Posterior fossa and vermian morphometry in the characterization of fetal cerebellar abnormalities: a prospective threedimensional 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. Issue

Ultrasound in Obstetrics & Gynecology

Volume 27, Issue 5, pages 482489, May 2006 Additional Information(Show All) How to CiteAuthor InformationPublication History How to Cite 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: 482489. 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 (paladini@unina.it)
*

Via Petrarca, 72, 80122Naples, 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; DandyWalker syndrome; magnetic resonance imaging;

prenatal diagnosis; ultrasonography

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Abstract
1. 2. 3. 4. 5. 6. 7. Top of page Abstract Introduction Methods Results Discussion 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 DandyWalker malformation (n = 5), DandyWalker 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

The tentoroclivus angle was increased only in fetuses with DandyWalker malformation (P < 0.001). Upward rotation of the vermis was demonstrated both by the tentorovermian and the clivovermian angles in fetuses with DandyWalker variant (P < 0.001), while in those with DandyWalker 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 DandyWalker malformation compared with DandyWalker 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 MRIand 3D ultrasound-derived morphometric measurements of the vermis. Copyright 2006 ISUOG. Published by John Wiley & Sons, Ltd.
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Introduction
1. 2. 3. 4. 5. 6. 7. Top of page Abstract Introduction Methods Results Discussion References
Cystic malformations of the posterior fossa include anomalies of the meninges (arachnoid cyst, megacisterna magna) and the cerebellum (DandyWalker malformation and variant). Postnatally, the classification of these abnormalities is based mainly on examination of the midsagittal view of the head on magnetic resonance imaging (MRI)14. Although there is no unanimous agreement on the criteria for the diagnosis of the three anomalies which represent the object of this investigation, namely DandyWalker malformation, DandyWalker variant and megacisterna magna, those most frequently accepted are the following: in DandyWalker malformation, the cerebellar vermis is hypoplastic and often rotated upward, the fourth ventricle

is cystic and the tentorium is elevated; DandyWalker 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 them69 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 axial610. 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.
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Methods
1. Top of page 2. Abstract

3. 4. 5. 6. 7.

Introduction Methods Results Discussion References

This was a prospective observational study between January 2003 and January 2005. The control group consisted of 51 consecutive fetuses at 1837 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 DandyWalker 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

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 23 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 (aa'); craniocaudal vermian diameter (bb'); clivus (cc'). 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) DandyWalker variant; (d) DandyWalker malformation. Download figure to PowerPoint 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 midsagittal 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; aa' in Figure 2a) and the maximum craniocaudal vermian diameter (bb' in

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 (bb' 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 (cc' 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 DandyWalker 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 DandyWalker malformation, one DandyWalker 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 MannWhitney U-test and the KruskalWallis 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.
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Results

1. 2. 3. 4. 5. 6. 7.

Top of page Abstract Introduction Methods Results Discussion References

The mean gestational age at ultrasound examination was 26 (SD, 5; range, 1837) weeks in the control group and 25 (SD, 5; range, 1936) 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 DandyWalker malformation, 7/8 with DandyWalker variant and 2/7 with megacisterna magna). The five variables were assessed with respect to their usefulness in differentiating between fetuses with DandyWalker malformation, DandyWalker 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). Download figure to PowerPoint The differences detected in the anatomical landmarks in the various abnormalities of the posterior fossa are shown in Figure 2bd. 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 DandyWalker malformation, Dandy Walker variant or megacisterna magna) are summarized in Table 1. DandyWalker malformation was found to be characterized by gross upward displacement of the tentorium (tentoroclivus angle: P < 0.001 vs. normal, P < 0.01 vs. DandyWalker variant and P < 0.05 vs.

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. DandyWalker variant) (Figure 2d). The upward rotation of the vermis characteristic of DandyWalker 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. DandyWalker variant was found to be characterized by an underdeveloped vermis, though less so than DandyWalker 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 SD

95% CI

Minimum Maximum value 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, DandyWalker malformation; DWv, DandyWalker variant; MCM, megacisterna magna; TC angle, tentoroclivus angle; TV angle, tentorovermian angle; VD/BPD, vermian maximum diameter/biparietal diameter ratio. Control TC angle () DW DWv 51 4.0 4.2 2.9 to 5.1 18.4 to 73.1 0.5 to 16.1 0.1 20.0 1.4 21.0 76.3 29.0

5 45.8 22.0 8 8.3 9.3

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 SD 95% CI 0.6 to 23.4 53.1 to 58.0 80.9 to 98.6 6.5 to 26.3 46.5 to 68.4 45.6 to 50.0 98.9 to 72.5 10.4 to 9.2 48.0 to 60.2 21.6 to 23.2 Minimum Maximum value value 1.9 42.9 74.0 25.1 42.4 33.1 67.0 18.0 46.5 16.0 10.7 38.8 84.0 89.1 42.7 69.0 65.1 76.9 15.0 60.9 27.7 18.4

MCM Control DW TV angle () DWv MCM Control DW CV angle () DWv MCM Control VD/BPD DW

7 11.4 13.0 51 55.6 9.0 5 8 8.9 72.3 9.9 21.3

7 57.4 11.8 51 47.8 7.3 5 13.2* 69.1 8 0.6* 11.7 7 54.1 5.8 51 22.4 2.9

5 15.1 3.0 11.4 to

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 SD 95% CI 18.8 DWv MCM 8 18.9 2.1 7 24.0 2.1 17.1 to 20.6 22.0 to 25.9 16.0 20.6 22.8 27.4 Minimum Maximum value value

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); DandyWalker malformation in a 29-week fetus on ultrasound (b) and MRI (d). Download figure to PowerPoint 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.

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Discussion
1. 2. 3. 4. 5. 6. 7. Top of page Abstract Introduction Methods Results Discussion References
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 fossa711, 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, DandyWalker malformation, DandyWalker 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 ponsfastigium 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 DandyWalker malformation in postnatal life1, 2, it did not reach statistical significance due to the small number of fetuses with DandyWalker malformation in the series. We were also able to demonstrate that DandyWalker variant shows a lesser degree of vermian hypoplasia, and that it often shares with DandyWalker 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 neonate14, 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 23 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 DandyWalker 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 DandyWalker 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 DandyWalker variant) may help in identifying the correct vermian axis. Finally, the number of cases in which the ultrasoundMRI 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 DandyWalker malformation, DandyWalker 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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References

1. 2. 3. 4. 5. 6. 7.

Top of page Abstract Introduction Methods Results Discussion References

Parisi MA, Dobyns WB. Human malformations of the mid-brain and hind-brain: review and proposed classification scheme. Mol Genet Metab 2003; 80: 3653.
o o o o

CrossRef, PubMed, CAS, Web of Science Times Cited: 38 2

Patel S, Barkovich AJ. Analysis and classification of cerebellar anomalies. Am J Neuroradiol 2002; 23: 10741087.
o o

PubMed, Web of Science Times Cited: 106 3

Garel C, Chantrel E, Elmaleh M, Brisse H, Sebag G. Fetal MRI: normal gestational landmarks for cerebral biometry, gyration and myelination. Childs Nerv Syst 2003; 19: 422425.
o o o

CrossRef, PubMed, Web of Science Times Cited: 37 4

GarelC (ed). MRI of the fetal brain. Normal development and cerebral pathologies. Berlin, Heidelberg, New York: Springer: 2004; 13114.

Pierre-Kahn A, Sonigo P. Malformative intra-cranial cysts: diagnosis and outcome. Childs Nerv Syst 2003; 19: 477483.
o o o

CrossRef, PubMed, Web of Science Times Cited: 16 6

Nyberg DA, Mahony BS, Hegge FN, Hickok D, Luthy DA, Kapur R. Enlarged cisterna magna and the Dandy-Walker malformation: factors associated with chromosome abnormalities. Obstet Gynecol, 1991; 77: 436442.
o o o

PubMed, CAS, Web of Science Times Cited: 63 7

Pilu G, Goldstein I, Reece EA, Perolo A, Foschini MP, Hobbins JC, Bovicelli L. Sonography of fetal Dandy-Walker malformation: a reappraisal. Ultrasound Obstet Gynecol 1992; 2: 151157. Direct Link:
o o

Abstract PDF(1054K)

Ecker JL, Shipp TD, Bromley Benacerraf B. The sonographic diagnosis of Dandy-Walker and Dandy-Walker variant: associated findings and outcomes. Prenat Diagn 2000; 20: 328332. Direct Link:
o o o

Abstract PDF(120K) References

Klble N, Visser J, Kurmanavicius J, Bolthauser E, Stallmach T, Huch A, Huch R. DandyWalker malformation: prenatal diagnosis and outcome. Prenat Diagn 2000; 20: 318327.

Direct Link:
o o o

Abstract PDF(304K) References

10

Ulm B, Ulm MR, Deutinger J, Bernaschek G. Dandy-Walker malformation diagnosed before 21 weeks of gestation: associated malformations and chromosomal abnormalities. Ultrasound Obstet Gynecol 1997; 10: 167170. Direct Link:
o o

Abstract PDF(427K)

11

Adamsbaum C, Moutard ML, Andr C, Merzoug V, Ferey S, Qur MP, Lewin F, Fallet-Bianco C. MRI of the posterior fossa. Pediatric Radiol 2005; 35: 124140.
o o o

CrossRef, PubMed, Web of Science Times Cited: 51 12

Courchesne E, Saitoh O, Yeung-Courchesne R, Press GA, Lincoln AJ, Haas RH, Schreibman L. Abnormality of cerebellar vermian lobules VI and VII in patients with infantile autism: identification of hypoplastic and hyperplastic subgroups with MR imaging. AJR Am J Roentgenol 1994; 162: 123130.
o o o

PubMed, CAS, Web of Science Times Cited: 131 13

Carroll SGM, Porter H, Abdel-Fattah S, Kyle PM, Soothil PW. Correlation of prenatal ultrasound diagnosis and pathologic findings in fetal brain abnormalities. Ultrasound Obstet Gynecol, 2000; 16: 149153.

Direct Link:
o o

Abstract PDF(70K)

14

Malinger G, Ginath S, Lerman-Sagie T, Watemberg N, Lev D, Glazerman M. The cerebellar vermis: normal development as shown by trans-vaginal ultrasound. Prenat Diagn 2001; 21: 687692. Direct Link:
o o o

Abstract PDF(193K) References

15

Zalel Y, Seidman DS, Brandt N, Lipitz S, Achiron R. The development of the fetal vermis: an in utero sonographic evaluation. Ultrasound Obstet Gynecol 2002; 19: 136139. Direct Link:
o o

Abstract PDF(103K)

16

Achiron R, Kivilevitch V, Lipitz S, Gamzu R, Almog B, Zalel Y. Development of the human fetal pons: in utero ultrasonographic study. Ultrasound Obstet Gynecol 2004; 24: 506510. Direct Link:
o o o o

Abstract Full Article (HTML) PDF(224K) References

17

Simon EM, Goldstein RB, Coakley FV, Filly RA, Broderick KC, Musci TJ, Barkovich AJ. Fast MR imaging of fetal CNS anomalies in utero. Am J Neuroradiol 2000; 21: 16881698.
o o o

PubMed, CAS, Web of Science Times Cited: 91 18

Boddaert N, Klein O, Ferguson N, Sonigo P, Parisot D, Hertz-Pannier L, Baraton J, Emond S, Simon I, Chigot V, Schmit P, Pierre-Kahn A, Brunelle F. Intellectual prognosis of the DandyWalker malformation in children: the importance of vermian lobulation. Neuroradiology 2003; 45: 320324.
o o o

PubMed, CAS, Web of Science Times Cited: 27 19

Anatebi SA, Fung KS. Neurodevelopmental outcome after antenatal diagnosis of posterior fossa abnormalities. J Ultrasound Med 1999; 18: 683689.
o o

PubMed, Web of Science Times Cited: 14 20

Klein O, Pierre-Kahn A, Boddaert N, Parisot D, Brunelle F. Dandy-Walker malformation: prenatal diagnosis and prognosis. Childs Nerv Syst 2003; 19: 484489.
o o o o

CrossRef, PubMed, CAS, Web of Science Times Cited: 44 21

Monteagudo A, Timor-Tritsch IE, Mayberry P. Three-dimensional transvaginal neurosonography of the fetal brain: navigating in the volume scan. Ultrasound Obstet Gynecol 2000; 16: 307313.

Direct Link:
o o

Abstract PDF(171K)