ESPACIO DE NEURORRADIOLOGÍA

FETAL MAGNETIC RESONANCE A CONTRIBUTION TO THE DIAGNOSIS OF CENTRAL NERVOUS SYSTEM MALFORMATIONS

Nicolás Sgarbi MD, Verónica Etchegoimberry MD

RESUMEN ABSTRACT

Las malformaciones del sistema nervioso son relativa- Central Nervous System malformations are relatively mente frecuentes e impactan de forma significativa en frequent and have a negative impact in postnatal la morbi-mortalidad postnatal. morbidity and mortality. Su diagnóstico pre-natal se basa en una técnica vali- Prenatal diagnosis is based on the obstetric ultra- dada desde hace varias décadas como es la ecografía sound, which has been validated throughout the years cuyo rendimiento general es excelente. with an excellent performance. En los últimos años se ha producido un cambio sustan- In the last years, there has been a substantial change cial en el paradigma diagnóstico de las malformaciones in the prenatal diagnosis, not only for deciding the no sólo por las implicancias que esto tiene en decidir termination of pregnancy, but also to assess in the la continuidad del embarazo, sino además por el de- opportunity of intrauterine surgery. sarrollo de técnicas de cirugía intrauterina. In this revision we will analyze the most important En esta revisión analizaremos los principales aspectos technical aspects and indications of Fetal MRI, and técnicos de la resonancia magnética fetal y sus aportes its importance in the prenatal diagnosis of Central al diagnóstico de las malformaciones más frecuentes Nervous System Malformations. del sistema nervioso. Key Words: Fetal MRI, Central Nervous System Mal- Palabras clave: resonancia magnética fetal, malforma- formations, neurosonography. ciones del sistema nervioso, neurosonografía.

INTRODUCTION That is why Fetal Magnetic Resonance (fMR) has become a complementary technique to US in the study of the The study of fetal anatomy is done as a routine part of central nervous system (CNS). prenatal care. Ultrasound (US) is the diagnostic method of choice, because it gives excellent global results for the The objectives of this review are: to analyze the contri- complete anatomic assessment of the fetus during its bution of fMR to the study of the central nervous system different developmental stages. of the fetus and its more frequent malformations, and to It has been long been clearly established that US is a highly highlight the general principles of this technique, as well sensitive method for the detection of malformations, even as its scope and its limitations. in their early stages of development. During the last few years new technologies have advanced the study of fetal anatomy, MR among them. The use of TECHNICAL ASPECTS MR in this field is constantly increasing. In this respect some authors point out that anomalies that MR has developed considerably in the last few years, were not diagnosed by US can be detected by MR in 20% due to the changed paradigm for the study of congenital of patients (1). malformations. Corresponding author: At the same time, changes in law and health policy have This change came about essentially on account of ad- [email protected] allowed for voluntary interruption of pregnancy and have vances in treatment for some malformations (corrective Received april 19th in this way impacted the diagnosis and management of intrauterine fetal surgery), the need of a diagnosis in view Accepted may 5th malformations. of prenatal genetic advice and planned parenthood, and 2018

REVISION WORK / N. Sgarbi MD, V. Etchegoimberry MD 92 the legal modification related to interruption of pregnancy. and anatomy of the fetus. The subsequent use of MR along with the different va- Then comes the planning of the scan. It is necessary to rieties of US has modified the diagnostic approach to obtain fast T2-weighted cranium images in the three spa- malformations. tial planes (4). Sagittal spine images are obtained, axial or coronal planes may be used too if considered necessary The first concept to be highlighted is that MR must be or complementary. performed only after an ultrasound scan was performed by an expert in the assessment of fetal anatomy (2). Many Single-shot sequences must be used, such as Single Shot factors must be taken into account when ordering and Fast Spin Echo (SSFSE) or the Half Fourier Acquisition performing fMR. Turbo Spin-Echo (HASTE). Slice thickness must be adequate to fetal size, not exce- As a general recommendation, in the first place the scan eding 3 mm; an adequate field of vision (FOV) must be must focus on the anatomical region or organ that pre- chosen in order to obtain specific images of the region sented some alteration on US, so that the technique can of interest. be shown to best advantage. In special cases, study protocol may include other sequen- Then other factors concerning the maternal-fetus unit must ces such as T1-weighted sequences for fat analysis, or come into consideration. the susceptibility sequences such as T2- or SWI-weighted To achieve good imaging one must acquire images while GRE sequences for the assessment of hemorrhage, as well the fetus is immobile. as diffusion sequences (DWI) for the study of ischemia. Longer acquisition time is a limiting factor in such cases. Sedation is not recommended, it is preferable to ask the It is important to take into account some safety parameters. mother to fast during 4 to 6 hours, so as to restrict fetal The FDA has set clear limits to the specific absorption rate movements as much as possible. (SAR) of radio frequency, but its effects on the maternal-fe- The mother must receive precise and detailed information tal unit remain unclear (1). about the duration of the study, the position to maintain during that time and the respiratory movements that will All patients must receive clear information about the fMR be asked of her. modality in use, its benefits, its scope and its limitations.

The patient must be placed on her back or even on her side, whichever is more comfortable for her, so as to ensure NORMAL CHARACTERISTICS OF FETAL her collaboration during the study. BRAIN Usually fMR is performed with 1.5 T equipment, but in the last few years some centers have reviewed the contribution In order to interpret and analyze an fMR scan correctly of 3T magnets (1), although it is known that their routine it is essential to know the usual appearance of the brain use is not recommended yet (3). during its development. A review of fetal brain reveals three basic components Although image resolution may improve, movement arti- that permit a fairly accurate diagnosis of the stage of de- facts increase likewise. That is why the use of high magnetic velopment. These components are: brain parenchyma, fields calls for more rigorous technique if optimal results germinal matrix and sulcation pattern (1). are to be achieved. During development white matter presents with high signal Surface coils must be used on the body, with as many in T2-weighted scans, on account of its high water content receptor channels as possible, so that high-resolution and scant myelinization. images are obtained in the least possible acquisition time. Brain parenchyma (or cerebral mantle) appears as several The timing of the pregnancy scan is a point of the utmost layers that can be accurately observed between the 28th importance. and the 30th week of development. The germinal matrix is the cell layer that will produce Most centers recommend performing the fMR scan after neurons; it is to be found on the walls of the ventricular the 19-20th week of pregnancy. Earlier on, structures system. In T2-weighted scans it has a low signal on account are very small and some of them (corpus callosum, for of its high cellular density. instance) are undeveloped and both factors make inter- During the second trimester the cells in this layer will mi- pretation difficult. grate to the surface, where they will form the brain cortex. Later on, in the third trimester, only small foci of germinal It is basic to have a previous recent ultrasound study as matrix persist in the temporal and occipital horns of the a guide, not only for the direct assessment of the malfor- lateral ventricles. The pattern of gyri and sulci undergoes mation under study, but also to have some orientation modifications during the process of development, going regarding fetal position and most of all, fetal neural axis, from a relatively agyral brain up to the 20th week to a for the third-trimester scan. First of all a localizer scan in all more complex pattern in the third trimester. Through three planes is done, so as to get an overview of position knowledge of the temporal sequence of appearance of the

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main sulci it is possible to assess fetal brain development TABLE 1 chronologically. Table 1 Time of development of the main brain sulci

Following this course, we will find that the interhemisphe- Main brain sulci Gestational age in Fissures weeks ric fissure is already present before the 20th week, the callosomarginal fissure appears around the 22nd week, the Interhemispheric fissure 10 - 12 calcarine fissure between the 20th and the 22nd week, the central sulcus in the 26th week and the postcentral Callosomarginal fissure 20 - 24 sulcus is to be found shortly before the 30th week, around Calcarine fissure 18 -22 the 28th week. Figure 1 Morphology and size of lateral ventricles are important Sylvian fissure 16 - 20 items in the assessment, because as we shall see later, Intraparietal sulcus 24 - 26 these values are among the most commonly obtained. The presence of septum pellucidum must be assessed; it Insula 32 - 34 should be present by the 18th week, beyond that date its Central sulcus (fissure of Rolando) 22 - 26 absence is considered abnormal.

Posterior fossa structures must also be evaluated. Precentral sulcus 24 - 26 The cerebellar vermis, a medial structure, must be present between the 18th and the 21st week, as a part of the fourth Postcentral sulcus 26 - 28 ventricle. (5) Figure 2

Figure 1 Normal fMR scan (gestational age: 27 weeks) (A), sagittal slice along the midline and (B) axial slice at bithalamic level of normal fetal brain in the 27th week, fast T2-weighted sequence. In the midline image the callous body (CC) and the calcarine fissure (è) can be clearly identified, as well as posterior fossa structures, all of which have developed according to age. In the axial plane it is possible to identify the midline and the basal ganglia region, both anatomically normal, with a gyral pattern according to gestational age, the Sylvian fissure (CS) just beginning to appear. Different structures of the ventricular system can be clearly identified: lateral ventricles (VL), third ventricle (sited between both thalami [T]), and fourth ventricle (sited between cerebellum [Ce] and brain stem [Te]).

Figure 2 Normal fetal MR scan (gestational age: 32 weeks) Multiplanar images of normal fetal brain at 32 weeks of gestational age. The gyral pattern already resembles the newborn pattern. In the midline slice (A), both calcarine fissure (CCal) and the callosomarginal sulcus (SPC) can be identified surrounding the homonymous commisure (CC). Brainstem (Te) and cerebellum (Ce) can also be accurately identified. In the coronal slice (B) the cerebellum (Ce) with its two hemispheres and the inferior vermis (Vi) can be accurately assessed. In the axial slice at posterior fossa level, (C), it is possible to evaluate posterior fossa structures, along with the vermis (V) and the fourth ventricle (è) at its usual site. The proximal portion of the Sylvian fissure (CS) can also be clearly visualized. Finally in the supratentorial axial slice (D) several structures are clearly visualized: a well-developed gyral pattern, the basal ganglia region, thalamus (T) and the cavum of the septum pellucidum (CSP) in the usual stage of development.

REVISION WORK / N. Sgarbi MD, V. Etchegoimberry MD 94 MAIN INDICATIONS OR CLINICAL SITUA- The most important issue is to differentiate patients with isolated ventriculomegaly from those with ventriculome- TIONS galy associated to other anomalies or malformations (the Performance of an fMR scan is indicated in various clini- percentage ranges from 20 to 50% of the total, according cal situations, with the purpose of analyzing the nervous to the series) (9). It has been pointed out that the more system. In some centers nearly 80% of fetal studies are severe the ventriculomegaly, the higher the risk of asso- ordered to analyze a probable encephalic malformation. ciated malformations. In spite of excellent global results, some authors have reported a discrepancy between prenatal findings and The anomalies most frequently associated are those of postnatal MR of nearly 10% (6). the corpus callosum, which will be discussed further on. It is important to differentiate fetal ventriculomegaly from Ventriculomegaly. According to several authors, the increa- fetal hydrocephalus, because of the therapeutic implica- se in size of lateral ventricles (ventriculomegaly, VM) is the tions and the impact on prognosis. most frequent indication for fMR, about 40 to 50 % of the total. In the brief personal experience of one of the present One of the most frequently diagnosed causes of intrau- authors, this indication represents 60% of all fMR scans terine hydrocephalus is stenosis of the Sylvian aqueduct, performed in one of our community health institutions. which significantly dilates the lateral ventricles and may VM is defined as implying a ventricular diameter higher be amenable to treatment in order to improve its prog- than 10 mm measured at the body in an axial slice at nosis. Figure 4 bithalamic level, although there are different systems for In case of extreme HCF it is fundamental to differentiate its diagnosis and classification (7, 8). Figure 3 it from hydranencephaly, a destructive vascular process,

Figure 3 Fetal MR scan with ventriculomegaly (gestational age: 28 weeks) Selected fMR images of a patient referred on account of enlargement of the ventricular system in the US scan. In (A), midline image where normal structures are recognizable and appear normal: callous body (CC), brain stem (Te) and cerebellum (Ce). In (B), axial slice at ventricular body level in order to assess ventricular size (16 mm on the left side). The completely formed interhemispheric fissure (CIE) can be identified, as well as the Sylvian fissure (CS) at the convexity. (C) and (D) are coronal slices that complement anatomical assessment. A detailed review of the whole scan did not yield associated anomalies.

Figure 4 Fetal MR scans: Hydrocephalus caused by aqueductal stenosis Two cases of fetal hydrocephalus (HCF) caused by aqueductal stenosis are presented. The first case presents with mild-moderate HCF (sagittal slice A, axial slice B). Supratentorial ventricular dilation with normal fourth ventricle can be observed, which suggests the diagnosis of aqueductal stenosis. C shows the sagittal image of the second case, with severe HCF and absence of signal at the Sylvian aqueduct, which suggests the diagnosis (è). AV: body of lateral ventricle CC: corpus callosum Te: brain stem Ce: cerebellum

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and from prosencephalies, a group of entities with very TABLE 2 different prognosis. Figure 5 Main midline malformations

Midline alterations. Alterations of the midline include a Midline malformations group of malformations of varying complexity and prog- Dysgenesis/Agenesis of corpus callosum (isolated or associated nosis. Table 2 to other malformations)

Lipomas Fetal MR is a highly sensitive method for the diagnosis of midline structure anomalies, especially corpus callosum Prosencephalies: anomalies (10). Alobar/Semilobar/Lobar Holoprosencephaly

Corpus callosum agenesis is one of the most frequent Middle interhemispheric variant (Barcovich) developmental anomalies, with an incidence of 2 cases per 10000 live births. Septo-optic dysplasia In most patients it is associated with other malformations and its prognosis is quite variable and uncertain, depen- There are both direct and indirect signs of developmental ding on multiple associated factors. alteration (1). Those signs include: alterations of the presence of sep- The CC is the most important cerebral commissure; it takes tum pellucidum, VM and colpocephalic shape of lateral on its usual appearance in the 20th gestational week, when ventricles, absence of callosomarginal sulcus and midline its anterior sector is formed. lipomas (11). Figure 6

Figure 5 Fetal MR. Hydranencephaly. fMR scan at 29 weeks of gestational age in a patient referred for confirmation of diagnosis of hydranencephaly as differentiated from extreme hydrocephalus. In A, sagittal image where the dilated ventricular system can be observed, as well as normal anatomy of posterior fossa structures and fourth ventricle. In coronal image B, severe dilation of lateral ventricles can be observed, while both thalami (T) present a normal aspect, with the third ventricle between them. In the axial slices (C and D) the aforementioned elements are also observed and the presence of another midline structure, the falx cerebri (HC), is confirmed, as well as the thin cerebral mantle (MC) at occipital level. All this makes it possible to differentiate this entity from holoprosencephalies. Te: Brainstem Ce: Cerebellum

Figure 6 Fetal MR. Corpus Callosum agenesis. Scan performed at 27 weeks of gestational age, following a diagnosis of CC agenesis. In sagittal image (A), neither CC nor callosomarginal sulcus are observed. The medial gyri have the radiating appearance usually observed in this entity. Lateral ventricles (è) assume a colpocephalic shape and an anteroposterior course as seen in the axial slice (B). Posterior fossa structures are normal. Te: Brainstem Ce: Cerebellum

REVISION WORK / N. Sgarbi MD, V. Etchegoimberry MD 96 The developmental anomalies most commonly associated has been flattened by the centrifugal mass effect exerted with CC dysgenesis include cortical development malfor- by ventricular pressure. Midline structures are well-de- mations, which will be discussed further on. CC dysgenesis veloped. may also associate with midline cysts, posterior fossa Malformations of cortical development. The malformations malformations or even extraneural alterations. of cortical development (MCD) include a wide range of It is important to assess other group of more severe midline entities whose diagnosis is not simple, even in the postnatal malformations, that of prosencephalies (12). stage (13). Prognosis varies to a wide extent, which is why These malformations are linked to undetermined outcome a precise early diagnosis is so important. and also to a not inconsiderable incidence of facial mal- This group includes alterations of the usual gyral pattern formations, especially in the most severe forms. like polygyria or pachygyria, extreme situations like The differentiation between extreme forms of these alte- lissencephaly in its various presentations, gray matter rations, such as alobar holoprosencephaly or hydranen- heterotopias and schizencephaly. cephaly from extreme hydrocephalus is a special situation. Polygyria and pachygyria are alterations of cortical develo- As mentioned above, fMR can provide important findings pment that arise at the stage of migration and organization. of therapeutic and prognostic value. The result is an unusual gyral pattern of the cortex, with Alobar holoprosencephaly is characterized by the lack of multiple small gyri for polygyria, or a lesser number of normal development of midline structures (falx cerebri, bigger gyri for pachygyria. for instance), a single ventricular cavity with no septum On the other hand, lissencephaly is the result of an inte- pellucidum, and cerebral mantle of varying thickness rruption in the migration process, which produces a thick surrounding this cavity. At the center the fused thalami cerebral cortex and a smooth cerebral surface. can be seen, forming the structure known as intermediate Gray matter heterotopia is, as its name implies, a classical mass. Figure 7 migration alteration that produces single or multiple foci In the case of hydranencephaly encephalic parenchyma of gray matter in anomalous localizations. Such foci may appears destroyed to a variable extent, which results in the be periventricular, deep-seated, sited in the white matter disappearance of the cerebral mantle surrounding both between the lateral ventricles, cortical or even more su- ventricles. These cavities have developed independently perficial (subcortical). and midline structures are present. Figure 5 Finally, schizencephaly is a cleft linking the cortical surface Finally, as was mentioned above, extreme hydrocephalus to the lateral ventricles. It may be a single cleft or more presents with a severe dilation of the lateral ventricles, than one, varying as to depth and width. Ectopic gray whose shape is partially preserved. The ventricles are matter is to be found on the borders of the cleft. Figure 8 surrounded by a well-developed cerebral mantle which These alterations may be a part of more complex genetic

Figure 7 Fetal MR. Holoprosencephaly. fMR scan performed at 28 weeks. Patient referred for confirmation of US diagnosis of holoprosencephaly. In the coronal plane (A) the single ventricular cavity can be identified, as well as the surrounding thin cerebral mantle and the characteristic intermediate mass (MI) produced by the lack of thalamic division. In the axial plane (B) the findings are similar, with a lack of midline structures like the interhemispheric fissure or the falx cerebri. Te: Brainstem

Figure 8 Fetal MR. Bilateral schizencephaly. MR scan performed at 29 weeks. US diagnosis: bilateral schizencephaly. In both axial (A) and coronal (B) slices the classical clefts can be identified, communicating the ventricular system with the subarachnoid space at the convexity of both hemispheres. Midline structures are normal, as well as the brainstem (Te) and the remaining intracranial structures.

97 Rev. Imagenol. 2da Ep. Jan./Jun. 2018 XXI (2): 92-101 FETAL MAGNETIC RESONANCE A CONTRIBUTION TO THE DIAGNOSIS OF CENTRAL NERVOUS SYSTEM MALFORMATIONS syndromes, or they may relate to infections of pregnancy on multiple factors, the main factor being association with such as cytomegalovirus infection. supratentorial malformations, which occurs in up to 70 % Choosing the right moment for the assessment is critical of the cases (5). Figure 9 for this group of alterations. Fetal MR can also evaluate the presence and localization Several authors propose the period between the 28th and of the cerebellar tonsils, which leads to the possibility of the 32nd week of pregnancy as the ideal moment for the the Chiari group of malformations. assessment of these alterations. Among this Chiari group, the most important entity is Posterior fossa alterations. Developmental alterations the Chiari II malformation on account of its therapy and that compromise posterior fossa structures are relatively prognosis. It includes not only a small posterior fossa, frequent and their diagnosis is not so simple. but may also associate with supratentorial malformations The last few years have seen a considerable modification (dysgenesis of corpus callosum and hydrocephalus, main- of the classification of these alterations, based on a better ly) and with closure alterations of the neural tube (spinal understanding of their production. dysrhaphisms). Figure 10 In consequence, at this moment this vast group of mal- It is basic to evaluate not only the cranium and its content, formations is divided in several subgroups: predominantly but also the distal spine in order to rule out dysraphisms cerebellar malformations, cerebellar malformations plus like myelomeningocele or other varieties (17). brain stem malformations, malformations affecting prima- Compared to the cerebellum, the brain stem is more rily the brainstem, and mesencephalic malformations (14). complex structure regarding visualization and accurate Malformations compromising mainly the cerebellum in- review. Therefore, prenatal diagnosis of brain stem alte- clude those affecting the vermis; in this group we find the rations proves to be complex by RM techniques, although entities previously defined as Dandy-Walker malformation, their contributions are more considerable than those of vermian hypoplasia and rhombencephalosynapsis. ultrasound. Fetal MR can assess both the cerebellar vermis and the Other indications. The contributions of fMR to the diag- cisterna magna accurately in order to investigate Dandy- nosis of malformations are clearly established, but in other Walker malformation; it visualizes the torcular herophili pathological situations indication varies and the technique and the tentorium, as well as the morphology of cerebe- contributes differently. llum and fourth ventricle (14-16). It is frequently used in extreme situations of grave fetal Dandy-Walker malformations consist of cerebellar vermian distress, such as destruction of encephalic parenchyma agenesis of varying degree, along with dilation of fourth due to vascular damage, or hemorrhages that may occur ventricle and retrocerebellar cyst. during fetal development. Figure 11 Prognosis varies considerably within this group; it depends Fetal MR can also contribute to the diagnosis of vascular

Figure 9 Fetal MR in posterior fossa malformation. Two cases diagnosed with Dandy-Walker malformation are presented, both with cystic malformation sited at the posterior fossa (è). This cyst communicates with the fourth ventricle at the expense of a developmental alteration of the cerebellar vermis. In A and B, sagittal and axial images of fMR scan performed at 27 weeks. Moderate supratentorial dilation of the ventricular system. In the second case (C and D) severe dilation of the supratentorial ventricular system is observed, along with thinning of corpus callosum in a fetus 29 weeks of gestational age. Te: brainstem Ce: cerebellum

REVISION WORK / N. Sgarbi MD, V. Etchegoimberry MD 98 malformations, such as vein of Galen malformations, or patients with a past history of malformations, who are to the characterization of space-occupying lesions whose in need of guidance regarding genetic counseling and nature cannot be clearly established in the ultrasound scan. planned parenthood. It is also indicated in craniofacial and cervical malfor- Some characteristic of the maternal constitution may mations, a high percentage of which are associated with suggest the need of performing an fMR scan. In obese encephalic malformations. mothers with a high body mass index ultrasound performs In the last few years there has been an increasing awa- very poorly, this situation may provide a valid indication in reness of the benefit of using fMR as a screening tool in order to achieve a better anatomical evaluation.

Figure 10 Fetal MR in Chiari malformation. Scan performed at 29 weeks of gestational age, on account of US-diagnosed myelomeningocele. In the coronal image (A) severe dilation of supratentorial ventricular system is observed, which is confirmed in the axial image (B). Also to be seen in (B): colpocephaly of lateral ventricles (VL). In the sagittal image of the fetus (C) both cerebellum (Ce) and brainstem (Te) can be identified, but the fourth ventricle is not clearly evident, which suggests the presence of a small posterior fossa. In the same plane a defect of neural tube closure (è) can be observed, with a meningocele sac. The axial slice at sac level (D) shows a clear posterior spinal defect (è), but the neural content of the same is not quite evident.

Figure 11 Fetal MR in severe fetal distress. fMR scan performed as a complement of US scan suggestive of destruction of encephalic parenchyma. An axial slice of the posterior fossa (A) presents structures of normal appearance in this compartment. The supratentorial axial slice (B) shows multiple cystic cavities that cannot be clearly differentiated from the ventricular system. The cortical mantle is thin and there are multiple septi. The midline structures (è) are well- developed. In the coronal plane (C) both midline structures and posterior fossa again show no evidence of alteration and mildly dilated lateral ventricles (VL) can be partially identified. Finally in the sagittal plane (D) a thin corpus callosum (CC) can be seen and it is possible to check the posterior fossa again. The final diagnosis was multicystic encephalomalacia due to vascular damage. Te: Brainstem Ce: Cerebellum

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Even if the MR images are not optimal either, the informa- affords image acquisition in the sagittal and coronal planes, tion they provide is generally of better quality. which provides a more accurate anatomical study, espe- Oligohydramnios is another indication for fMR, because cially in the case of midline structures (corpus callosum, it affects US imaging negatively, while MR images are not third ventricle and cerebellar vermis) which cannot be damaged at all. If diagnostic doubts arise and more ana- correctly evaluated in the axial plane. tomic definition is needed, oligohydramnios is a formal Being an ultrasound study, it is innocuous and less costly indication for fMR. than fMR, which is why it may be repeated as often as necessary during pregnancy. In this way, it can determine CORRELATION BETWEEN ULTRASOUND more accurately the development and the prognosis of the malformation. FINDINGS AND FETAL MR It must be taken into account that the examiner must be quite experienced in order to achieve good imaging, as is As mentioned above, ultrasound remains the study of always the case in focused and specific studies. It is also choice for the fetus, the fetal study par excellence. For known that the fetus must be in the cephalic presentation the nervous system two levels of complexity are provided: position, so that the scan can be performed transvaginally ultrasound screening and neurosonography (NSG). with an endocavitary transducer. In this way excellent The first level, ultrasound screening, will either determine anatomic resolution can be achieved. Figure 12 if an anomaly is suspected or will arrive at a definitive On the other hand, there exists a certain consensus that diagnosis. The latter occurs mainly with first-trimester fMR provides better information than NSG for some anomalies, which are the most severe ones. anomalies. That is the case with malformations of cortical On the other hand, the second level is represented by development, where it has been proved that fMR provides neurosonography, a study focusing on the nervous system. more information in up to 20% of the cases. Keeping this Neurosonography is indicated when ultrasound screening in mind, one must consider that NSG has excellent corre- diagnosed the aforementioned anomalies, when it did lation with fMR findings (18, 19). Figures 13, 14 not arrive at a diagnosis or in patients at a high risk of What is more important is that, as we mentioned earlier, malformation (18). these two imaging methods are not mutually exclusive but NSG has an advantage over conventional ultrasound: it complementary, if the respective limitations are kept in mind, as well as the best moment for each one.

Figure 12 NSG, normal midline anatomy. Ultrasound study focused on the nervous system. Sagittal slice performed at 29 weeks for the assessment of midline structures. The chosen image shows in excellent detail the anatomy of supra- and infratentorial structures. The corpus callosum (CC) is observed, as well as a part of the lateral ventricles (VL). Brain stem (Te) and cerebellum (Ce) can be clearly differentiated from the fourth ventricle sited between them. Primary and secondary fissures of Ce can be clearly identified. T: Thalamus A B

Figure 13 Correlation between NSG and fMR in C D malformations. Correlation between ultrasound findings and fMR in the study of a fetus 29 weeks of gestational age. Abdominal (A) scan and transvaginal NSG (B). An occipital gap with meningeal content is observed, with no herniation of encephalic parenchyma (è). All this was confirmed by fMR (axial slice C and sagittal slice D), which settles the diagnosis of occipital meningocele. CSP: cavum septum pellucidum V: cerebellar vermis Te: brain stem

REVISION WORK / N. Sgarbi MD, V. Etchegoimberry MD 100 A B

Figure 14 Correlation between NSG and fMR in malformations. Correlation between fMR and NSG, both in sagittal plane. The case shown is a fetus with venous thrombosis C D at torcular herophili and dilation of the superior sagittal sinus. In figures A and B the echogenic thrombus (è) can be seen, as well as the dilated hypogenic sagittal sinus (*) which compresses and displaces encephalic structures. The fMR scan performed a few days later confirms those findings, because it shows a subacute thrombosis in the region of the torcular herophili (è), associated with a dilated sagittal sinus (C). The fetus then underwent an intraventricular hemorrhage, which is shown in figure D (**). Ce: cerebellum Te: brain stem

FINAL CONCEPTS

Nervous system malformations are frequent and impact considerably on postnatal life. At present we have two prenatal diagnostic techniques of proven value like US (with its different levels of complexity) and fMR. It must be taken into account that in most cases the US scan suffices for the diagnosis, especially if we are dealing with first-trimester malformations.

Fetal MR is a very useful tool when indicated, because it can contribute to the diagnosis of CNS malfor- mations in up to 20% of the cases; it remains, however, a complement of the US scan.

SUMMARY

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101 Rev. Imagenol. 2da Ep. Jan./Jun. 2018 XXI (2): 92-101