds should begin to emerge with a smile response by the infant at about 3 to 6 weeks of age. The rooting reflex is present, along with sucking and swallowing activities. The psychosocial interactions during feeding that occur between the infant and caregiver (usually the mother) begin at birth. The give-and-take exchange is necessary for the emergence not only of adequate feeding skills, but also positive behavior and attitudes toward eating (Satter, 1999). The normal newborn readily provides a set of cues for the caregiver to recognize a need to be fed (e.g., arousal, crying, rooting, sucking). The infant should feed until satiety and then demonstrate positive signs of fullness. Responsive and attentive early feeding is important in helping infants organize their behavior and work toward the process of self-regulation (Satter, 1990, 1995). During the first 2 to 3 months of life, the infant’s primary goal is to achieve homeostasis with the environment. Sleep regulation, regular eating schedules, and developmentally advantageous awake states are some of the basic goals. Increasing interaction with the environment allows the infant to develop emotional attachment to the primary caregiver(s) and others. Early feeding skills can vary from one feeding to the

next and even across an individual feeding (Thoyre, Shaker, & Pridham, 2005). Infants gain greater control of sucking, swallowing, and breathing coordination for breast- and bottle-/nipple-feeding. Reaching, smiling, and social play are all fostered by pleasurable and successful feeding experiences. Feeding gradually becomes a social time (Greenspan & Lourie, 1981; Pridham, 1990; Pridham, Martin, Sondel, & Tluczek, 1989). Pauses between sucking bursts become more apparent and should not be interpreted as a need for burping or early satiety. Although uncommon, incorrectly interpreted breaks in feeding can be associated with undernutrition (Whitten, Pettit, & Fischoff, 1969). If engagement between infant and caregiver fails to develop, the infant may indicate lack of pleasure, loss of appetite, and in its most severe forms, vomiting and rumination.

Infancy (3 to 6 months) Infants receive essentially all of their nourishment through nipple-feedings for the first 4 to 6 months. Breastfed and formulafed infants do not require additional types of food through the 1st year. The World Health Organization (WHO, 2001) and American Academy of Pediatrics (AAP, 2012) recommend exclusive breastfeeding for the first 6 months (Eidelman, 2012). AAP suggests that infants be supplemented with oral iron and vitamin D by 4 to 6 months until they are eating age-appropriate iron-containing foods (Iannelli, 2018, downloaded from AAP website, 09/14/18). For healthy infants at 4 to 6 months who are breastfeeding exclusively, Smith and Becker (2016) in a Cochrane review found no evidence of benefit from additional foods nor any risks related to morbidity or weight change. Thus, they concluded that they could not disagree with the recommendations by WHO and

2. Anatomy, Embryology, Physiology, and Normal Development   61

AAP for exclusive breastfeeding for the first 6 months of life in healthy infants. Most typically developing infants begin taking food when they reach the first transitional feeding stage at 6 months. CNS maturation allows the graduation from nipple-feeding to transitional feeding with thin smooth foods initially. Physical characteristics of the face and mouth (particularly teeth) are less important at this stage (Bosma, 1986). However, not all parents follow that 6-month guideline. In Britain, 75% of British mothers introduced solids before 5 months, and 26% reported that decisions were based on infants waking during the night. A randomized clinical trial found that early introduction of solids at 3 months was associated with longer sleep duration, less frequent waking at night, and a reduction in reported serious sleep problems (Perkin et al., 2018). Self-weaning from breast or bottle to a cup is related to the infant’s transition toward self-regulation. A decreased interest in sucking at the breast or from the bottle often begins at about 5 to 6 months of age. This coincides with developmental advances and increased visual interest in surroundings (Brazelton, 1969). Thus, by 4 to 6 months of age, considerations can be made for spoon-feeding and, usually about 1 month later, the introduction of cup drinking. Variability of commercially available cups is extensive in design parameters, suction pressure, rate of flow, and residual fluid with no one type that can be called the “best” (Scarborough et al., 2010). Caution is urged with considerations based on individual child characteristics. Cultural variability needs to be considered. Successful feeding requires appropriate reciprocal relationships between caregivers and child. Multiple factors need to be considered as the child is learning to attain a sense of self (Delaney & Arvedson, 2008) involving a

balance between autonomy and dependency that is often particularly revolved around feeding. Foods are introduced one at a time per guidelines by dietitians as a means to prevent or at least to minimize potential food allergies (e.g., Fomon, 2001a, 2001b; Fiocchi, Assa’ad, & Bahna, 2006). Single ingredient foods are recommended, which may vary in different cultures. Gradually food with texture can be added to make food thicker, pastier, and grainier, but not chunky. Foods that contain “pieces” in a thin liquid (e.g., vegetable soup) may result in coughing, gagging, and at times vomiting. Introduction of those types of foods may precipitate a feeding disorder as children become scared and begin to refuse such foods that may generalize to other foods over time. A developmental “critical or sensitive period” has been suggested for the introduction of chewable textures in humans (Illingworth & Lister, 1964) and in other animals (e.g., Denenberg, 1959). The term critical period is applied to a fairly welldelineated time period in which specific stimuli must be applied to produce a particular developmental advancement. After that critical time, the desired action can no longer be learned. This can result in faulty neurologic growth, resulting in long-lasting, far-reaching negative impacts on multiple systems. The term sensitive period is applied to an optimal time for the application of such stimuli, after which it is more difficult and takes longer to learn a desired action or pattern of behavior. For children with and without developmental delays or disorders, there is evidence that solid foods need to be introduced at appropriate times or those milestones of development will be missed. If introduced at a later time, rejection of solids may then occur. The longer the delay, the more difficult it is for many children to accept texture changes.

62  Pediatric Swallowing and Feeding: Assessment and Management

By 6 months of age, foods (typically smooth soft foods not requiring chewing) on the tongue promote posterior propulsion followed by a swallow (Schechter, 1990). Interestingly, this skill development coincides with the time when healthy children begin to reach for objects. Children who have motor coordination problems due to cerebral palsy or other neuromotor conditions may not yet be ready for these foods. Illingworth and Lister (1964) posed that withholding solids at a time when a child should be able to chew (6 to 7 months developmental level) can result in food refusal and vomiting. As described later in this chapter and in Chapter 13, psychosocial development, personality, and environmental factors may complicate feeding problems. The introduction of food to a child with developmental delay can be challenging. The time for introduction of solid foods is estimated based on a developmental quotient (DQ) that generally correlates to a level of functioning. A comprehensive developmental examination should yield an estimated DQ that can be used to determine the expected age of development for chewing. The DQ can be estimated on the basis of a variety of developmental scales (Chapter 3). Most typical children with an average DQ of 100 are ready for introduction of food at usual ages. Variability may be observed in the speed at which children move through the steps of thin smooth to thick smooth to slightly lumpy, to easily dissolvable and soft chewable food. Although there may be variability in the speed at which children move through the steps of thin smooth to thick smooth to slightly lumpy, to easily dissolvable and soft chewable food, the sequential order of progression is relatively constant. Developmental milestones during the 5th to 7th months include visual recognition of parents, followed by the recognition

of small objects, reaching, and grasping. Parents are the preferred feeders, and the child is now ready to assume an upright posture during feeding. Oral sensorimotor development is supported by the overall development of postural stability and associated increased movements of the body. Postural control develops within a range of muscle tension that is not static and therefore allows for adaptation to demands of the environment (Langley, 1991). For example, by about age 4 to 6 months, increasing head control and midline postural stability enable the temporomandibular joint to control jaw opening. By that age, the infant can open the mouth wide in anticipation of a spoon or a nipple. The jaw remains open in extension until food has entered the mouth at which time the jaw flexors take over. The development of jaw flexor control occurs later than jaw extensor control. Extensor and flexor components gradually become balanced so postural stability of the jaw appears consistent by 24 months (Morris, 1985). The increasing jaw stability permits increased tongue and lip movements not only for feeding, but also “sound” play. Vocalizations occur in conjunction with oral movements. For example, as the infant adapts to changes in position or attempts to mold the body into a caregiver’s arms, pleasurable cooing or babbling sounds are likely to be produced (Connor, Williamson, & Siepp, 1978).

Late Infancy (6 months to 1 year) In the second 6 months of the first year, four categories of feeding skills develop. These skills include (a) taking food from a spoon, (b) handling thicker and lumpier foods that may require munching or chewing, (c) self-feeding with fingers or a spoon,

2. Anatomy, Embryology, Physiology, and Normal Development   63

and (d) drinking from a cup and managing the bottle independently (Pridham, 1990). These feeding skills emerge within the broader context of oral sensorimotor development, hand-to-mouth and fine motor coordination, body positioning, and communication. Infants communicate interest in feeding by their posture, head and mouth movements, and vocalizations. As previously noted, readiness for spoon-feeding usually occurs around 4 to 6 months of age, when a reduction in the typical anteroposterior tongue action for suckling is seen. At age 5 to 7 months, the infant learns to get semisolid food from a spoon, and by about age 8 months, the infant can remove food from the spoon quickly and efficiently (Pridham, 1990). Healthy infants between 4 and 8 months of age were found to need an average of 6 weeks (range of 2–10 weeks) to acquire the skill of assisted spoon-feeding (van den Engel-Hoek, van Hulst, van Gerven, van Haaften, & de Groot, 2014). A forward head motion and use of both upper and lower lips help bring the spoon into the mouth. Improved trunk control and a stable sitting posture enable improved head control (see text that follows). It is during the second 6 months of the 1st year of life that position and tone have the greatest impact on the rapidly developing feeding skills. The ability to sit without support is basic to the ability to swallow thicker foods. At about 6 months of age, oral-motor activity is characterized by a kind of munching with vertical movements of the jaw. At approximately 7 months of age, coincident with a spurt in gross motor development, rotary jaw action begins for chewing. Rotary chewing is refined over the next 5 months. The tongue’s increased flexibility, especially for lateral motion, allows for a greater range of bolus manipulation before swallowing. The ability to manage a thicker bolus makes

feasible the introduction of soft food with a lumpy texture. New textures should be introduced gradually. Mixed textures in the same bite tend to be confusing to many children, particularly to those with neurologic impairment. For example, commercially prepared baby food may contain chunky pieces mixed in a liquid base. Some children find this difficult to handle, and may appear unsure whether to swallow it like liquid or to munch the lumpier texture. The risks for choking and aspiration are higher for a single bite of food with a mixed texture rather than a homogeneous consistency. Illingworth and Lister (1964) stressed that it is critical to introduce lumpy textures at this stage of development if the child is to learn to accept the consistency. Otherwise, the probability increases that the child will resist changes in texture to a much greater degree than a child who was introduced to lumpier textures within the critical or sensitive time periods. Chewing skills have been shown to vary according to different textures (Saitoh et al., 2007). In 143 healthy children, not surprisingly, chewing time was found to be the longest for solids and shortest for pureed foods. The chewing time for viscous foods was in between the time for the other two textures (Gisel, 1991). Even though the chewing time for solids was found to be longer than it was for other textures, children developed mature chewing skills for solid foods earlier than for viscous and pureed foods. As expected, as children get older, less chewing time is needed for all textures (Gisel & Patrick, 1988). The refinement of rotary chewing patterns has been shown to develop later, after 30 months. Rotary chewing was not found in children studied at 30 months of age (Wilson & Green, 2009). As expected, as children get older, less chewing time is needed for all textures (Gisel & Patrick, 1988),

64  Pediatric Swallowing and Feeding: Assessment and Management

Cup drinking is often introduced within a month or two following the introduction of spoon-feeding. This developmental advance often presents infants with new challenges. Parents face challenges as well, especially given the myriad types of “training” cups available in many areas of the United States and other countries (Scarborough et al., 2010). From 6 to 12 months, infants and their families enjoy a burst of progress relative to the development of posture and muscle tone. As the infant gains trunk stability, the extremities gain mobility, setting the stage for self-feeding activities. In addition, with neck and shoulder stability control, the respiratory muscles, the larynx, and the oral–pharyngeal structures gain stability. The emergence of positional (external) and postural (proximal and internal) stability is a prerequisite for the infant to be able to reach for an object (Hadders-Algra, 2013). One arm may be held close to the body to stabilize the shoulder girdle and upper arm (by resting the elbow on the chest), providing external stability. The fingers can then open and reach for the object. As time passes, internal or postural stability emerges. The infant can now reach for an object without needing external support for the arm. Contraction of muscles around the shoulder joint provides postural stabilization necessary for movement of other muscles. This postural stability enables the child to perform distal movements more freely and precisely. With newfound motor skills, infants begin to exert increased control over their environment. Transition feeding, beginning at age 6 months with spoon-feeding of smooth purees, coincides with the beginning of the developmental period of separation-individuation. (Chatoor, Schaefer, Dickson, & Egan, 1984). As young children

begin self-feeding, the mealtime experience broadens from an intimate relationship with a primary caregiver to participation in the social event of the family meal. Similar situations occur in child care settings with staff members and peers. Caregivers and children typically work toward scheduled feeding times that by the end of the first year should coincide with family mealtimes. Effective feeding includes selection of developmentally appropriate feeding methods, as well as types and quantities of food. Older infants need opportunities to achieve independence in the feeding process. It is during this period that self-control must be balanced with independence. Further discussion regarding roles of children and their caregivers is found in Chapter 13. As children become more independent in eating and drinking, fewer focuses are needed for oral feeding, that in turn allows intellectual and social development to prevail.

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Storey, A. T. (1968). A functional analysis of sensory units innervating epiglottis and larynx. Experimental Neurology, 20, 366–383. Sumi, T. (1970). Changes of hypoglossal nerve activity during inhibition of chewing and swallowing by lingual nerve stimulation. Pflugers Archives of European Journal of Physiology, 317, 303–309. Thach, B. T. (2001). Maturation and transformation of reflexes that protect the laryngeal airway from liquid aspiration from fetal to adult life. American Journal of Medicine, 111(Suppl. 8A), 69S–77S. Thach, B. T. (2007). Maturation of cough and other reflexes that protect the fetal and neonatal airway. Pulmonary Pharmacology and Therapeutics, 20(4), 365–370. Thoyre, S. M., Shaker, C. S., & Pridham, K. F. (2005). The early feeding skills assessment for preterm infants. Neonatal Network, 24(3), 7–16. Thurlbeck, W. M. (1982). Postnatal human lung growth. Thorax, 37(8), 564–571. Törölä, H., Lehtihalmes, M., Yliherva, A., & Olsén, P. (2012). Feeding skill milestones of preterm infants born with extremely low birth weight (ELBW). Infant Behavior and Development, 35(2), 187–194. doi:10.1016/j​ .infbeh.2012.01.005 van den Engel-Hoek, L., van Hulst, K. C., van Gerven, M. H., van Haaften, L., & de Groot, S. A. (2014). Development of oral motor behavior related to the skill assisted spoon feeding. Infant Behavior and Development, 37(2), 187– 191. doi:10.1016/j.infbeh.2014.01.008 van der Linde, D., Konings, E. E., Slager, M. A., Witsenburg, M., Helbing, W. A., Takkenberg, J. J., & Roos-Hesselink, J. W. (2011). Birth prevalence of congenital heart disease worldwide: A systematic review and meta-analysis. Journal of the American College of Cardiology, 58(21), 2241–2247. doi:10.1016/j​.jacc.2011.08.025 Vitti, M., & Basmajian, J. V. (1975). Muscles of mastication in small children: An electromyographic analysis. American Journal of Orthodontics, 68, 412–419.

Weiffenbach, J. M., & Thach, B. T. (1973). Elicited tongue-movements: Touch and taste in the mouth of the neonate. Symposium Oral Sensory Perception, 4, 232–244. Whitten, C. R., Pettit, M. G., & Fischoff, J. (1969). Evidence that growth failure from maternal deprivation is secondary to undereating. Journal of the American Medical Association, 209, 1675–1682. Wilson, E. M., & Green, J. R. (2009). The development of jaw motion for mastication. Early Human Development, 85, 303–311. Wilson, S. L., Thach, B. T., Brouillette, R. T., & Abu, O. Y. K. (1981). Coordination of breathing and swallowing in human infants. Journal of Applied Physiology: Respiratory, Environmental and Exercise Physiology, 50, 851–858. Winberg, J., & Porter, R. H. (1998). Olfaction and human neonatal behaviour: Clinical implications. Acta Paediatrica, 87(1), 6–10. Wolf, L. S., & Glass, R. P. (1992). Feeding and swallowing disorders in infancy: Assessment and management. Tucson, AZ: Therapy Skill Builders. World Health Organization. (2001). The World Health Organization’s infant feeding recommendation. Retrieved from http://www.who​ .int/nutrition/topics/infantfeeding_recom​ mendation/en/index.html Yayan, E. H., Kucukoglu, S., Dag, Y. S., & Karsavuran Boyraz, N. (2018). Does the postfeeding position affect gastric residue in preterm infants? Breastfeeding Medicine, 13(6), 438–443. doi:10.1089/bfm.2018.0028 Zaichkin, J., Weiner, G., & Loren, D. (Eds.). (2016). Understanding the NICU: What parents of preemies and other hospitalized newborns need to know (4th ed.). Itasca, IL: American Academy of Pediatrics (AAP). Zancan, M., Luchesi, K. F., Mituuti, C. T., & Furkim, A. M. (2017). Onset locations of the pharyngeal phase of swallowing: Meta-analysis. CoDAS, 29(2), e20160067. doi:10.1590/23171782/20172016067

3

Neurodevelopmental Assessment of Swallowing and Feeding

Brian Rogers and Shannon M. Theis

Summary Successful swallowing and feeding represent the culmination of complex neurodevelopmental processes within the framework of each child’s physical well-being and environment. The complex, integrated neurologic and developmental processes controlling or influencing swallowing and feeding are represented in all levels of the central and peripheral nervous systems (see Chapter 2). Maturation and timing of these processes are critical components of successful swallowing and feeding as well as other “streams of development,” including cognitive, communicative, and motor skills. Disorders of swallowing and feeding in childhood are predominantly of neurologic origin but are greatly influenced by aerodigestive structure and function, general health, and a variety of environmental factors. The purpose of this chapter is to provide an overview of important neurodevelopmental aspects of swallowing and feeding. This overview will include a brief discussion of central nervous system (CNS) development and associated swallowing and feeding skills, neurodevelopmental history and examination methods, and case studies.

Morphogenesis of the Central Nervous System Human brain development is a prolonged process that begins in the third gestational week (GW) and extends through the life span. Complex molecular events of gene expression and environmental input interact to guide brain development through the traditional embryonic, fetal, and postnatal periods. It is important to keep in mind that these maturational processes are not rigidly sequential in which one needs to be completed before the next, but they overlap and in many instances occur simultaneously (Sarnat & Flores-Sarnat, 2013). Disruption of these processes can significantly alter neurodevelopmental outcomes (Stiles & Jernigan, 2010). Emphasis will be placed on normal and abnormal brain development and its relationship to feeding, swallowing, and general development.

Embryonic Period The human embryonic period extends through the 8th gestational week (GW). By the end of this period, the major rudimentary 75

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structures and compartments of the central and peripheral nervous systems will be defined (Sarnat, 2013; Stiles & Jernigan, 2010). By the end of the 3rd GW the embryo is transformed through a series of processes referred to as gastrulation, into a threelayered structure (Stiles & Jernigan, 2010). The upper cell layer, composed of epiblasts, will eventually give rise to all of the structures in the developing embryo. Among the epiblasts, the neural stem cells or neuroprogenitor cells appear between embryonic days (E) 13 and 20 and are positioned along the rostral-caudal midline of the upper layer of the three-layer embryo resulting in the development of the neural plate. These neuroprogenitor cells will eventually give rise to all the different cells of the brain and spinal cord. Neurulation or the formation of the neural tube occurs during the 3rd week of gestation. The first sign of the neural tube development is the appearance of two ridges that form along the two sides of the neural plate at approximately E21. Over the course of several days, the ridges rise and fold inward to form the neural tube. Fusion of the neural tube first occurs centrally and then spreads rostral and caudal. When the neural tube is closed, the neural progenitor cells form a single layer of cells that lines the center of the tube, adjacent to the hollow center. Rostrally, the hollow neural tube will give rise to the ventricular system, and the adjacent neural progenitor cells will compose the “ventricular zone” (VZ) that will eventually form the brain. More caudally located progenitor cells will give rise to the hindbrain and eventually the spinal cord. Between the 3rd and 8th weeks of the embryonic period, there is a 10-fold increase in the length of the embryo, and the shape of the nervous system significantly changes. The anterior end of the neural tube begins to expand to form three primary brain vesicles, including the anterior prosencephalon

(forebrain), the middle or mesencephalon (midbrain), and the posterior or rhombencephalon (hindbrain). By the end of the embryonic period, these three segments further divide into the five secondary brain vesicles. The prosencephalon divides into the “telencephalon” and “diencephalon,” and the rhomboencephalon divides into “metencephalon” (pons and cerebellum) and the “myelencephalon” (medulla oblongata). Disturbances of neurulation result in various errors of neural tube closure ranging from anencephaly (lack of forebrain development with variable anomalies of the upper brain stem that are incompatible with life), encephalocele (restricted closure of the anterior neural tube), and myelomeningocele (restricted closure of the posterior neural tube). Myelomeningocele is usually associated with other brain anomalies including Chiari type II malformation and hydrocephalus. The Chiari type II malformation can result in various cranial nerve deficits that may lead to significant swallowing and feeding problems (see discussion on cranial nerves). Prosencephalic development refers to the inductive influences of the prechordal mesoderm that result in the formation of the face and the forebrain. The peak period of prosencephalic development occurs in the 2nd and 3rd months of gestation (overlapping embryonic and fetal periods). Prosencephalic formation begins at the rostral end of the neural tube at the end of the 1st month of gestation. Prosencephalic cleavage occurs in the following 2 weeks and results in the development of paired optic vesicles, olfactory tracts, separation of the telencephalon from the diencephalon, and the sagittal cleavage of the telencephalon to form the paired cerebral hemispheres, lateral ventricles, and basal ganglia. Midline prosencephalic development involves the formation of three thickenings of tis-

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sue including the commissural, chiasmatic, and hypothalamic plates. These structures are important in the formation of the corpus callosum, septum pellucidum, optic chiasm, and hypothalamic structures, respectively. Disorders of prosencephalic development usually result in abnormalities of both face and brain development. Abnormalities of prosencephalic formation that are usually incompatible with life include aprosencephaly (lack of development of the telencephalon and diencephalon) and atelencephaly (lack of telencephalon). The holoprosencephalies result from failed prosencephalic cleavages in the horizontal, transverse, and sagittal planes. A common anomaly includes the formation of a singlesphered telencephalon and a less involved diencephalon. Common disorders of midline prosencephalic development include agensis of the corpus callosum, septum pellucidum, and septo-optic dysplasia. Common facial anomalies associated with these disturbances of midline brain development include hypotelorism, midline cleft lip and palate, and a single front incisor. Children with disorders of prosencephalic brain development are at higher risk for various developmental disabilities that include intellectual disabilities, cerebral palsy (CP), communication disorders, and neurogeneic dysphagia.

Fetal Period The fetal period of human development extends from the 9th gestational week until birth. During this time, the brain cortical development goes through gradual but striking changes from a smooth or “lissencephalic” structure to the more recognizable pattern of gyral and sulcal folding. These gross anatomic changes reflect significant changes at the cellular level, including cell

proliferation, neuronal migration, and postmigrational cortical organization and connectivity (Guerrini & Dobyns, 2014; Stiles & Jernigan, 2010). The human brain contains billions of neurons. Most are produced by midgestation (Bayer et al., 1993; Rakic, 1995). Cell proliferation begins in the embryonic period (E42) and extends through midgestation in most regions of the brain (Stiles & Jernigan, 2010). The neural progenitor cells in the ventricular zone undergo mitosis to form neurons, which when formed are unable to divide and form new cells. It takes only 33 mitotic cycles to produce all of the neurons of the cerebral neocortex. Overproduction of neurons in all parts of the neural tube by 30% to 50% is followed by apoptosis or programed death of redundant neurons (Sarnat & Flores-Sarnat, 2013). Processes including congenital infections or a genetic disorder that arrests the proliferation of ventricular zone neural progenitor cells sooner than the requisite number of mitotic cycles are completed can result in micrencephaly or small brain. Inadequate apoptosis of redundant neurons has been speculated to be the basis of macrocephaly or large brain in Sotos syndrome (Sarnat & Flores-Sarnat, 2013). The preplate plexus containing the Cajal-Retzius or “pioneer” neurons of the molecular zone are positioned to control the expression of patterns of layer-specific mRNA and protein expression, which results in a laminar architecture of the neocortical plate even prior to the first wave of neuroblast migration (Hevner, 2007). This laminar architecture and the resulting cortical plate (cortex layers two through six) are largely regulated by the gene Reelen (RELN) contained on chromosome 7q22.1 in the Cajal-Retzius neurons. Most of the migratory neurons to the cerebellum and brain stem arise from the margin of the primordial fourth ventricle. At least six mutations

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of the RELN gene have been found to cause lissencephaly (smooth brain) with cerebellar hypoplasia. Guerrini and Dobyns (2014) identified 12 lissencephaly genes that accounted for 90% of reported patients. Lissencephaly is characterized by absent or abnormally wide gyri plus an abnormally thick cortex (Guerrini & Dobyns, 2014). Most patients with lissencephaly come to medical attention in the first year of life due to poor feeding, hypotonia, delayed motor milestones, and/or seizures. Neuroblast migration to the cerebral cortex begins at 7 to 8 GW, and over 90% is completed by 16 GW. In the cerebrum, specialized radial glial cells in the subventricular zone have long, slender processes along which neurons migrate to the cortical plate in waves, the earliest migrations forming the deepest layers, and the last waves form the most outer or Layer 2 cortical layer. An additional tangential neuronal migration wave arises from the forebrain and is responsible for GABAergic inhibitory interneurons in the cortical plate that comprise up to 20% of total cortical neurons (Sarnat & Flores-Sarnat, 2013). Abnormalities of early neuronal migration have traditionally been classified based on the effects on sulcation and gyration that include lissencephaly, pachygyria, and polymicrogryria. However, there often are abnormalities in the development of the brain stem and cerebellum (Sarnat & Flores-Sarnat, 2013). Disorders of early migratory arrest include periventricular nodular heterotopia and subcortical laminar heterotopia. It is important to recognize that abnormalities of neuronal migration can result not only from defects of genetic programing, but also from acquired lesions during the fetal period. Sarnat (1992) demonstrated that severe telencephalic hypoplasia or “smooth brain” could result from early infarcts. Ischemic lesions have also been

linked to polymicrogyria. Congenital infections can cause vascular lesions that lead to abnormalities of sulcation and gyration. Axons form earlier than dendrites. Axons sprout from migratory neurons before they reach their destinations. Axonal terminals proliferate to innervate many neurons during maturation. In some brain malformations, axons project to aberrant sites of the brain. An example of a disorder of axonal projection is agenesis of the corpus callosum (Sarnat & Flores-Sarnat, 2013). The dendritic tree of each neuron starts to proliferate only after the neuron reaches its final site within the brain. Specialized structures called dendritic spines form to enlarge the synaptic surface and for specialization. There is a predictable timetable for dendritic spine development in the neocortex. Dendrites and axons form synapses, and synapses allow the transmission of electrochemical information that is the essential means of communication between neurons in the brain. Dendritic spine dysgenesis is the underlying synaptopathology that is found in many patients with intellectual and communicative disabilities, including Down, Rett, and fragile-X syndromes and autism (Penzes, Cahill, Jones, VanLeeuwen, & Woolfrey, 2011; Phillips & Pozzo-Miller, 2015).

Myelination Myelination is the last stage of white matter development that begins after axonal overproduction, pruning, and follows premyelinating stages including the formation and maturation of oligodendrocytes (Dubois et al., 2014). This process includes the proliferation and migration of oligodendrocyte precursors to form “initiator” processes, which align along axons and identify targeting axons followed by spiral ensheathment, elongation, and wrapping around the axon.

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This is followed by the myelin becoming more compact. Myelin is a lipoprotein outer cover for axons. Its function is to increase the rate and efficiency of electrochemical signaling down the axonal shaft. Myelination is a marker of maturation in the developing brain. Myelination of the CNS begins as early as the 4th month of gestation and continues in some regions of the brain into the third and fourth decades of life. Areas of the CNS may differ in the onset and rate of myelination (Kinney, Brody, Kloman, & Gilles, 1988; Yakovlev & Lecours, 1967). However, there are recognizable patterns of myelination of the CNS. Its progression varies across cerebral regions, following a caudo-rostral gradient and progressing from center to the periphery. Proximal pathways myelinate earlier and faster than distal pathways. Sensory tracts myelinate before motor tracts. Cerebral myelination occurs in projection (e.g., thalamocortical) before associative pathways (e.g., occipitotemporal pathways). Myelination, in general, progresses from the central sulcus outward toward the occipital, frontal, and temporal poles. Neural tracts mediating general proprioceptive (position sense) and exteroceptive somatic experience (tactile and pain), including the medial lemniscus, outer division of the inferior cerebellar peduncle, and the brachium conjunctivum, myelinate beginning at 6 months’ gestation and extending to 1 year of age. Myelination of specific thalamic projection fibers to respective cortical areas appears to be synchronized with cycles of myelination of descending efferent corticospinal and corticobulbar tracts from these areas. Myelination of the corticospinal and corticobulbar tracts appears initially near term or 40 weeks’ gestation and increases steadily with a “burst” at 8 to 9 months of age. Myelination events are correlated with

motor-skill acquisition and other neurodevelopmental milestones during the 1st year of life. As myelination proceeds, the loss of primitive or brain-stem-mediated reflexes occurs. The Moro, asymmetric tonic neck, and suckle reflexes are replaced by voluntary motor skills including rolling, sitting, crawling, mature sucking, and vertical chewing. The proximal to distal myelination pattern is manifested by the observed motor pattern that batting or reaching for objects appears before the development of a voluntary grasp. Myelination of the brain stem initially appears at 5 months’ gestation. The myelination of the statoacoustic system (vestibular and cochlear) commences at 5 months’ gestation and is completed by 9 months’ gestation (term birth). At 5 to 6 months’ gestation, the roots of cranial nerves III (oculomotor), IV (trochlear), and VI (abducens), and the intramedullary roots of cranial nerves VII (facial), IX (glossopharyngeal), and XII (hypoglossal) are myelinated. A review of the neurophysiology of swallowing is found in Chapter 2, but a few key points are made concerning the synaptogenesis and myelination of the nucleus tractus solitarius and ventral medial reticular formation or central pattern generator for swallowing in the medulla. The nucleus solitarius (brain stem pneumotaxic center) is synaptically mature before 15 weeks’ gestation, coinciding with the appearance of swallowing and onset of fetal respiratory movements. Myelination of the tractus solitariuis is a later event, commencing at around 33 weeks’ gestation, and is not fully complete even at term (Sarnat & FloresSarnat, 2016). Myelination of the reticular formation around the nucleus ambiguus and the nucleus tractus solitarius (site of the central pattern generator for swallowing) continues beyond 2 years of age. These myelination patterns coincide with the

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appearance of suckling at 18 to 24 weeks’ gestation and the continued development and refinement of the oral and pharyngeal phases of deglutition in the first few years of life (see Chapter 2 for further discussion of the neurophysiology of swallowing). Hypoxia, metabolic disturbances, and other complications occurring late in the first and second trimester have been linked to impaired rates of synapse formation in the nucleus solitarius, and apnea of prematurity. Symmetrical watershed tegmental infarcts of the brain stem may involve the nucleus solitarius, and account for the respiratory insufficiency and dysphagia that may occur in infants with Mobius syndrome (Igarashi, Rose, & Storgion,1997; Sarnat, 2004).

Prevalence of Swallowing and Feeding Disorders Information regarding the incidence/prevalence of swallowing and feeding disorders in the general population of children and various higher-risk groups has surprisingly been somewhat limited. Better prevalence data are gradually increasing in recent years. Using the National Health Interview Survey (NHIS) in 2012, Bhattacharyya (2015) surveyed the general population in the United States of children aged 3 to 17 years for voice or swallowing problems lasting greater than 1 week. Out of the total population of 61 million children, 569 thousand children (0.9% or nine per 1,000) had a swallowing problem, but only 13% were given a diagnosis for their swallowing problem, and the most common cause was “neurological problems.” Hvelplund, Hansen, Koch, Andersson, and Skovgaard (2016) surveyed all children born in Denmark from 1997 to 2010 (N = 918,280) for

the International Classification of Diseases, 10th Revision (ICD-10) diagnoses of feeding and eating disorders (FEDs) in the first 48 months of life. They identified a cumulative incidence of 1.6 per 1,000 live births. Preterm infants were more likely to have FEDs, but over 84% of children with FEDs were term infants. On univariate and multivariate analyses, prematurity, small for gestational age, and congenital malformations were strongly associated with FED. A significantly increased risk of FED was seen in girls, firstborn children, and children of mothers who smoked during pregnancy. A  survey of all children between 4 and 7 years of age from a complete geographical area in Germany was completed in 2008 by Equit and colleagues (2013). Parents completed a 25-item questionnaire regarding their child’s eating behavior as well as anxious or oppositional behaviors. Interestingly, 23% of the children were described as only eating a narrow range of foods. Much smaller percentages were noted to avoid all foods (4.8%); have a profound refusal to eat, drink, or be cared for (0.7%); or have a fear of swallowing, choking, or vomiting (1%). This survey as well as others have found high rates of “picky” eating in the general population of children. A study in Thailand highlighted how feeding problems affect feeding practices in the home. Pediatricians interviewed the parents of 402 children between 1 and 4 years of age (Benjasuwantep, Chaithirayanon, & Eiamundomkan, 2013). The investigators found that 4.5% of the children were described as having a limited appetite, and 15% were described as having a highly selective food intake. Children with feeding problems were fed less frequently, were less likely to be fed at their own table or at the family table, and had mealtimes longer than 30 minutes.

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Antecedents/Risk Factors Birth Weight and Gestational Age Very low (