posterior fossa and vermian morphometry in the characterization of fetal cerebellar abnormalities

Posterior fossa and vermian morphometry in the characterization of fetal cerebellar abnormalities: a prospective three-dimensional ultrasound study

1. D. Paladini1,*, 2. P. Volpe2

Article first published online: 18 APR 2006

DOI: 10.1002/uog.2748

Copyright © 2006 ISUOG. Published by John Wiley & Sons, Ltd.

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Ultrasound in Obstetrics & Gynecology

Volume 27, Issue 5, pages 482–489, May 2006

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How to Cite Author Information Publication History

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Paladini, D. and Volpe, P. (2006), Posterior fossa and vermian morphometry in the characterization of fetal cerebellar abnormalities: a prospective three-dimensional ultrasound study. Ultrasound Obstet Gynecol, 27: 482–489. doi: 10.1002/uog.2748

Author Information

1. 1

Prenatal Diagnosis Unit, Department of Gynecology and Obstetrics, University Federico II of Naples, Naples, Italy

2. 2

Department of Obstetrics and Gynecology, “Di Venere-Giovanni XXIII” Hospital, Bari, Italy

Email: D. Paladini ([email protected])

*Via Petrarca, 72, 80122—Naples, Italy

Publication History

1. Issue published online: 18 APR 2006 2. Article first published online: 18 APR 2006 3. Manuscript Accepted: 15 DEC 2005

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Keywords:

cerebellum;

cisterna magna;

Dandy–Walker syndrome;

magnetic resonance imaging;

prenatal diagnosis;

ultrasonography

Abstract

1. Top of page 2. Abstract 3. Introduction 4. Methods 5. Results 6. Discussion 7. References

Objectives

To assess whether, by applying a predefined set of morphometric measurements to the posterior

fossa and the cerebellar vermis, it is possible to detect and quantify the following parameters,

which represent key features of abnormalities of the vermis and posterior fossa: 1) upward

rotation of the vermis; 2) upward displacement of the tentorium; 3) underdevelopment of the

vermis. Also to assess, in a small subset of cases, the correlation between ultrasound and

magnetic resonance imaging (MRI) in the measurement of these three parameters.

Methods

This was a prospective observational trial. The study population included 51 normal fetuses and

20 abnormal fetuses with Dandy–Walker malformation (n = 5), Dandy–Walker variant (n = 8) or

megacisterna magna (n = 7). Three-dimensional (3D) ultrasound volumes of the fetal head were

acquired from the posterior fontanelle or the posterior part of the sagittal suture and processed

offline with dedicated software. The following parameters were analyzed: tentorovermian angle;

tentoroclivus angle; clivovermian angle; vermian diameter/biparietal diameter × 100 ratio

(VD/BPD ratio). In seven cases, MRI performed on the same day as sonography was available

for comparison. Non-parametric statistics were used to assess differences in means and

correlations.

Results

Jump to…

The tentoroclivus angle was increased only in fetuses with Dandy–Walker malformation (P <

0.001). Upward rotation of the vermis was demonstrated both by the tentorovermian and the

clivovermian angles in fetuses with Dandy–Walker variant (P < 0.001), while in those with

Dandy–Walker malformation the difference was not statistically significant, probably due to the

small number of cases. Finally, the VD/BPD ratio demonstrated that the degree of vermian

hypoplasia was higher in Dandy–Walker malformation compared with Dandy–Walker variant (P

< 0.001).

Conclusions

Using 3D ultrasound, we have demonstrated in the fetus the key elements characterizing most

anomalies of the posterior fossa, namely the upward displacement of the tentorium, the

counterclockwise rotation and the significant hypoplasia of the cerebellar vermis. In addition, our

observations in a small number of cases indicate that there is a good correlation between MRI-

and 3D ultrasound-derived morphometric measurements of the vermis. Copyright © 2006

ISUOG. Published by John Wiley & Sons, Ltd.

Introduction


Cystic malformations of the posterior fossa include anomalies of the meninges (arachnoid cyst,

megacisterna magna) and the cerebellum (Dandy–Walker malformation and variant).

Postnatally, the classification of these abnormalities is based mainly on examination of the mid-

sagittal view of the head on magnetic resonance imaging (MRI)1–4. Although there is no

unanimous agreement on the criteria for the diagnosis of the three anomalies which represent the

object of this investigation, namely Dandy–Walker malformation, Dandy–Walker variant and

megacisterna magna, those most frequently accepted are the following: in Dandy–Walker

malformation, the cerebellar vermis is hypoplastic and often rotated upward, the fourth ventricle

Jump to…

is cystic and the tentorium is elevated; Dandy–Walker variant is characterized by less severe

cerebellar vermian hypoplasia, often confined to the posteroinferior part, less evident upward

rotation of the vermis, and generally a smaller posterior fossa fluid collection communicating

with the fourth ventricle; megacisterna magna designates a particularly wide cistern exerting no

compression over the underlying cerebellum and communicating freely with the subarachnoid

spaces and, according to most but not all authors, the fourth ventricle5, 6.

These abnormalities of the posterior fossa have been recognized sonographically in the fetus, but

the differential diagnosis can sometimes be extremely difficult7 or even impossible8 because of

the subtle anatomical differences between them6–9 and, above all, because of the limited

possibilities offered so far by two-dimensional (2D) ultrasound. In fact, in most ultrasound

reports dealing with the diagnosis of abnormalities of the fetal posterior fossa, the reference view

for detection and differentiation of these anomalies was axial6–10. The inadequacy of this axial

approach to the differential diagnosis of cerebellar anomalies in the fetus is demonstrated by the

upward rotation of the vermis and the upward displacement of the tentorium in two of the most

recent fetal series of cerebellar malformations. Either these were not considered among the

diagnostic criteria10, or, while they were mentioned, no indication was given as to how they

were demonstrated or quantified9. These difficulties have led to the relatively frequent

employment of MRI to characterize such lesions and to detect associated central nervous system

malformations4, 11.

In this study we employed a morphometric approach to the prenatal diagnosis of anomalies of

the posterior fossa and cerebellar vermis based on the mid-sagittal transcranial view obtained by

three-dimensional (3D) ultrasound. The primary aim of this investigation was to assess whether,

by applying a predefined set of morphometric measurements to the posterior fossa and the

cerebellar vermis, it is possible to detect and quantify the following parameters, which represent

key features of abnormalities of the vermis and posterior fossa: 1) the upward rotation of the

vermis; 2) the upward displacement of the tentorium; 3) the underdevelopment of the vermis.

The second aim of the study was to assess, in a small subset of cases, the correlation between

ultrasound and MRI in the measurement of these three parameters.

Methods

1. Top of page 2. Abstract

Jump to…

3. Introduction 4. Methods 5. Results 6. Discussion 7. References

This was a prospective observational study between January 2003 and January 2005. The control

group consisted of 51 consecutive fetuses at 18–37 weeks of gestation undergoing routine

second- and third-trimester sonography at the outpatient clinic of our two institutions. The study

group included all 20 fetuses with anomalies of the posterior fossa and/or the cerebellar vermis

seen at either of our two institutions during the study period: these included five cases of Dandy–

Walker malformation, eight cases of Dandy–Walker variant and seven cases of megacisterna

magna. In all cases the diagnosis was confirmed, either at autopsy (n = 11) or postnatally by MRI

(n = 9). The study was approved by the internal review boards of the two institutions and all

women gave their consent to participate.

All patients underwent 2D and 3D sonography performed with a Voluson 730 Expert (GE

Medical systems, Kretz Ultrasound, Zipf, Austria) ultrasound machine. As a reference view we

used the mid-sagittal plane of the fetal head, obtained from the posterior fontanelle or the

posterior part of the sagittal suture, so that the ultrasound beam was almost perpendicular to the

tentorium (Figures 1 and 2). Once the sagittal view was obtained, with a good display of the

corpus callosum, the tentorium and the cerebellar vermis, the volume acquisition procedure was

activated. Fetuses in vertex presentation were studied with a transvaginal approach, whereas

those with a persistent breech presentation were approached transabdominally. The machine was

set up to allow good contrast between the tentorium, the hyperechoic vermis and the fluid-filled

spaces represented by the posterior fossa and the fourth ventricle. In case of breech presentation,

the women were asked to hold their breath during volume acquisition to avoid motion artifacts.

Figure 1. Mid-sagittal view of the normal fetal head at 29 (a, b) and 32 (c, d) weeks of gestation.

Comparison of two-dimensional (2D) (a, c) with three-dimensional (3D) ultrasound with static

volume contrast imaging (b, d) from the same volumes. The difference in resolution and contrast

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of the images is evident; in particular, the edges of the vermis and the tentorium are much more

clearly displayed with 3D ultrasound. This is due to the fact that with 3D ultrasound the 2D slice,

which is a single pixel in thickness, is replaced by a multi-pixel slice 2–3 mm thick. As a result,

the signal-to-noise ratio is enhanced.

Download figure to PowerPoint

Figure 2. Mid-sagittal view of the fetal head from three-dimensional volumes. (a) The

anatomical landmarks considered in the study are indicated in a normal fetus: tentorium (a–a');

craniocaudal vermian diameter (b–b'); clivus (c–c'). From these anatomical markers, the

following morphometric parameters were derived and used in our analysis: tentoroclivus angle,

tentorovermian angle, clivovermian angle, vermian diameter/biparietal diameter ratio.

Differences in these anatomical landmarks are shown for various abnormalities of the posterior

fossa: (b) megacisterna magna (arrow); (c) Dandy–Walker variant; (d) Dandy–Walker

malformation.


All volumes were stored and then processed offline using dedicated software (4d-viewer 5.0, GE

Medical systems, Kretz Ultrasound) as follows. Each volume was opened, the static volume

contrast imaging (VCI) option was activated and, using the multiplanar mode, which allows fine

calibration of the slice, the mid-sagittal plane of the fetal head most suitable for the

measurements was obtained. The reference plane for the measurements was identified by the

presence of the whole of the corpus callosum, the tentorium and the cerebellar vermis. The mid-

sagittal plane of the vermis was defined by a section passing through the rostral and caudal

convexities at the levels of its superior, middle and inferior portions12. The fastigium was also

visible in this plane (Figures 1 and 2).

The selected image was then magnified and the following parameters were measured (Figure

2a): 1) tentorovermian angle, defined as the angle between a line drawn along the tentorium

(from the posterior end of the corpus callosum to the attachment on the inner aspect of the

occipital bone; a–a' in Figure 2a) and the maximum craniocaudal vermian diameter (b–b' in

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Figure 2a); 2) maximum craniocaudal vermian diameter, defined as the maximum distance

between the uppermost part of the culmen and the caudal edge of the uvula (b–b' in Figure 2a);

this was normalized for gestational age in the vermian diameter/biparietal diameter × 100 ratio

(VD/BPD ratio); 3) vermian area, which was normalized for gestational age in the vermian

area/BPD × 100 ratio (VA/BPD ratio); 4) tentoroclivus angle, defined as the angle between a line

drawn along the tentorium and one drawn along the clivus (c–c' in Figure 2a); 5) clivovermian

angle, defined as the angle between a line drawn along the clivus and the maximum craniocaudal

vermian diameter. Specification of the procedure for the calculation of the tentorovermian and

the clivovermian angles is important. As evident from Figure 2, in normal conditions the

tentorovermian angle is open posteriorly, while the clivovermian angle is open anteriorly.

However, in Dandy–Walker malformation, the upward rotation of the vermis can be so great that

the angles are reversed. In these cases, if the major axis of the vermis crossed that of the

tentorium or the clivus, the angle was considered to be negative.

In seven cases (two controls, two Dandy–Walker malformation, one Dandy–Walker variant and

two megacisterna magna), the patient had undergone both ultrasound and MRI on the same day.

In these cases, all measurements performed sonographically were also measured on the MRI

scans and the results were compared.

Statistical analysis

Statistical analysis was performed using the SPSS 8.0 package for Windows (SPSS, Chicago, IL,

USA). Non-parametric statistics, including the Mann–Whitney U-test and the Kruskal–Wallis

test, were employed to assess differences in means due to the non-normal distribution of the

cases. Spearman's rho correlation coefficient was used to assess the differences between

ultrasound-derived and MRI-derived values and the inter- and intraobserver variability in the

measurement of the various angles. Inter- and intraobserver variability was assessed in an

arbitrary sample of 10 affected and 10 normal fetuses: still images of the reference views were

stored in a directory, then each of the two authors opened the image and measured the angles

separately. The same procedure was repeated by one of the authors who was blinded to his

previous results. P-values < 0.05 were considered statistically significant. Confidence intervals

for all measurements were calculated.

ResultsJump to…


The mean gestational age at ultrasound examination was 26 (SD, 5; range, 18–37) weeks in the

control group and 25 (SD, 5; range, 19–36) weeks in the group of affected fetuses. In the latter

group, 13/20 fetuses were seen prior to 24 weeks of gestation (4/5 with Dandy–Walker

malformation, 7/8 with Dandy–Walker variant and 2/7 with megacisterna magna). The five

variables were assessed with respect to their usefulness in differentiating between fetuses with

Dandy–Walker malformation, Dandy–Walker variant and megacisterna magna, and between

affected fetuses and normal ones. Since the performance of the VA/BPD ratio was not different

from that of the VD/BPD ratio, and the latter is less prone to measurement errors, the former was

excluded from further evaluation. Of all the assessed variables, only the maximum craniocaudal

vermian diameter showed a positive linear correlation with advancing gestational age (r = 0.922;

Figure 3).

Figure 3. Scatterplot showing the relationship between the craniocaudal vermian diameter and

gestational age (r = 0.922).


The differences detected in the anatomical landmarks in the various abnormalities of the

posterior fossa are shown in Figure 2b–d. The descriptive statistics of the four assessed variables

(tentoroclivus angle, tentorovermian angle, clivovermian angle, vermian diameter/BPD ratio) in

the four subsets of cases (normal fetuses and those with Dandy–Walker malformation, Dandy–

Walker variant or megacisterna magna) are summarized in Table 1. Dandy–Walker

malformation was found to be characterized by gross upward displacement of the tentorium

(tentoroclivus angle: P < 0.001 vs. normal, P < 0.01 vs. Dandy–Walker variant and P < 0.05 vs.

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megacisterna magna) and by a significantly hypoplastic vermis (VD/BPD ratio: P < 0.001 vs.

normal, P < 0.01 vs. megacisterna magna and P < 0.05 vs. Dandy–Walker variant) (Figure 2d).

The upward rotation of the vermis characteristic of Dandy–Walker malformation

(tentorovermian and clivovermis angles) did not reach statistical significance due to the small

number of fetuses (n = 5) and the wide range of rotation angles. Dandy–Walker variant was

found to be characterized by an underdeveloped vermis, though less so than Dandy–Walker

malformation (P < 0.05), by an upward rotation of the vermis (P < 0.001 vs. normal) and by the

absence of any upward displacement of the tentorium (Figure 2c). In comparison with normal

fetuses, those with megacisterna magna showed only a moderate increase in the clivovermian

angle (P < 0.05; Figure 2b).

Table 1. Descriptive statistics for the four morphometric parameters assessed in normal fetuses and those with abnormalities of the posterior fossa

Parameter Abnormality n Mean SD95% CI

Minimum value

Maximum value

*

The anatomical angle was increased but the values were reduced in comparison with the controls because if the major axis of the vermis crossed the clivus line the angle value was expressed as a negative. CV angle, clivovermian angle; DW, Dandy–Walker malformation; DWv, Dandy–Walker variant; MCM, megacisterna magna; TC angle, tentoroclivus angle; TV angle, tentorovermian angle; VD/BPD, vermian maximum diameter/biparietal diameter ratio.

TC angle (°)Control 51 4.0 4.2

2.9 to 5.1

0.1 21.0

DW 5 45.8 22.018.4 to

73.120.0 76.3

DWv 8 8.3 9.30.5 to 16.1

1.4 29.0

MCM 7 11.4 13.0 −0.6 to 1.9 38.8



Minimum value

Maximum value

23.4

TV angle (°)

Control 51 55.6 9.053.1 to

58.042.9 84.0

DW 5 8.9 72.3−80.9 to 98.6

−74.0 89.1

DWv 8 9.9 21.3−6.5 to

26.3−25.1 42.7

MCM 7 57.4 11.846.5 to

68.442.4 69.0

CV angle (°)

Control 51 47.8 7.345.6 to

50.033.1 65.1

DW 5 −13.2* 69.1−98.9 to 72.5

−67.0 76.9

DWv 8 −0.6* 11.7−10.4 to 9.2

−18.0 15.0

MCM 7 54.1 5.848.0 to

60.246.5 60.9

VD/BPDControl 51 22.4 2.9

21.6 to 23.2

16.0 27.7

DW 5 15.1 3.011.4 to

18.810.7 18.4

DWv 8 18.9 2.1 17.1 to 16.0 22.8



Minimum value

Maximum value

20.6

MCM 7 24.0 2.122.0 to

25.920.6 27.4

The correlation between ultrasound and MRI-derived variables (Figure 4) was good, with

Spearman's rho correlation coefficients of 0.991, 0.975, 0.949 and 0.943 for the tentoroclivus

angle, the tentorovermian angle, the clivovermian angle, and the VD/BPD ratio, respectively.

Figure 4. Comparison between magnetic resonance imaging (MRI) and ultrasonography in

visualizing various abnormalities of the posterior fossa. Megacisterna magna in a 29-week fetus

on ultrasound (a) and MRI (c); Dandy–Walker malformation in a 29-week fetus on ultrasound

(b) and MRI (d).


With respect to the inter- and intraobserver variability, Spearman's correlation coefficients were

> 0.90 for the three angles measured (tentoroclivus angle, 0.95 and 0.93; tentorovermian angle,

0.94 and 0.91; clivovermian angle, 0.93 and 0.91, respectively). For the VD/BPD ratio, the

intraobserver variability coefficient was 0.91, but that for interobserver variability was 0.871.

DiscussionJump to…

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The prenatal ultrasound recognition of cerebellar abnormalities has always been based upon the

appearance of the posterior fossa on axial views of the fetal head. Despite several publications on

the differential diagnosis of malformations of the posterior fossa7–11, 13, the mid-sagittal view

routinely employed postnatally to classify these anomalies has generally been sought prenatally

only to create normative curves of vermian diameters and area14, 15. The main aim of this study

was to demonstrate that the key anatomical features of the three most frequent fetal abnormalities

of the posterior fossa, Dandy–Walker malformation, Dandy–Walker variant and megacisterna

magna, can be detected and quantified prenatally by ultrasound. We focused on simple

anatomical landmarks that would be easy to detect and to measure on the mid-sagittal ultrasound

image of the fetal head (tentorium, maximum craniocaudal vermian diameter, clivus); at the

same time, we discarded other measurements that, in our experience, despite their important

prognostic significance and other authors' results16, showed a higher intraobserver variability,

such as the pons diameter or the pons–fastigium distance. The measurements proposed in this

study allowed us to detect the upward rotation of the vermis, the upward displacement of the

tentorium and the occurrence of vermian hypoplasia (Figure 2 and Table 1) that represent the key

features of severe cerebellar anomalies1, 2. By studying how and by how much these four

parameters differed in the various abnormalities of the posterior fossa in comparison with the

normal situation, it was possible to demonstrate in the fetus using 3D ultrasound that Dandy–

Walker malformation is characterized by gross upward displacement of the tentorium and severe

hypoplasia of the vermis. As for the counterclockwise rotation of the vermis characteristic of

Dandy–Walker malformation in postnatal life1, 2, it did not reach statistical significance due to

the small number of fetuses with Dandy–Walker malformation in the series. We were also able

to demonstrate that Dandy–Walker variant shows a lesser degree of vermian hypoplasia, and that

it often shares with Dandy–Walker malformation the upward rotation of the vermis, but lacks the

displacement of the tentorium, due to the smaller fluid collection in the posterior fossa. All these

features are consistent with those detected by MRI in the fetus and neonate1–4, 9, 17, but, to the

best of our knowledge, this is the first time that their occurrence has been objectively assessed in

the fetus by ultrasound.

The sonographic recognition of vermian hypoplasia, upward rotation of the vermis and upward

displacement of the tentorium also has prognostic significance, because the degree of vermian

hypoplasia has been demonstrated to correlate significantly with the occurrence and severity of

mental retardation18, 19. However, it should be underscored that our data do not allow us to

address the thorny issue of the classification of cerebellar abnormalities1, 2, 20, nor was it our

original idea to do so. Our aim was only to provide additional tools that may be used in the

comparison of ultrasound and MRI images of fetal malformations of the posterior fossa and,

possibly, in the assessment of their natural history. In this respect, the good correlation between

ultrasound-derived and MRI-derived values (all correlation coefficients > 0.90), if confirmed in

larger series, may contribute to a better combined ultrasound/MRI follow-up of the fetus/neonate

with vermian malformations. This comparison was not performed in order to challenge the

apparent superior diagnostic performance of MRI, which, unlike ultrasound, may detect

myelinization abnormalities, diagnose reliably associated brain-stem hypoplasia, and

differentiate confidently between partial agenesis and hypoplasia of the vermis3, 4, 11, 17.

However, in the fetus, the diagnosis of cerebellar anomalies relies almost entirely on ultrasound

as a first-line technique and only referral centers have the possibility to integrate MRI into the

diagnostic process. Therefore, we believed the possibility to develop a set of morphometric

measures able to characterize and differentiate the various abnormalities of the posterior fossa on

ultrasound examination to be of interest.

A correlation between gestational age and one of the measured variables was observed: the

maximum craniocaudal vermian diameter. The positive linear correlation (Figure 3)

demonstrated by our data is in close agreement with the results published recently by Zalel et

al.15.

Our choice of 3D rather than conventional 2D ultrasound in the assessment of posterior fossa and

vermian anatomy requires discussion. In our opinion, there are at least two advantages provided

by 3D ultrasound. The first is the possibility of offline navigation of the volume21, which allows,

thanks to multiplanar imaging, fine calibration of the slice to be used for reference and

measurements. The second is the possibility of selecting different rendering filters in order to

improve the visibility of the various anatomical landmarks, such as the tentorium cerebelli. After

evaluating most of the possible rendering modes and filters, we found that the combination of the

static VCI modality with multiplanar imaging was the best in terms of focus, calibration and

image detail. Technically, because the VCI image consists of a slice 2–3 mm in thickness, the

overlay of various thinner slices enhances the signal-to-background noise ratio. This in turn

improves both the resolution and the contrast in comparison with the 2D ultrasound image,

which is 1 pixel in thickness (Figure 1). This approach was therefore used in the evaluation of all

volumes.

This study had a number of limitations, the first being the relatively small number of cases,

especially for Dandy–Walker malformation; this was because, due to the prospective design of

the study and the ultrasound approach used (i.e. assessed from the posterior fontanelle by 3D

ultrasound in the VCI mode), we could enrol into the study only patients seen in the last 2 years.

Another important limitation of the investigation is that, in the case of Dandy–Walker variant,

the real axis of the craniocaudal vermian diameter is not well defined, due to the fact that in this

anomaly it is the posteroinferior part of the vermis that is underdeveloped. This may lead to an

error in the measurement of the various angles, which, in turn, may lead to an overestimation of

the counterclockwise rotation of the vermis. In this situation, the assessment of the linear

distance between the uppermost part of the culmen and the tentorium, which is reduced on

upward rotation of the vermis (the tentorium is almost never displaced in Dandy–Walker variant)

may help in identifying the correct vermian axis. Finally, the number of cases in which the

ultrasound–MRI comparison could be carried out was limited (n = 7), due to the fact that in the

other cases, the fetuses did not undergo MRI and 3D sonography on the same day.

In conclusion, we have demonstrated how abnormalities of the cerebellar vermis and posterior

fossa can be differentiated sonographically thanks to the employment of a set of morphometric

parameters (tentoroclivus, tentorovermian and clivovermian angles and VD/BPD × 100 ratio).

By using these measurements on the mid-sagittal plane of the fetal head obtained by 3D

ultrasound it was possible for the first time to quantify in the fetus the volumetric and

topographic changes of the posterior fossa and its content that have been described postnatally

for Dandy–Walker malformation, Dandy–Walker variant and megacisterna magna. In a small

series of cases, it was also possible to demonstrate good correlation between MRI and 3D

ultrasound for these measurements. We hope that these findings may contribute to creating a

bridge between fetal ultrasound findings and those on neonatal MRI.

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5. Results 6. Discussion 7. References

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