Before We Are Born: Essentials of Embryology and Birth Defects, 10e

359 Pages·2019·77.86 MB·English

by  Keith L. Moore BA MSc PhD DSc FIAC FRSM FAAA, T. V. N. Persaud MD PhD DSc FRCPath (Lond.) FAAA, Mark G. Torchia MSc PhD

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2015v1.0
KEITH L. MOORE
Dr. Moore has been the recipient of many prestigious awards and recognitions. He has received
the highest awards for his remarkable record of textbook publications in clinically oriented anatomy
and embryology. He was the recipient of the inaugural Henry Gray/Elsevier Distinguished Educator
Award in 2007—the American Association of Anatomists’ highest award for excellence in human
anatomy education at the medical/dental, graduate, and undergraduate levels of teaching; the
Honored Member Award of the American Association of Clinical Anatomists (1994) for significant
contributions to the field of clinically relevant anatomy; and the J.C.B. Grant Award of the Canadian
Association of Anatomists (1984) “in recognition of meritorious service and outstanding scholarly
accomplishments in the field of anatomical sciences.” In 2008 Professor Moore was inducted as
a Fellow of the American Association of Anatomists. The rank of Fellow honors distinguished
AAA members who have demonstrated excellence in science and in their overall contributions to
the medical sciences. In 2012 Dr. Moore received an Honorary Doctor of Science degree from
The Ohio State University and the University of Western Ontario in 2015; The Queen Elizabeth
II Diamond Jubilee Medal honoring significant contributions and achievements by Canadians;
and the Benton Adkins Jr. Distinguished Service Award for an outstanding record of service to
the American Association of Clinical Anatomists.
T.V.N. (VID) PERSAUD
Dr. Persaud was the recipient of the Henry Gray/Elsevier Distinguished Educator Award in 2010—“the
American Association of Anatomists’ highest honor in recognition of sustained excellence and
leadership in human anatomy education”; the Honored Member Award of the American Association
of Clinical Anatomists (2008) for “his distinguished career and significant contributions to the
field of clinically relevant anatomy, embryology, and the history of anatomy”; and the J.C.B. Grant
Award of the Canadian Association of Anatomists (1991) “in recognition of meritorious service
and outstanding scholarly accomplishments in the field of anatomical sciences.” In 2010 Professor
Persaud was inducted as a Fellow of the American Association of Anatomists. The rank of Fellow
“honors distinguished AAA members who have demonstrated excellence in science and in their
overall contributions to the medical sciences.” In 2003 Dr. Persaud was a recipient of the Queen
Elizabeth II Golden Jubilee Medal, presented by the Government of Canada for “significant
contribution to the nation, the community, and fellow Canadians.”
MARK G. TORCHIA
Dr. Mark G. Torchia was the recipient of the distinguished Inaugural Governor General Award
for Innovation which “recognize(s) and celebrate(s) outstanding Canadian individuals, teams and
organizations—trailblazers and creators who contribute to our country’s success, who help shape
our future and who inspire the next generation.” Dr. Torchia is also a Manning Principle Prize
Laureate (2015), which recognizes “leaders and visionaries who are positively impacting the Canadian
economy while improving the human experience in its various dimensions around the world.”
He is also a recipient of the Norman and Marion Bright Memorial Medal and Award for “individuals
who have made an outstanding contribution to chemical technology” and the TIMEC Medical
Device Champion Award. Dr. Torchia continues to engage learners at all levels through outreach
opportunities and formal curricula. He has been nominated for MMSA teaching awards since
their initiation and most recently received the Award for Teaching Excellence 2016 from the Rady
Faculty of Health Sciences, University of Manitoba.
Tenth Edition
BEFORE WE
ARE BORN:
ESSENTIALS OF
EMBRYOLOGY AND
BIRTH DEFECTS
Keith L. Moore, BA, MSc, PhD, DSc (OSU),
DSc (WU), FIAC, FRSM, FAAA
Professor Emeritus, Division of Anatomy, Department of Surgery
Former Professor and Chair, Department of Anatomy,
and Associate Dean for Basic Medical Sciences
Faculty of Medicine, University of Toronto, Toronto, Ontario, Canada
Former Professor and Head of Anatomy, Faculty of Medicine,
University of Manitoba, Winnipeg, Manitoba, Canada
T.V.N. (Vid) Persaud, MD, PhD, DSc,
FRCPath (Lond.), FAAA
Professor Emeritus and Former Head,
Department of Human Anatomy and Cell Science
Professor of Pediatrics and Child Health
Associate Professor of Obstetrics, Gynecology, and Reproductive Sciences,
Max Rady College of Medicine, Faculty of Health Sciences, Faculty of
Medicine, University of Manitoba, Winnipeg, Manitoba, Canada
Part-Time Professor of Anatomy, St. George’s University, Grenada, West Indies
Mark G. Torchia, MSc, PhD
Associate Professor, Department of Surgery; Associate Professor,
Department of Human Anatomy and Cell Sciences,
Max Rady College of Medicine, Rady Faculty of Health Sciences
Executive Director, Centre for the Advancement of Teaching and Learning,
Vice-Provost (Teaching and Learning) University of Manitoba,
Winnipeg, Manitoba, Canada
For additional online content visit ExpertConsult.com
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In Memory of Marion
To my lovely wife and best friend for her endless support and patience. I am
grateful for her encouragement and understanding during the countless hours
spent writing the first three editions of Before We Are Born. Wonderful
memories keep her in my heart and mind. I appreciate the continued support
given to me by my daughters, Pam and Kate, and to my son-in-law, Ron Crowe,
for his technical skills. I am very proud of our five children: Warren, Pam,
Karen, Laurel, and Kate, our nine grandchildren—Kristin, Lauren, Caitlin,
Mitchel, Jayme, Courtney, Brooke, Melissa, and Alicia,
and great-grandchildren, James and Charlotte.
–KLM
For Gisela
My lovely wife and best friend, for her endless support and patience; our three
children—Indrani, Sunita, and Rainer (Ren)—and grandchildren (Brian,
Amy, and Lucas).
–TVNP
For Barbara, Muriel, and Erik
Thank you for your support, encouragement, laughs, and love. Your own
personal accomplishments continue to amaze me—this book is dedicated to you.
–MGT
For Students and Their Teachers
To our students: We hope you will enjoy reading this book, increase your under-
standing of human embryology, pass all of your exams, and be excited and well
prepared for your careers in patient care, research, and teaching. You will
remember some of what you hear, much of what you read, more of what you see,
and almost all of what you experience and understand fully.
To their teachers: May this book be a helpful resource to you and your students.
We appreciate the numerous constructive comments we have received over the
years from both students and teachers. Your remarks have been invaluable to us
in improving this book.
Contributors
CONTRIBUTORS CLINICAL REVIEWERS
David D. Eisenstat, MD, MA, FRCPC Albert E. Chudley, MD, FRCPC, FCCMG
Professor and Chair, Department of Oncology, University Professor Emeritus of Pediatrics and Child Health,
of Alberta, Muriel & Ada Hole Kids with Cancer Society and Biochemistry and Medical Genetics, Max Rady
Chair in Pediatric Oncology; Professor, Departments of College of Medicine, Faculty of Health Sciences,
Medical Genetics and Pediatrics, Faculty of Medicine, University of Manitoba, Winnipeg, Manitoba,
University of Alberta, Edmonton, Canada Canada
Jeffrey T. Wigle, PhD Michael Narvey, MD, FRCPC, FAAP
Principal Investigator, Institute of Cardiovascular Sciences, Section Head, Neonatal Medicine, Health Sciences Centre
St. Boniface Hospital Research Centre; Associate and St. Boniface Hospital; Assistant Professor of
Professor, Department of Biochemistry and Medical Pediatrics and Child Health, Max Rady College of
Genetics, University of Manitoba, Winnipeg, Medicine, Faculty of Health Sciences, University of
Manitoba, Canada Manitoba, Winnipeg, Manitoba, Canada
vi
Contributors vii
Heather Dean, MD, FRCPC
FIGURES AND IMAGES (SOURCES)
Department of Pediatrics and Child Health, University of
We are grateful to the following colleagues for the clinical Manitoba, Winnipeg, Manitoba, Canada
images they have given us for this book and also for granting Figures 13.17, 13.25, and 19.13
us permission to use figures from their published works:
Marc Del Bigio, MD, PhD, FRCPC
Steve Ahing, DDS Department of Pathology (Neuropathology), University of
Division of Oral Diagnosis and Radiology, Faculty of Manitoba, Winnipeg, Manitoba, Canada
Dentistry, Department of Pathology, University of Figures 15.10, 16.22, and 16.26
Manitoba, Winnipeg, Manitoba, Canada
Figure 18.10B–D João Carlos Fernandes Rodrigues, MD
Servico de Dermatologia, Hospital de Desterro, Lisbon,
Franco Antoniazzi, MD, and Vassilios Fanos, MD Portugal
Department of Pediatrics, University of Verona, Verona, Figure 18.3
Italy
Figure 19.3 Frank Gaillard, MB, BS, MMed
Department of Radiology, Royal Melbourne Hospital,
Volker Becker, MD† Melbourne, Victoria, Australia; Radiopaedia.org
Pathologisches Institut der Universität, Erlangen, Germany Figures 9.8C and 10.17
Figures 8.12 and 8.14
Gary Geddes, MD
J. Been, MD, M. Shuurman, MD, and S. Robben, MD Lake Oswego, Oregon, USA
Maastricht University Medical Centre, Maastricht, The Figure 15.13B
Netherlands
Figure 11.6B Barry H. Grayson, MD, and Bruno L. Vendittelli, MD
New York University Medical Center, Institute of
David Bolender, MD Reconstructive Plastic Surgery, New York, New York,
Department of Cell Biology, Neurobiology, and Anatomy, USA
Medical College of Wisconsin, Milwaukee, Wisconsin, Figure 10.31
USA
Figure 15.13A Christopher R. Harman, MD, FRCSC, FACOG
Department of Obstetrics, Gynecology, and Reproductive
Peter C. Brugger, MD, PhD Sciences, Women’s Hospital and University of Maryland,
Associate Professor/Privat Dozent, Center for Anatomy Baltimore, Maryland, USA
and Cell Biology, Medical University of Vienna, Vienna, Figure 12.16
Austria
Cover image (MRI of breech fetus) Jean Hay, MSc†
University of Manitoba, Winnipeg, Manitoba, Canada
Jack C.Y. Cheng, MD Figures 7.2 and 7.4
Department of Orthopaedics and Traumatology, The Health Sciences Centre
Chinese University of Hong Kong, Hong Kong, China Children’s Hospital and University of Manitoba, Winnipeg,
Figure 15.18 Manitoba, Canada
Figures 10.13 and 19.7
Albert E. Chudley, MD, FRCPC, FCCMG
Department of Pediatrics and Child Health, Section of Lyndon M. Hill, MD
Genetics and Metabolism, Children’s Hospital, Magee-Women’s Hospital, Pittsburgh, Pennsylvania, USA
University of Manitoba, Winnipeg, Manitoba, Canada Figure 12.5
Figures 5.12, 10.30, 12.17AB, 12.24, 13.13, 13.26, 15.24,
15.25, 15.26, 16.10, 16.11, 16.23, 17.14, 19.4, 19.5, 19.6, Klaus V. Hinrichsen, MD†
19.9, 19.10, 19.12, and 19.14A Medizinische Fakultät, Institut für Anatomie, Ruhr-
Universität Bochum, Bochum, Germany
Blaine M. Cleghorn, DMD, MSc Figures 10.2 and 10.25
Faculty of Dentistry, Dalhousie University, Halifax, Nova
Scotia, Canada Evelyn Jain, MD, FCFP
Figure 18.10A Breastfeeding Clinic, Calgary, Alberta, Canada
Figure 10.22
†Deceased.
viii Contributors
John A. Jane, Sr., MD Prem S. Sahni, MD
Department of Neurological Surgery, University of Formerly of the Department of Radiology, Children’s
Virginia Health System, Charlottesville, Virginia, USA Hospital, Winnipeg, Manitoba, Canada
Figure 15.11AB Figure 15.14
Dagmar K. Kalousek, MD Gerald S. Smyser, MD
Department of Pathology, University of British Columbia; Formerly of the Altru Health System, Grand Forks, North
Children’s Hospital, Vancouver, British Columbia, Dakota, USA
Canada Figures 10.17, 15.11C, and 17.13
Figures 12.12A and 13.10
Pierre Soucy, MD, FRCSC
James Koenig, MD, FRCPC Division of Pediatric Surgery, Children’s Hospital of
Department of Radiology, Health Sciences Centre, Eastern Ontario, Ottawa, Ontario, Canada
Winnipeg, Manitoba, Canada Figures 10.10 and 10.11
Figure 14.28D
Alexandra Stanislavsky, MD
Wesley Lee, MD Department of Radiology, Mercy Hospital for Women,
Department of Obstetrics and Gynecology, Division of Royal Melbourne Hospital, Melbourne, Victoria,
Fetal Imaging, William Beaumont Hospital, Royal Oak, Australia; Radiopaedia.com
Michigan, USA Figure 12.12B
Figure 16.12A
R. Shane Tubbs, PhD, and W. Jerry Oakes, MD
Deborah Levine, MD, FACR Department of Pediatric Neurosurgery, Children’s
Department of Radiology, Obstetric and Gynecologic Hospital, Birmingham, Alabama, USA
Ultrasound, Beth Israel Deaconess Medical Center, Figure 16.24
Boston, Massachusetts, USA
Figures 7.5B, 16.12B, and cover image (MRI of 27-week fetus) Edward O. Uthman, MD
Consultant Pathologist, Houston/Richmond, Texas, USA
Mina Leyder, MD Figure 5.3C
Universitair Ziekenhaus Brussels, Brussels, Belgium
Figure 14.19 Elspeth H. Whitby, BSc, MB, ChB (Hons), FFDRCSI
Academic Unit of Reproductive and Developmental
E. A. (Ted) Lyons, OC, MD, FRCPC, FACR Medicine, Department of Academic Pathology,
Departments of Radiology, Obstetrics & Gynecology, and University of Sheffield, Sheffield, England, United
Human Anatomy & Cell Science, Division of Kingdom
Ultrasound, Health Sciences Centre, University of Figure 16.25
Manitoba, Winnipeg, Manitoba, Canada
Figures 4.6B, 5.1, 5.10, 6.6, 7.1, 7.9, 8.4, 12.17CD, and Nathan E. Wiseman, MD, FRCSC
cover image (ultrasound of 9-week fetus) Department of Surgery, Section of Pediatric and
Cardiothoracic Surgery, Children’s Hospital, University
Maulik S. Patel, MD of Manitoba, Winnipeg, Manitoba, Canada
Consultant Pathologist, Surat, India; Radiopaedia.org Figures 9.8B and 12.15
Figure 5.13
Martin H. Reed, MD, FRCPC
Department of Radiology, University of Manitoba and
Children’s Hospital, Winnipeg, Manitoba, Canada
Figure 12.23
Gregory J. Reid, MD, FRCSC
Department of Obstetrics, Gynecology, and Reproductive
Sciences, University of Manitoba, Women’s Hospital,
Winnipeg, Manitoba, Canada
Figure 14.9
Michael and Michele Rice
Figure 7.6
Preface
Before We Are Born has been in print for more than 46 years. there are many helpful clinical case studies and questions
This concise work is based on our larger book, The Developing with answers and explanations. These will benefit students
Human: Clinically Oriented Embryology, Eleventh Edition. preparing for USMLE Step 1 and similar examinations.
The tenth edition of Before We Are Born has been completely Accompanying this tenth edition of Before We Are Born is
updated to reflect current understanding of clinical human an innovative set of 18 full-color animations that will assist
embryology. It provides the essentials of normal and abnormal students in learning the complexities of embryologic develop-
development. As in earlier editions, clinically oriented materials ment. These animations are available at studentconsult.com.
are highlighted in green color (often called clinical green High-resolution animations are available to teachers for their
boxes). Every chapter has been revised thoroughly to reflect lectures if they have adopted this book or The Developing
new research findings and their clinical significance, as well Human (consult your Elsevier representative). When one of
as new understanding of the developmental biology. the animations is especially relevant to the book’s text, an
This edition follows the official international list of embryologi- icon has been added in the margin.
cal terms (Terminologia Embryonica, 2013). It is important that The teratology (studies concerned with birth defects)
physicians, nurses, physician assistants, dentists, physical and section has been updated because the study of abnormal
occupational therapists, other health professionals, scientists, development is required for understanding the causes of birth
and students in the health professions throughout the world defects and how these may be prevented. Molecular aspects
use the same name for each structure. of developmental biology have been highlighted throughout
We have included numerous new color photographs of the book, especially in areas that appear promising for clini-
embryos, fetuses (normal and abnormal), neonates (new- cal medicine and future research. Moreover, Chapter 20 is
borns), and children. There are also many new diagnostic devoted exclusively to more detailed information related to
images: US (ultrasound), CT (computed tomography) scans, the cellular and molecular basis of embryonic development.
and MRI (magnetic resonance imaging) studies of embryos
and fetuses. Keith L. Moore
An important feature of this book is the Clinically Oriented
T.V.N. (Vid) Persaud
Questions, which appear at the end of each chapter. In addi-
tion, available through Elsevier’s studentconsult.com website, Mark G. Torchia
ix