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x Contributors
Eldad Katorza, MD
Department of Obstetrics and Gynecology
The Chaim Sheba Medical Center
Sackler School of Medicine
Tel Aviv University
Tel Aviv, Israel
(Chapter 17)
Tally Lerman-Sagie, MD
Associate Clinical Professor
Fetal Neurology Clinic
Division of Pediatric Neurology
Department of Pediatrics
Edith Wolfson Medical Center
Sackler School of Medicine
Tel Aviv University
Holon, Israel
(Chapter 7, 9, 12)
Gustavo Malinger, MD
Associate Clinical Professor of Obstetrics
and Gynecology
Director, Division of Prenatal Diagnosis
Co-Director, Fetal Neurology Clinic
Department of Obstetrics and Gynecology
Edith Wolfson Medical Center
Sackler School of Medicine
Tel Aviv University
Holon, Israel
(Chapters 4, 6, 7, 8, 9, 10, 12, 16)
Israel Meizner, MD
Professor of Obstetrics and Gynecology
Ultrasound Unit
The Helen Schneider Hospital for Women
Rabin Medical Center—Beilinson Campus
Sackler School of Medicine
Tel Aviv University
Tel Aviv, Israel
(Chapter 13)
Ana Monteagudo, MD
Professor of Obstetrics and Gynecology
Director, Bellevue Medical Center Obstetrics and
Gynecology, Ultrasound Unit
Fellowship Director
Maternal-Fetal Medicine
Department of Obstetrics and Gynecology
New York University School of Medicine
New York, New York
(Chapters 2, 3, 5, 10, 11)
Fabiola Müller, Dr. habil.rer.nat.
Professor Emeritus
School of Medicine
University of California, Davis
Davis, California
(Chapter 1)
Ronan O’Rahilly, MD, DSc
Professor Emeritus
School of Medicine
University of California, Davis
Davis, California
(Chapter 1)
Gianluigi Pilu, MD
Associate Professor of Obstetrics and Gynecology
Department of Obstetrics and Gynecology
University of Bologna, Italy
Bologna, Italy
(Chapters 4, 6, 8, 10, 16)
Ritsuko K. Pooh, MD, PhD
Chief Director, Fetal Diagnostic Unit
Clinical Research Institute of Fetal Medicine
Osaka, Japan
(Chapter 15)
Asuri N. Prasad, MBBS
Associate Professor of Pediatrics
Section of Clinical Neurosciences
Department of Pediatrics and Child Health
University of Western Ontario, London
Ontario, Canada
(Chapter 12)
Ilan E. Timor-Tritsch, MD
Professor of Obstetrics and Gynecology
Director, Division of Obstetrical and Gynecological
Ultrasound
Department of Obstetrics and Gynecology
New York University School of Medicine
New York, New York
(Chapters 2, 3, 5, 11)
Ants Toi, MD, FRCPC, FAIUM
Professor of Radiology, and of Obstetrics and Gynecology
Associate Professor
University of Toronto
Department of Medical Imaging
Mount Sinai Hospital and University Health Network
Toronto, Canada
(Chapter 7)
Foreword xi
wowowowowowowowowo
FOREWORD
Recent advances in imaging of the fetus have furthered our
understanding of the neurodevelopment of the fetal brain.
This third edition of Ultrasonography of the Prenatal Brain
has capitalized on incorporating these new technologies
in this textbook, to bring to the reader the most advanced
information alongside the most impressive images. What
Drs. Timor and Monteagudo provided in their first two
editions, while nothing short of outstanding, has now been
outdone in this third edition. Their choice of Drs. Pilu
and Malinger as the additional editors was a work of
genius. These two individuals, along with Drs. Timor and
Monteagudo, are without a doubt the most talented and
knowledgeable in imaging the fetal brain. While expecting excellence from these authors is the norm, the reader
will not be disappointed. This text is all you would want
and more. In the few chapters in which the editors are not
contributors, they have chosen experts who are clearly the
most knowledgeable on the specific subjects.
In reading this outstanding text, the reader will quickly
marvel at how easily the text flows and is complimented by
exquisite companion images. This edition uses advances
in MRI fetal imaging to perfection. The just-right use of
this modality highlights its most appropriate applications.
At the same time the highest quality 2D and 3D images
beautifully demonstrate how and why ultrasound remains
the frontline modality for prenatal assessment of the fetal
brain. The reader can easily follow normal fetal development from the early embryonic period all the way to the
third trimester. The authors have created a near-perfect
approach that allows the reader to easily recognize even
subtle malformations in development. Along with the
impeccable images the authors of all chapters have incorporated management recommendations including the
appropriate follow-up or use of additional imaging and/or
laboratory methods.
This textbook is a major contribution to the literature.
It is a must for anyone doing prenatal diagnosis and for
every ultrasound laboratory doing any obstetric imaging.
Changes made warrant the addition of this text to one’s
library even if one has the second edition. Whether it is
the new information on the molecular diagnosis, metabolic
disorders, or infectious or vascular changes, any one of these
areas provides enough value in and of itself to warrant
ownership of this third edition. In reading this new book
I can say that I have been given the advanced privilege of
capitalizing on the new information of this edition. I have
already translated many of the newly described diagnostic
pearls into daily practice. While it was already clear to me
before reading this edition that Drs. Timor, Monteagudo,
Pilu, and Malinger are the giants of our field and my expectations were high, after reading the text I was not—and you
will not be—disappointed. Their prolific writing style, combined with the beautiful diagnostic images and pathological
correlation, is impeccable. While many textbooks cannot
be easily read in their entirety, this text reads like a novel.
The reader gets deeper and deeper involved and cannot put
the book down without reading another chapter or two.
You learn from every page read. You marvel at the images.
Drs. Timor, Monteagudo, Pilu, and Malinger are to be
congratulated for bringing us closer to understanding fetal
neurodevelopment and anatomy. I am forever humbled by
being given this honor to write this foreword.
Lawrence D. Platt, MD
Professor of Obstetrics and Gynecology
David Geffen School of Medicine at UCLA
Director Center for Fetal Medicine
and Women’s Ultrasound
Los Angeles, California
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PREFACE TO THE FIRST EDITION
The concept for this book was born many years ago and
was preceded by careful acquisition and selection of representative neurosonograms of normal and abnormal cases.
The central nervous system is probably the most elaborate
and intricate organ or system in the human body. Minute
structural abnormalities can, at times, reflect major functional deficiencies. On the other hand, it would appear that
at times major anatomic defects do not seem to be associated with significantly deviant function. It is extremely
important to study and understand the normal and abnormal fetal and neonatal central nervous system. The central
nervous system is one of the common sites of anatomical
malformation in the fetus with chromosomal abnormality.
The detection of anomalies within the fetal and neonatal
brain is feasible using modern imaging techniques, such
as ultrasound, computed tomography, and magnetic resonance imaging.
The aim of prenatal ultrasonography is to be able to
reassure the pregnant patient as early as possible that fetal
development is normal; or if a malformation is detected to
counsel the patient about the nature of the problem. Most
anomalies of the central nervous system develop early, and
we have the tools to detect these as early as 10 to 16 weeks.
Early detection of such central nervous system anomalies
is probably the most important advance in modern perinatology. Neonatal ultrasound confirms the prenatal diagnosis. In addition, neonatal neurosonography is a powerful
tool in diagnosing central nervous system pathology.
The first chapter deals with the development of the
human central nervous system. Its authors are the distinguished professors Ronan O’Rahilly and Fabiola Müller,
who have a lifetime of professional experience. Professor
O’Rahilly not only took time to write about the embryology
of the brain, but also invested valuable time in overseeing
the correct anatomical terminology used throughout most
of the chapters.
The vast imaging possibilities of ultrasound in general
and that of transvaginal sonography in particular regarding the fetal brain, are dealt with at the beginning of our
book and lead into the chapters describing the detectable
pathology in the fetal and neonatal central nervous system. Because fetal and neonatal neurosonographic scanning is performed using the anterior fontanelle and other
calvarial openings, the “classical” axial planes cannot be
used to describe the images obtained in the fan-shaped
sonographic sections. It was our goal to keep the “classic”
planes in use by CT and by MRI imaging of the brain and
create a separate and well-defined set of planes and sections for the fetal brain imaging. A new nomenclature
regarding the scanning planes of the fetal brain is introduced in Chapters 1, 2, 3, and 4.
We felt that a special and dedicated chapter dealing
with biometry of the fetal brain should be included. A large
number of tables and graphs as well as measurements of
the fetal brain are incorporated for reference.
Because the fetal eye and the fetal face are frequently
associated with brain pathology, two special chapters are
devoted to these structures. Dr. Israel Meizner and Dr.
Moshe Bronshtein’s group from Israel have the most imaging experience in these two areas and contributed these
two important chapters, which we believe are the most
detailed in the literature dealing with those subjects.
Neonatal neurosonology is an established diagnostic
entity which has earned its well-deserved place in the
armamentarium of the neuroimager since its introduction
in 1979. Chapters concerning imaging of the normal and
abnormal neonatal brain, and the chapter by Dr. Madhuri
Kirpekar dealing with the spine, are included to form a
continuum as far as the sonographic neuroimaging workup of the prenatal and neonatal CNS.
The chapter written by Gianluigi Pilu and Vincenso
D’Addario and their co-workers from Italy, made a significant contribution to the book by touching on the subject of
the midline brain pathologies and the recently introduced
attempts to image the fetal brain using MRI.
It is hard and labor intensive to study the physiological
aspects of the brain. This was successfully done by recognized authors such as Jan Nijhuis who reviewed the fetal
behavioral states coordinated by the brain and by Shimon
Degani and Reuven Lewin sky summarizing the clinical
uses of measuring the blood flow to the central nervous
system.
Finally, the ethical aspects of neurosonography are
explored by Frank Chervenak, who over the years has
become an authority in the field of medical ethics.
This book was written for the perinatologists, neonatologists. perinatal geneticists, as well as the imaging
specialists such as radiologists, obstetricians, and sonographers who see the fetus and neonate in their clinical practice. These specialists scan the fetal and neonatal brain
themselves or are directly involved with managing pregnancies with structural malformations or anomalies of
xiv Preface to the First Edition
the central nervous system. Special emphasis was placed
on the creation of an objective and exhaustive updated
review of the pertinent literature so that the reader would
have a wide reference base on each subject. As far as the
illustrations are concerned, the authors were encouraged
to be liberal about including an unrestricted number
of cases and their sonographic manifestations in their
respective chapters. This may, therefore, lead to some
duplication by presenting the same disease or pathology
more than once. However, by allowing some deliberate
repetition in depicting various cases, we, hopefully, covered the commonly occurring pathologies. We consider
such occasional and repetitive presentations as one of the
advantages of the text enabling the reader to be educated
by the experiences of the different authors and their various points of view.
One of the particular strengths of presenting the sonograms is that we chose to include small body images so that
readers could orient themselves as to how an individual
sonographic view was obtained. This will, we hope, enable
readers to quickly grasp and understand the actual planes
used to generate the pictures.
We suggest that neuroimaging of the fetus be included
in the structural evaluation of the fetus at any gestational
age. We also believe that practitioners involved in fetal
and/or neonatal neuroimaging will benefit from using this
carefully prepared text.
Ilan E. Timor-Tritsch, MD
Ana Monteagudo, MD
Harris L. Cohen, MD
PREFACE TO THE SECOND EDITION
Responding to the positive feedback to the First Edi tion of
our book we decided to update it and expand its content.
An additional reason for this decision was the amount of
new and pertinent articles which have accumulated in the
last 3–4 years. We wanted to review them and add most
of them to the more than 1100 references we used in the
First Edition.
As far as the chapters are concerned, every previously
written chapter was updated and there are several new
chapters. Major changes were made in Chapters 2, 4, 5
and 8 to reflect the new clinical experience in the field of
fetal neuroscan and fetal neuro-MRI. New sonographic
images of commonly encountered entities were added to
the previously published ones. Several rarely seen fetal neuropathologies were also illustrated and were in cluded. All
chapters were updated with the newest articles from the literature to justify the term “refer ence textbook,” a term used
by many as they men tion the First Edition of the book.
Two new chapters (9 and 14) were added deal ing
with three-dimensional fetal and neonatal neuroscans.
Pediatric neurologists and neurosurgeons rely on neonatal
CT and MRI images to study the neonatal brain. So far
they seemed hesitant to coun sel and to plan postnatal (and
prenatal) manage ment of pathologies based upon prenatal
ultrasound imaging studies. The reason was the prenatal
images were obtained at planes unfamiliar to them. They
were waiting to see the postnatal imaging studies. Since the
introduction of 2D and now 3D transfontanelle fetal neuroimaging by high-fre quency, high-resolution ultrasound
clear images can be generated in the planes which are
familiar to pe diatric neurologists and neurosurgeons. The
ex pected result of these images is a better understand ing
of the pathologies leading to an earlier prenatal counseling and planning for postpartum manage ment before the
neonatal studies are available. We predict that the 3D fetal
and neonatal brain scan will expand and will be widely
employed as effective diagnostic means.
The addition of two new chapters deals with devastating diseases of the fetal brain and attempts for their correction. Chapter 16 summarizes possi ble causes of cerebral
palsy and Chapter 18 is a de scription of attempts to correct neurological patholo gies in utero. It seems that after
the well-known moratorium to treat diseases of the brain,
while the fetus is still in the womb, there may be a place for
intrauterine treatment for a well-selected patient population after adequately researched surgical pro cedures.
The use of the icons at the side of ultrasound images,
to indicate the particular plane or section at which the
image was generated, was extended to several more chapters. This ensures a better under standing of the anatomy
depicted.
We tried (quite successfully) to standardize the anatomic nomenclature throughout the book and based it
on the latest issue of the internationally ac cepted Nomina
Anatomica. Correctly or incorrectly, some terms are so
deeply “embedded” in the daily use, that it may be impossible to constantly correct them. One such example is the
word “hydrocephaly” (the accepted, correct way to use it)
which over time was changed to “hydrocephalus” and (probably in correctly) used in many publications. We selected to
use the correct term “hydrocephalus” in all chapters.
We hope that the Second Edition of this book will
contribute to the understanding and most im portantly the
earliest possible detection of neurolog ical diseases of the
fetus and the newborn.
Ilan E. Timor-Tritsch, MD
Ana Monteagudo, MD
Harris L. Cohen, MD
PREFACE TO THE THIRD EDITION
It is hard to believe, but the first edition of this book saw
the light 15 years ago. At the time, it became a useful reference for those who wanted to understand the development,
the anatomy, and the pathophysiology of the fetal central
nervous system from the viewpoint of ultrasonography.
After a relatively short 5 years—in 2001—the second
edition of the book was published. We received encouraging feedback from the ultrasound and the feto-maternal
specialists to add the necessary incremental knowledge
and include relevant information to publish an updated
second edition.
During the time from 2001 to recent days, several
things happened that led us to consider the publication of
the third edition of the book.
The first compelling reason to update the book was
the “outburst” of new clinical research regarding imaging of the fetal brain. The use of high frequency and deep
penetrating ultrasound transducer probes yielded increasing resolution, hence more accurate pictures of the fetal
brain and spine. These high-resolution pictures found
their way into the traditional “printed journals,” but even
more so into the electronic media. Lectures at courses and
webinars, and teaching on CDs and the Internet, spread
the understanding and knowledge, requiring an organized
way to compile it and reach out to those interested in the
subject.
The second impetus to practically rewrite the previous
edition was the tremendous improvement and dissemination of three-dimensional ultrasound techniques and
magnetic resonance imaging. By resonating to these, we
decided to incorporate those two imaging modalities into
the individual chapters wherever necessary to enhance
understanding, rather than leaving them as stand-alone
chapters. In the previous editions, we had placed these
two subjects in their separate chapters. Our intention was
to emphasize, teach, and incorporate these two important
imaging technologies. Now that they are used daily to
complement traditional ultrasound imaging of the fetal
brain, we incorporated this use as an integral part of the
many “older” as well as the new chapters.
The third and not less important reason to redo and
rejuvenate the book was the increasing interest in imaging
the fetal nervous system as it pertains to imaging the fetal
brain. The surging clinical research in Europe, North
America, South America, and Israel, to name only a few
locations, gave birth to a new generation of young and
enthusiastic imagers, maternal–fetal medicine specialists,
radiologists, and basic scientists, who literally inundated
the field with new observations. As a result of this data
surge, conference goers and others kept asking when a new
edition of the book would be released.
To answer all three issues and explain the horizons of
the new edition, Gustavo Malinger of Israel and Gianluigi
Pilu of Italy graciously agreed to serve as co-editors. It was
the widening of our perception of teaching that led us to
change the format of the chapters completely, making
them easier to read and easier to find points of interest.
There is no doubt that adding new chapter authors, as
well as scores of new 2D and 3D ultrasound images and
updated literature were the necessary ingredients to consider this textbook of fetal neuroimaging a relevant reference source.
As to the newly added chapters, we would like to
mention them briefly. Ventriculomegaly was given its
own importance. It is the most common presenting sonographic sign of brain pathology; therefore, the possible
underlying clinico-pathologic reasons for it were “carved
out” from the many different sites that were mentioned,
creating a dedicated chapter for easy reference.
The different anomalies were reclassified, such as
those of the ventral and dorsal induction, and that of
cortical development. We tried to pour light upon a
diagnostically problematic area of the fetal brain, namely
the posterior fossa, focusing on a small but nevertheless
important structure, the vermis. Three new chapters
dealing with intrauterine insults, intrauterine infections,
and metabolic disorders were also added to cover the
progress made in those areas that became pertinent to
fetal neuroscans.
In short, the newly incorporated chapters, along with
those updated and carried over from our last edition, may
render this new edition useful for those engaging in the
clinical evaluation of the fetal brain.
Ilan E. Timor-Tritsch, MD
Ana Monteagudo, MD
Gianluigi Pilu, MD
Gustavo Malinger, MD
ACKNOWLEDGMENTS
We thank Ms. Christonia Joseph for her tireless editorial and secretarial work and for coordinating the production
of this book. We also thank the editorial team of McGraw-Hill Medical for their work in producing this new edition
of our book.
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Ultrasonography of the
Prenatal Brain