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The Egyptian Journal of Hospital Medicine (July 2019) Vol. 76 (5), Page 4077-4084
4077
Received:3/5/2019
Accepted:2/6/2019
Prenatal Diagnostics for Neurosurgical Pathologies
Hamdy Mohamed Bhiry, Adel Ragab Al Melesy, Ahmed Mohamed Kamer Eldawla abdelmotaal*
Department of Neurosurgery, Faculty of Medicine, Al-Azhar University
*Correspondence author: Ahmed Mohamed Kamer Eldawla abdelmotaal, Mobile: (+20)01002074740,
E-mail: ahmadkamer@yahoo.com
ABSTRACT
Background: The advance in the prenatal diagnostics, particularly in imaging tools during the pregnancy (ultrasound
and magnetic resonance) allowed the early diagnose of many fetal diseases, including the neurological conditions.
This progress brought the neurosurgeons the possibility to propose treatments even before birth.
Objective: The aim is to study the role and effect of prenatal diagnostics for neurosurgical pathologies as regard to
early detection and management.
Conclusion: Further progress is necessary to enable fetal neurosurgery in becoming the main technique used in treating fetal
neurosurgical diseases. However, we believe that correct prenatal diagnosis and adequate selection of fetuses with
myelomeningocele, hydrocephalus, and occipital encephalocele may contribute to the benefits provided by neurosurgical
procedures during the fetal period.
Keywords: Prenatal Diagnostics, Neurosurgical Pathologies
INTRODUCTION
The advance in the prenatal diagnostics,
particularly in imaging tools during the pregnancy
(ultrasound and magnetic resonance) allowed the early
diagnose of many fetal diseases, including the
neurological conditions. This progress brought the
neurosurgeons the possibility to propose treatments
even before birth (1).
The neurosurgeon can be called on to interpret
the meaning of diagnostic studies and must be ready to
meet this emerging challenge and benefit from
knowledge about which anomalies may require pre- or
postnatal intervention, where the birth should take place
and how the baby should be born (2).
The prenatal neurosurgical consultation serves
three primary purposes. First, it enables prospective
parents to learn from a physician knowledgeable about
the care and prognosis of infants with a particular
condition. Second, it enables the prospective parents and
the neurosurgeon to get a head start forging a therapeutic
alliance. Finally, prospective parents can participate in
decisions about specific interventions such as fetal
surgery, the timing and route of delivery, and any surgery
that may be required soon after birth (3).
Aims of ultrasonography include
determination of gestational age and fetal number,
evaluation for malformations, testing of fetal well-
being, and assistance with invasive diagnostic and
therapeutic procedures (4).
Amniocentesis, the first available prenatal
chromosomal diagnostic testing option, was first
described in the 1950s (1). Amniocentesis became
increasingly safe and is now used for several purposes,
including genetic screening and infectious
evaluations. Chorionic villus sampling (CVS) is
another diagnostic test and can be performed earlier in
gestation(5).
Myelomeningocele is the most recognized
disease that can be treated during pregnancy with a
high rate of success. Additionally, this field can be
extended to other conditions such as hydrocephalus
and encephaloceles. However, each one of these
diseases has nuances in the diagnostic evaluation that
should fit the requirements to perform the fetal
procedure and overbalance the benefits to the patients
(6).
AIM OF THE WORK
The aim is to study the role and effect of prenatal
diagnostics for neurosurgical pathologies as regard to
early detection and management.
I. Diagnostic Tools
Different types of tests are available during
pregnancy, but they can be classified into two main
categories (7).
A screening test shows if a pregnancy is at
‘increased risk’ of a birth defect. Different screening
tests are available in the first or the second trimester
of pregnancy. These results indicate the risk that a
baby may have a syndrome. A screening test does not
give a definite answer, but it does tell us which babies
have an increased risk of having a pathology. The
results may then help you decide if you want to have
a diagnostic test (8).
A diagnostic test can identify a condition,
and is very accurate. Diagnostic invasive tests (e.g.
chorionic villus sampling and amniocentesis)
however, increase the risk of miscarriage. This is why
diagnostic tests are not routinely offered to all women.
Instead, tests are offered in two stages. All women
should be offered a screening test which carries no risk
of miscarriage or harm to the baby (8).
Ultrasonography:
Ultrasonography is the method most
commonly used for fetal imaging because it allows
real-time examination of the fetus and avoids radiation
exposure. Ultrasonography is exquisitely sensitive to
the interfaces between solid tissue and water;
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therefore, the size and shape of the fetal ventricular
system are easily seen (9).
Figure (1): 13 weeks fetus with anencephaly (9).
Magnetic Resonance Imaging
A valuable complement to prenatal
sonography, fetal MR imaging is a powerful technique
used to evaluate the fetal brain. Fetal MR imaging has
higher contrast resolution than prenatal sonography
and allows better differentiation of normal from
abnormal tissue. Structural abnormalities such as
cerebral malformations and destructive lesions can be
sonographically occult on prenatal sonography yet
detectable by fetal MR imaging (10).
Diagnostic fetal specimen or tissue
Chorionic villus sampling (CVS) has decreased
in frequency with the recent increased uptake of cell-free
DNA screening. It remains the only diagnostic test
available in the first trimester and allows for diagnostic
analyses, including fluorescence in situ hybridization
(FISH), karyotype, microarray, molecular testing, and
gene sequencing. CVS is performed between 10 and 14
weeks’ gestation. CVS has been performed before 9
weeks in the past, though this has shown to increase the
risk of limb deformities and, therefore, is no longer
recommended. It may be performed via either
transcervical or transabdominal approach. Via either
approach, chorionic villi are collected for genetic
evaluation under ultrasound guidance without entering
the amniotic sac (6).
CVS allows for earlier prenatal diagnosis,
subsequently decreasing time of uncertainty and
allowing for earlier (and, therefore, safer) pregnancy
termination if desired. A disadvantage of CVS, however,
is that approximately 1% to 2% of CVS results may
reflect confined placental mosaicism rather than true
fetal chromosomal abnormalities. Confined placental
mosaicism may increase the risk of having a small-for-
gestational-age infant. Pregnancy loss attributed to CVS
is approximately 1 in 455 on the most recent estimates
(7).
II. Fetal CNS Developmental Anatomy
Brain and spinal cord development begins
with neurulation, which is the process of neural tube
formation that occurs in the third and fourth weeks of
gestation. In the fifth and sixth weeks, prosencephalic
development occurs, giving shape to the developing
brain. Cortical development is divided into stages of
cell proliferation, neuronal migration, and
postmigrational cortical organization. Myelination
and cortical organization are the final steps of brain
development and continue well beyond birth (11).
Embryology of Central Nervous system
The central nervous system (CNS) consists of
the brain and spinal cord, which develop from the
neural tube. The peripheral nervous system (PNS)
contains cranial and spinal nerves that consist of
neurons that give rise to axons, which grow out of the
neural tube, and neurons derived from neural crest
cells. Skeletal motor neurons and axons of
preganglionic autonomic neurons are derived from the
neural tube.Neural crest cells form sensory neurons
and postganglionic autonomic neurons. The neuronal
cell bodies of these neurons are found in ganglia.
Therefore, all ganglia found in the PNS contain either
sensory or postganglionic autonomic neurons and are
derived from neural crest cells. Chromaffin cells are
neural crest cells, which migrate into the adrenal
medulla to form postganglionic sympathetic neurons.
Neurulation begins in the third week; both CNS and
PNS derived from neuroectoderm. The notochord
induces the overlying ectoderm to form the neural
plate (neuroectoderm). By end of the third week,
neural folds grow over midline and fuse to form neural
tube (12).
Sonographic Anatomy
The early embryo is best examined transvaginally.
The cephalic end is identiiable by about 8 weeks. By 10 or
11 weeks, bones of the vault show mineralization (13).
At this age, the brain mantle is very thin. The
ventricles are large and illed with choroid, which provides
nourishment for the developing brain. A large, echo-free
space behind the hindbrain represents the rhombecephalic
cavity, which decreases in size as the cerebellum forms and
is destined to become the fourth ventricle (14).
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Figure (2): Early normal fetal head images obtained with
transvaginal probe. (A) At 8 menstrual weeks (B) Scan at
12 weeks(14).
Normal Fetal MR Imaging
MR imaging of the fetal cerebrum is
characterized initially by the presence of multiple
layers that disappear as the brain matures and the sulci
form (15).
Knowledge of the timing and appearance of
these layers and sulci are very important in the proper
interpretation of fetal brain MR imaging studies(15).
The ventricular zone, or germinal matrix, is
the innermost layer of the fetal cerebral hemisphere; it
forms a smooth, dark band of low T2 and high T1
signal intensity lining the lateral ventricles from early
gestation (15).
Figure (3): Coronal SS-FSE T2-weighted image at
gestational week 23. Germinal matrix (arrowhead)
periventricular zone (arrow). Subventricular and
intermediate zones (double arrows). Subplate (double
arrowheads). Germinal matrix (triple arrows) (15).
The size of the lateral ventricles is best
assessed by sonographic measurements of the atria,
because both the technique of measurement and the
normative values are well established. In particular,
the measurement must be made through the posterior
aspect of the glomus of the choroid plexus on an axial
plane obtained through the thalami, which is easy to
obtain with sonography (10).
Fetal MR imaging can be helpful in assessing
the shape of the entire ventricular system, and in
assessing the walls of the lateral ventricles, which
should be smooth throughout gestation. It should also
be noted that fetal subarachnoid spaces are prominent,
particularly before gestational week 30, relative to a
term neonate (10).
III. Hydrocephalus
Fetal hydrocephalus continues to present a
challenge, not only for neurosurgeons but also for
obstetricians and the entire community involved in the
medical, religious, ethical, and legal aspects related to
this condition (16).
In the early twentieth century, fetal
hydrocephalus was a cause of maternal mortality due
to uterine rupture. Currently, however, with the use of
diagnostic tools such as ultrasonography and magnetic
resonance imaging (MRI), a pregnant woman has the
option to terminate her pregnancy, especially in
countries where abortion is legal (1).
Epidemiology
The real incidence of fetal hydrocephalus is
probably underestimated because many cases of fetal
death early in gestation are often not studied. In fact,
it is not even known how often abortions are
performed among mothers of hydrocephalic fetuses. It
is believed that the incidence rate of such cases varies
between 0.2 and 1.5 per 1000 live births. The
incidence varies significantly according to different
authors and locations (17).
Diagnostic
Obstetric ultrasonography as part of routine
prenatal monitoring is the standard method for
diagnosing intrauterine ventriculomegaly. Fetal
ventriculomegaly or hydrocephalus are complex
definitions and are often difficult to differentiate and
accurately identify (18).
Advances in ultrasonography caused a
revolution in the practice of obstetrics. Especially
when used after the 15th week of pregnancy,
ultrasound allowed the easy diagnosis of numerous
malformations (19).
Clinically, most cases of fetal hydrocephalus
are accompanied by polyhydramnios, a fact that may
lead the obstetrician into a false diagnosis and
suspicion of an error in the gestational age. An
ultrasonographic image is then requested for
clarification and the hydrocephalus is finally
diagnosed (20).
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Figure (4): Assessment of ventricles at 23 weeks
shows normal, mild asymmetry.
(A) Axial view shows the usually measured lower
ventricle (calipers).
(B) By viewing through the posterior squamosal suture,
one can visualize the upper ventricle in the oblique axial
plane (calipers). Oblique image planes can increase the
ventricular measurement; thus it is important to obtain a
true axial view that shows both ventricles for
measurement if the upper ventricle appears enlarged.
(C) and (D) Coronal “owl’s eye” view through the
lambdoid suture shows asymmetry of the occipital horns
(calipers). Mild asymmetry less than 2 to 3 mm is
common and normal. c, Cerebellum.
(E) and (F) Views taken through the anterior fontanelle
analogous to neonatal head ultrasound are an alternate
approach to assessing both ventricles. (E) shows the
occipital horns and (F) shows the anterior horns and
conirms slight ventricular asymmetry (20).
Etiology and Classification
Congenital hydrocephalus is one of the most
common congenital anomalies affecting the central
nervous system and results from an imbalance of CSF
formation and absorption (17). This imbalance results
in the accumulation of CSF, increased ICP, and
dilation of the ventricles (20).
In fetal ventricular dilatation, it is very
important to differentiate between ventriculomegaly
and hydrocephalus. Ventriculomegaly may be the
result of atrophy or hypoplasia of the central nervous
system or malformation associated with agenesis of
the corpus callosum, while in hydrocephalus the
ventriculomegaly is hypertensive(20).
Technical notes
In order for the intrauterine treatment of
hydrocephalus to be successful, the cases should be
isolated, progressive, without chromosomal
abnormalities and a gestational age less than 30
weeks, with a diagnosis of severe, isolated, acute,
progressive, or obstructive hydrocephalus(12).
Repeated cephalocentesis was performed
under ultrasound guidance with the mother under
opioid sedation. The volume of liquor removed varied
from 20 to 120 ml. The fetal heart beat was monitored
throughout the procedure, and removal of liquor
discontinued as soon as any deceleration occurred in
the fetal heart rate (1).
Cephalocentesis was performed as necessary
until pulmonary maturity. Corticosteroid
administration to the mother is recommended before
the first cephalo- centesis in order to accelerate fetal
lung maturity. On average, 4–8 procedures were
performed per fetus, with intervals of 4–5 days in
between. The indications were mainly for cases of
hydrocephalus with hemorrhagic liquor or
cerebrospinal fluid with high protein rates, especially
when close to fetal lung maturity (21).
Ventriculoamniotic shunting was
performed percutaneously under ultrasound guidance,
and a pigtail catheter (KCH-Rocket Medical PLC,
New England) was inserted. One tip of the catheter
was left in the fetal lateral ventricle and the other in
the amniotic cavity(21).
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Figure (5): Scheme of ventriculoamniotic shunt placement. (a) Ultrasound-guided transabdominal puncture reaching the
occipital horn of the lateral ventricle. (b) Catheter insertion and intraventricular portion released after partial removal of the
trocar. (c) Complete removal of the trocar to release the catheter in the amniotic cavity and decrease hydrocephaly. (d) Double
pigtail catheter. (e) Patient at birth exposing the ventriculoamniotic shunt used during the uterine life to treat a fetal
hydrocephalus, in detail can be seen that the catheter was still working. (f) Example of a fetal hydrocephalus due to aquecdutal
stenosis treated by ventriculoaminiotic shunt. The pre and post MRIs show the reduction of the ventricular cavities after
procedure(21).
Third ventriculostomy was performed under
fetal anesthesia. Always under ultrasound guidance, the
umbilical cord was punctured with a thin needle, the
umbilical vein catheterized, and a total dose of 5 μg/kg of
fentanyl citrate and 0.1 mg/kg pancuronium bromide was
administered. Five minutes after fetal anesthesia, a small
incision was made in the mother’s abdominal skin with an
11-blade scalpel. Again, under ultrasound guidance, the
fetal skull was punctured with a 2.5-mm-diameter needle
on the brim of the bregmatic fontanelle, providing access
to the lateral ventricle. As soon as the mandrel was
withdrawn, liquor exited under increased pressure. A 2.3-
mm-diameter neuroendoscope (Neuroview, flexible
scope, 25C, Traatek, USA) was inserted through the
needle, as well as a 1 mm working channel connected to a
300 W xenon lighting system. Monro’s foramen could be
identified and the endoscope was inserted into the third
ventricle, its floor was opened, and the fetal basilar artery
could be visualized. The opening was sufficiently enlarged
with a 2-Fr Fogarty catheter, and the endoscope was
withdrawn along with the needle. A small occlusive
dressing was applied to the mother’s abdomen(21).
IV. Neural Tube Defect
Open neural tube defects (ONTDs) are the most
frequent malformations of the central nervous system
(CNS). Myelomeningocele (MM) is the most severe
open neural tube defect that is compatible with life. This
closure disorder occurs in the third week of gestation,
and biochemical, genetic, and environmental
phenomena are involved in its genesis (22).
Comparison of fetal and postnatal surgeries
Some of these changes can be explained during
the fetal surgical procedures but cannot be verified in
postnatal surgical procedures. These changes include
the Bdry brain^ that is verified by the lemon
sonographic sign and features intracranial hypotension.
Another alteration is the presence of a fibrous ligament in
the apex of the placode adhered to the dura mater in the
apical portion of the malformation that results in a tethered
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cord and pulls the brainstem and cerebellum down and into
the rachidian canal resulting in a microcephaly, a small
posterior fossa, and poor development of the subarachnoid
space of the posterior fossa. With the development of a
pregnancy that is associated with intracranial hypotension,
the occipital bone, which consists of 8 segments, fuses
rapidly, making the posterior fossa inelastic, similar to that
in craniosynostosis. In addition, the cerebral aqueduct
becomes patent, there is no Chiari type II, and the CSF is
circulating; however, globally, there is an accumulation of
CSF in the subarachnoid space. This leads to an increase
in the head circumference without signs of intracranial
hypertension and normal neuropsychomotor development
(23).
V. Other Fetal Neurosurgical Pathologies
Encephalocele is a congenital neural tube defect
characterized by a median cranial bone cleft defect that
results in protrusion of the meninges (meningocele) or
of the meninges and neural tissue (encephalocele) (1).
Encephalocele
It has an estimated prevalence of 0.8–2.0 per
10,000 live births [48–50]. One third of patients die from
this condition, with 76% of deaths occurring in the first day
of life. Half of the patients who live beyond the first day
will experience some degree of neurodevelopmental
delay. The strongest risk factors for death are
hydrocephalus and microcephaly (1).
Tethered spinal cord
Tethered spinal cord syndrome is a clinical
entity in which spinal cord function is compromised by
inappropriate attachment of and traction upon the cord,
which appears to be associated with compromised tissue
perfusion. Tethering of the cord is associated with a
variety of etiologies, including scar formation from
prior surgery (such as myelomeningocele repair) or an
anomaly of secondary neurulation resulting in
inappropriate conus traction from a filum lipoma or
lipomyelomeningocele (11).
Diastematomyelia
Diastematomyelia is a rare congenital anomaly that
results in a longitudinal split of the spinal cord usually
occurring at the level of the upper lumbar vertebrae. The
genesis of this anomaly is thought to occur very early in
gestation during gastrulation and prior to neural tube
closure. The two hemicords are typically separated by a
fibrous, cartilaginous, or osseous septum and reside in two
separate dural tubes (type I split cord malformation) (24).
Type II split cord malformations have both
hemicords within a single, non-duplicated, dural tube.
Each hemicord usually contains a central canal, one dorsal
horn and one ventral horn. The two hemicords typically
reunite caudally, though two coni medullarae may be seen
in diplomyelia, an embryologically distinct entity.
Diastematomyelia is typically associated with vertebral
segmental anomalies (9).
Vascular anomalies
Brain vascular malformations are rarely
diagnosed in fetuses. The most common is the vein of
Galen aneurysm. The vein of Galen aneurysm (VGM)
is a vascular malformation of the choroid plexuses that
drains into the vein of Galen. Because of the high flow
the vein dilates and resembles an aneurysm. Other
malformations are not usually seen as the draining veins
are smaller and therefore not detected by ultrasound (25).
Diagnosis: The diagnosis is suspected during the
third trimester ultrasound examination when a cyst-like
structure is seen in the region of the posterior fossa (18).
The Doppler ultrasound and in particular the
colour Doppler makes the diagnosis by showing high
flow in the structure. The feeding arteries are difficult to
analyse but dilated arteries are visible in the region of
the malformation (26).
Fetal Brain Tumours
Congenital central nervous system tumors
diagnosed during pregnancy are rare, and often have a
poor prognosis. The most frequent type is the teratoma.
Use of ultrasound and magnetic resonance image allows
the suspicion of brain tumors during pregnancy.
However, the definitive diagnosis is only confirmed after
birth by histology (27).
Intracranial teratoma
Teratomas are the most frequent type of
congenital CNS tumors. They represent approximately
62% of all types of brain tumors diagnosed during
pregnancy. The majority of fetal brain teratomas is
histologically benign and generally contains both mature
components from all three germ layers and immature
neuroglial elements. Since the first US description,
approximately 100 reports on the prenatal diagnosis of
fetal intracranial teratomas were published (28).
Choroid plexus papilloma
Choroid plexus papilloma (CPP) is a rare and
benign tumor composed of epithelial cells that line the
ventricular choroid plexus, and correspond to 0.4%-0.6%
of fetal intracranial tumors. The incidence is inversely
correlated with age, and 50% of patients in the pediatric
age group are diagnosed during the first year of life (22).
CPP may develop in the lateral ventricle, third
ventricle, and fourth ventricle. It is generally diagnosed
during the third trimester and is always associated with
unilateral or bilateral ventriculomegaly. CPP has slow
growth and noninvasive behavior; however, because of its
specific location, CPP can block the drainage of
cerebrospinal fluid and cause hydrocephalus (29).
Craniopharyngioma
Craniopharyngiomas are benign and represent
2%-5% of all congenital CNS tumors. They develop from
remnants of squamous cells originating from Rathke’s
pouch (ectodermal diverticulum originating from the
upper limit of the oropharynx) and are most commonly
found in the suprasellar region(30).
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Although histologically benign, tumor expansion
can cause significant destruction of the brain parenchyma
and hydrocephalus. An intracranial large echogenic mass
(basically indistinguishable from teratomas) is diagnosed
by ultrasound (3).
MRI can help in determining the remaining brain
structures and exact localization of the tumor. The head
circumference may be increased because of the size of the
tumor, and hydrocephalus may be present because of
secondary obstruction of cerebrospinal fluid drainage.
Differential diagnoses include: teratomas, astrocytomas,
and hamartomas (3).
SUMMARY
Thirty years after the first in utero procedure for the
treatment of fetal hydrocephalus, and other neurosurgical
anomalies, little progress has been made with respect to the
neurosurgical techniques for the management of that disease
during the gestational period.
Diagnostic techniques have improved vastly and
they now have a better ability to evaluate cases of fetal
hydrocephalus and associated malformations of the central
nervous system.
It is believed that in utero fetal procedures should be
performed in cases of acute instances of evolving but
nondestructive hydrocephaly without any other associated
malformation.
Procedures to prevent hydrocephalus, such as closure
of myelomeningoceles in fetuses before the 26th gestational
week, should be encouraged.
With the development of diagnostic methods for
identifying fetal neurosurgical diseases, it is crucial that
neurosurgeons develop minimally invasive surgical
techniques that allow fetuses to benefit from the procedures
performed early in the intrauterine life.
The main errors made in the treatment of fetal
hydrocephalus arise from the difficulty of accurately
diagnosing hydrocephalus. It is clear that fetuses with acute
obstructive hydrocephalus, which is often caused by a
Coxsackie virus infection, benefit from hydrocephalus
treatments, while fetuses with chronic destructive
ventriculomegaly, such as those seen in Bicker-Adams
syndrome or after infection by the Zika virus, will show a
catastrophic evolution.
Thus, a multicenter cooperative study is required for
the treatment of evolutive fetal obstructive hydrocephalus.
Further, the inclusion of an efficient surgical technique is
also important.
Cephalocentesis can be performed safely, as it allows
not only a better diagnosis but also an isolated measure of
intracranial pressure; it can also be used therapeutically
when the fetus reaches lung maturity.
They rarely used fetal endoscopic third
ventriculostomy due to the difficulty to enter the Kocher’s
point to access the third ventricle. However, it is possible to
initiate the procedure, and in case the third ventriculostomy
cannot be performed, a ventriculoamniotic shunt can be
placed.
The MOMS results show that it is crucial that
several neurosurgery centers are dedicated to this type of
treatment during the fetal period. The open surgery
technique is the main form of treatment and produces
excellent results when compared with those obtained
through the traditional technique of closure after birth.
Failure can occur during the treatment of fetal
myelomeningocele. In most cases, they found a fibrous
ligament that attaches the medulla to the dura mater in the
upper part of the dysraphism. This ligament is not always
found in postnatal procedures, or it is located in cranial
positions, which determine the clinical condition of tethered
cords. Another phenomenon observed in most cases in the
postoperative period is the increase in the posterior fossa
volume, which is related to the embryogenesis of the
occipital bone and increased intracranial pressure after
correction of the fistula.
Further progress is necessary to enable fetal
neurosurgery in becoming the main technique used in
treating fetal neurosurgical diseases. However, we believe
that correct prenatal diagnosis and adequate selection of
fetuses with myelomeningocele, hydrocephalus, and
occipital encephalocele may contribute to the benefits
provided by neurosurgical procedures during the fetal
period.
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