fetal neuroimaging - cerpo

Fetal and Maternal Medicine Review 2008; 19:1 1–31 C© 2008 Cambridge University Pressdoi:10.1017/S0965539508002106

FETAL NEUROIMAGING

1R.K. POOH AND2K.H. POOH

1CRIFM Clinical Research Institute of Fetal Medicine PMC, Osaka, Japan. 2Department of Neurosurgery,Kagawa National Children’s Hospital, Kagawa, Japan.

INTRODUCTION

Imaging technologies have been remarkably improved and contribute to prenatalevaluation of fetal central nervous system (CNS) development and assessment ofCNS abnormalities in utero.

Conventional transabdominal ultrasonography, by which it is possible to observefetuses through the maternal abdominal wall, uterine wall and sometimes placenta,has been most widely utilized for antenatal imaging. By the transabdominal approach,the whole CNS of the fetus can be well demonstrated, for instance, the brain in theaxial section and the spine in the sagittal section. However, tissues between theultrasound probe and the fetus, such as the maternal abdominal wall, placenta andfetal cranial bones, may at times pose significant obstacles to the ultrasound signalsand therefore make it difficult to obtain clear and detailed images of the fetal CNSstructure.

The introduction of high-frequency transvaginal transducers have contributedto the development of “sonoembryology”1 and recent liberal use of transvaginalsonography in early pregnancy has enabled early diagnoses of major fetal anomalies.2

The brain is a three-dimensional structure, and should be assessed in sagittal, coronaland axial planes. Sonographic assessment of the fetal brain in the sagittal and coronalsections requires an approach through the anterior/posterior fontanelle and/or thesagittal suture. Transvaginal sonography of the fetal brain opened a new field inmedicine, “neurosonography”.3 Application to the normal fetal brain during thesecond and third trimesters was introduced in the beginning of 1990s. It was thefirst practical application of three-dimensional central nervous system assessment bytwo-dimensional (2D) ultrasound.4 Transvaginal observation of the fetal brain offerssagittal and coronal views of the brain5–8 through the fontanelles and/or the sagittalsuture as ultrasound windows. Serial oblique sections3 via the same ultrasound win-dow reveal the intracranial morphology in detail. This method has contributed to theprenatal assessment of congenital CNS anomalies and acquired brain damage in utero.

Ritsuko K Pooh, MD, PhD, CRIFM Clinical Research Institute of Fetal Medicine PMC, 3–7, Uehommachi7 Chome, Tennoji, Osaka #543–0001, Japan.

2 R.K. Pooh and K.H. Pooh

Figure 1 Basic anatomy of the fetal brain.Axial (upper left), sagittal (upper right), anterior coronal (lower left) and posterior coronal (lower right)sections.

BASIC ANATOMICAL KNOWLEDGE OF THE BRAIN

The brain should be understood as a three-dimensional structure. It is generallybelieved that the brain anatomy is complicated. However, in order to demonstratethe brain structure and evaluate fetal CNS disorders, it is not necessary to rememberall these detailed structures. Here, only essential anatomical structures are selectedfor neuroimaging and comprehension of fetal CNS diseases. Figure 1 shows the basicbrain anatomy for fetal neuroimaging.

TRANSVAGINAL 3D SONOGRAPHIC ASSESSMENT OF FETAL CNS

Three-dimensional (3D) ultrasound is one of the most attractive modalities in thefield of fetal ultrasound imaging. There are two scanning methods: free-hand scanand automatic scan. An automatic scan by a dedicated 3D transducer produces motordriven automatic sweeping (a fan scan). With this method, a shift and/or angle-changeof the transducer are not required during scanning, and the scan duration takes only

Fetal Neuroimaging 3

several seconds. After acquisition of the target organ, multiplanar imaging analysisand tomographic imaging analysis are possible. The combination of both transvaginalsonography and 3D ultrasound9–12 produces a great diagnostic tool for evaluationof three-dimensional structure of the fetal CNS. Recent advanced 3D ultrasoundequipment has several useful functions:

1 Surface anatomy imaging2 Bony structural imaging of the calvaria and vertebrae3 Multiplanar imaging of the intracranial structures4 Tomographic ultrasound imaging of the fetal brain in any section5 Thick slice imaging of the intracranial structures6 Simultaneous volume contrast imaging of the same section or vertical section of

the fetal brain7 Volume calculation of target organs such as intracranial cavity, ventricle, choroid

plexus and intracranial lesions8 Three-dimensional sono-angiography of the cerebral circulation (3D power Doppler

or 3D colour Doppler)

It is well known that 3D ultrasound demonstrates the surface anatomy beautifully.In cases of CNS abnormalities, associated facial and limb abnormalities areoften complicated. Therefore, surface reconstructed images could be helpful. Bonystructural imaging of the calvaria and vertebrae (Figure 2) are useful in cases ofcraniosynostosis and spina bifida. The precise delineation of the level of involvementin spina bifida may provide important information to predict postnatal neurologicaldeficits. In multiplanar imaging of the cerebral structure, it is possible to demonstratenot only the sagittal and coronal sections but also the axial section of the brain,which cannot be demonstrated by transfontanelle approach with a conventional 2Dtransvaginal sonography.

Magnetic resonance imaging (MRI), like 3D ultrasound, provides a multiplanarcross-sectional analysis of fetal CNS structures. In general, transvaginal 3D ultrasoundis the imaging modality of first choice during the first and early second trimesters.During this gestational period, 3D ultrasound usually enables a more detaileddemonstration of the fetal brain structure than MRI. In the late second and thirdtrimester, MRI is valuable because it can visualise structures which transvaginal 3Dultrasound cannot because of scan-angle limitations and acoustic shadowing due toossification of the cranial bones.13

Parallel slicing of 3D volumes provides a tomographic visualization of internalmorphology similar to MR imaging. Parallel slicing used to be displayed as a singleimage plane only. However, recent technology enables the display of tomographicultrasound images as a series of parallel cutting slices on a single screen similar toMRI. (Figure 3) Images obtained by tomographic ultrasound imaging (TUI) are similarto those obtained with MRI. The advantage of TUI over MRI is that it is easy tochange slice width, to rotate and magnify images. This function is extremely useful fordetailed CNS assessment and also consultations with neurosurgeons and neurologists.


Figure 2 3D maximum mode image of normal craniofacial structure at 13–14 weeks (upper) and vertebralstructure at 16 weeks (lower).Upper left; Frontal oblique view. Upper right; Occipital view. Note the premature occipital bone appearance.Midline crack is demonstrated. Anterior fontanelle (AF), sphenoidal fontanelle (SF), frontal suture (FS), coro-nal suture (CS) are gradually formed according to cranial bony development. S; Sagittal suture, P; Parietalbone, PF; Posterior fontanelle, O; Occipital bone, Cla; Clavicula, Sca; Scapula, LS; Lambdoid suture.Lower figures show normal vertebral structure at 16 weeks, at the vertebral arch level (left) and vertebralbody level (right). Intervertebral disc spaces are well demonstrated.

Thick slice imaging of the intracranial structures and simultaneous volume contrastimaging (VCI) of the same plane are useful to observe the gyral formation and insidethe lateral ventricles.14


Figure 3 Tomographic ultrasound imaging (TUI) of the fetal brain.Normal brain in the coronal section at 31 weeks of gestation. Intracranial structure including gyral formationare clearly demonstrated.

Volume extracted images and volume calculation of the fetal brain in earlypregnancy were first reported in the 1990s.15,16 The authors have used volumeextraction and volume estimation of the brain structure.17–19 On three orthogonalimages, the target organ can be traced automatically or manually with rotation ofvolume imaging data. After tracing, the volume extracted image is demonstrated andvolume calculation data is shown. 3D fetal brain volume measurements have a goodintraobserver and interobserver reliability20,21 and could be used for estimation ofgestational age.20 Volume analysis by 3D ultrasound provides informative imagingdata, an intelligible evaluation of the brain structure in total, and longitudinal andobjective assessment of enlarged ventricles and intracranial space occupying lesions.Any intracranial structure can be chosen as a target for volumetry no matter howdistorted its shape and appearance may be.

The cerebral circulation demonstrated by transvaginal 2D power Doppler wasfirst reported in 1996.22 Thereafter, transvaginal 3D power Doppler assessment offetal brain vascularity was successful.18,23 Recently with the advanced technologyof bidirectional power Doppler, 3D angiostructural imaging has become even moresophisticated. (Figure 4). Moreover it has been possible to demonstrate the finemedullary veins running from the cortex towards the subependymal area (Figure 4,lower).


Figure 4 3D angiography of normal cerebral circulation at 28–31 weeks.Upper two figures show normal intracranial vasculature at 31 weeks. Anterior cerebral arteries and theirbranches are seen on the sagittal plane (upper left), middle cerebral arteries and their branches on thecoronal plane (upper right) Lower figure shows 3D reconstructed image of normal medullary veins at 28weeksUpper large vessel is the superior sagittal sinus. Cerebral superficial vessels are on the surface of cerebrum.The numerous linear vessels run down from the cortex towards the subependymal region are medullaryveins.

Fetal neuroimaging with advanced 3D technology is an easy, non-invasive, andreproducible method. It produces not only comprehensible images but also objectiveimaging data. Easy storage/extraction of the raw volume data set enables easy off-lineanalysis facilitating consultation with neurologists and neurosurgeons.

VENTRICULOMEGALY AND HYDROCEPHALUS

“Hydrocephalus” and “ventriculomegaly” are both terms used to describe dilatationof the lateral ventricles. However, these two terms should be distinguished fromeach other. Hydrocephalus signifies dilated lateral ventricles resulting from increasedCSF inside the ventricles and increased intracranial pressure, while ventriculomegalyis dilatation of the lateral ventricles without increased intracranial pressure, due to


Figure 5 Subarachnoid space in normal 25-week-brain.Left; Posterior coronal image. Asterisks indicate subarachnoid space. Right; Parasagittal image.

cerebral hypoplasia or CNS anomaly such as agenesis of the corpus callosum.8,24

Ventriculomegaly can sometimes progress to hydrocephalus. Sonographic imagingpermits differentiation of those two intracranial conditions by visualization ofthe subarachnoid space and the choroid plexus. Normally the subarachnoid space,visualized around both cerebral hemispheres, is well preserved during pregnancy(Figure 5). The choroid plexus is a soft tissue and easily affected by external pressure.Obliteration of the subarachnoid space and ‘dangling’ of the choroid plexus areobserved in hydrocephalus. In contrast, the subarachnoid space and choroid plexus arewell preserved in cases of ventriculomegaly. It is difficult to evaluate the subarachnoidspace in the axial plane because the subarachnoid space is observed over the parietalarea of the hemispheres. Therefore, transabdominal sonography may not differentiateaccurately hydrocephalus with increased intracranial pressure from ventriculomegalywithout increased pressure. It is suggested that the evaluation of enlarged ventriclesshould be done in the parasagittal and coronal views by transvaginal imaging or3D multidimensional analysis. As a screening procedure, measurement of atrialwideth (AW) (Figure 6) is useful using a cut-off of 10 mm.25,26 In normal fetuses,blood flow waveforms from the dural sinuses, such as the superior sagittal sinus,vein of Galen and straight sinus, have a pulsatile pattern.27 However, in cases withprogressive hydrocephalus, this normal pulsation disappears and waveforms becomeflat.27 Intracranial venous blood flow may be useful to assess pressure.

Mild ventriculomegaly (atrial width 10–15 mm)

Mild ventriculomegaly is defined as an AW of 10–15 mm. It has been reported that mildventriculomegaly resolves in 29% of cases, remains stable in 57%, and progresses in14% of cases.28 In cases of ventriculomegaly with atrial width of 10–15 mm at referral,the ultimate fetal outcome and prognosis depends on associated abnormalities.


Figure 6 Atrial width measurement.

In general, in cases of mild fetal ventriculomegaly without karyotype or other asso-ciate malformations, the outcome appears to be favorable.29 Pilu and his colleagues30

reviewed 234 cases of borderline ventriculomegaly, which included an abnormaloutcome in 22.8% of cases. They concluded that borderline ventriculomegaly carriesan increased risk of cerebral maldevelopment, delayed neurological development and,possibly, chromosomal aberrations. Isolated mild ventriculomegaly with atrial widthof 10–12 mm may be a normal variant; Signorelli and colleagues31 reported normalneurodevelopment between 18 months and 10 years after birth in cases of isolatedmild ventriculomegaly (AW 10–12 mm). Ouahba and colleagues32 recently reportedthe outcome of 167 cases of mild isolated ventriculomegaly and concluded that inaddition to associated anomalies, three criteria were associated with an unfavourableoutcome: atrial width greater than 12 mm, progression of the ventriculomegaly andasymmetrical and bilateral ventriculomegaly.

Moderate to severe ventriculomegaly and hydrocephalus (AW > 15 mm)

The term ‘hydrocephalus’ does not identify a specified disease, but is a generic term fora group of pathologic conditions due to abnormal circulation of the CSF. Congenitalhydrocephalus is classified into three categories by causes which disturb the CSFcirculation pathway:24

1 Simple hydrocephalus

Simple hydrocephalus, caused by a developmental abnormality within the CSFcirculation, includes aqueductal stenosis, atresia of the foramen Monro, andmaldevelopment of arachnoid granulation.

2 Dysgenetic hydrocephalus

Dysgenetic hydrocephalus indicates hydrocephalus resulting from a cereb-ral developmental disorder and includes hydranencephaly, holoprosencephaly,


Figure 7 Hydrocephalus due to aqueduct obstruction (left) and Chiari type II malformation (right).Left figures; Hydrocephalus due to aquedact obstruction detected by transvaginal scan at 19 weeks ofgestation. Upper left; axial section, upper right; parasagittal section, lower left; anterior coronal section,lower right; posterior coronal section. Bilateral ventriculomegaly with dilated foramen of Monro and IIIrdventriculomegaly, with dangling choroid plexus (CP). Note the ventricular shape is round.Right figure; Hydrocephalus due to myelomeningocele and Chiari type II malformation demonstrated bytransvaginal scan at 17 weeks of gestation. Upper left; axial section, upper right; parasagittal section, lowerleft; anterior coronal section, lower right; posterior coronal section. Note the ventricular shape is squarishcompared with venticles in the left figures, and especially in the posterior coronal section, the triangle shapeof the enlarged ventricles (arrows) which is often seen in cases of Chiari II malformation in the secondtrimester.

porencephaly, shizencephaly, Dandy-Walker malformation, dysraphism, and Chiarimalformation.

3 Secondary hydrocephalus

Secondary hydrocephalus indicates hydrocephalus caused by intracranial pathologies,such as a brain tumour, intracranial infection and intracranial haemorrhage.

In cases with progressive hydrocephalus, there may be seven stages

1 increased fluid collection within the lateral ventricles2 increased intracranial pressure3 dangling choroid plexus4 disappearance of the subarachnoid space5 excessive extension of the dura and superior sagittal sinus6 disappearance of venous pulsation7 enlarged skull.24

In general, both hydrocephalus and ventriculomegaly are still evaluated by themeasurement of biparietal diameter (BPD) and AW in the transabdominal axialsection.

Figure 7 and 8 show prenatal sonographic imaging of fetal ventriculomegaly withan AW of over 15 mm. Although these cases have similar ventricular appearances,


Figure 8 Hydrocephalus due to amniotic band syndrome (20 weeks).Upper left; Tomographic ultrasound imaging in axial section of the fetal brain at referral. Bilateral atrial widthswere 17 and 21mm respectively. From the observation of enlarged ventricles, simple hydrocephalus due toforamen of Monro obstruction was suspected. However, the fetus was also found to have cleft lip, amputationof fingers and an amniotic band. Lower; Small cephalocele with the remnant of an amniotic band (arrowhead).

the causes of ventriculomegaly vary; Chiari type II malformation (Figure 7, right),aqueduct obstruction (Figure 7, left), and amniotic band syndrome(ABS)(Figure 8). Inthe latter case, an amniotic band attached to the skull resulted in a partial cranial bonedefect and a small cephalocele, which may have caused obstruction of the Foramenof Monro and enlarged ventricles.

From our data of 23 ventriculomegaly cases with atrial width > 15 mm,33 nine(39.1%) had no other CNS abnormality but two of these 9 had a chromosomal anomaly.Four of the remaining seven had a favorable postnatal outcome after postnatalventricular-peritoneal shunting. Among the remaining 14 cases with other CNS ab-normalities, holoprosencephaly was detected in 5 cases and myelomeningocele in 5.33

NEURAL TUBE DEFECTS

Cranium bifidum

Cranium bifidum is classified into four types of encephaloschisis (including anen-cephaly and exencephaly), meningocele, encephalomeningocele, encephalocystocele,


Figure 9 Encephalocele at 18 weeks of gestation.Upper left; Tomographic sagittal imaging of encephalocele.Lower left; 3D reconstructed image. Microcephaly and occipital encephalocele are demonstrated. (lowerright) 3D maximum mode of the occipital bone defect. S; sagittal suture, L; lambdoid suture.

and cranium bifidum occulutum. Encephalocele occurs in the occipital region in70–80%. Acrania, exencephaly and anencephaly are not independent anomalies. Itis considered that dysraphia (absent cranial vault, acrania) occurs at a very earlystage while disintegration of the exposed brain (exencephaly) during the fetal periodresults in anencephaly. Encephalocele (Figure 9) is often observed in the median


Figure 10 Myelomeningocele with severe kphosis detected at 20 weeks of gestation.Left; Three orthogonal views of vertebral structure and myelomeningocele with severe kyphosis. 3Dreconstruction of the bony structure in the sagittal section clearly demonstrating the vertebral bodies.Middle; 3D surface reconstruction image of fetal back shows the large myelomeningocele from T12. Right;Macroscopic picture of the same baby born at 37 weeks.

section and in the parieto-occipital area. Amniotic band syndrome (ABS) should bedifferentiated from acrania during early pregnancy, because ABS has a completelydifferent pathogenesis from acrania/excencephaly. In cases of ABS, cranial destructionoccurs secondarily to an amniotic band, although appearances are often similar.

Spina bifida

Spina bifida aperta is classified into 4 types; meningocele, myelomeningocele,myelocystocele and myeloschisis. In myelomeningocele, the spinal cord and itsprotective covering (the meninges) protrude from an opening in the spine. Inmeningocele, the spinal cord develops normally but the meninges protrude through aspinal opening. The most common location of these malformations is the lumbarand sacral areas of the spinal cord. Chiari type II malformation and subsequenthydrocephalus/ventriculomegaly are frequently associated with open spina bifidawhile scoliosis or kyphosis are occasional. Surface anatomy of the lesion and clubfoot,which occasionally manifests early in mid-gestation as a complication of spinalbifida, are easily demonstrable by 3D ultrasound. 3D ultrasound with maximummode can demonstrate bony structure (Figure 10) and is helpful in detecting thelevel of the spinal lesion and to predict neurological prognosis. Although mostmyelomeningoceles are demonstrated as a protruding swelling as shown in Figure 10,the fetal back often appears flat in myeloschisis and therefore open spina bifidamay be overlooked. Because more than 80% of cases of open spina bifida areassociated with ventriculomegaly due to Chiari type II malformation, demonstrationof ventriculomegaly is usually the first observable sign and should lead to a detailedexamination of the spine.


Figure 11 Alobar holoprosencephaly at 15 weeks (left) and semilobar holoprosencephaly at 33 weeks(right).Coronal (upper left) and axial (lower left) images of intracranial structure show a complete single ventriclewithin a single-sphered cerebral structure. Sonogram in the median section (upper right). Arrows indicate adorsal sac. Fetal MR coronal image (lower right). Fused ventricle is demonstrated.

PROSENCEPHALIC DEVELOPMENTAL DISORDER

Holoprosencephaly

Holoprosencephalies are classified into three varieties; alobar, semilobar and lobartypes. Facial abnormalities such as cyclopia, ethmocephaly, cebocephaly, flat nose,cleft lip and palate are often associated with holoprosencephaly as are extracerebralabnormalities. Alobar type at 15 weeks of gestation and semilobar type in latepregnancy are shown in Figure 11.

Agenesis of the corpus callosum

Absence of the corpus callosum (ACC) is divided into complete agenesis,partial agenesis or hypogenesis. Chromosomal anomalies or syndromic diseases


Figure 12 Agenesis of the corpus callosum (ACC).Upper left; mid sagittal section in a case of ACC. Typical radial sulcus formation is seen instead of normalcingulate sulcus and gyrus formed with normal development of the corpus callosum (arrows) seen in theupper right figure. Lower left; Angiostructure by 3D power Doppler in AOCC case. Normal callosomarginalartery (CMA, lower right) does not exist and radial formation of the branches of anterior cerebral arteries(ACA) is seen.

may occasionally be related to agenesis of the corpus callosum. Colpocephalicventriculomegaly with disproportionate enlargement of the trigones, occipital hornsand temporal horns together with superior elongation of the third ventricle is usuallyobserved. Interhemispheric cyst is often associated with ACC and some cases have apericallosal lipoma. Complete ACC can be demonstrated in the coronal and sagittalsection by sonograpy and fetal MRI. The typical shape of enlarged ventricles associatedwith ACC is colpocephaly with large occipital horns. The typical radiated formation ofbrain vessels in the sagittal section is demonstrated in Figure 12. The corpus callosumis viable after 17 or 18 weeks of gestation by ultrasound, it is therefore impossible todiagnose agenesis of the corpus callosum before this gestational age.34

POSTERIOR FOSSA ANOMALY

Chiari malformation

Chiari classified anomalies with cerebellar herniation into the spinal canal into threetypes depending on the herniated tissue; lip of cerebellum in type I, part of cerebellum,


Figure 13 Chiari type II malformation. Schema, macroscopic picture and ultrasound.Upper left; Schema of Chiari type II malformation and macroscopic picture of specimen from aborted fetusat 21 weeks of gestation. P; pons, M; medulla oblongata, C; cerebellum.Lower left; Typical lemon sign of cranial shape. Indentations of anterolateral parts (arrows) are conspicuousbefore 26 weeks of gestation. Lower middle; Typical banana sign. Disappearance of the cisterna magna andcerebellar deformity (arrows) due to cerebellar tonsil herniation into spinal canal form a banana sign. Lowermacroscopic picture; Lemon sign from aborted fetus at 21 weeks of gestation. Asterisks indicate anterolateralindentations.Upper right; Normal cerebrospinal region demonstrated by ultrasound in the sagittal section at 19 weeks.C; cerebellum, CM; cisterna magnum. Middle right; Sonogrphic picture in the sagittal section of Chiari typeII malformation at 19 weeks of gestation. Herniation of the cerebellum and medulla oblongata (arrows)into spinal canal is clearly demonstrated. Lower right; Sagittal ultrasound image of medullary kink at19 weeks(arrowhead) occasionally seen in some cases of Chiari type II malformation.

fourth ventricle medulla oblongata and pons in type II and a large herniation ofthe posterior fossa in type III. Type IV, with just cerebellar hypogenesis, was addedlater. However, this classification occasionally leads to confusion in neuroimaging.Therefore, at present, the following classification is advocated; type I not associatedwith myelomeningocele, type II (Figure 13, upper left) associated with myelomenin-gocele, type III associated with cephalocele or craniocervical meningocele, and typeIV associated with marked cerebellar hypogenesis and posterior fossa shrinking.

Chiari malformation occurs because of;

1 inferior displacement of the medulla and fourth ventricle into the upper cervicalcanal

2 elongation and thinning of the upper medulla and lower pons and persistence of theembryonic flexure of these structures


3 inferior displacement of the lower cerebellum through the foramen magnum intothe upper cervical region, and

4 a variety of bony defects of the foramen magnum, occiput, and upper cervicalvertebra.35

Hydrocephalus results from obstruction of the fourth ventricular outflow orassociated aqueductal stenosis. Eighty eight percent of fetuses with open spina bifidadevelop ventriculomegaly, and the majority do so by 21 weeks’ gestation.36

Lemon and banana signs37 are circumstantial evidences of a Chiari malformationwhich are easily demonstrated in the second trimester. The lemon sign indicatesdeformity of the cranium, while the banana sign indicates an abnormal shape of thecerebellum with loss of the cisterna magna space (Figure 13, lower). Herniation ofthe cerebellar tonsil and medulla oblongata and medullary kink are demonstrable(Figure13, right). A small clivus-supraocciput angle is seen in cases of Chiarimalformation.38

Dandy-Walker malformation, Dandy-Walker variant, megacisterna magna

During development of the fourth ventricular roof, a delay or failure of the foramenof Magendie to open results in a buildup of CSF and the development of cysticdilation of the fourth ventricle. Despite the subsequent opening of the foraminaof Luschka (usually patent in Dandy-Walker malformation), cystic dilatation of thefourth ventricle persists and CSF flow is impaired. At present, the term Dandy-Walkercomplex, coined by Barkovich et al,39 is used to indicate a spectrum of anomalies ofthe posterior fossa that are classified by axial CT scans. Dandy-Walker malformation,Dandy-Walker variant, and mega-cisterna magna seem to represent a continuum ofdevelopmental anomalies of the posterior fossa.39 Figure 14 shows the differentialdiagnosis of hypoechoic lesion of the posterior fossa.

Classic Dandy-Walker malformation; cystic dilatation of fourth ventricle, enlarged posterior fossa,elevated tentorium and complete or partial agenesis of the cerebellar vermis

Dandy-Walker variant; variable hypoplasia of the cerebellar vermis with or without enlargement ofthe posterior fossa

Megacisterna magna; enlarged cisterna magna with integrity of both cerebellar vermis and fourthventricle

Sonographic detection of DW malformation is shown in Figure 15. To observe theagenesis of the cerebellar vermis, an axial section is preferable. To observe the elevatedtentorium, a sagittal section is preferable.


Figure 14 Differential diagnosis of “hypoechoic lesion” of the posterior fossa.

NEURONAL PROLIFERATION DISORDERS

Microcephaly

Microcephaly is defined as a head circumference more than 2 standard deviationsbelow the normal mean for age, sex, race, and gestation. Infections such as rubella,cytomegalovirus (CMV), varicella (chicken pox) and toxoplasmosis, radiation, med-ications, chromosome abnormalities and genetic diseases may cause microcephaly.Ultrasound and MR images of typical microcephaly are shown in Figure 16.Occasionally, microcephaly occurs late in pregnancy.40

NEURONAL MIGRATION DISORDERS

Neuronal migration disorders are caused by the abnormal migration of neurons in thedeveloping brain and nervous system. Neurons must migrate from the areas wherethey are formed to the areas where they will form their neural circuits. Neuronalmigration, which occurs as early as the second month of gestation, is controlled bya complex array of chemical guides and signals. When these signals are absent orincorrect, neurons do not end up in the correct place. This can result in structurallyabnormal or missing areas of the brain in the cerebral hemispheres, cerebellum,


Figure 15 Dandy Walker malformation at 28 weeks of gestation.Left; Median section of the brain. Corpus callosum (CC) is normally demonstrated and Dandy Walkercyst (DWC, arrows) is seen in the posterior fossa. Right upper; 3D view in the posterior coronal section.Hypoplastic vermis of the cerebellum (arrowhead) is seen. Right lower figures, three orthogonal views andan extracted ventricular appearance, demonstrate moderate ventriculomegaly in this case.

brainstem, or hippocampus, including schizencephaly, porencephaly, lissencephaly,agyria, macrogyria, pachygyria, microgyria, micropolygyria, neuronal heterotopias(including band heterotopia), agenesis of the corpus callosum, and agenesis of thecranial nerves. Symptoms vary according to the specific disorder and the degree ofbrain abnormality and subsequent neurological loss, but often feature poor muscletone and motor function, seizures, developmental delays, mental retardation, failureto grow and thrive, difficulties with feeding, swelling in the extremities, and a smallerthan normal head. Most infants with a neuronal migration disorder appear normal,but some disorders have characteristic facial or skull features.

Lissencephaly

Lissencephaly is very rare and characterized by a lack of gyral development.Lissencephaly type I shows a smooth surface of the brain and the cerebral wallis similar to that of an approximately 12-week-old fetus.41 Lissencephaly may beisolated or associated with additional craniofacial abnormalities, cardiac anomalies,genital anomalies, sacral dimple, creases, and/or clinodactyly as in the Miller-Diekersyndrome. Figure 17 (left side) shows isolated lissencephaly at 30 weeks of gestation. In


Figure 16 Microcephaly at 28 weeks of gestation.Upper left; Fetal face in the sagittal section. Note the flat face with the frontal bone and nasal bone (NB)on a single line, compared to the normal face. Upper middle; Sagittal section of the brain. Microcephaly andmicro-brain are detectable. Upper right; 3D reconstruction image of fetal craniofacial expression. Lower;MR image in the sagittal, anteror-coronal and posterior-coronal sections from the left.

lissencephaly type II, the brain surface has a cobblestone appearance. This abnormalityis found in Walker-Warburg syndrome with macrocephaly, congenital musculardystrophy, cerebellar malformation, retinal malformation or Fukuyama congenitalmuscular dystrophy with microcephaly and congenital muscular dystrophy. Isolatedlissencephaly is linked to chromosome 17p13.3 and chromosome Xq24-q24. Miller-Dieker syndrome is also linked to chromosome 17p13.3. Walker-Warburg syndromeis of autosomal recessive inheritance. Fukuyama congenital muscular dystrophy islinked to chromosome 9q31.42 A few reports of prenatal diagnosis of lissencephalyhave been published.43–45 Without a previous history of an affected child, the diagnosisprobably cannot be reliably made until 26 to 28 weeks’ gestation.46

Schizencephaly

Schizencephaly is a disorder characterized by congenital clefts in the cerebralmantle, lined by pia-ependyma, with communication between the subarachnoidspace laterally and the ventricular system medially. Sixty three percent of cases are


Figure 17 Isolated lissencephaly at 30 weeks (left) and schizencephaly at 33 weeks (right).Upper left; Sonogram of coronal section of lissencephaly. Lower image is an MR image. No gyral formationand the smooth brain surface are clearly demonstrated. Upper right; Sonogram of coronal section ofschizencephaly. Lower right; MR coronal image. Bilateral schizencephaly is clearly demonstrated.

unilateral and 37% bilateral (Figure 17, right). Clefting affects the frontal region in 44%and frontoparietal region in 30%.41Ventriculomegaly, microcephaly, polymicrogyria,grey matter heterotopias, dysgenesis of the corpus callosum, absence of the septumpellucidum, and optic nerve hypoplasia may also be present.

OTHER CONGENITAL ANOMALIES

Arachnoid cyst, Interhemispheric cyst

These are congenital or acquired cysts and constitute about 1% of all intracranialmasses in newborns. They are lined by arachnoid membranes, and filled with fluidwhich is the same character as the cerebrospinal fluid. Cysts are mostly single, but


Figure 18 US and MR images of interhemispheric cyst and arachnoid cysts.Left; Interhemispheric(IHS) cyst with agenesis of the corpus callosum at 24 weeks in the coronal and sagittalsections by US and coronal by MRI.Middle; Middle fossa arachnoid cyst at 29 weeks of gestation Coronal and parasagittal sections by US and axialsection by MRI. The arachnoid cyst is arising from the middle fossa and compressing the cerebral hemisphere.Right; Suprasellar arachnoid cyst. Sagittal and coronal sections by US and axial section by MRI. Suprasellararachnoid cyst compressing the brain stem and bilateral hemispheres.

two or more cysts can be occasionally observed. The location of arachnoid cysts varies;50% occur from the Sylvian fissure (middle fossa), 20% from the posterior fossa, and10–20% each from the convexity, suprasellar, interhemisphere, and quadrigeminalcistern. Interhemispheric cysts are commonly associated with agenesis or hypogenesisof the corpus callosum. Callosal agenesis with interhemispheric cyst is classified astwo types.47 Type 1 cysts appear to be an extension or diverticulum of the third orlateral ventricles, whereas Type 2 cysts are loculated and do not communicate withthe ventricular system. Prenatal neuroimaging examples of an interhemispheric cyst,middle fossa arachnoid cyst, and suprasellar arachnoid cyst are shown in Figure 18. Asspontaneous resolution or changes in cyst size are often seen during the fetal period,serial scanning is important. Detection in the first trimester has been reported.48 Theprognosis is generally good. Many cysts are asymptomatic and remain quiescent for


Table 1 Craniosynostoses: Involvement of cranial suture and resulting head shape.

Sagittal suture scaphocephaly or dolichocephalyBilateral coronal suture brachycephalyUnilateral coronal suture anterior plagiocephalyMetopic suture trigonocephalyLambdoid suture acrocephalyUnilateral lambdoid suture posterior plagiocephalyCoronal/lambdoid/metopic or

squamous/sagittal suturecloverleaf skull

Total cranial sutures oxycephaly

years, although others may expand and cause neurological symptoms by compressingthe adjacent brain, development of ventriculomegaly, and/or expanding the overlyingskull.

Brain tumours

Brain tumours are divided into teratoma, which are the commonest reportedbrain tumours, and non-teratomatous tumours. Non-teratomatous tumours includeneuroepithelial tumours, such as medulloblastoma, astrocytoma, choroids plexuspapilloma, choroids plexus carcinoma, ependymoma and ependymoblastoma, mesen-chymal tumour such as craniopharyngioma, sarcoma, fibroma, haemangioblastoma,haemangioma and miningoma, and others such as lipoma of the corpus callosumand subependymal giant-cell astrocytoma associated with tuberous sclerosis (oftenaccompanied by cardiac rhabdomyoma).49,50 Depending on the site and vascularity,these tumours may lead to macrocrania or local skull swelling, epignathus,secondary hydrocephalus, intracranial haemorrhage, intraventricular haemorrhage,polyhydramnios, heart failure by high-cardiac output51 or hydrops. Intracranialmasses with solid, cystic or a mixed pattern, with or without visualization ofhypervascularity, can be detected by ultrasound and fetal MRI. A brain tumour shouldbe considered in cases with unexplained intracranial haemorrhage. Prenatal diagnosisof intracranial tumour at 18 weeks is shown in Figure 19.

Craniosynostosis

Premature closure may affect one or more cranial sutures. Simple sagittal synostosisis the most common. The resulting cranial shapes depend on the affected suture(s).(Table 1)

Craniosynostosis due to specific syndromes (syndromic craniosynostosis) is usuallyassociated with additional specific features and therefore correct differentiationbetween these conditions is usually possible. Examples include Crouzon syndrome(acrocephaly, synostosis of coronal, sagittal and lambdoid sutures and ocular proptosis,maxillary hypoplasia), Apert syndrome (brachycephaly, irregular synostosis,


Figure 19 Brain tumor at 18 weeks of gestation.Upper left; Tomographic coronal image of the brain. Unilateral hemisphere is compressed by echogenic mass.Lower left; MR images. Coronal, sagittal and axial planes from the left. Lower right; Brain specimen fromaborted fetus at 21 weeks of gestation. The tumor is indicated by green arrows.

especially coronal suture and midfacial hypoplasia, syndactyly, broad distal phalanxof thumb and big toe), Pfeiffer syndrome (brachycephaly, synostosis of coronaland/or sagittal sutures, hypertelorism, broad thumbs and toes, partial syndactyly),and Antley-Bixler syndrome (brachycephaly, multiple synostosis, especially of thecoronal suture and maxillary hypoplasia, radiohymeral synostosis, choanal atresia,arthrogryposis). Abnormal craniofacial appearance can be detected prenatally by2D/3D ultrasound.52–54 The facial abnormality and intracranial structures in a caseof Pfeiffer syndrome are shown in Figure 20.

Vein of Galen aneurysmal malformation (VGAM)

This is a congenital malformation of cerebral blood vessels involving arteriovenousfistulas in which blood shunts from choroidal and/or quadrigeminal arteriesinto an overlying single median venous sac. A Vein of Galen aneurysm is


Figure 20 Craniosynostosis (Pfiffer syndrome) at 26 weeks.Upper left; Tomographic ultrasound imaging of the brain. Fused ventricle with mild enlargement isdemonstrated. Atrial width measurement is 12 to 13 mm.Upper right; 3D surface images of fetal face and foot. Exophthalmos with flat face and large big toe are seen.Lower left; Three orthogonal view of fetal face. Right lower; Abnormal facial expression and appearance ofthe toe after birth.

not an ‘aneurysm’ but a choroidal type of ‘arteriovenous malformation (AVM)’involving the Vein of Galen precurser. This is distinct from an arteriovenousmalformation with venous drainage into a dilated, but already formed, vein ofGalen.55 Associated anomalies are cardiomegaly, high cardiac output, secondaryhydrocephalus, macrocrania, cerebral ischaemia (intracranial steal phenomenon)and subarachnoid/cerebral/intraventricular haemorrhages. Two dimensional and 3Dcolour/power Doppler and 3D B-flow images of VGAM are shown in Figure 21.

Pericallosal lipoma

Intracranial lipomas are congenital malformations composed of mature adipocytes.They are usually located in the midline, particularly in the pericallosal region, witha haemispheric location accounting for only 3 to 7% of cases. Two morphologic


Figure 21 Vein of Galen aneurysm at 28 weeks of gestation.Upper left; Transvaginal sagittal image. Dilated dural sinuses are demonstrated. Lower left; Transvaginalcoronal image. Interhemispheric space occupying lesion is the dilated vein. Upper middle; 3D B-flow image ofintracranial vasculature. Many intracranial arteries run directly toward aneurysmal sac. Lower middle; PowerDoppler image. Upper right; Fetal MR sagittal image. Lower right; Fetal MR axial image.

types of pericallosal lipoma have been described.56,57 The Tubulonodular type isgenerally greater than 2 cm in diameter (although often smaller in the fetal period)and frequently associated with corpus callosum dysgenesis, frontal lobe anomalies,and frontal encephaloceles. The Curvilinear type which typically comprises thin,posteriorly situated lipomas curving around the splenium, is generally associated witha normal corpus callosum and otherwise has a low incidence of associated anomalies.The highly echogenic mass can be easily demonstrated by ultrasound. Several reportson prenatal diagnosis have been published.58–60

ACQUIRED BRAIN ABNORMALITIES IN UTERO

In terms of encephalopathy or cerebral palsy, ‘the timing of brain insult’ is one of themost controversial issues.24 Although brain insults may relate to antepartum eventsin a substantial number of term infants with hypoxic-ischaemic encephalopathy, thetiming of insult cannot always be certain. It is very difficult to provide a preciseprediction of subsequent development of cerebral palsy after a given antepartumevent or complication. Fetal heart rate monitoring cannot reveal the presence ofencephalopathy, and neuroimaging by ultrasound and MR imaging is the most reliable


Figure 22 Cerebral hemorrhage and i.e. ischaemic change with mild ventriculomegaly at 28 weeks ofgestation.Upper; Anterior coronal sections. Brain damage due to cerebral haemorrhage or an ischemic-hypoxicepisode. Note multiple area of low and high echogenicity around the mildly enlarged ventricles. The case hadvein of Galen aneurysm malformation. Lower left; Axial image. Atrial width measurement was just 10 mm atthis stage. Lower right; Parasagittal section. Periventricular brain damage and ventriculomegaly are seen.

modality for detection of silent encephalopathy. In many cases with cerebral palsywith acquired brain insults, especially term-delivered infants with reactive fetal heartrate tracing and good Apgar score at delivery, imaging has confirmed the presence a ofbrain insult in utero, suggesting that the majority of cerebral palsy is of antepartumrather than intrapartum origin.

Intracranial haemorrhage

Intracranial haemorrhage includes subdural haemorrhage, primary subarachnoidhaemorrhage, intracerebellar haemorrhage, intraventricular haemorrhage andintraparenchymal haemorrhage.61 Hydrocephalus, hydranencephaly, porencephaly, ormicrocephaly are possible secondary complications, which are often detectable byimaging studies. Examples of multiple haemorrhage and ischaemic change due tovein of Galen aneurysm malformation at 28 weeks are shown in Figure 22. The lesionoften progresses into porencephaly in a short period.


Figure 23 Fetal US and MR images of porencephaly at 25 weeks of gestation.Upper left; Transvaginal US coronal image. Defect of parietolateral part of the unilateral cerebrum. This casealso has an absent septum pellucidum. Upper middle; Parasagittal US image. Porencephalic cyst is fused withthe unilateral ventricle. Echogenicity inside the ventricular wall indicates intraventricular hemorrhage. Upperright; Transabdominal US axial image. Lower; Fetal MR images. Coronal, parasagittal and axial sections fromthe left side.

Porencephaly

Porencephaly or porencephalic cyst is defined as a fluid filled space replacing normalbrain parenchyma which may or may not communicate with the lateral ventricles orsubarachnoid space. The causes may be ischaemic, trauma,62 demise of one twin,intercerebral haemorrhage or infection with cytomegalo virus.63 Figure 23 showsporencephaly after intracerebral haemorrhage at 25 weeks. Some cases in utero havebeen reported.64,65 Porencephalic cyst never causes a mass effect, which is observed incases of arachnoid cyst or other cystic mass lesions. This condition is an acquired braininsult and needs to be differentiated from schizencephaly and migration disorders.

Fetal periventricular leukomalacia (PVL)

Multifocal areas of necrosis are found deep in the cortical white matter. They are oftensymmetrical and occur adjacent to the lateral ventricles. Periventricular leucomalaciarepresents a major precursor for neurological and intellectual impairment andcerebral palsy in later life. Between 25–75% of premature infants at autopsy haveperiventricular white matter injury. However, clinically, the incidence is much lower


with 5 to 10% of infants less than 1500g birth weight affected. In term infants, PVLis very rare.

CONCLUSIONS

Recent advances in imaging technology have allowed objective neuroimagingdiagnosis. However, longitudinal and careful evaluation of neurological short-term/long-term prognosis is required for proper counselling and managementfollowing prenatal diagnosis.

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