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Dysphagia
Evaluation and
Treatment
From the Perspective of
Rehabilitation Medicine

Eiichi Saitoh
Kannit Pongpipatpaiboon
Yoko Inamoto
Hitoshi Kagaya
Editors

123
Dysphagia Evaluation and Treatment
Eiichi Saitoh • Kannit Pongpipatpaiboon
Yoko Inamoto • Hitoshi Kagaya
Editors

Dysphagia Evaluation
and Treatment
From the Perspective of Rehabilitation
Medicine
Editors
Eiichi Saitoh Kannit Pongpipatpaiboon
Department of Rehabilitation Medicine I, Department of Rehabilitation Medicine I,
School of Medicine, Fujita Health School of Medicine, Fujita Health
University University
Toyoake, Aichi Toyoake, Aichi
Japan Japan

Yoko Inamoto Hitoshi Kagaya

Faculty of Rehabilitation, School of Department of Rehabilitation Medicine I,
Health Sciences, Fujita Health School of Medicine, Fujita Health
University University
Toyoake, Aichi Toyoake, Aichi
Japan Japan

Japanese-language and Thai-language rights are retained to the editors.

ISBN 978-981-10-5031-2    ISBN 978-981-10-5032-9 (eBook)
https://doi.org/10.1007/978-981-10-5032-9

Library of Congress Control Number: 2017954327

© Springer Nature Singapore Pte Ltd. 2018

This work is subject to copyright. All rights are reserved by the Publisher, whether the whole or part of
the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation,
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Foreword

Dysphagia is a common and potentially serious problem, especially in neurological

disorders, and is particularly frequent in elderly individuals. Dysphagia is associated
with significant morbidity and mortality including dehydration, malnutrition, airway
obstruction, and aspiration pneumonia. Severe dysphagia has a devastating impact
on quality of life as it can eliminate the pleasure of eating and drinking. Less recog-
nized is the impact of dysphagia on psychosocial functions. It can lead to isolation as
the patient withdraws from activities involving food such as family mealtimes, group
dinners, and teatime. These issues are especially important in rapidly aging societies
such as Japan, which has the highest percentage of elderly people in the world.
Japan is unique in its early recognition and embrace of the team approach to
dysphagia rehabilitation among professionals across a spectrum of disciplines and
specialties. Speech language hearing therapists (SHLTs), dentists, nurses, dental
hygienists, dieticians, and physiatrists (rehabilitation physicians) actively collabo-
rate in the Japanese dysphagia team. Indeed, the Japanese Society for Dysphagia
Rehabilitation is the world’s largest multidisciplinary organization dedicated to
research, education, and patient care in swallowing disorders. This team approach
contributes to both the effectiveness and efficiency of patient care.
Fujita Health University (FHU) is one of the pioneering facilities where dyspha-
gia rehabilitation is approached systematically and scientifically using the concept
of the team approach. Their new textbook, Dysphagia Evaluation and Treatment:
From the Perspective of Rehabilitation Medicine, is designed to support the highest
level of practice, scientifically, clinically, and ethically. The chapter authors and edi-
tors are highly skilled experts in dysphagia rehabilitation.
I can attest to the exceptional knowledge and expertise of my colleagues at Fujita
Health University based on our close and ongoing collaboration since my first visit
to Japan in 1996. I have had the good fortune to witness and learn from my col-
leagues at FHU during many visits to Japan as a visiting professor, especially
Professor Eiichi Saitoh, a pioneer and renowned leader in dysphagia research and
practice. Additionally, more than 30 Japanese clinicians and researchers have taken
research fellowships in my laboratory at Johns Hopkins University, including six
current FHU faulty members.

v
vi Foreword

Along with the anatomy and physiology, this textbook highlights basic as well as
advanced principles of patient care, including the approach to the patient, bedside
examination and screening, instrumental evaluation including traditional as well as
novel methods (such as swallowing CT and high resolution manometry), and an
approach to treatment based on the science of motor learning. Case studies illustrate
the comprehensive team approach to patient care.
This textbook serves as an excellent guide to the latest developments in the prac-
tice of dysphagia rehabilitation. This approach, if implemented early and main-
tained over time, can enhance the health and quality of life of people with dysphagia.
It also points the way to improving our knowledge and practice in the future.

Jeffrey B. Palmer, MD
Professor Emeritus, Johns Hopkins University
Baltimore MD 21218, USA
Distinguished Professor, Fujita Health University
Toyoake, Aichi, Japan
Overview

Difficulty swallowing (dysphagia) occurs in all age groups, with a high prevalence
in older individuals. The swallowing process requires intricate coordination
between the central nervous system and multiple muscles of the face, mouth, phar-
ynx, larynx, and esophagus for safe and effective deglutition. Consequently, dys-
phagia significantly impacts survival and may become a life-threatening
disability.
The older adult population is increasing worldwide. The proportion of indi-
viduals ≥60 years of age increased from 9.2% in 1990 to 11.7% in 2013 and is
expected to reach 21.1% by 2050 [1]. Japan is at the forefront of the aging popula-
tion. The older population in Japan is increasing more rapidly than in any of the
developed Western European countries or the United States [2]. Japan surpasses
all other nations with the highest proportion of older citizens; 26.5% of citizens
are >65 years, 12.8% are ≥75 years, and 3.9% are ≥85 years, according to the
most recent government statistics in 2015 (final estimates) [3]. Thailand is another
Asian country with a growing population of older adults. The number of Thai
people aged ≥60 years in 2013 was approximately 9.6 million, accounting for
14% of the population [4]. By 2040, Thailand’s older population is expected to
increase to 17 million, accounting for 25% of the population [5]. As the older
population increases, the incidence of dysphagia associated with the aging pro-
cess and/or diseases that affect older patients may also increase. For this reason,
dysphagia is an increasingly common and concerning problem in Asian
societies.
Pneumonia is one of the most common adverse effects of dysphagia and has been
a leading cause of death during the past decade. The World Health Organization
reported that pneumonia was ranked the fourth leading cause of death worldwide in
2012 (Fig. 1), with a similar trend in Asian countries such as Japan and Thailand
(Fig. 2).
Furthermore, pneumonia contributes to increased rates of hospitalization and
mortality. The impact of pneumonia in older patients may be more substantial than
in other age groups. Data reported by the Nationwide Hospital Admission of

vii
viii Overview

16%

Ischemic heart
disease

11%
46% Stroke
Others
LRI
6%
COPD

6%
3%
3% Trachea bronchus
2% 2% 2% 3%
lung cancer
Road injury DM
Tuberculosis
Diarrhoeal Alzheimer disease
disease and other dementias

Fig. 1 The 10 leading causes of death worldwide by percentage in 2015 as reported by the World
Health Organization. Lower respiratory infections were within the top five leading causes of death
worldwide [6]. COPD chronic obstructive pulmonary disease, DM diabetes mellitus, LRI lower respi-
ratory infections

16%
22% 29% Malignant neoplasm
Chronic obstructive
Others
pulmonary disease
Malignant neoplasm 7%
Cerebrovascular
1% disease
Aortic aneurysm 1% 47% Others
2%
Sucide Accident
2% 7%
Renal
disease 3% Cardiac disease
Senility Cardiac disease
Accident 6% Pheumonia 6%
Cerebrovascular
15% Renal
diasease
Pneumonia disease 6%
9%
Human 1% 2% 4%
9% immunodeficiency 1% 3%
virus (HIV)
Tuberculosis Hepatopancreatic disease
Suicide
© FHUR 2017

Fig. 2 Left: Death rates per 100,000 population by leading cause of death in Japan in 2014 (data
derived from the Ministry of Health, Labour and Welfare) [7]. Right: Death rates per 100,000
population by leading cause of death in Thailand in 2014 (data derived from the office of the
Permanent Secretary for Public Health, Ministry of Public Health) [8]
Overview ix

Fig. 3 Increase in % Mortality rate

pneumonia-associated 20
mortality rate
with advancing age in
Thailand [9]
15

10

0
19–25 26–40 41–60 61–70 71–80 80 or more
Age ranges (years)
© FHUR 2017

Fig. 4 Increase in % Mortality rate

pneumonia-associated 20
mortality rate with
advancing age in
Japan [10] 15

10

0
2–24 25–39 40–59 60–69 70–79 80 or more
Age ranges (years)
© FHUR 2017

Thailand in 2010 and a demographic survey performed by the Japanese Ministry of

Health, Labour and Welfare in 2015 indicated a rising trend of pneumonia with
advancing age and showed a substantially higher mortality rate in afflicted persons
aged >60 years (Figs. 3 and 4).
In 2013, a population survey reported by the Japanese Ministry of Health, Labour
and Welfare showed that pneumonia was the third leading cause of death overall [7].
Approximately 60% of hospitalized older patients were diagnosed with aspiration
pneumonia; this was particularly notable in patients aged ≥70 years [11]. In addition,
asphyxiation accounted for the highest proportion of accidental deaths (fifth leading
cause of death) in Japan. Many of these patients had dysphagia. These data indicate
x Overview

that dysphagia-related deaths have been increasing and that dysphagia must be thor-
oughly recognized and understood by healthcare professionals. In 2012, the Fujita
Swallowing Team at the Fujita Health University Rehabilitation Complex (FHUR)
surveyed the prevalence of dysphagia in Japan and reported 73.7% in chronic hospi-
tals, 59.7% in nursing homes, and 58.7% in long-term care facilities [12]. Similarly,
a national survey in 2009 found a relatively large number of ­geriatric long-term care
residents with feeding tubes as well as difficulty swallowing in orally fed residents
[13]. This study also indicated that swallowing evaluation in patients with dysphagia
is often limited and incomplete [13]. These findings suggest that older residents with
dysphagia are not receiving appropriate swallowing evaluation and intervention.
Dysphagia is associated with several problematic outcomes. The severity of dys-
phagia ranges from mild difficulty to complete inability to swallow and may subse-
quently give rise to aspiration pneumonia, suffocation, dehydration, malnutrition,
and declining quality of life. From the viewpoint of rehabilitation medicine, swal-
lowing is one of the major targets of “activity medicine” (medicine to improve func-
tion). Thus, physiatrists and all therapists who play a role in dysphagia management
require fundamental knowledge and skills in evaluation and intervention to facili-
tate safe swallowing and prevent recurrence and other adverse events.
A team approach is indispensable to dysphagia rehabilitation. Interdisciplinary
teamwork is a complex process in which staff members from different disciplines
work together to share expertise, knowledge, and skills to provide the highest stan-
dard of care to patients with dysphagia. Another team approach that involves a joint
effort from varying disciplines and is particularly suitable for dysphagia rehabilita-
tion is the transdisciplinary teamwork model. In this model, participating disciplines
collaboratively develop a total healthcare plan that addresses all necessary diagno-
ses and treatments. The Japanese Society of Dysphagia Rehabilitation (JSDR) was
founded under the concept of transdisciplinary teamwork [14].
Swallowing teams include specialists from different disciplines, such as physiat-
rists, dentists, speech-language-hearing therapists, dysphagia-certified nurses, ward
nurses, dental hygienists, and dieticians. However, the team may be led by different
practitioners based on availability. In Japan, for example, a teamwork-centered
approach to dysphagia rehabilitation is emphasized, and speech-language-hearing
therapists lead the team in implementing direct and indirect dysphagia training exer-
cises and integrating comprehensive treatment with other disciplines. In other Asian
countries, such as Thailand, occupational therapists primarily provide dysphagia
rehabilitation services in the form of exercise training regimens for patients with
swallowing disorders.
JSDR is a leader in the development and advancement of dysphagia rehabilita-
tion in both clinical and research settings. During the past 20 years, the membership
of the JSDR has rapidly risen to more than 11,000 medical professionals (11,653 as
of 30 August 2014) from several disciplines (Fig. 5).
Moreover, the JSDR is currently developing relationships with other dysphagia
societies in North America, Europe, Asia, and elsewhere across the world to pro-
mote international collaboration in the emerging field of deglutition.
Overview xi

Fig. 5 Disciplines Occupational therapist

Others
comprising the Japanese Physical therapist
Society of Dysphagia
Rehabilitation. DH dental 4%
hygienist, OT occupational 2%
2%
therapist, PT physical
therapist, SLHT speech- 8%
language-hearing therapist Nutritionist
34%

8%
Speech-language-hearing
Dental hygienist
therapist

Physician
8%

Nurse
Dentist
14%
20%

© FHUR 2017

In many Asian countries, dysphagia has become a pressing issue for both phys-
iatrists and rehabilitation therapists. Unfortunately, there may be limited recogni-
tion of the prevalence of dysphagia and dysphagia professionals despite the
effectiveness of a dysphagia healthcare team. Furthermore, many clinicians are still
unfamiliar with dysphagia and lack detailed guidance and practice protocols.
Individual clinicians may assess and treat dysphagia differently, complicating
research methodology and development of practice consensus. Additionally, patients
who present with rare etiologies or subtle signs and symptoms of dysphagia may
pose a challenge to clinicians with limited practice.
Instrumental evaluation is necessary to a comprehensive assessment of swallow-
ing of both known and undiagnosed etiologies. Imaging is critical for diagnosing
the cause of dysphagia, selecting optimal treatments, and assessing the effects of
treatment by accurate measurement of the oropharyngeal swallowing response. The
instrumental assessment of dysphagia is a relatively new area of expertise within the
field of rehabilitation that has developed over the past several decades in Asian
countries. Additionally, considering the shortage of formal dysphagia rehabilitation
teams with several specialized clinicians, highly trained professionals are essential
for dysphagia management in all settings.
The purpose of this book is to provide all healthcare professionals who are inter-
ested in swallowing with the basic practical knowledge required for a broad clinical
perspective on dysphagia rehabilitation. This book is neither exhaustive nor ency-
clopedic; instead, it presents a practical approach to the management and treatment
of patients with dysphagia in a real-world clinical setting.
xii Overview

This book is divided into four parts. Part I introduces the general aspects of
deglutition and dysphagia with a focus on anatomy and physiology. Part II discusses
clinical approaches using both non-instrumental and instrumental evaluation of
swallowing. The instrumental evaluations presented include videofluoroscopy,
which is considered the gold standard evaluation technique for swallowing ­disorders,
videoendoscopy, and, in brief, 320-row area detector computed tomography, which
was recently introduced to analyze three-dimensional swallowing kinematics.
Part III addresses the management and treatment of swallowing disorders. Finally,
Part IV presents case studies that demonstrate clinical approaches to dysphagia as
well as common etiologies encountered in a clinical setting.
The contents of this book follow the model of dysphagia rehabilitation used at
FHUR. The Fujita Swallowing Team hopes that it will guide healthcare ­professionals
at all levels and serve as an excellent starting point for the development of expertise
in swallowing rehabilitation.

References

1. United Nations, Department of Economic and Social Affairs, Population

Division. World Population Ageing 2013. ST/ESA/SER.A/348. 2013.
2. Kuzuya M. Process of physical disability among older adults — contribution of
frailty in the super-aged society. Nagoya J Med Sci. 2012;74:31–7.
3. Population estimates by Age. Statistics Bureau, Ministry of Internal Affairs and
Communications website. 2015. http://www.stat.go.jp/english/index.htm.
Accessed 31 July 2015.
4. Situation of The Thai Elderly 2013, Foundation of Thai Gerontology Research
and Development Institute (TGRI). 2013. http://thaitgri.org/?p=37134.
Accessed 31 July 2015.
5. UN Department of Economic and Social Affairs, Population Division, 2001,
World Population Ageing 1950–2050. 2014. http://ageingasia.org/ageing-
population-­thailand1/. Accessed 31 July 2015.
6. The World Health Organization (WHO). 2012. http://www.who.int/mediacen-
tre/factsheets/en/. Accessed 24 October 2017.
7. The demographic population survey by Ministry of Health, Labour and Welfare.
2014. http://www.mhlw.go.jp/toukei/saikin/hw/jinkou/geppo/nengai14/dl/gai-
kyou26.pdf (Japanese). Accessed 31 July 2015.
8. National Statistical Office. Office of the Permanent Secretary for Public Health,
Ministry of Public Health, Thailand. 2014. http://www.nso.go.th/ (Thai).
Accessed 31 July 2015.
9. Reechaipichitkul W, Thavornpitak Y, Sutra S. Burden of adult pneumonia in
Thailand: a nationwide hospital admission data 2010. J Med Assoc Thai.
2014;97(3):283–92.
10. The e-Stat data (an official site of Japanese Government Statistics) by Ministry
of Internal Affairs and Communications. http://www.e-stat.go.jp/SG1/estat/
List.do?lid=000001137965 (Japanese). Accessed 31 July 2015.
Overview xiii

11. Teramoto S, Fukuchi Y, Sasaki H, Sato K, Sekizawa K, Matsuse T, et al. High

incidence of aspiration pneumonia in community and hospital-acquired pneu-
monia in hospitalized patients: a multicenter, prospective study in Japan. J Am
Geriatr Soc. 2008;56:577–9.
12. Saitoh E, et al. Survey of distribution of dysphasia patients using Dysphagia
Severity Scale 2012 Grant-in-aid of Geriatric Health promotion project, Report
of achievement in investigation research of swallowing disorders.
13. Sugiyama M, Takada K, Shinde M, Matsumoto N, Tanaka K, Kiriya Y, et al.
National survey of the prevalence of swallowing difficulty and tube feeding use
as well as implementation of swallowing evaluation in long-term care settings
in Japan. Geriatr Gerontol Int. 2014;14(3):577–81.
14. Saitoh E, Matsuo K, Inamoto Y, Ishikawa M, Tsubahara A. Twenty years of
trans-disciplinary approach development for dysphagia rehabilitation in Japan.
Dysphagia. 2015;30(1):102–3.

Toyoake, Aichi, Japan Eiichi Saitoh

Toyoake, Aichi, Japan Kannit Pongpipatpaiboon
Toyoake, Aichi, Japan Yoko Inamoto
Toyoake, Aichi, Japan Hitoshi Kagaya
Acknowledgments

This book would not be possible without the gracious support, unfaltering patience,
and shared expertise of our coauthors and all the members of the Fujita Swallowing
Team. We are fortunate to have a strong transdisciplinary team approach for dyspha-
gia rehabilitation, and we believe our team provides an excellent model for the
management of dysphagic patients. We would like to express our deep appreciation
and sincerest thanks to Professor Jeffrey B. Palmer, our mentor, for his significant
contributions, to Dr. Rachel Mulheren for editorial assistance, and to Dr. Cathy
Lazarus for providing patient instruction on how to perform the Effortful swallow.
And we must thank our patients, who generously participated in some of the imag-
ing studies presented in this text.

xv
Contents

Part I Overview and Physiology

1 Overview of Structures and Essential Terms. . . . . . . . . . . . . . . . . . . . . .   3
Kannit Pongpipatpaiboon, Yoko Inamoto, Koichiro Matsuo,
Yoichiro Aoyagi, Seiko Shibata, and Hitoshi Kagaya
2 Evolution and Development of Human Swallowing . . . . . . . . . . . . . . . . 11
Kannit Pongpipatpaiboon, Yoko Inamoto, Koichiro Matsuo,
Yoichiro Aoyagi, Seiko Shibata, and Hitoshi Kagaya
3 Physiological Models of Swallowing. . . . . . . . . . . . . . . . . . . . . . . . . . . . . 17
Kannit Pongpipatpaiboon, Yoko Inamoto, Koichiro Matsuo,
Yoichiro Aoyagi, Seiko Shibata, and Hitoshi Kagaya

Part II Clinical Approaches

4 Dysphagia from the Viewpoint of Rehabilitation Medicine. . . . . . . . . . 29
Kannit Pongpipatpaiboon, Yoko Inamoto, Yoichiro Aoyagi,
Seiko Shibata, Hitoshi Kagaya, and Koichiro Matsuo
5 Clinical Evaluation of Dysphagia . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 35
Kannit Pongpipatpaiboon, Yoko Inamoto, Yoichiro Aoyagi,
Seiko Shibata, Hitoshi Kagaya, and Koichiro Matsuo

Part III Treatment

6 Oral Hygiene Care . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 101
Yoko Inamoto, Kannit Pongpipatpaiboon, Seiko Shibata,
Yoichiro Aoyagi, Hitoshi Kagaya, and Koichiro Matsuo
7 Swallowing Exercises . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 109
Yoko Inamoto, Kannit Pongpipatpaiboon, Seiko Shibata,
Yoichiro Aoyagai, Hitoshi Kagaya, and Koichiro Matsuo

xvii
xviii Contents

8 Other Swallowing Treatments. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 157

Yoko Inamoto, Kannit Pongpipatpaiboon, Seiko Shibata,
Yoichiro Aoyagai, Hitoshi Kagaya, and Koichiro Matsuo

Part IV Case Studies

9 Case Studies. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 167
Yoko Inamoto, Kannit Pongpipatpaiboon, Seiko Shibata,
Yoichiro Aoyagai, Hitoshi Kagaya, and Koichiro Matsuo

Index. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 195
About the Editors

Eiichi Saitoh, MD, DMSc

Physiatrist, Executive Vice President of Fujita Health University,
Professor and Chairperson of Department of Rehabilitation
Medicine I, School of Medicine, Fujita Health University, Toyoake,
Aichi, Japan

Kannit Pongpipatpaiboon, MD
Physiatrist, Research Fellow of Department of Rehabilitation
Medicine I, School of Medicine, Fujita, Health University,
Toyoake, Aichi, Japan

Yoko Inamoto, SLHT, PhD

Speech-Language-Hearing Therapist, Associate Professor of
Faculty of Rehabilitation, School of Health Sciences, Fujita Health
University, Toyoake, Aichi, Japan

Hitoshi Kagaya, MD, DMSc

Physiatrist, Professor of Department of Rehabilitation Medicine I,
School of Medicine, Fujita Health University, Toyoake, Aichi,
Japan

xix
About the Authors

Seiko Shibata, MD, DMSc

Physiatrist, Senior Assistant Professor of Department of
Rehabilitation Medicine, School of Medicine, Fujita Health
University, Toyoake, Aichi, Japan

Yoichiro Aoyagi, MD, PhD

Physiatrist, Associate Professor of Department of Rehabilitation
Medicine I, School of Medicine, Fujita Health University, Toyoake,
Aichi, Japan

Koichiro Matsuo, DDS, PhD

Dentist, Professor and Chairperson of Department of Dentistry,
School of Medicine, Fujita Health University, Toyoake, Aichi,
Japan

xxi
Abbreviations

3D Three-dimensional
320-ADCT 320-row area detector CT
ADL Activities of daily living
CT Computed tomography
DSS Dysphagia Severity Scale
EMST Expiratory muscle-strengthening exercise
ESS Eating Status Scale
FHUR Fujita Health University Rehabilitation Complex
FIM Functional independence measure
HRM High-resolution manometry
JSDR Japan Society of Dysphagia Rehabilitation
LES Lower esophageal sphincter
MEP Maximum expiratory pressure
mGy Milligray
MPR Multiplanar reconstruction
mSv Millisievert
MWST Modified water swallowing test
NG Nasogastric tube
RSST Repetitive saliva swallowing test
SLHT Speech-language-hearing pathologist
SWR Swallowing ward rounds
Threshold PEP™ Threshold positive expiratory pressure device
TOR-BSST© Toronto Bedside Swallowing Screening Test
TVFs True vocal folds
UES Upper esophageal sphincter
VE Videoendoscopy
VF Videofluorography
WST Water swallowing test
W/V Weight/Volume

xxiii
 Part I
Overview and Physiology
Chapter 1
Overview of Structures and Essential Terms

Kannit Pongpipatpaiboon, Yoko Inamoto, Koichiro Matsuo,

Yoichiro Aoyagi, Seiko Shibata, and Hitoshi Kagaya

Abstract This chapter discusses common dysphagia terminology. A common

understanding of important terms relevant to dysphagia enables healthcare
­professionals to communicate clearly and rapidly. The basic knowledge of ana-
tomical structures associated with swallowing is fundamental to understanding
the whole swallow process including the evaluation and treatment of
dysphagia.

1.1 Terminology of Dysphagia

Swallowing is one of the most frequent activities of humans. Swallowing serves as

a vital primary function to ensure nutrition and hydration and contributes to quality
of life. Specific terminology is used among healthcare workers to communicate in
a common language and is used every day for speaking and writing in medical
charts.
A description of the common terms used in the field of dysphagia is provided in
Table 1.1.

K. Pongpipatpaiboon • Y. Aoyagi • S. Shibata • H. Kagaya

Department of Rehabilitation Medicine I, School of Medicine, Fujita Health University,
Toyoake, Aichi, Japan
e-mail: ning665@gmail.com; yyy@rc5.so-net.ne.jp; sshibata@fujita-hu.ac.jp;
hkagaya2@fujita-hu.ac.jp
Y. Inamoto (*)
Faculty of Rehabilitation, School of Health Sciences, Fujita Health University,
Toyoake, Aichi, Japan
e-mail: inamoto@fujita-hu.ac.jp
K. Matsuo
Department of Dentistry, School of Medicine, Fujita Health University, Toyoake, Aichi, Japan
e-mail: kmatsuo@fujita-hu.ac.jp

© Springer Nature Singapore Pte Ltd. 2018 3

E. Saitoh et al. (eds.), Dysphagia Evaluation and Treatment,
https://doi.org/10.1007/978-981-10-5032-9_1
4 K. Pongpipatpaiboon et al.

Table 1.1 Terminology of dysphagiaa

Swallowing/deglutition A series of movements that promote bolus transportation from the
mouth to the stomach
Eating/ingestion The process of taking a bolus into the body by mouth
Eating disorder A psychological disorder characterized by abnormal or disturbed
eating behaviors (e.g., anorexia nervosa, bulimia nervosa)
Dys- Impaired or abnormal
Phag- Eating
Eating problem/dysphagia Eating failure or dysfunction, defined as a disturbance of the
passage of a swallowed bolus from the mouth to the stomach
Aspiration Entry of saliva, liquid, or food into the airway under the level of
the true vocal folds
Penetration Entry of swallowed material into the laryngeal vestibule during
swallowing, as above of the level of the true vocal folds
Retention Presence of a residual swallowed bolus locating in the oral cavity,
vallecula, and/or hypopharynx (pyriform sinus) that is left behind
after the swallow
Additional terminology is shown in Appendix (Table 1.2)
a

1.2 Overview of Structures

Fundamental knowledge of the anatomy and motor control of eating and

­swallowing is imperative and serves as an important basis for evaluating the
physiology of the swallow. Swallowing is a complicated sequence of move-
ments. A normal swallow requires the precise coordination of more than 30
muscles located within and around the oral cavity, pharynx, larynx, and esopha-
gus. These muscles are controlled by cranial and peripheral nerves that are cen-
trally mediated via the brain stem (mainly the medulla oblongata as the
swallowing center) and cooperate with the cortical and subcortical regions of
the brain [1, 2].

1.2.1 Anatomical Structures [1–3]

The oral cavity serves as the entrance to both the digestive pathway and upper
airway. The tongue rests on the floor on the mouth, exposing both the oral and
pharyngeal surfaces. The arched opening of the posterior oral cavity is bordered
by the fauces, which separate the oral cavity from the pharynx. The pharyngeal
wall consists of three main pharyngeal constrictor muscle groups (the superior,
middle, and inferior parts) and long pharyngeal muscles (stylopharyngeus, salpin-
gopharyngeus, and palatopharyngeus). The upper esophageal sphincter (UES) is
defined as a high-­pressure zone located at the pharyngoesophageal junction and
1 Overview of Structures and Essential Terms 5

has a semicircular shape in the horizontal view. It consists of three muscular por-
tions: the inferior fibers of the inferior pharyngeal constrictor, the cricopharyngeal
muscle, and the upper fibers of the esophagus. The UES ­contracts at rest and
relaxes during swallowing to allow a swallowed bolus to enter the esophagus and
to prevent regurgitation of bolus from esophagus and stomach (Figs. 1.1 and 1.2).
The hyoid bone plays an important role in swallowing function. The suprahy-
oid muscles, which include the mylohyoid, geniohyoid, anterior and posterior
bellies of the digastric, and stylohyoid, and one of the infrahyoid muscles,
­thyrohyoid, play one of the key roles in opening of the UES because they control
hyoid and laryngeal excursion in the superoanterior direction, allowing a bolus
to pass into the esophagus. The larynx acts as an airway valve, separating the
trachea from the upper aerodigestive tract. The airway is protected by laryngeal
closure, a process that occurs at three levels: approximation of the true vocal
folds (TVFs, glottis), approximation of the false vocal folds, and approximation
of the aryepiglottic folds to the base of the epiglottis. The tongue base, pharynx,
epiglottis, larynx, and UES comprise the oropharynx and hypopharynx. Three
pockets or recesses exist in the oropharyngeal area (vallecula) and in the
­hypopharyngeal area (two pyriform sinuses), providing a physiologic storage
area for food and fluid and decreasing the risk of aspiration. Figure 1.1 provides
an ­overall image of the anatomical structures in the oral cavity, pharynx, and
larynx. The swallowing muscles that contribute to the pharyngeal stage are illus-
trated in Appendix (Figs. 1.4 and 1.5).

Base of skull
(basilar part of occipital bone)
Nasal septum

Nasal cavity Pharyngeal

Soft palate
Nasopharynx recess
Hard palate
Vallecula
Soft palate

Lip Pharynx Uvula

Oropharynx Root of tongue
Tongue Epiglottis Epiglottis
Oral cavity Laryngeal inlet
Pyriform sinus
Aryepiglottic fold
Mandible Larynx Cuneiform tubercle
Laryngopharynx Corniculate tubercle
Hyoid bone Esophagus
Piriform fossa
Thyroid cartilage Interarytenoid notch
(Adam’s apple)
Vocal cord Trachea
Prominence over
Esophagus lamina of cricoid
cartilage

Trachea
© FHUR 2017

Fig. 1.1 Illustration of the anatomical structures (including oral cavity, pharynx, and larynx)
­contributing to the swallowing function
6 K. Pongpipatpaiboon et al.

Fig. 1.2 Two-plane computed tomography images of the upper esophageal sphincter illustrate its
semicircular shape in the horizontal view at the pharyngoesophageal junction

Fig. 1.3 Diagram of neural Cerebral cortex

control of the pharyngeal
stage of swallowing. NTS
nucleus tractus solitaries; Afferent fibers
BS-SW brain stem swallowing
center; CPG central NTS (dorsal)
pattern generator; BS-SW (CPG)
VLM ventrolateral medulla;
NA nucleus ambiguous
VLM (ventral)

Motor neurons NA

Sensory receptors in the

oropharynx, laynx, and V VIII IX X XII C1-3
esophagus:
CN V, VII, IX, X Swallowing muscles
© FHUR 2017

1.2.2 Neural Control of Swallowing [1, 4]

Swallowing is a dynamic process involving complex neuronal networks with voli-

tional and reflexive components. The parts of the central nervous system that con-
trol swallowing are mainly the supratentorium (cortical and subcortical cortex) and
infratentorium (brain stem). These central networks collaborate with the peripheral
nervous system, including several cranial nerves that control sensorimotor swallow-
ing function, to integrate coordination of several structures and muscles as illus-
trated in Fig. 1.3 and Appendix (Table 1.3).
1 Overview of Structures and Essential Terms 7

Appendix

Additional Terminology of Dysphagia

Table 1.2 Additional terminology of dysphagia
Drooling Defined as flowing of food, liquid, or saliva outside of the mouth
unintentionally
Nasal regurgitation Passing out of food from the oral cavity into the nasal cavity
Pharyngeal Swallowed bolus flows back into the pharynx through the junction of
regurgitation pharynx and esophagus passing the cricopharyngeal sphincter
Gastroesophageal Retrograde movement of the stomach’s contents back up into the
regurgitation esophagus

Swallowing Muscles Contributing to the Pharyngeal Stage

Tensor veli palatini m.

Levator veli palatini m.

Buccinator m.

Superior pharyngeal constrictor m.

Styloglossus m.
Stylohyoid ligament
Stylopharyngeus m.
Middle pharyngeal constrictor m.

Hyoglossus m.

Digastric m.
(anterior belly) Mylohyoid m. Thyrohyoid membrane

Hyoid bone Inferior pharyngeal constrictor m.

Thyroid cartilage

Cricothyroid ligament Cricopharyngeus m.

(part of inferior pharyngeal constrictor)
Cricothyroid m.
Esophagus
Cricoid cartilage

Trachea
© FHUR 2017

Fig. 1.4 Lateral view of the pharynx illustrating constrictor and suspensory muscles of the
­pharynx as viewed from the side (m muscle)
8 K. Pongpipatpaiboon et al.

Basilar part of occipital bone

Levator veli palatini m.

Digastric m. Salpingopharyngeus m.
(posterior belly)
Stylohyoid m. Superior pharyngeal constrictor m.
Uvula
Medial pterygoid m.
Palatopharygeus m.
Stylopharngeus m. Middle pharyngeal constrictor m.
Superior pharyngeal
constrictor m. Stylopharyngeus m.
Middle pharyngeal Longitudinal
constrictor m. pharyngeal m.
Epiglottis
Arytenoid m.
Inferior pharyngeal constrictor m. (Transverse and oblique)
Pharyngeal aponeurosis
Cuneiform tubercle
Posterior cricoarytenoid m.
Corniculate tubercle Cricopharyngeus m.
(part of inferior pharyngeal constrictor)
Cricopharyngeus m. Circular esophageal m.
(part of inferior pharyngeal constrictor)
Longitudinal esophageal m.

© FHUR 2017

Fig. 1.5 Pharyngeal muscles seen in the posterior view and with the right side of the pharynx cut
open, allowing it to be viewed from the inside (m muscle)

Neural Control of Swallowing

Table 1.3 Major swallowing-related muscles, innervations, and actions

Category Muscle Innervation Action
Base of tongue Hyoglossus XII Retraction of base of tongue
Styloglossus
Palatoglossus X
Pharyngeal Superior pharyngeal X Generating positive pressure to the
constrictors constrictor bolus tail through superiorly to
Middle pharyngeal inferiorly sequential contractions
constrictor
UES Thyropharyngeus
Cricopharyngeus Contracting tonically at rest and
relaxing during swallowing
Long Stylopharyngeus X Pharyngeal shortening, assisting
pharyngeus Salpingopharyngeus X laryngeal elevation
Palatopharyngeus X
1 Overview of Structures and Essential Terms 9

Table 1.3 (continued)

Category Muscle Innervation Action
Suprahyoid Geniohyoid C1 Hyolaryngeal superoanterior
Mylohyoid V movement of trajectory
Digastrics V
Stylohyoid VII
Infrahyoid Thyrohyoid XII, C1 Depressing and posteriorly displacing
Sternohyoid C1–C3 hyoid and larynx
Sternothyroid
Omohyoid

References

1. Shaw SM, Martino R. The normal swallow: muscular and neurophysiological control.
Otolaryngol Clin N Am. 2013;46(6):937–56. doi:10.1016/j.otc.2013.09.006.
2. Matsuo K, Palmer JB. Anatomy and physiology of feeding and swallowing: normal and abnor-
mal. Phys Med Rehabil Clin N Am. 2008;19(4):691–707.
3. Logemann JA. Evaluation and treatment of swallowing disorders. 2nd ed. Austin, TX: Pro-Ed;
1998.
4. Malandraki G, Robbins J. Dysphagia. In: Barnes MP, Good DC, editors. Handbook of clinical
neurology, vol. 110. New York: Elsevier; 2013. p. 255–71.
Chapter 2
Evolution and Development
of Human Swallowing

Kannit Pongpipatpaiboon, Yoko Inamoto, Koichiro Matsuo,

Yoichiro Aoyagi, Seiko Shibata, and Hitoshi Kagaya

Abstract This chapter will describe the human swallowing in comparison with
other mammals.
Besides, the context will focus on swallowing and feeding development in
infants. The basic knowledge of how evolutionary and developmental changes of
human swallowing allows an insight into which swallowing-related problems may
directly relate.

An understanding of the evolution of human swallowing begins from a comparative

mammalian context. The larynx is a focal point in this comparison. Many other
mammals, such as the rat, horse, pig, cat, and others, have remarkably similar ana-
tomical templates of the structures involved in swallowing (Fig. 2.1).
The position of the larynx is relatively high in the neck relative to the base of the
cranium. The larynx is located in the opening of the intranarial array, providing a
continuous airway from the nose to the lungs. Other than the anatomically high
position of the larynx in many other mamals, the part of the epiglottis that touches
or overlaps above the soft palate (so-called intranarial larynx) permits the margins
of the soft palate to seal the airway from food passage. This structure enables the
larynx to open directly into the nasopharynx and generates a physical separation of
the two pathways (breathing and swallowing) to ensure survival. Furthermore, the

K. Pongpipatpaiboon • Y. Aoyagi • S. Shibata • H. Kagaya

Department of Rehabilitation Medicine I, School of Medicine, Fujita Health University,
Toyoake, Aichi, Japan
e-mail: ning665@gmail.com; yyy@rc5.so-net.ne.jp; sshibata@fujita-hu.ac.jp;
hkagaya2@fujita-hu.ac.jp
Y. Inamoto (*)
Faculty of Rehabilitation, School of Health Sciences, Fujita Health University,
Toyoake, Aichi, Japan
e-mail: inamoto@fujita-hu.ac.jp
K. Matsuo
Department of Dentistry, School of Medicine, Fujita Health University, Toyoake, Aichi, Japan
e-mail: kmatsuo@fujita-hu.ac.jp

© Springer Nature Singapore Pte Ltd. 2018 11

E. Saitoh et al. (eds.), Dysphagia Evaluation and Treatment,
https://doi.org/10.1007/978-981-10-5032-9_2
12 K. Pongpipatpaiboon et al.

Fig. 2.1 Illustration of the Nasal cavity

midsagittal section of the
head and neck regions of
the horse

Tongue

Oral cavity
Hyoid bone
Intranatial larynx

Esophagus
© FHUR 2017

Enlarged pharynx

Posterior part of tongue is

totally inside the oral cavity
Posterior part of tongue
connects with pharynx

Relatively low larynx © FHUR 2017

Fig. 2.2 Comparative oropharyngolaryngeal structures between humans and other mammals

tongue in other mammals lies almost entirely within the oral cavity; no portion is
present in the pharyngeal part [1, 2].
Comparison of the oropharyngolaryngeal anatomy in humans and other mam-
mals (Fig. 2.2) illustrates three main principles of swallowing:
1. In the standing position, the oral and pharyngeal regions in humans are at a right
angle to each other, bending sharply at 90°, as shown in Fig. 2.2. In contrast, the
angle between the oral and pharyngeal regions is relatively flat in other mam-
mals. This means that in humans, liquid easily enters the larynx before flowing
into the esophagus.
2. The pharynx of other mammals is comparatively small, with the laryngeal open-
ing to the nasal cavity (intranarial larynx). This structure therefore serves as a
protective mechanism to prevent aspiration during swallowing.
3. The entire posterior part of other mammals’ tongues is located inside the mouth.
In contrast, the posterior part of the human’s tongue is connected to the pharynx,
forming part of the anterior pharyngeal wall (Fig. 2.3).
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Capm. xv. O quam virginitas prior omni laude refulget,
Agnum que sequitur cuncta per arua poli;
Splendet et in terris deitati nupta, relinquens
650 Corporis humani que genus acta docet.
Fetet vt incasta, fragrat sine labe pudica,
Ista deum retinet, illa cadauer habet.
Centeno trina fructu cumulata perornant
Virginis ante deum florida serta caput:
Angelicas turmas transcendit virginis ordo,
Quam magis in celo trina corona colit.
Iura sequens aquile mens virginis alta cupiscens
Celsius ante deum, teste Iohanne, volat.
Vt rosa de spinis oriens supereminet illas,
660 Sic superat reliquos virginis ille status;
Vt margarita placet alba magis preciosa,
Sic placet in claustro virgo professa deo.443
Talis enim claustris monialis dignior extat
Sanccior et meritis, dum sua vota tenet.
Set quecumque tamen sub velo claustra requirit,
Regula quam seruat sanctificabit eam:
Si fuerit mulier bona, reddit eam meliorem,
Moribus et mores addit vbique magis;
Si polluta prius sit quam velata, que caste
670 Ammodo viuat, erit preuia culpa nichil.
Non licet ergo viris monachas violare sacratas,
Velum namque sacrum signa pudica gerit.
Alterius sponsam presumens deuiolare,
Quam graue iudiciis perpetrat ipse scelus!
Crede tamen grauius peccat, qui claustra
resoluens
Presumit sponsam deuiolare dei.

Postquam tractauit de illis qui in religione

possessoria sui ordinis professionem
offendunt, dicendum est iam de hiis qui errant
in ordine fratrum mendicancium; et primo dicet
 de illis qui sub ficte paupertatis vmbra terrena
lucra conspirantes, quasi tocius mundi
dominium subiugarunt.

Capm. xvi. Dum fuit in terris, non omnes quos sibi legit
Cristus, erant fidi, lege nouante dei:
Non tamen est equm, quod crimen preuaricantis
680 Ledat eos rectam qui coluere fidem.
Sic sterilis locus est nullus, quod non sit in illo
Mixta reprobatis vtilis herba malis;
Nec fecundus ita locus est, quo non reprobata
Mixta sit vtilibus herba nociua bonis:
Tam neque iustorum stat concio lata virorum,
Est quibus iniusti mixtio nulla viri.
Sic excusandos, quos sanctos approbat ordo,
Fratres consimili iure fatetur opus:
Non volo pro paucis diffundere crimen in omnes,
690 Spectetur meritis quilibet immo suis;
Quos tamen error agit, veniens ego nuncius illis,
Que michi vox tribuit verba loquenda fero.
Sicut pastor oues, sic segregat istud ab edis
Quos opus a reprobis senserit ordo probos:
Que magis huius habet vocis sentencia scribam
Hiis quos transgressos plus notat ordo reos.
Crimina que Iudas commisit ponere Petro
Nolo, ferat proprium pondus vterque suum.
Ordinis officia fateor primi fore sancta,
700 Eius et auctores primitus esse pios;
Hos qui consequitur frater manet ille beatus,
Qui mundum renuens querit habere deum,
Qui sibi pauperiem claustralis adoptat, et vltro
Hanc gerit, et paciens ordinis acta subit:
Talis enim meritis extat laudabilis altis,
Eius nam precibus viuificatur humus.
Set sine materia qui laruat in ordine formam,
Predicat exterius, spirat et intus opes,
Talibus iste liber profert sua verba modernis,
710 Vt sibi vox populi contulit illa loqui.
Ordine mendico supervndat concio fratrum,
De quibus exvndans regula prima fugit:
Molles deveniunt tales, qui dura solebant
Ordinis ex voto ferre placenda deo.
Acephalum nomen sib i d a n t primo statuendum,
Seque vocant inopes fert quibus omnis opem:
Cristi discipulos affirmant se fore fratres,
Eius et exempli singula iura sequi:
Hoc mentita fides dicit, tamen hoc satis illis
720 Conuenit, vt dicunt qui sacra scripta sciunt.
Sunt quasi nunc gentes nil proprietatis habentes,
Et tamen in forma pauperis omne tenent.
Gracia si fuerit aut fatum fratribus istis
Nescio, set mundus totus habundat eis.
In manibus retinent papam, qui dura relaxat
Ordinis et statuit plura licere modo;
Et si quas causas pape negat ipsa potestas,
Clam faciet licitas ordo sinister eas.
Nec rex nec princeps nec magnas talis in orbe est,
730 Qui sua secreta non fateatur eis.
Et sic mendici dominos superant, et ab orbe
Vsurpant tacite quod negat ordo palam.
Non hos discipulos, magis immo deos fore dicam,
Mors quibus et vita dedita lucra ferunt:
Mortua namque sibi, quibus hic confessor adhesit,
Corpora, si fuerint digna, sepulta petit;
Set si corpus inops fuerit, nil vendicat ipse,
Nam sua nil pietas, sint nisi lucra, sapit.
Baptizare fidem nolunt, quia res sine lucro
740 Non erit in manibus culta vel acta suis.
Vt sibi mercator emit omne genus specierum,
Lucra quod ex multis multa tenere queat;
Sic omnes mundi causas amplectit auarus
Frater, vt in variis gaudeat ipse lucris.
Hii sunt quos retinens mundus non horruit, immo
Diligit, hiisque statum tradidit ipse suum:
 Istos conuersos set peruersos magis esse
Constat, vt ex factis nomina vera trahant.
Transtulit a vite se palmes sic pharisea,
750 Eius et in gustu fructus acerbus olet.

Hic loquitur de fratribus illis, qui per

ypocrisim predicando populi peccata publice
redarguentes, blandiciis tamen et voluptatibus
clanculo deseruiunt.

Capm. xvii. Seminat ypocrisis sermones dedita fratris,

Messis vt inde sui crescat in orbe lucri.
Horrida verba tonat, dum publica per loca dampnat
Vsum peccandi seruus vt ipse dei;
Seruus et vt Sathane, priuatis cum residere
Venerit in thalamis, glosa remittit eis;
Et quos alta prius stimulabat vox reboantis,
Postera blandicies vnget in aure leuis:
Et sic peccator aliis peccata ministrat,
760 Namque fouens vicium percipit inde lucrum.
Hoc bene scit frater, peccatum cum moriatur,
Tunc moritur lucrum tempus in omne suum.
Dic vbi ter veniet frater, nisi lucra reportet,
Est vbi sors vacua, non redit ipse via.
De fundamentis fratrum si crimina tollas,
Sic domus alta diu corruet absque manu.
O quam prophete iam verificantur Osee
Sermones, qui sic vera locutus ait:
‘In terris quedam gens surget, que populorum
770 Peccatum comedet et mala multa sciet.’
Hancque propheciam nostris venisse diebus
Cernimus, atque notam fratribus inde damus,
Ad quorum victum, fuerit quodc u m q u e
n e c e s s e,
Sors de peccatis omne ministrat eis.
Delicie tales non sunt, que fratribus escam,
 Si confessores sint, aliquando negant.
Aspicis vt veniunt ad candida tecta columbe,
Nec capiet tales sordida turris aues:
Sic nisi magnatum dat curia nulla modernis
780 Fratribus hospicium quo remanere volunt.
Horrea formice tendunt ad inania numquam,
Nec vagus amissas frater adibit opes:
Immemores florum gestaminis anterioris,
Contempnunt spinam cum cecidere rose;
Sic et amicicie fratres benefacta prioris
Diuitis aspernunt, cum dare plura nequit.
Nomine sunt plures, pauci tamen ordine fratres;
Vt dicunt aliqui, Pseudo prophetat ibi.
Est facies tunice pauper, stat cistaque diues,
790 Sub verbis sanctis turpia facta latent:
Sic sine pauperie pauper, sanctus sine Cristo,
Eminet ille bonus, qui bonitate caret.
Ore deum clamant isti, venerantur et aurum
Corde, viam cuius vndique scire volunt.
Omnia sub pedibus demon subiecit eorum,
Ficta set ypocrisis nil retinere docet:
Sic mundana tenet qui spernit in ordine mundum,
Dum tegit hostilem vestis ouina lupum;
Et sic ficticiis plebs incantata putabit444
800 Sanctos exterius, quos dolus intus habet.
Vix est alterius fraudem qui corripit vnus,
Set magis vt fallant auget vterque dolos:
Sic magis infecti morbo iactantur eodem,
Inficiuntque suis fraudibus omne solum.
Comprimat hos dominus saltem, quos nouit in isto
Tempore primeuam preuaricare fidem.
Non peto quod periant, set fracti consolidentur,445
Et subeant primum quem dedit ordo statum.

Hic loquitur de fratribus illis, qui propter

huius mundi famam, et vt ipsi eciam, quasi ab
 ordinis sui iugo exempti, ad confessiones
audiendum digniores efficiantur, summas in
studio scole cathedras affectant.

Capm. xviii. Est qui precessor fiat velut ipse minister,

810 Cuius in exemplum Cristus agebat idem:
Set qui discipulum Cristi se dicit, ad altum446
Cum venit ipse statum, non tenet inde modum.
Quamuis signa tenet mendici pauperis, ecce
Frater honore suum spirat habere locum:
Appetit ipse scolis nomen sibi ferre magistri,
Quem post exemptum regula nulla ligat:
Solus habet cameram, propriat commune, que
nullum
Tunc sibi claustralem computat esse parem.
Vt latriam statuis claustrales ferre magistris
820 Debent et pedibus flectere colla suis:
Sic tumor et pompa latitant sub theologia,
Ducere nec duci dum fauet ordo sibi.
Tunc thalamos penetrat sublimes, curia nulla
Est cuius porta clauditur ante virum.
Aspiciens varias species variatur et ipse
Camelion, et tot signa coloris habet:
Frater ei similis, perpendens velle virorum,
Vult in consimili par sit vt ipse pari;
Et quia sic similem sibi sentit curia fratrem,
830 Eius in aduentu presulis acta vacant.
Circuit exterius, explorat et interiora,
Non opus occultum nec locus extat ei:
Nunc medicus, nunc confessor, nunc est mediator,
Et super et subtus mittit ad omne manum.
Spiritus vt domini, sic frater spirat vbique,
Et venit ad lectum quando maritus abest:
Sic absente viro temerarius intrat adulter
Frater, et alterius propriat acta sibi:
Sic venit ad strati capitata cubicula lecti,
840 Sepius et prima sorte futurus erit.
 Sic genitus Salomon est hac que nupsit Vrie,
Dum pius intrusor occupat inde locum:
Sponsi defectus suplet deuocio fratris,
Et genus amplificans atria plena facit.
Verberat iste vepres, volucrem capit alter; et iste
Seminat in fundum, set metet alter agrum:
In stadio currunt ambo, brauium tamen vnus
Accipit iniuste longius ipse retro:
Sic intrat sponsus aliorum sepe labores,
850 Ac vbi non soluit in lucra, vana tamen.
Credit et exultat prolem genuisse maritus,
Vngula nec prolis pertinet vna sibi.
Predicat ypocrita cum sponso carmina sancta,
Vt deus ex verbo staret in ore suo:
Cum sponsa Veneris laudes decantat, et eius
Officium summe suplet honore dee:
Sic opus in basso tenementum construit altum,
Cuius egens nocte fabrica poscit opem.
O pietas fratris, que circuit et iuuat omnes,
860 Et gerit alterius sic pacienter onus:
O qui non animas tantum, set corpora nostra,
In sudore suo sanctificare venit.
Hic est confessor domini non, set dominarum,447
Qui magis est blandus quam Titiuillus eis:
Hic est confessor quasi fur quem furca fatetur,
Sic quia ius nostrum de muliere rapit.
Hic est confessor in peius qui male vertit,
Sordida namque lauans sordidiora facit:
Pellem pro pelle, quod habet sibi frater et omne
870 Pro nostri sponsa, se dabit atque sua.
O condigna viro tali quis premia reddet,
Aut deus aut demon? vltima verba ligant.
Peccati finis fert namque stipendia mortis,
Est dum culpa vetus plena pudore nouo:
Horum, viuentes qui tot miracula prestant,
In libro mortis nomina scripta manent.
Inter apes statuit natura quod esse notandum
 Sencio, quo poterit frater habere notam.
Nam si pungat apis, pungenti culpa repugnat,
880 Amplius vt stimulum non habet ipse suum;
Postque domi latebras tenet et non euolat vltra,
Floribus vt campi mellificare queat.
O deus, in simili forma si frater adulter
Perderet inflatum, dum stimularet, acum,
Amplius vt flores non colligat in muliere,
Nec vagus a domibus pergat in orbe suis!
Causa cessante quia tunc cessaret ab ipsis
Effectus, quo nunc plura pericla latent.

Hic loquitur qualiter isti fratres inordinate

viuentes ad ecclesie Cristi regimen non sunt
aliqualiter necessarii.

Capm. xix. Vna michi mira res est, quam mente reuoluens
890 Nescio finali qua racione foret.
Quam prius ordo fuit fratrum, quoscumque
necesse
Congruit ecclesie fertur inesse gradus.
Papa fuit princeps, alios qui substituebat,
Vt plebem regerent singula iura dedit:
Ius sibi presul habet, sub eo curatus, et ille
Admittens curas pondera plebis agit:
Proprietarius est presul qui proprietatem
Curato tribuit, qua sua iura regat:
Presulis inde loco curatus iurat, vt ipse
900 Tempore iudicii que tulit acta dabit.
Est igitur racio que vel tibi causa videtur,
Alterius proprium quod sibi frater habet?
Inter aues albas vetitur consistere coruum,
Quem notat ingratum quodlibet esse pecus;
Inter et ecclesie ciues consistere fratrem,
Qui negat eius onus, omnia iura vetant.
Caucius in rebus dubiis est semper agendum,
 Causa nec est mundi talis vt ipsa dei:
Si tamen vsurpet mundi quis iura, refrenant
910 Legis eum vires nec variare sinunt.
Que mea sunt propria mundo si tolleret alter,
Taliter iniustum lex reputabit eum:
In preiudicium partis lex non sinit equa,
Possit vt alterius alter habere locum:
Que bona corporea sunt alterius, nequit alter
Tollere, ni legum condita iura neget:
Set que sunt anime frater rapiens aliena,
Nescio qua lege iustificabit opus.
Si dic a t, ‘Papa dispensat,’ tunc videamus,
920 Est sibi suggestum, sponte vel illud agit.
Papa mero motu scimus quod talia numquam
Concessit, set ea supplicat ordo frequens:
Papa potest falli, set qui videt interiora,
Est hoc pro lucri scit vel amore dei.
Lingua petit curas anime, mens postulat aurum,
Bina sicque manu propria nostra rapit:
Defraudans animas, talis rapit inde salutem,
Et super hoc nostras tollere temptat opes.
Non ita Franciscus peciit, set singula linquens
930 Mundi pauperiem simplicitate tulit.
Gignit humus tribulos, vbi torpet cultor in agris,
Quo minus ad messes fert sua lucra Ceres:
Pungitur ecclesia, fratrum quos sentit abortos
Inuidie stimulis lesa per omne latus.
Quilibet ergo bonus tribulos extirpet arator,
Ne pharisea sacrum polluat herba locum.

Hic loquitur qualiter isti fratres inordinate

viuentes ad commune bonum vtiles aliqualiter
non existunt.

Capm. xx.Fratribus vt redimant celum non est labor Ade,

Quo sibi vel reliquis vina vel arua colunt;
 Corporis immo quies, quam querunt forcius, illos
940 Iam fouet, et mundi tedia nulla grauant:
Hiis neque perspicuus armorum pertinet actus,
Publica quo seruant iura vigore suo:
Sic neque milicies neque terre cultus adornat
Hos, set in orbe vagos linquit vterque status.
Nec sunt de clero f r a t r e s, quamuis sibi temptent
Vsurpare statum, quem sinit vmbra scole:
Non onus admittunt fratres cleri set honorem,
In cathedra primi quo residere petunt.
Non curant animas populi neque corpora pascunt:
950 Ad commune bonum quid magis ergo valent?
Vt neque ramosa numerabis in ilice glandes,
Tu fratrum numerum dinumerare nequis:
Immo, velut torrens vndis pluuialibus auctus,
Aut niue, que zephiro victa tepente fluit,
Ordo supercreuit habitu, set ab ordine virtus
Cessit, et in primis desinit ire viis.
Si racio fieret, famulorum poscit egestas
Tales quod sulcus posset habere suos.
Hos Dauid affirmat hominum nec inesse labore,
960 Nec posite legis vlla flagella pati.
Regia i u r a n i c h i l aut presulis acta valebunt,
Excessus fratrum quo moderare queant.
Que sua sunt mundus ea diligit, fratribus ergo
Attulit vt caris prospera queque suis:
Non sulcant neque nent, falcant nec in horrea
ponunt;
Pascit eos mundus non tamen inde minus.
Pectora sic gaudent, nec sunt attrita dolore,
Anterior celo dum reputatur humus:
Cordis in affectum sic transit frater, et illum
970 Quem querit cursum complet in orbe suum.
Dic quid honoris habet, si filius Hectoris arma
Deserit et vecors predicat acta patris?
Aut quid et ipse valet, si frater Apostata sanctum
Clamat Franciscum, quem negat ipse sequi?
 Fictis set verbis mundi sine lumine sensum
Obfuscant, que sua sic maledicta tegunt:
Sic vbi non ordo, manet error in ordinis vmbra,
Et quasi laruatus stat sacer ordo nouus.
Hiis qui Francisci seruant tamen ordine iusto
980 Debita mandata, debitus extat honor.

Hic loquitur de fratribus illis, qui incautos

pueros etatis discrecionem non habentes in sui
ordinis professionem attractando colloquiis
blandis multipliciter illaqueant.

Est michi suspectum de fratribus hoc, quod

Capm. xxi.
eorum
Reddere se primo nullus adultus adest:
Non sic Franciscum puerilis traxerat etas
Ordinis ad votum, quando recepit eum:
Sic nec eum pueri primo coluere sequaces,
Nec blande lingue fabula traxit eos.
Estimo maturos Franciscus sumpserat annos,
Dum per discreta viscera cepit opus;
Et puto quod similes sua dogmata sponte
sequentes
990 Nec prece nec precio reddidit ordo deo.
Set vetus vsus abest, nam circumvencio facta
Nunc trahit infantes, qui nichil inde sciunt;
Et sic de teneri tener ordo mollia querit,
Vmbraque sola manet atque nouerca quasi.
Vt vocat ad laqueos volucrem dum fistulat
auceps,
Sic trahit infantes fratris ab ore sonus:
Vt laqueatur auis laqueorum nescia fraudis,
Sic puer in fratrem fraude latente cadit:
Et cum sic poterit puerum vetus illaqueare,
1000 Debet ob hoc frater nomen habere patris.
Sic generata dolis patrem sequitur sua proles,
 Addit et ad patrios facta dolosa dolos;
Solaque sic radix centenos inficit ex se
Ramos, qui fructus fraudis in orbe ferunt.
Nam puer a veteri deceptus fratre per illud
Decipit exemplum, quando senecta venit:
Sic post decipiunt qui primo decipiuntur,
Et fraus de fraude multiplicata viget:
Sic crescit numerus fratrum, fit et ordo minutus,
1010 Dum miser in miseris gaudet habere pares.
‘Ve, qui proselitum vobis faciatis vt vnum,
Mundum circuitis,’ dixerat ipse deus:448
Illud erat dictum phariseis, et modo possum
Fratribus hec verba dicere lege noua.

Hic loquitur de apostazia fratrum ordinis

mendicancium, precipue de hiis qui sub ficta
ypocrisis simplicitate quasi vniuersorum curias
magnatum subuertunt, et inestimabiles suis
ficticiis sepissime causant errores.

Vt bona multa bonum fratrem quocumque

Capm. xxii.
sequntur,
Sic mala multa malum constat vbique sequi.
Sunt etenim domini tres, quorum quilibet vni
Seruit homo, per quem se petit ipse regi:
Est deus, est mundus, est demon apostata, cuius
1020 Ordine transgressus fert sibi frater onus.
Regula namque dei non nouit eum, neque mundi
Dat sibi milicies libera nulla statum:
Non habet ipse deum, nec habere valet sibi
mundum,
Demonis vt proprium sic subit ipse iugum:
Omnis enim vicii viciosus apostata motor
Aut fautor nutrit quod videt esse malum.
Testis erit Salomon, vir talis invtilis extat,
Et peiora sue crimina mentis agit:
 Arte vel ingenio, quo talis in orbe frequentat,
1030 Ducit in effectum plura timenda satis.
Non obstat paries illi, non clausa resistunt,
Invia consistunt peruia queque sibi:
Per mare, per terras, per totum circuit orbem;
Vt sibi plus placeat, cernere cuncta potest.
Nititur in fraudes, componit verba dolosa,
Auget et accumulat multiplicatque dolos;
Proponit lites, rixas accendit in iram,
Liuores nutrit invidiamque fouet;
Vincula disrumpit pacis, socialis amoris
1040 Federa perturbat, dissociatque fidem;
Suggerit incestum, suadet violare pudorem,
Soluere coniugium, commaculare thorum;
Vsurpando fidem vultum mentitur honestum,
Caucius vt fraudem palleat ipse suam.
In dampnis dandis promissor vbique fidelis,
Comoda si dederit, disce subesse dolum:
Sub grossa lana linum subtile tenetur,
Simplicitas vultus corda dolosa tegit;
Lingua venenato dum verba subornat in ore,
1050 Mellificat virus melque venena facit.
Vt sub virtutum specie lateat viciorum
Actus, et vt turpis Simea fiat homo;
Ipse tumens humilem mentitur sepe professum,
Quem fugit occulto spiritus ille dei.
Ordinis ipse sacri quicquid Franciscus honeste
Virtutis statuit, hic viciare studet:
Cuncta colore tamen operit, facieque decora
Fallit, dumque latent viscera plena dolo.
Invenies scriptum quod pennas strucio gestat
1060 Herodii pennis ancipitrisque pares;
Set non tam celeri viget eius penna volatu,
Ypocritamque notat, qui similando volat.
Aurea facta foras similans ypocrita fingit,
Set mala mens intus plumbea vota gerit:
Sunt etenim multi tales qui verba colorant,
 Qui pascunt aures, aurea verba sonant,
Verbis frondescunt, set non est fructus in actu,
Simplicium mentes dulce loquendo mouent:
Set templum domini tales excludit, abhorret
1070 Verborum phaleras, verba polita fugit.
Scripta poetarum, que sermo pictus inaurat,
Aurea dicuntur lingua, set illa caue:449
Est simplex verbum fidei bonus vnde meretur,
Set duplex animo predicat absque deo.
Despicit eloquia deus omnia, quando polita
Tecta sub eloquii melle venena fouent:
Qui bona verba serit, agit et male, turpiter errat,
Nam post verba solet accio sancta sequi.
Quos magis alta scola colit, hii sermone polito
1080 Scandala subtili picta colore serunt.
Sepius aut lucrum vel honoris adepcio vani450
Fratrum sermones dat magis esse reos:
Sub tritici specie zizannia sepe refundunt,
Dum doctrina tumens laudis amore studet:
Sepe suis meritis ascribere facta, mouere
Scisma, peritorum mens studiosa solet.
Phiton siue Magus est scismaticus, quia turbat
Verum quod credis et dubitanda mouet;
Set contra voces incantantis sapienter
1090 Aures obtura, ne cor adheret eis.
Non sunt hii fratres recti nec amore fideles
Ecclesie Cristi, sicut habetur ibi;
Inperfecta magis Sinagoga notabit eorum
Doctrinam, plene que neque vera docet:
Multociens igitur aliis nocet illa superba
Copia librorum quos Sinagoga tenet.
Non sunt ecclesie recti ciues, Agar immo
Parturit ancilla, perfida mater, eos:
Ergo recedat Agar, pariat quoque Sarra fidelem
1100 Ecclesie clerum, det Sinagoga locum.
Plantauit pietas et amor primordia fratrum,
Quos furor ad presens ambiciosus agit:
 Frater adest Odium, qui federa pacis abhorret,
Cuius ab inferno cepit origo viam;
Ille professus enim claustralia iura resoluit,
Nec fore concordes quos sinit ipse pares.
Qui tamen in culpa frater se sentit, et illam
Non delet, tali talia verba loquor:
‘Culpa mali laudem non debet tollere iusto,
1110 Nam lux in tenebris fulget honore magis:
Quisque suum portabit onus, culpetur iniqus,
Laudeturque suis actibus ipse bonus.’

Hic loquitur qualiter isti fratres mendicantes

mundum circuiendo amplioresque querendo
delicias de loco in locum cum ocio se
transferunt: loquitur eciam de superfluis eorum
edificiis, que quasi ab huius seculi
potencioribus vltra modum delicate
construuntur.

Iudeos spersos fratrum dispersio signat,

Capm. xxiii.
Quos modo per mundum deuius error agit;
Iste nec ille loco stabilis manet, immo vicissim
Se mouet, et varia mutat vbique loca.
Sic in circuitu nunc ambulat impius orbis,
Nec domus est in qua non petit ipse locum;
Pauperis in specie sibi sic elemosina predas
1120 Prebet, et ora lupi vellere laruat ouis:
Absque labore suo bona nemo meretur, et ergo
Omne solum lustrant, idque piamen habent.
Nescio si supera sibi clauserit ostia celum;
Dat mare, dant ampnes, totaque terra viam.
Hoc lego, quod raro crescit que sepe mouetur
Planta, set ex sterili sorte frequenter eget:
Non tamen est aliqua quin regula fallit in orbe,
Mocio nam fratris crescere causat eum;
 Nam quocumque suos mouet ille per arida
gressus,
1130 Mundus eum sequitur et famulatur ei.
Vt pila facta pilis solito dum voluitur ipsis
Crescit, et ex modico magnificatur opus,
Sic, vbi se voluit frater, sibi mundus habundat,
Quicquid et ipse manu tangit adheret ei:
Federa cum mundo sua frater apostata stringit,
Sic vt in occulto sint quasi semper idem.
Multis set quedam virtutes esse videntur,
Qui nil virtutis nec bonitatis habent;
Ista dabunt vocem, set erunt deformia mente,
1140 Multaque dum fiunt absque salute placent.
Ad decus ecclesie deuocio seruit eorum,
Et veluti quedam signa salutis habent:
Eminet ecclesia constructa sibi super omnes,
Edificant petras sculptaque ligna fouent;
Porticibus valuas operosis, atria, quales
Quotque putas thalamos hic laberintus habet:
Ostia multa quidem, varie sunt mille fenestre,
Mille columpnarum marmore fulta domus.
Fabrica lata domus erit, alta decoraque muris,
1150 Picturis variis splendet et omne decus;
Omnis enim cella, manet in qua frater inanis,
Sculpture vario compta decore nitet:
Postibus insculpunt longum mansura per euum
Signa, quibus populi corda ligare putant.
Fingentes Cristum mundum querunt, et in eius
Conspirant laudem clamque sequntur eum:
Talis sub facie deuocio sancta figure
Fingitur, et testis fit magis inde domus:
Qui tamen omne videt, rimatur et intima cordis,
1160 Scit quia pro mundo tale paratur opus.
Set docet exemplis historia Parisiensis,
Quod contentus homo sit breuiore domo.
Non sibi de propriis habet vlla potencia regis
Illorum thalamis tecta polita magis:
 Non ita fit vestis fratrum nota simplicitatis,
Quin magis in domibus pompa notabit eos.
In fabrice studio vigilat conuentus eorum
Ecclesie, prompti corpore, mente pigri:
Sic patet exterius fratrum deuocio sancta,
1170 Vana set interius cordis ymago latet:
Sunt similes vlno tales, qui sunt sine fructu,
In quibus impietas plurima, pauca fides.
Dic, tibi quid, frater, confert, tantas quod honestas
Cum feda mente construis ipse domos?
Esto domus domini, quam sacris moribus orna,
Virtutem cultor religionis ama.
Omnia fine patent, tibi fingere nil valet extra,
Per quod ab interius premia nulla feres:
Si tibi laus mundi maneat furtiua diebus,
1180 Cum celum perdis, laus erit illa pudor.
Ordinis es, norma tibi sit, nec ab ordine cedas,
Est aliter cassum quicquid ab inde geris.

Hic loquitur qualiter, non solum in ordine

fratrum mendicancium set eciam in singulis
cleri gradibus, ea que virtutis esse solebant a
viciis quasi generaliter subuertuntur: dicit
tamen quod secundum quasdam Burnelli
constituciones istis precipue diebus modus et
regula specialius451 obseruantur.

Diuersat fratres tantummodo vestis eorum,

Capm. xxiiii.
Hii tamen existunt condicione pares:
Regula nulla manet, fuerat que facta per ante,
Set nouus ordo nouum iam facit omne forum.
Sicut enim fratrum nunc ordo resoluitur, ecce
Ecclesie norma fit quasi tota noua;
Set sacer ordo tamen remanet, quem sanxerat
olim
1190 Frater Burnellus, crescit et ille magis.
 Hec decreta modo, Burnellus que statuebat,
Omnia non resero nec reserare volo;
Set duo iam tantum que iussit in ordine dicam,
Et sunt presenti tempore iura quasi.
Mandatum primum tibi contulit, omne iocosum,
Quicquid in orbe placet, illud habere licet:
Si vis mercari, sis mercenarius, autem452
Si vis mechari, dat tibi, mechus eris:453
Que magis vlla caro desiderat, illa beato
1200 Sunt fratri nostro debita iura modo.
Precipiens vltra statuit de lege secunda,
Quod nocuum carni sit procul omne tibi:
Omne quod est anime reputatur in ordine vile,
Et caro delicias debet habere suas:
Cor dissolue tuum, te nullus namque ligabit,
Quo vis vade tuas liber vbique vias.
Mollibus ornatus sic dignior ordo nouellus
Restat Burnelli, vult quia velle viri.
Nil michi Bernardus, nichil ammodo seu
Benedictus454
1210 Sint, set Burnellus sit Prior ipse meus;
Quo viget en carnis requies, quo lingua precantis
A prece torpescens fit quasi tota silens:455
Ordoque sic precibus dum vult succurrere nobis,
Linquo choax ranis et nichil inde magis:456
Si veniantque michi mala tempora, credo quod
isti457
De clero causam dant nimis inde grauem;
Quis poterit namque nobis bona tempora ferre,
Ordine claustrali dum perit ordo dei,
Et fugit a reliquo deuocio celica clero?
1220 Sic fugit a nobis vndique nostra salus.
Nam quia sic medii fallunt discorditer ipsi,
Ignaui populi stamus in orbe vagi.
Quid sibi corpus habet in eo, nisi spiritus extet,
Quid nisi nos clerus suplet in orbe pius?
 A planta capiti set qui discernere cleri
Vult genus aut speciem, vix sciet inde bonum.
Sic vbi lux, tenebre, sic mors, vbi normula vite
Instrueret sanam gentibus ire viam.
Vt dicunt alii de clero, sic ego dixi,
1230 Quo creuit reliquis error in orbe magis:
Nam sine pastore grex est dispersus, et ecce
Pascua peccati querit vbique noui.

1221-1232. Text STH₂ As follows in CEHGDL,

Nunc quia sic Cleri sors errat ab ordine Cristi,

Vsurpat mundus que negat ipse deus.
Dum tua, Burnelle, scola sit communis in orbe,
A planta capiti fallitur omnis ibi:
Sed cum Gregorii scola fulsit in orbe beati,458
Vera fides viguit, cunctaque pace tulit.
Nunc tamen est Arius nouus, est quasi Iouinianus,
Doctor in ecclesiis scisma mouendo scolis.
Sic vbi lux, tenebre, sic mors, vbi regula vite
1230* Instrueret rectam gentibus ire viam.
Quilibet ergo bonus, sit miles siue Colonus,
Orans pro Clero det sua vota deo.

FOOTNOTES:
424 14 subtrahet CE
425 52 erat ... vrbe DL
426 72 esse SG ipse CEHDL
427 79 dum CE
428 103 No paragr. S
429 177 oculis T oculus SCEHGDLH₂
430 216 rara CE
431 273 vt (ut) CEHGDLT et S
432 295 sibi om. S (p. m.) vir inserted later bona qui sibi D
433 Cap. vi. Heading 2 f. religionis sibi CE
434 315 No paragr. S
435 336 iam CEHGDLTH₂ non S
436 404 ghemendo SH gemendo CEDL
437 489 fomes est res C fomes res est L
438 Heading 1 quasi om. D
439 587 Marginal note ins. SCG om. EHDLH₂ Nota quod Genius
secundum Ouidium dicitur sacerdos Veneris G
440 593 ibi SE
441 635 qui CE
442 645 perextra SHGTL per extra CED
443 662 placet CEH patet SGDL
444 799 putabit CEHD putabat SGL
445 807 pereant CEL
446 811 ad CEHGDL et S
447 863 sed non D
448 1012 margin Nota C
449 1072 lingua SH₂ verba CEHGDLT
450 1081 adepcio CEHGDL adopcio S
451 Heading 5 specialiter S
452 1197 autem STH₂ et si CEHGDL
453 1198 Text STH₂ Mechari cupias dat tibi GDL Mechari cupias
ordine CEH
454 1209 seu] uel C
455 1212 Text STH₂ Auribus alma sonat menteque vana petit
CEHGDL
456 1214 Text STH₂ Folia non fructus percipit inde deus
CEHGDL
457 1215 Text STH₂ Si veniant mundi CEHGDL
458 1225* fulscit HG