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92 NEURORRADIOLOGÍA ESPACIO DE FETAL MAGNETIC RESONANCE A CONTRIBUTION TO THE DIAGNOSIS OF CENTRAL NERVOUS SYSTEM MALFORMATIONS Nicolás Sgarbi MD, Verónica Etchegoimberry MD ABSTRACT Central Nervous System malformations are relatively frequent and have a negative impact in postnatal morbidity and mortality. Prenatal diagnosis is based on the obstetric ultra- sound, which has been validated throughout the years with an excellent performance. In the last years, there has been a substantial change in the prenatal diagnosis, not only for deciding the termination of pregnancy, but also to assess in the opportunity of intrauterine surgery. In this revision we will analyze the most important technical aspects and indications of Fetal MRI, and its importance in the prenatal diagnosis of Central Nervous System Malformations. Key Words: Fetal MRI, Central Nervous System Mal- formations, neurosonography. RESUMEN Las malformaciones del sistema nervioso son relativa- mente frecuentes e impactan de forma significativa en la morbi-mortalidad postnatal. Su diagnóstico pre-natal se basa en una técnica vali- dada desde hace varias décadas como es la ecografía cuyo rendimiento general es excelente. En los últimos años se ha producido un cambio sustan- cial en el paradigma diagnóstico de las malformaciones no sólo por las implicancias que esto tiene en decidir la continuidad del embarazo, sino además por el de- sarrollo de técnicas de cirugía intrauterina. En esta revisión analizaremos los principales aspectos técnicos de la resonancia magnética fetal y sus aportes al diagnóstico de las malformaciones más frecuentes del sistema nervioso. Palabras clave: resonancia magnética fetal, malforma- ciones del sistema nervioso, neurosonografía. INTRODUCTION The study of fetal anatomy is done as a routine part of prenatal care. Ultrasound (US) is the diagnostic method of choice, because it gives excellent global results for the complete anatomic assessment of the fetus during its different developmental stages. It has been long been clearly established that US is a highly sensitive method for the detection of malformations, even 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 MR in this field is constantly increasing. In this respect some authors point out that anomalies that were not diagnosed by US can be detected by MR in 20% of patients (1). At the same time, changes in law and health policy have allowed for voluntary interruption of pregnancy and have in this way impacted the diagnosis and management of malformations. That is why Fetal Magnetic Resonance (fMR) has become a complementary technique to US in the study of the central nervous system (CNS). The objectives of this review are: to analyze the contri- bution of fMR to the study of the central nervous system of the fetus and its more frequent malformations, and to highlight the general principles of this technique, as well as its scope and its limitations. TECHNICAL ASPECTS MR has developed considerably in the last few years, due to the changed paradigm for the study of congenital malformations. This change came about essentially on account of ad- vances in treatment for some malformations (corrective intrauterine fetal surgery), the need of a diagnosis in view of prenatal genetic advice and planned parenthood, and Corresponding author: [email protected] Received april 19 th Accepted may 5 th 2018 REVISION WORK / N. Sgarbi MD, V. Etchegoimberry MD

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Page 1: Fetal Magnetic Resonance - webcir.org

92

NEURORRADIOLOGÍAESPACIO DE

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

Nicolás Sgarbi MD, Verónica Etchegoimberry MD

ABSTRACT

Central Nervous System malformations are relatively frequent and have a negative impact in postnatal morbidity and mortality. Prenatal diagnosis is based on the obstetric ultra-sound, which has been validated throughout the years with an excellent performance. In the last years, there has been a substantial change in the prenatal diagnosis, not only for deciding the termination of pregnancy, but also to assess in the opportunity of intrauterine surgery. In this revision we will analyze the most important technical aspects and indications of Fetal MRI, and its importance in the prenatal diagnosis of Central Nervous System Malformations.

Key Words: Fetal MRI, Central Nervous System Mal-

formations, neurosonography.

RESUMEN

Las malformaciones del sistema nervioso son relativa-mente frecuentes e impactan de forma significativa en la morbi-mortalidad postnatal.Su diagnóstico pre-natal se basa en una técnica vali-dada desde hace varias décadas como es la ecografía cuyo rendimiento general es excelente.En los últimos años se ha producido un cambio sustan-cial en el paradigma diagnóstico de las malformaciones no sólo por las implicancias que esto tiene en decidir la continuidad del embarazo, sino además por el de-sarrollo de técnicas de cirugía intrauterina.En esta revisión analizaremos los principales aspectos técnicos de la resonancia magnética fetal y sus aportes al diagnóstico de las malformaciones más frecuentes del sistema nervioso.

Palabras clave: resonancia magnética fetal, malforma-

ciones del sistema nervioso, neurosonografía.

INTRODUCTION

The study of fetal anatomy is done as a routine part of prenatal care. Ultrasound (US) is the diagnostic method of choice, because it gives excellent global results for the complete anatomic assessment of the fetus during its different developmental stages.It has been long been clearly established that US is a highly sensitive method for the detection of malformations, even 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 MR in this field is constantly increasing. In this respect some authors point out that anomalies that were not diagnosed by US can be detected by MR in 20% of patients (1).At the same time, changes in law and health policy have allowed for voluntary interruption of pregnancy and have in this way impacted the diagnosis and management of malformations.

That is why Fetal Magnetic Resonance (fMR) has become a complementary technique to US in the study of the central nervous system (CNS).

The objectives of this review are: to analyze the contri-bution of fMR to the study of the central nervous system of the fetus and its more frequent malformations, and to highlight the general principles of this technique, as well as its scope and its limitations.

TECHNICAL ASPECTS

MR has developed considerably in the last few years, due to the changed paradigm for the study of congenital malformations.This change came about essentially on account of ad-vances in treatment for some malformations (corrective intrauterine fetal surgery), the need of a diagnosis in view of prenatal genetic advice and planned parenthood, and

Corresponding author:

[email protected]

Received april 19th

Accepted may 5th

2018

REVISION WORK / N. Sgarbi MD, V. Etchegoimberry MD

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Rev. Imagenol. 2da Ep. Jan./Jun. 2018 XXI (2):93

the legal modification related to interruption of pregnancy. The subsequent use of MR along with the different va-rieties of US has modified the diagnostic approach to malformations.

The first concept to be highlighted is that MR must be performed only after an ultrasound scan was performed by an expert in the assessment of fetal anatomy (2). Many factors must be taken into account when ordering and performing fMR.

As a general recommendation, in the first place the scan must focus on the anatomical region or organ that pre-sented some alteration on US, so that the technique can be shown to best advantage.

Then other factors concerning the maternal-fetus unit must come into consideration. To achieve good imaging one must acquire images while the fetus is immobile.

Sedation is not recommended, it is preferable to ask the mother to fast during 4 to 6 hours, so as to restrict fetal movements as much as possible.The mother must receive precise and detailed information about the duration of the study, the position to maintain during that time and the respiratory movements that will be asked of her.

The patient must be placed on her back or even on her side, whichever is more comfortable for her, so as to ensure her collaboration during the study.Usually fMR is performed with 1.5 T equipment, but in the last few years some centers have reviewed the contribution of 3T magnets (1), although it is known that their routine use is not recommended yet (3).

Although image resolution may improve, movement arti-facts increase likewise. That is why the use of high magnetic fields calls for more rigorous technique if optimal results are to be achieved.Surface coils must be used on the body, with as many receptor channels as possible, so that high-resolution images are obtained in the least possible acquisition time.The timing of the pregnancy scan is a point of the utmost importance.

Most centers recommend performing the fMR scan after the 19-20th week of pregnancy. Earlier on, structures are very small and some of them (corpus callosum, for instance) are undeveloped and both factors make inter-pretation difficult.

It is basic to have a previous recent ultrasound study as a guide, not only for the direct assessment of the malfor-mation under study, but also to have some orientation regarding fetal position and most of all, fetal neural axis, for the third-trimester scan. First of all a localizer scan in all three planes is done, so as to get an overview of position

and anatomy of the fetus. Then comes the planning of the scan. It is necessary to obtain fast T2-weighted cranium images in the three spa-tial planes (4). Sagittal spine images are obtained, axial or coronal planes may be used too if considered necessary or complementary.

Single-shot sequences must be used, such as Single Shot Fast Spin Echo (SSFSE) or the Half Fourier Acquisition Turbo Spin-Echo (HASTE).Slice thickness must be adequate to fetal size, not exce-eding 3 mm; an adequate field of vision (FOV) must be chosen in order to obtain specific images of the region of interest.

In special cases, study protocol may include other sequen-ces such as T1-weighted sequences for fat analysis, or the susceptibility sequences such as T2- or SWI-weighted GRE sequences for the assessment of hemorrhage, as well as diffusion sequences (DWI) for the study of ischemia. Longer acquisition time is a limiting factor in such cases.It is important to take into account some safety parameters.The FDA has set clear limits to the specific absorption rate (SAR) of radio frequency, but its effects on the maternal-fe-tal unit remain unclear (1).

All patients must receive clear information about the fMR modality in use, its benefits, its scope and its limitations.

In order to interpret and analyze an fMR scan correctly it is essential to know the usual appearance of the brain during its development.A review of fetal brain reveals three basic components that permit a fairly accurate diagnosis of the stage of de-velopment. These components are: brain parenchyma, germinal matrix and sulcation pattern (1).During development white matter presents with high signal in T2-weighted scans, on account of its high water content and scant myelinization.Brain parenchyma (or cerebral mantle) appears as several layers that can be accurately observed between the 28th and the 30th week of development.The germinal matrix is the cell layer that will produce neurons; it is to be found on the walls of the ventricular system. In T2-weighted scans it has a low signal on account of its high cellular density.During the second trimester the cells in this layer will mi-grate to the surface, where they will form the brain cortex. Later on, in the third trimester, only small foci of germinal matrix persist in the temporal and occipital horns of the lateral ventricles. The pattern of gyri and sulci undergoes modifications during the process of development, going from a relatively agyral brain up to the 20th week to a more complex pattern in the third trimester. Through knowledge of the temporal sequence of appearance of the

NORMAL CHARACTERISTICS OF FETAL BRAIN

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FETAL MAGNETIC RESONANCE A CONTRIBUTION TO THE DIAGNOSIS OF CENTRAL

NERVOUS SYSTEM MALFORMATIONS

main sulci it is possible to assess fetal brain development chronologically. Table 1

Following this course, we will find that the interhemisphe-ric fissure is already present before the 20th week, the callosomarginal fissure appears around the 22nd week, the calcarine fissure between the 20th and the 22nd week, the central sulcus in the 26th week and the postcentral sulcus is to be found shortly before the 30th week, around the 28th week. Figure 1Morphology and size of lateral ventricles are important items in the assessment, because as we shall see later, these values are among the most commonly obtained.The presence of septum pellucidum must be assessed; it should be present by the 18th week, beyond that date its absence is considered abnormal.Posterior fossa structures must also be evaluated.The cerebellar vermis, a medial structure, must be present between the 18th and the 21st week, as a part of the fourth ventricle. (5) Figure 2

Interhemispheric fissure

Callosomarginal fissure

Calcarine fissure

Sylvian fissure

10 - 12

20 - 24

18 -22

16 - 20

TABLE 1

Main brain sulci Fissures

Gestational age in weeks

Insula

Central sulcus (fissure of Rolando)

32 - 34

22 - 26

Intraparietal sulcus

Time of development of the main brain sulci

Precentral sulcus

Postcentral sulcus

24 - 26

26 - 28

24 - 26

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

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Rev. Imagenol. 2da Ep. Jan./Jun. 2018 XXI (2):95

Performance of an fMR scan is indicated in various clini-cal situations, with the purpose of analyzing the nervous system. In some centers nearly 80% of fetal studies are ordered to analyze a probable encephalic malformation. In spite of excellent global results, some authors have reported a discrepancy between prenatal findings and postnatal MR of nearly 10% (6).

Ventriculomegaly. According to several authors, the increa-se in size of lateral ventricles (ventriculomegaly, VM) is the most frequent indication for fMR, about 40 to 50 % of the total. In the brief personal experience of one of the present authors, this indication represents 60% of all fMR scans performed in one of our community health institutions. VM is defined as implying a ventricular diameter higher than 10 mm measured at the body in an axial slice at bithalamic level, although there are different systems for its diagnosis and classification (7, 8). Figure 3

The most important issue is to differentiate patients with isolated ventriculomegaly from those with ventriculome-galy associated to other anomalies or malformations (the percentage ranges from 20 to 50% of the total, according to the series) (9). It has been pointed out that the more severe the ventriculomegaly, the higher the risk of asso-ciated malformations.

The anomalies most frequently associated are those of the corpus callosum, which will be discussed further on.It is important to differentiate fetal ventriculomegaly from fetal hydrocephalus, because of the therapeutic implica-tions and the impact on prognosis.

One of the most frequently diagnosed causes of intrau-terine hydrocephalus is stenosis of the Sylvian aqueduct, which significantly dilates the lateral ventricles and may be amenable to treatment in order to improve its prog-nosis. Figure 4In case of extreme HCF it is fundamental to differentiate it from hydranencephaly, a destructive vascular process,

MAIN INDICATIONS OR CLINICAL SITUA-TIONS

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

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.

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96

and from prosencephalies, a group of entities with very different prognosis. Figure 5

Midline alterations. Alterations of the midline include a group of malformations of varying complexity and prog-nosis. Table 2

Fetal MR is a highly sensitive method for the diagnosis of midline structure anomalies, especially corpus callosum anomalies (10).

Corpus callosum agenesis is one of the most frequent developmental anomalies, with an incidence of 2 cases per 10000 live births. In most patients it is associated with other malformations and its prognosis is quite variable and uncertain, depen-ding on multiple associated factors.

The CC is the most important cerebral commissure; it takes on its usual appearance in the 20th gestational week, when its anterior sector is formed.

There are both direct and indirect signs of developmental alteration (1).Those signs include: alterations of the presence of sep-tum pellucidum, VM and colpocephalic shape of lateral ventricles, absence of callosomarginal sulcus and midline lipomas (11). Figure 6

Dysgenesis/Agenesis of corpus callosum (isolated or associated to other malformations)

Lipomas

Prosencephalies:

Alobar/Semilobar/Lobar Holoprosencephaly

TABLE 2

Midline malformations

Septo-optic dysplasia

Middle interhemispheric variant (Barcovich)

Main midline malformations

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

FETAL MAGNETIC RESONANCE A CONTRIBUTION TO THE DIAGNOSIS OF CENTRAL

NERVOUS SYSTEM MALFORMATIONS

REVISION WORK / N. Sgarbi MD, V. Etchegoimberry MD

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Rev. Imagenol. 2da Ep. Jan./Jun. 2018 XXI (2):97

The developmental anomalies most commonly associated with CC dysgenesis include cortical development malfor-mations, which will be discussed further on. CC dysgenesis may also associate with midline cysts, posterior fossa malformations or even extraneural alterations.It is important to assess other group of more severe midline malformations, that of prosencephalies (12). These malformations are linked to undetermined outcome and also to a not inconsiderable incidence of facial mal-formations, especially in the most severe forms.The differentiation between extreme forms of these alte-rations, such as alobar holoprosencephaly or hydranen-cephaly from extreme hydrocephalus is a special situation. As mentioned above, fMR can provide important findings of therapeutic and prognostic value.Alobar holoprosencephaly is characterized by the lack of normal development of midline structures (falx cerebri, for instance), a single ventricular cavity with no septum pellucidum, and cerebral mantle of varying thickness surrounding this cavity. At the center the fused thalami can be seen, forming the structure known as intermediate mass. Figure 7In the case of hydranencephaly encephalic parenchyma appears destroyed to a variable extent, which results in the disappearance of the cerebral mantle surrounding both ventricles. These cavities have developed independently and midline structures are present. Figure 5Finally, as was mentioned above, extreme hydrocephalus presents with a severe dilation of the lateral ventricles, whose shape is partially preserved. The ventricles are surrounded by a well-developed cerebral mantle which

has been flattened by the centrifugal mass effect exerted by ventricular pressure. Midline structures are well-de-veloped.Malformations of cortical development. The malformations of cortical development (MCD) include a wide range of entities whose diagnosis is not simple, even in the postnatal stage (13). Prognosis varies to a wide extent, which is why a precise early diagnosis is so important.This group includes alterations of the usual gyral pattern like polygyria or pachygyria, extreme situations like lissencephaly in its various presentations, gray matter heterotopias and schizencephaly. Polygyria and pachygyria are alterations of cortical develo-pment that arise at the stage of migration and organization. The result is an unusual gyral pattern of the cortex, with multiple small gyri for polygyria, or a lesser number of bigger gyri for pachygyria.On the other hand, lissencephaly is the result of an inte-rruption in the migration process, which produces a thick cerebral cortex and a smooth cerebral surface.Gray matter heterotopia is, as its name implies, a classical migration alteration that produces single or multiple foci of gray matter in anomalous localizations. Such foci may be periventricular, deep-seated, sited in the white matter between the lateral ventricles, cortical or even more su-perficial (subcortical).Finally, schizencephaly is a cleft linking the cortical surface to the lateral ventricles. It may be a single cleft or more than one, varying as to depth and width. Ectopic gray matter is to be found on the borders of the cleft. Figure 8These alterations may be a part of more complex genetic

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.

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

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98

syndromes, or they may relate to infections of pregnancy such as cytomegalovirus infection.Choosing the right moment for the assessment is critical for this group of alterations.Several authors propose the period between the 28th and the 32nd week of pregnancy as the ideal moment for the assessment of these alterations.Posterior fossa alterations. Developmental alterations that compromise posterior fossa structures are relatively frequent and their diagnosis is not so simple.The last few years have seen a considerable modification of the classification of these alterations, based on a better understanding of their production. In consequence, at this moment this vast group of mal-formations is divided in several subgroups: predominantly cerebellar malformations, cerebellar malformations plus brain stem malformations, malformations affecting prima-rily the brainstem, and mesencephalic malformations (14). Malformations compromising mainly the cerebellum in-clude those affecting the vermis; in this group we find the entities previously defined as Dandy-Walker malformation, vermian hypoplasia and rhombencephalosynapsis.Fetal MR can assess both the cerebellar vermis and the cisterna magna accurately in order to investigate Dandy-Walker malformation; it visualizes the torcular herophili and the tentorium, as well as the morphology of cerebe-llum and fourth ventricle (14-16).Dandy-Walker malformations consist of cerebellar vermian agenesis of varying degree, along with dilation of fourth ventricle and retrocerebellar cyst.Prognosis varies considerably within this group; it depends

on multiple factors, the main factor being association with supratentorial malformations, which occurs in up to 70 % of the cases (5). Figure 9Fetal MR can also evaluate the presence and localization of the cerebellar tonsils, which leads to the possibility of the Chiari group of malformations.Among this Chiari group, the most important entity is the Chiari II malformation on account of its therapy and prognosis. It includes not only a small posterior fossa, but may also associate with supratentorial malformations (dysgenesis of corpus callosum and hydrocephalus, main-ly) and with closure alterations of the neural tube (spinal dysrhaphisms). Figure 10It is basic to evaluate not only the cranium and its content, but also the distal spine in order to rule out dysraphisms like myelomeningocele or other varieties (17).Compared to the cerebellum, the brain stem is more complex structure regarding visualization and accurate review. Therefore, prenatal diagnosis of brain stem alte-rations proves to be complex by RM techniques, although their contributions are more considerable than those of ultrasound.Other indications. The contributions of fMR to the diag-nosis of malformations are clearly established, but in other pathological situations indication varies and the technique contributes differently.It is frequently used in extreme situations of grave fetal distress, such as destruction of encephalic parenchyma due to vascular damage, or hemorrhages that may occur during fetal development. Figure 11 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

FETAL MAGNETIC RESONANCE A CONTRIBUTION TO THE DIAGNOSIS OF CENTRAL

NERVOUS SYSTEM MALFORMATIONS

REVISION WORK / N. Sgarbi MD, V. Etchegoimberry MD

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Rev. Imagenol. 2da Ep. Jan./Jun. 2018 XXI (2):99

malformations, such as vein of Galen malformations, or to the characterization of space-occupying lesions whose nature cannot be clearly established in the ultrasound scan.It is also indicated in craniofacial and cervical malfor-mations, a high percentage of which are associated with encephalic malformations.In the last few years there has been an increasing awa-reness of the benefit of using fMR as a screening tool in

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.

patients with a past history of malformations, who are in need of guidance regarding genetic counseling and planned parenthood.Some characteristic of the maternal constitution may suggest the need of performing an fMR scan. In obese mothers with a high body mass index ultrasound performs very poorly, this situation may provide a valid indication in order to achieve a better anatomical evaluation.

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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As mentioned above, ultrasound remains the study of choice for the fetus, the fetal study par excellence. For the nervous system two levels of complexity are provided: ultrasound screening and neurosonography (NSG).The first level, ultrasound screening, will either determine if an anomaly is suspected or will arrive at a definitive diagnosis. The latter occurs mainly with first-trimester anomalies, which are the most severe ones. On the other hand, the second level is represented by neurosonography, a study focusing on the nervous system. Neurosonography is indicated when ultrasound screening diagnosed the aforementioned anomalies, when it did not arrive at a diagnosis or in patients at a high risk of malformation (18).NSG has an advantage over conventional ultrasound: it

CORRELATION BETWEEN ULTRASOUND FINDINGS AND FETAL MR

Even if the MR images are not optimal either, the informa-tion they provide is generally of better quality.Oligohydramnios is another indication for fMR, because it affects US imaging negatively, while MR images are not damaged at all. If diagnostic doubts arise and more ana-tomic definition is needed, oligohydramnios is a formal indication for fMR.

affords image acquisition in the sagittal and coronal planes, which provides a more accurate anatomical study, espe-cially in the case of midline structures (corpus callosum, third ventricle and cerebellar vermis) which cannot be correctly evaluated in the axial plane.Being an ultrasound study, it is innocuous and less costly than fMR, which is why it may be repeated as often as necessary during pregnancy. In this way, it can determine more accurately the development and the prognosis of the malformation.It must be taken into account that the examiner must be quite experienced in order to achieve good imaging, as is always the case in focused and specific studies. It is also known that the fetus must be in the cephalic presentation position, so that the scan can be performed transvaginally with an endocavitary transducer. In this way excellent anatomic resolution can be achieved. Figure 12On the other hand, there exists a certain consensus that fMR provides better information than NSG for some anomalies. That is the case with malformations of cortical development, where it has been proved that fMR provides more information in up to 20% of the cases. Keeping this in mind, one must consider that NSG has excellent corre-lation with fMR findings (18, 19). Figures 13, 14What is more important is that, as we mentioned earlier, these two imaging methods are not mutually exclusive but 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

Figure 13

Correlation between NSG and fMR in

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

A B

C D

FETAL MAGNETIC RESONANCE A CONTRIBUTION TO THE DIAGNOSIS OF CENTRAL

NERVOUS SYSTEM MALFORMATIONS

REVISION WORK / N. Sgarbi MD, V. Etchegoimberry MD

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

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

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

SUMMARY

1- Lyons K, Cassady C, Jones J et al. Current role of fetal magnetic re-sonance imaging in neurologic anomalies. Semin Ultrasound CT MRI 2015; 36:298-3092- Prayer D, Brugger PC, Prayer L. Fetal MRI: techniques and protocols. Pediatr Radiol 2004; 34:685-6933- Malinger G, Prayer D, Brugger PC et al. ISUOG Practice Guidelines: performance of fetal magnetic resonance imaging. Ultrasound Obstet Gynecol 2017; 49: 671–6804- Glastonbury CM, Kennedy AM. Ultrafast MRI of the fetus. Australas Radiol 2002; 46:22–325- Robinson AJ, Blaser S, Toi A et al. The fetal cerebellar vermis: Assessment for abnormal development by ultrasonography and magnetic resonance imaging. Ultrasound Q 2007; 23:211-2236- Dhouib A, Blondiaux E, Moutard ML, et al. Correlation between pre- and postnatal cerebral magnetic resonance imaging. Ultrasound Obstet Gynecol 2011; 38:170–1787- Cardoza JD, Goldstein RB, Filly RA. Exclusion of fetal ventriculomegaly with a single measurement: The width of the lateral ventricular atrium. Radiology 1988; 169:711-7148- Levine D, Trop I, Metha TS et al. MR imaging appearance of fetal cerebral ventricular morphology. Radiology 2002; 223:652-6609- Morris JE, Rickard S, Paley MN, et al. The value of in-utero magnetic resonance imaging in ultrasound diagnosed foetal isolated cerebral ven-triculomegaly. Clin Radiol 2007; 62:140-14410- Dill P, Poretti A, Boltshauser E, et al. Fetal magnetic resonance imaging

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.

in midline malformations of the central nervous system and review of the literature. J Neuroradiol 2009; 36:138-14611- Achiron R, Achiron A. Development of the human fetal corpus ca-llosum: A high-resolution, cross-sectional sonographic study. Ultrasound Obstet Gynecol 2001; 18:343-34712- Winter TC, Kennedy AM, Woodward PF. Holoprosencephaly: a survey of the entity, with embriology and fetal imaging. Radiographics 2015; 35:275-29013- Toi A, Chitayat D, Blaser S. Abnormalities of the foetal cerebral cortex. Prenat Diagn 2009; 29:355-37114- Bosemani T, Orman G, Boltshauser E et al. Congenital abnormalities of the posterior fossa. Radiographics 2015; 35:200-22015- Triulzi F, Parazzini C, Righini A. Magnetic resonance imaging of fetal cerebellar development. Cerebellum 2006; 5:199-20516- Guibaud L. Practical approach to prenatal posterior fossa abnormalities using MRI. Pediatr Radiol 2004; 34:700-71117- Ben-Sira L, Garel C, Malinger G, et al. Prenatal diagnosis of spinal dysraphism. Childs Nerv Syst 2013; 29:1541-155218- Malinger G, Lev D, Lerman Sagie T. Normal and abnormal fetal brain development during the third trimester as demonstrated by neurosono-graphy. EJR 2006; 57:226–23219- Hagmann CF, Robertson NJ, Leung WC et al. Foetal brain Imaging: ultrasound or MRI. A comparison between magnetic resonance imaging and a dedicated multidisciplinary neurosonographic opinion. Acta Paediatr 2008; 97(4):414-419

A B

C D