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Chapter 2 Normal Two- and Three-Dimensional Neurosonography of the Prenatal Brain
PCA TC
V
CSP
CC
29
The
3V
4V
CM
(CSF): the choroid plexuses. These structures are found in all lateral ventricles.
The choroid plexuses consist of villi in large numbers, the outer (ventricular) surface of which is covered by a single-layered, modified cuboidal epithelium (ependyma). The inner layer is a stromal core derived from the pia. The capillaries found in each of these villi are the major source of CSF production.
Embryologically, the choroid plexuses develop from the anteriorly located ventricles, more precisely, from their medial and upper wall. The stroma and the covering pia are derived from the mesenchyme. Even though the choroid plexuses are present from 6 to 7 postmenstrual weeks on, it takes several weeks until it becomes large and echogenic enough to be detected by a high-frequency transvaginal probe. At 8 to 8½ postmenstrual weeks, it is small in size and already significantly echogenic ( Figure 2–18 ). Starting from the ninth postmenstrual week, it is consistently seen on the two sides of the falx within the lateral ventricles. It can be said that it is the most striking sonographic intracranial structure well beyond the end of the first trimester. At 9 to 11 postmenstrual weeks,
AH
TH
CP
OH
IH
Figure 2–48. The targeted or more detailed fetal neurosonogram contains other planes and sections; the sagittal planes are displayed in this figure.
The brain specimen supports the ultrasound image.
scanning sound waves if an extremely echogenic struc­ture, namely, the choroid plexus, did not highlight them. These connections were reportedly detected as early as 8½ postmenstrual weeks by the Trondheim group. interventricular foramina (Monro) are clearly visible from 14 to 16 postmenstrual weeks on and mark the most typical coronal (midcoronal–2) section of the fetal brain ( Figures 2–38C and 2–39C ).
The cerebral aqueduct (Sylvius), the connection between the third and fourth ventricles, was not reported to be detected by ultrasonography of the normal fetal brain. This may soon change using 3D imaging when a special plane to detect and study this extremely thin struc­ture can be created by the multiplanar capability of this technique.
Using a posterior (occipital) axial or median approach, the median aperture (Magendie) can be seen ( Figure 2–44 ). This aperture is wide open before 16 postmenstrual weeks and is more easily detected before 20 postmenstrual weeks than after. This aperture becomes wide open in cases of abnormal dilations of the cerebellomedullary cistern (the cisterna magna) and the fourth ventricle (see Chapter 4 ).
the choroid plexuses fill both lateral ventricles ( Figures
Choroid Plexuses
An integral part of the ventricular system is a complex tissue dedicated to the production of cerebrospinal fluid
2–21 , and 2–23 ). As pregnancy progresses, their relative size compared with the lateral ventricular size decreases. They “move” posteriorly and assume their permanent anatomical site within the atrium, “hugging” the thalami
Chapter 2 Normal Two- and Three-Dimensional Neurosonography of the Prenatal Brain
Anterior horns
Interventricular
foramen (Monro)
61
Body of lateral ventricle
Atrium
Posterior horns
Third ventricle
A
Inferior horns
Lateral aperture
(Luschka)
Central canal
Cerebral aqueduct
(Sylvius)
Fourth ventricle
Median aperture
(Magendie)
B
Figure 2–49.
the brain, seen from the left side.
The ventricular system of
Figure 2–50.
C
(A) 12, (B) 18, and (C) 32 postmenstrual weeks. (From Day, 1959, permission.)
The development of the human fetal lateral ventricles at
44
with
62
Chapter 2 Normal Two- and Three-Dimensional Neurosonography of the Prenatal Brain
AB
Figure 2–51. ( A, B) Two axial sections of the brain at 26 postmenstrual weeks, showing the obscured near field due to ineffective transabdominal
imaging of the hemisphere close to the transducer (open arrows).
Cisterna
Magna
4th Ventricle
28 Week fetus
Anterior
Horn
Stored Image #8
A
Third
Ventricle
Thalamus
Cerebellum
Stored Image #4
B
Figure 2–52.
fourth and third ventricles at 28 postmenstrual weeks. A and B axial sections tilted slightly backward.
The more advanced technology of the transabdominal transducer allows visualization of very fine detail of the cerebellum as well as the
Chapter 2 Normal Two- and Three-Dimensional Neurosonography of the Prenatal Brain
Table 2–4. DIAMETER OF THE NORMAL LATERAL VENTRICULAR ATRIUM
AS A FUNCTION OF POSTMENSTRUAL AGE
Postmenstrual Weeks Mean ± SD (mm) Range (mm)
14–20 7.6 ± 0.7 6.0–9.0
21–25 7.7 ± 0.5 7.0–9.0
26–30 7.5 ± 0.7 6.5–9.0
31–38 7.6 ± 0.5 7.0–8.5
Modified from Cardoza and colleagues, 1988,51 with permission.
63
from posterior and above ( Figure 2–35 ). Their posterior contour is smooth. If they lose their regular contour, one should suspect an adjacent intraventricular hemorrhage. An obviously thin or dangling choroid plexus should arouse suspicion of ventriculomegaly or hydrocephaly. The tela choroidea is the thin choroid plexus layer covering the thalami, extending into the third ventricle ( Figures 2–39C and 2–43 ). The choroid plexus of the fourth ventricle is extremely difficult to image. Therefore, to our knowledge, it is not mentioned in the pertinent literature.
It should be emphasized that the choroid plexus may give rise to tumors, such as choroid plexus papilloma and carcinoma.
THE CAVA
The cavum septi pellucidi and its posterior part, the cavum Vergae, are not strictly part of the ventricular system; if found at autopsies of infants and adults, they are generally considered insignificant. The cavum septi pellucidi and the cavum Vergae are, in fact, the same structure, the former located anteriorly and the latter positioned posteriorly to a vertical plane formed by the columns of the fornix. The two usually communicate with each other ( Figure 2–53A and B ). The presence or absence of the cavum septi pellucidi as a function of age was studied by Shaw and Alvord. of 374 normal subjects, they found that 100% of the pre­mature infants had a cavum septi pellucidi wider than 1 mm. The cavum Vergae closes first, well before term, and the cavum septi pellucidi starts to close just before term. Table 2–5 also shows that at 6 months of age only 12% of the brains had a recognizable cavum. This group did not report on the age of the premature infants.
Jou et al
68
measured the width of the cavum septi pel­lucidi from 19 to 42 weeks in 608 fetuses. They found that this measurement increased gradually to 27 weeks when it plateaued until term.
Larroche and Bandey
69
is typically absent at birth. This was observed following pneumoencephalographic studies in neonates.
The cava forms simultaneously with the corpus cal­losum. The appearance of the cava on ultrasonographic images is also limited to the first detection of the corpus
67
Dissecting the brains
noted that the cavum Vergae
callosum, that is, about 17 to 18 postmenstrual weeks. At term these spaces become almost obliterated.
Even though it will be discussed in detail later in this chapter when we describe the arteries of the brain, we have to mention here the pericallosal artery. This artery closely follows the corpus callosum. As a matter of fact, three structures and their development are closely interrelated: the corpus callosum; above it, the pericallosal artery; and below it, the cavum septi pellucidi. This parallel develop­ment becomes important when deviant development of the corpus callosum is discussed.
The cavum septi pellucidi is best imaged on the median ( Figures 2–42 , 2–43 , 2–44 , 2–45 ) and the mid­coronal–1 and –2 ( Figures 2–39 and 2–41B ) sections. Two lateral walls separate this structure from the ante­rior horns of the lateral ventricles ( Figure 2–41B ). Failing to detect these lateral walls should arouse suspicion of disease, such as agenesis of the corpus callosum, septo-optic dysplasia, schizencephaly, hydrocephaly, and porencephaly.
70
Corpus Callosum
The corpus callosum is one of the important structures of the brain, connecting the right and left hemispheres. In fact, it is the largest interconnecting structure and consists of myelin-coated nerve fibers that cross the median plane. It forms the roof of the cavum septi pel­lucidi and the cavum Vergae. The development of these structures (ie, the corpus callosum and the cava) is closely linked. Because the roof of the cavum septi pel­lucidi is the corpus callosum itself, it is clear that if there is no roof, there is no cavum.
If the corpus callosum is scanned through the ante­rior fontanelle, the sound waves meet this structure at almost a right angle. The sonographic picture in the median plane of the developed corpus callosum is that of two parallel echogenic lines with a sonolucent strip of ∼3 to 5 mm between them. The upper line is generated by the deepest points of the longitudinal fissure. The lower echogenic line is the roof of the cavum septi pellucidi and the cavum Vergae. The pericallosal artery closely follows the upper boundary of the corpus callosum. The midcoronal–1 and –2 sections depict this commissural structure as semilunar.
64
Chapter 2 Normal Two- and Three-Dimensional Neurosonography of the Prenatal Brain
A
F-1 MC-1 MC-2 MC-3 O-1
B
Figure 2–53.
images were generated along the white lines seen on the median plane. The anterior section “cuts” through the cavum septi pellucidi (CP). The posterior coronal section highlights the cavum Vergae (CV). (B) The systematic scanning using the transfontanelle approach reveals the normal cavum septi pel­lucidi on the MC–2 plane and the still open cavum Vergae on the MC–3 plane. This study uses the sequential “coronal” planes.
The cavum Vergae in the brain of this normal 28-week old fetus is the posterior part of the cavum septi pellucidi. (A) The two lower
Chapter 2 Normal Two- and Three-Dimensional Neurosonography of the Prenatal Brain
Table 2–5. INCIDENCE OF OPEN CAVUM SEPTI
PELLUCIDI AS A FUNCTION OF AGE
Age Percentage Present
Premature 100
Full term to 7 days 97
8 days to 1 month 85
6 month to 16 years 12
Modified from Shaw and Alvord, 1969,67 with permission.
65
After understanding the anatomy and the sono­graphic presentation of the corpus callosum in the various scanning planes, its development should be discussed. The corpus callosum is a relatively late- developing structure reported to develop between the 12th and 18th postmenstrual weeks. develops in an anterior-to-posterior direction, development can be followed sonographically.
71 , 72
It is also known that it
69
but this
20,24,72–74
(See Chapter 1 .)
In Figure 2–35 , which represent coronal and sagittal sections of fetuses at 14 postmenstrual weeks, it is not yet possible to discern the corpus callosum. At 16 postmen­strual weeks, the first hint of its sonographic appearance is present ( Figure 2–38 ). At 18 postmenstrual weeks ( Figures 2–38 and 2–42 ), the anterior portion of the genu and almost all of the central part are seen. Figure 2–44 depicts images of the corpus callosum from 18 to 28 postmen­strual weeks.
At 22 to 23 postmenstrual weeks, the median section shows the totally formed corpus callosum ( Figure 2–45 ). This structure has four parts, from anterior to posterior: the rostrum, the genu (knee), the trunk, and the splenium (see Figure 2–45C ).
The importance of knowing this pattern is because, at times and for various reasons, the development of the corpus callosum is incomplete.
72 , 73 , 75
Such a partial agenesis of the corpus callosum appears on the sonographic image as if it had been “caught” at an early stage of development. The lack of development of this structure is discussed in Chapter 5 .
Normative measurements of the length as well as the
thickness of the corpus callosum were published.
76
We have to mention here that on some of axial sec­tions there is a structure that can be mistaken for the cavum septi pellucidi. These structures are the columns of the fornix ( Figure 2–54 ). These are seen as parallel echogenic lines that appear if the BPD plane is slightly shifted (in a parallel fashion) toward the base of the skull. In a retrospective study of 20 consecutive sonograms on pregnant patients between 18 and 24 postmenstrual weeks, the columns of the fornix could be identified in all fetuses. To mistake the columns of the fornix in a case of agenesis of the corpus callosum may lead to misdiagnosis of this entity.
77
Figure 2–54. The columns of the fornix (arrow) appear as parallel echo-
genic lines in the “BPD plane” but slightly inferior.
Subarachnoid Spaces and Cisterns
In scanning the normal fetal brain, spaces of different shapes and sizes can be seen between the cortex and the bony skull or between structures of the brain itself. Fine cords of the arachnoid, delicate blood vessels, and prob­ably arachnoid granulations produce a variety of echoes within this space ( Figures 2–39B – E , 2–55 , and 2–56 ). Figures 2–55 and 2–56 show an ultrasonographic image and a drawing of the subarachnoid space.
Early in pregnancy, it is rare to detect subarach­noid spaces. However, around 14 to 16 postmenstrual weeks, they can be revealed using high-frequency TVS ( Figures 2–40 , 2–55 , and 2–57 ). The relative sizes of these spaces decrease as pregnancy advances. In a study by Laing and colleagues, weeks were scanned transabdominally. A subdural space was sought on a transaxial scan. Eighty-three percent of the fetuses with this subdural space were less than 30 post­menstrual weeks, whereas 77% lacking this sign were older than 30 weeks. All of the fetuses were normal at birth. These investigators concluded that if a wide subarachnoid space is seen in late pregnancy, it should be investigated following birth, as a prominent space may predispose a neonate to subdural hematoma.
It is possible that Laing’s group immediately adjacent to the lateral sulcus (of Sylvius). This fluid-filled space was also studied by Jeanty and col­laborators. structure (ie, the cortex) below the internal table of the bone overlapping this area in which the pulsations of the middle cerebral artery is seen should be termed the insula and not the sylvian fissure . Such an area is shown in Figure 2–58 .
The subarachnoid space overlying the insula is also shown in the subsection dealing with the sulci, fissures, and gyri in this chapter.
It is worth discussing the echoes appearing within the subarachnoid space seen in Figure 2–55 . These may be
78
122 fetuses from 21 to 40 postmenstrual
79
78
studied the space
80
The latter came to the conclusion that the
66
Chapter 2 Normal Two- and Three-Dimensional Neurosonography of the Prenatal Brain
Figure 2–55. The subarachnoid space is shown on this Frontal–1 section. The small arrows indicate the hyperechoic structures thought to repre-
sent cross-sections of blood vessels or arachnoid granulations in the subarachnoid space. The open arrow indicates the falx; the arrowhead marks the sagittal sinus.
Arachnoid granulations Sagittal sinus
Figure 2–56.
into the areas supplied by blood and which drain the cerebrospinal fluid.
Schematic drawing of a similar section depicted in Figure 2–55, showing the subarachnoid space and the arachnoid granulations bulging
Chapter 2 Normal Two- and Three-Dimensional Neurosonography of the Prenatal Brain
21
CM
C
V
C
4V
Figure 2–57. Axial section of the posterior fossa in a normal
fetus at 21 postmenstrual weeks. CM, cisterna magna; C, cer­ebellum; V, vermis; 4V, fourth ventricle.
67
cross sections of vessels; however, on color Doppler and power Doppler scans, these do not demonstrate flow. An additional hypothesis is that they may represent cross sec­tions of arachnoid granulations ( Figure 2–56 ).
Several cisterns in the subarachnoid space can be seen by neurosonography of the fetal brain. The cisterns are scattered around as well as within the folds of the brain. We could not detect cisterns such as that of the
lamina terminalis or the chiasmatic, interpeduncular, and pontine cisterns (cisterna magna); at times, the superior (interpeduncular) cistern below the cerebellum and the quadrigeminal cistern and the bilateral cisterna ambiens above the cerebellum have been imaged by ultrasonography.
81
The cisterna magna has been seen as early as 12 to
14 postmenstrual weeks ( Figures 2–36 , and 2–57 ). From
Insula
Figure 2–58. Left Oblique-2 section through the insula. Pulsations of the middle cerebral artery may be detected scanning through this view.
68
Chapter 2 Normal Two- and Three-Dimensional Neurosonography of the Prenatal Brain
AB
E
Figure 2–59. Structural evaluation of the brain at 15 postmenstrual weeks. The posterior fossa and the cerebellum are studied on these serial sections.
The two slanted arrows on both sides of the cerebellum throughout the six images point to the two cerebral hemispheres. (A) Low axial section depict­ing the cisterna magna (small arrow). (B) The higher axial plane reveals the widening cisterna magna (small arrow) and the lower pole of the fourth ventricle (arrowhead). (C) A somewhat “higher” axial section shows the hemispheres and the fourth ventricle (arrowhead). (D) This is the highest of axial sections depicting the cerebellum at the level where the bicerebellar diameter measurement is usually taken. Note the hyperechoic cortex surrounded by sonolucent cerebrospinal fluid and the low echogenicity of the medulla. (E) Coronal section showing the cisterna magna (small white arrow in the median plane), the inverted-funnel-shaped tentorium (two black arrows), and the choroid plexus (cp). (F) A combined oblique axial-coronal section showing the bicerebellar diameter, which measures 1.4 cm. The small arrow in the midline indicates the cisterna magna. (From Timor-Tritsch and col­leagues, 1995,
42
with permission.)
14 postmenstrual weeks on, it is easy to visualize this relatively large sonolucent structure in the posterior fossa ( 2–45 , 2–51 , and 2–57 ).
As mentioned before, using a posterior (occipital) approach and a transvaginal probe, some of the fine details of the posterior fossa and the cisterna magna, as well as the quadrigeminal cistern, can be revealed ( Figure 2–59 ). The connection between the fourth ventricle and the cisterna magna through the median aperture can also be seen if the correct section and plane are applied ( Figures 2–60 , 2–61 , 2–62 , 2–63 , and 2–64 ).
The exact anatomy of the posterior fossa, but more so the connections between the fourth ventricle and the cisterns around the cerebellum (eg, the cisterna magna), should be well known to those engaging in neurosonog­raphy of the fetal posterior fossa. Variations in the size of these CSF-filled spaces are not uncommon. The size of the cisterna magna in normal neonates was measured and ranges between 3 and 8 mm, with a mean value of
CD
+
+
F
4.5 mm.
78
As opposed to an increase in the size of this space due to disease, there is also restriction of this cistern due to pathology (Arnold-Chiari type II malformation). It is therefore of the utmost importance that this space be examined in the context of the entire CNS.
The use of high-frequency (possibly through the transvaginal route) transducers is probably warranted, along with sound knowledge of the anatomy and neuropa­thology of this region.
At times, only TAS of the ventricular system is feasible (eg, with breech or transverse positions of the fetus). In such cases one should be familiar with nomograms devel­oped for atrial measurements. One of these nomograms was suggested by Pilu and coworkers.
59
After conducting a prospective study of 171 normal pregnancies from 15 post­menstrual weeks to term, the following were found: (1) the atrial width remained fairly constant during pregnancy (0.69 ± 0.13 cm = 2 standard deviations); and (2) signifi­cant relationships were found between the cerebroatrial
Chapter 2 Normal Two- and Three-Dimensional Neurosonography of the Prenatal Brain
C
CM
A
69
C
V
CM
B
Figure 2–60. The cisterns around the cerebellum in a normal fetus at 17 postmenstrual weeks. (A) Median section. The two arrows indicate the
quadrigeminal cisterns. C, cerebellum; CM, cisterna magna. (B) Coronal view obtained along the white line in A. The two arrows point to the cisterna ambiens above the cerebellar hemispheres. Note the generous amount of cerebrospinal fluid around the cerebellar hemispheres (C). A small segment of the cisterna magna (CM) is also shown below the vermis (V).
distance ( Figure 2–65 ) and age ( R
2
= 0.936; P = 0.0001) and between the cerebroatrial distance and the biparietal diameter, as well as between the atrial width–cerebroatrial distance ratio and age.
It is hard to compare ventricular measurements taken on axial sections using TAS with those obtained on para­median sagittal sections using TVS. In spite of this, it seems that the general trend, for example, the very slow increase of fetal atrial size seen using the two methods, is comparable.
52
C
Posterior Fossa and Upper Spinal Cord
Transvaginal sonographic examination of the posterior fossa is feasible using a variety of approaches and scanning planes. All of them are useful and informative.
After 10 to 12 postmenstrual weeks, several larger structures of this anatomical area, such as the cerebel­lar hemispheres and the cisterna magna, are discernible ( Figures 2–35A, 1B, 2A, 2B ). At 16 to 18 postmenstrual weeks, the posterior fossa lends itself to excellent imaging.