The Developing Human: Clinically Oriented Embryology

679 Pages·2015·127.989 MB·English

by  Keith L. Moore, T. V. N. Persaud, Mark G. Torchia

THE DEVELOPING
HUMAN
CLINICALLY ORIENTED EMBRYOLOGY
KEITH L. MOORE
Recipient of the inaugural Henry Gray/Elsevier Distinguished Educator Award in 2007—the
American Association of Anatomists’ highest award for excellence in human anatomy educa-
tion 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 out-
standing 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; 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
Recipient of the Henry Gray/Elsevier Distinguished Educator Award in 2010—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 (2008) for significant contribu-
tions to the field of clinically relevant 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
Recipient of the Norman and Marion Bright Memorial Medal and Award and the Silver
Medal of the Chemical Institute of Canada in 1990 for outstanding contributions. In 1993
he was awarded the TIMEC Medical Device Champion Award. In 2008 and in 2014 Dr.
Torchia was a nominee for the Manning Innovation Awards, for innovation talent. Dr.
Torchia’s most cherished award has been the Award for Teaching Excellence in 2011 from
the Faculty of Medicine, University of Manitoba, and being asked to address the graduating
class of 2014.
THE DEVELOPING
HUMAN
CLINICALLY ORIENTED EMBRYOLOGY
10th Edition
Keith L. Moore,
BA, MSc, PhD, DSc, 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, Faculty of Medicine,
University of Manitoba, Winnipeg, Manitoba, Canada
Professor of Anatomy, St. George’s University, Grenada, West Indies
Mark G. Torchia,
MSc, PhD
Associate Professor and Director of Development, Department of Surgery
Associate Professor, Department of Human Anatomy and Cell Sciences
Director, Centre for the Advancement of Teaching and Learning, University of Manitoba,
Winnipeg, Manitoba, Canada
1600 John F. Kennedy Blvd.
Ste 1800
Philadelphia, PA 19103-2899
THE DEVELOPING HUMAN, TENTH EDITION ISBN: 978-0-323-31338-4
INTERNATIONAL EDITION ISBN: 978-0-323-31347-6
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Notices
Knowledge and best practice in this field are constantly changing. As new research and experience
broaden our understanding, changes in research methods, professional practices, or medical
treatment may become necessary.
Practitioners and researchers must always rely on their own experience and knowledge in
evaluating and using any information, methods, compounds, or experiments described herein. In
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With respect to any drug or pharmaceutical products identified, readers are advised to check
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Previous editions copyrighted 2013, 2008, 2003, 1998, 1993, 1988, 1982, 1977, and 1973.
Library of Congress Cataloging-in-Publication Data
Moore, Keith L., author.
The developing human : clinically oriented embryology / Keith L. Moore, T.V.N. (Vid) Persaud,
Mark G. Torchia.—10th edition.
p. ; cm.
Includes bibliographical references and index.
ISBN 978-0-323-31338-4 (pbk. : alk. paper)—ISBN 978-0-323-31347-6 (international edition : alk.
paper)
I. Persaud, T. V. N., author. II. Torchia, Mark G., author. III. Title.
[DNLM: 1. Embryology. QS 604]
QM601
612.6′4018—dc23
2015001490
Content Strategist: Meghan Ziegler
Senior Content Development Specialist: Jennifer Ehlers
Publishing Services Manager: Patricia Tannian
Senior Project Manager: Kristine Feeherty
Design Direction: Margaret Reid
The cover images show a magnetic resonance image of a 27-week-old fetus in the
uterus (Courtesy Dr. Deborah Levine, Beth Israel Deaconess Medical Center, Boston,
Massachusetts). The photograph of the baby (Kennedy Jackson) was taken 7 days
after her birthday. She is wrapped in a knitted cocoon that symbolizes the uterus.
Printed in the United States of America
Last digit is the print number: 9 8 7 6 5 4 3 2 1
In Loving Memory of Marion
My best friend, wife, colleague, mother of our five children and grandmother of our nine grandchildren, for her love,
unconditional support, and understanding. Wonderful memories keep you ever near our hearts.
—KLM and family
For Pam and Ron
I should like to thank my eldest daughter, Pam, who assumed the office duties previously carried out by her mother,
Marion. She has also been helpful in so many other ways (e.g., reviewing the text). I am also grateful to my son-in-law,
Ron Crowe, whose technical skills have helped me utilize the new technology when I was improving this book.
—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
Nothing could ever mean more to me than each of you. Thank you for your support and your love.
—MGT
For Our Students and Their Teachers
To our students: We hope you will enjoy reading this book, increase your understanding 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.
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.
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Contributors
CONTRIBUTORS FIGURES AND IMAGES (SOURCES)
David D. Eisenstat, MD, MA, FRCPC We are grateful to the following colleagues for the clinical
images they have given us for this book and also for
Professor, Departments of Pediatrics, Medical Genetics
granting us permission to use figures from their published
and Oncology, Faculty of Medicine and Dentistry,
works:
University of Alberta; Director, Division of Pediatric
Immunology, Hematology, Oncology, Palliative Care,
Steve Ahing, DDS
and Environmental Health, Department of Pediatrics,
Faculty of Dentistry, University of Manitoba, Winnipeg,
Stollery Children’s Hospital and the University of
Manitoba, Canada
Alberta; Inaugural Chair, Muriel and Ada Hole Kids
Figure 19-20F
with Cancer Society Chair in Pediatric Oncology,
Edmonton, Alberta, Canada
Franco Antoniazzi, MD
Department of Pediatrics, University of Verona,
Jeffrey T. Wigle, PhD
Verona, Italy
Principal Investigator, Institute of Cardiovascular
Figure 20-4
Sciences, St. Boniface Hospital Research Centre;
Associate Professor, Department of Biochemistry and
Dean Barringer and Marnie Danzinger
Medical Genetics, University of Manitoba, Winnipeg,
Figure 6-7
Manitoba, Canada
†Volker Becker, MD
Pathologisches Institut der Universität, Erlangen,
CLINICAL REVIEWERS
Germany
Albert E. Chudley, MD, FRCPC, FCCMG Figures 7-18 and 7-21
Professor, Department of Pediatrics and Child Health;
Professor, Department of Biochemistry and Medical J.V. Been, MD
Genetics, University of Manitoba, Winnipeg, Department of Pediatrics, Maastricht University
Manitoba, Canada Medical Centre, Maastricht, The Netherlands
Figure 10-7C
Michael Narvey, MD, FRCPC, FAAP
Section Head, Neonatal Medicine, Health Sciences Beryl Benacerraf, MD
Centre and St. Boniface Hospital; Associate Professor Diagnostic Ultrasound Associates, P.C., Boston,
of Pediatrics and Child Health, University of Massachusetts, USA
Manitoba, Winnipeg, Manitoba, Canada Figures 13-29A, 13-35A, and 13-37A
Kunwar Bhatnagar, MD
Department of Anatomical Sciences and Neurobiology,
School of Medicine University of Louisville,
Louisville, Kentucky, USA
Figures 9-33, 9-34, and 19-10
†Deceased.
vii
viii CONTRIBUTORS
David Bolender, MD João Carlos Fernandes Rodrigues, MD
Department of Cell Biology, Neurobiology, and Servico de Dermatologia, Hospital de Desterro, Lisbon,
Anatomy, Medical College of Wisconsin, Milwaukee, Portugal
Wisconsin, USA Figure 19-5B
Figure 14-14BC
Frank Gaillard, MB, BS, MMed
Dr. Mario João Branco Ferreira Department of Radiology, Royal Melbourne Hospital,
Servico de Dermatologia, Hospital de Desterro, Lisbon, Australia
Portugal Figures 4-15 and 9-19B
Figure 19-5A
Gary Geddes, MD
Albert E. Chudley, MD, FRCPC, FCCMG Lake Oswego, Oregon, USA
Department of Pediatrics and Child Health, Section of Figure 14-14A
Genetics and Metabolism, Children’s Hospital,
University of Manitoba, Winnipeg, Manitoba, Barry H. Grayson, MD, and Bruno L. Vendittelli, MD
Canada New York University Medical Center, Institute of
Figures 4-6, 9-38, 11-19AB, 11-28A, 12-24, 12-42, 12-43, Reconstructive Plastic Surgery, New York,
14-11, 15-6, 16-13DE, 16-14, 16-15, 17-14, 17-33, 17-36, New York, USA
18-20, 18-21, 18-23, 19-9, 20-3, 20-5, 20-6CD, 20-7, 20-8, Figure 9-40
20-13, 20-14, 20-17, and 20-19A
Christopher R. Harman, MD, FRCSC, FACOG
Blaine M. Cleghorn, DMD, MSc Department of Obstetrics, Gynecology, and
Faculty of Dentistry, Dalhousie University, Halifax, Reproductive Sciences, Women’s Hospital and
Nova Scotia, Canada University of Maryland, Baltimore, Maryland, USA
Figures 19-19 and 19-20A-E Figures 7-17 and 12-23
Dr. M.N. Golarz De Bourne †Jean Hay, MSc
St. George’s University Medical School, True Blue, Department of Anatomy, University of Manitoba,
Grenada Winnipeg, Manitoba, Canada
Figure 11-21 Figure 17-25
Heather Dean, MD, FRCPC Blair Henderson, MD
Department of Pediatrics and Child Health, University Department of Radiology, Health Sciences Centre,
of Manitoba, Winnipeg, Manitoba, Canada University of Manitoba, Winnipeg, Manitoba,
Figures 12-28 and 20-18 Canada
Figure 13-6
Marc Del Bigio, MD, PhD, FRCPC
Department of Pathology (Neuropathology), University Lyndon M. Hill, MD
of Manitoba, Winnipeg, Manitoba, Canada Magee-Women’s Hospital, Pittsburgh, Pennsylvania, USA
Figures 17-13, 17-29 (inset), 17-30BC, 17-32B, 17-37B, Figures 11-7 and 12-14
17-38, 17-40, and 17-42A
†Klaus V. Hinrichsen, MD
David D. Eisenstat, MD, MA, FRCPC Medizinische Fakultät, Institut für Anatomie,
Manitoba Institute of Cell Biology, Department of Ruhr-Universität Bochum, Bochum, Germany
Human Anatomy and Cell Science, University of Figures 5-12A, 9-2, and 9-26
Manitoba, Winnipeg, Manitoba, Canada
Figure 17-2 Dr. Jon and Mrs. Margaret Jackson
Figure 6-9B
Vassilios Fanos, MD
Department of Pediatrics, University of Verona,
Verona, Italy
Figure 20-4
†Deceased.
CONTRIBUTORS ix
Evelyn Jain, MD, FCFP Margaret Morris, MD, FRCSC, MEd
Breastfeeding Clinic, Calgary, Alberta, Canada Professor of Obstetrics, Gynaecology, and Reproductive
Figure 9-24 Sciences, Women’s Hospital and University of
Manitoba, Winnipeg, Manitoba, Canada
John A. Jane, Sr., MD Figure 12-46
David D. Weaver Professor of Neurosurgery,
Department of Neurological Surgery, University of Stuart C. Morrison, MD
Virginia Health System, Charlottesville, Virginia, USA Section of Pediatric Radiology, The Children’s Hospital,
Figure 14-12 Cleveland Clinic, Cleveland, Ohio, USA
Figures 7-13, 11-20, 17-29E, and 17-41
Robert Jordan, MD
St. George’s University Medical School, True Blue, John B. Mulliken, MD
Grenada Children’s Hospital Boston, Harvard Medical School,
Figures 6-6B and 7-25 Boston, Massachusetts, USA
Figure 9-42
Linda J. Juretschke, MD
Ronald McDonald Children’s Hospital, Loyola W. Jerry Oakes, MD
University Medical Center, Maywood, Illinois, USA Children’s Hospital Birmingham, Birmingham,
Figure 7-31 Alabama, USA
Figure 17-42B
Dagmar K. Kalousek, MD
Department of Pathology, University of British †Dwight Parkinson, MD
Columbia, Children’s Hospital, Vancouver, British Departments of Surgery and Human Anatomy &
Columbia, Canada Cell Science, University of Manitoba, Winnipeg,
Figures 8-11AB, 11-14A, 12-12C, 12-16, and 20-6AB Manitoba, Canada
Figure 17-14
E.C. Klatt, MD
Department of Biomedical Sciences, Mercer University Maulik S. Patel, MD
School of Medicine, Savannah, Georgia, USA Consultant Pathologist, Surat, India
Figure 7-16 Figure 4-15
Wesley Lee, MD Dr. Susan Phillips
Division of Fetal Imaging, William Beaumont Hospital, Department of Pathology, Health Sciences Centre,
Royal Oak, Michigan, USA Winnipeg, Manitoba, Canada
Figures 13-20 and 13-30A Figure 18-6
Deborah Levine, MD, FACR Srinivasa Ramachandra, MD
Departments of Radiology and Obstetric & Figure 9-13A
Gynecologic Ultrasound, Beth Israel Deaconess
Medical Center, Boston, Massachusetts, USA †Dr. M. Ray
Figures 6-8, 6-15, 8-10, 9-43CD, 17-35B, and cover image Department of Human Genetics, University of
(magnetic resonance image of 27-week fetus) Manitoba, Winnipeg, Manitoba, Canada
Figure 20-12B
E.A. (Ted) Lyons, OC, MD, FRCPC, FACR
Departments of Radiology, Obstetrics & Gynecology, Martin H. Reed, MD, FRCPC
and Human Anatomy & Cell Science, Division of Department of Radiology, University of Manitoba and
Ultrasound, Health Sciences Centre, University of Children’s Hospital, Winnipeg, Manitoba, Canada
Manitoba, Winnipeg, Manitoba, Canada Figure 11-27
Figures 3-7, 3-9, 4-1, 4-13, 5-19, 6-1, 6-10, 6-12, 7-23,
7-26, 7-29, 11-19CD, 12-45, and 13-3
†Deceased.