Abstract
Diagnosis of fetal isolated mild ventriculomegaly (IMVM) is the most common brain abnormality on prenatal ultrasound. We have set to identify potential alterations in brain development specific to IMVM in tissue volume and cortical and ventricular local surface curvature derived from in utero magnetic resonance imaging (MRI). Multislice 2D T2-weighted MRI were acquired from 32 fetuses (16 IMVM, 16 controls) between 22 and 25.5 gestational weeks. The images were motion-corrected and reconstructed into 3D volumes for volumetric and curvature analyses. The brain images were automatically segmented into cortical plate, cerebral mantle, deep gray nuclei, and ventricles. Volumes were compared between IMVM and control subjects. Surfaces were extracted from the segmentations for local mean surface curvature measurement on the inner cortical plate and the ventricles. Linear models were estimated for age-related and ventricular volume-associated changes in local curvature in both the inner cortical plate and ventricles. While ventricular volume was enlarged in IMVM, all other tissue volumes were not different from the control group. Ventricles increased in curvature with age along the atrium and anterior body. Increasing ventricular volume was associated with reduced curvature over most of the ventricular surface. The cortical plate changed in curvature with age at multiple sites of primary sulcal formation. Reduced cortical folding was detected near the parieto-occipital sulcus in IMVM subjects. While tissue volume appears to be preserved in brains with IMVM, cortical folding may be affected in regions where ventricles are dilated.
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Beeghly M, Ware J, Soul J, du Plessis A, Khwaja O, Senapati GM, Robson CD, Robertson RL, Poussaint TY, Barnewolt CE, Feldman HA, Estroff JA, Levine D (2010) Neurodevelopmental outcome of fetuses referred for ventriculomegaly. Ultrasound Obstet Gynecol 35(4):405–416
Dhouib A, Blondiaux E, Moutard ML, Billettede Villemeur T, Chalard F, Jouannic JM, Ducoule Pointe H, Garel C (2011) Correlation between pre- and postnatal cerebral magnetic resonance imaging. Ultrasound Obstet Gynecol 38(2):170–178
Do Carmo MP (1976) Differential geometry of curves and surfaces. Prentice Hall, Englewood Cliffs
Falip C, Blanc N, Maes E, Zaccaria I, Oury JF, Sebag G, Garel C (2007) Postnatal clinical and imaging follow-up of infants with prenatal isolated mild ventriculomegaly: a series of 101 cases. Pediatr Radiol 37(10):981–989
Gaglioti P, Oberto M, Todros T (2009) The significance of fetal ventriculomegaly: etiology, short- and long-term outcomes. Prenat Diagn 29(4):381–388
Gholipour A, Estroff JA, Barnewolt CE, Connolly SA, Warfield SK (2011) Fetal brain volumetry through MRI volumetric reconstruction and segmentation. Int J Comput Assist Radiol Surg 6(3):329–339
Gilmore JH, Smith LC, Wolfe HM, Hertzberg BS, Smith JK, Chescheir NC, Evans DD, Kang C, Hamer RM, Lin W, Gerig G (2008) Prenatal mild ventriculomegaly predicts abnormal development of the neonatal brain. Biol Psychiatry 64(12):1069–1076
Glenn OA, Barkovich AJ (2006) Magnetic resonance imaging of the fetal brain and spine: an increasingly important tool in prenatal diagnosis, part 1. AJNR Am J Neuroradiol 27(8):1604–1611
Grossman R, Hoffman C, Mardor Y, Biegon A (2006) Quantitative MRI measurements of human fetal brain development in utero. Neuroimage 33(2):463–470
Guibaud L (2009) Contribution of fetal cerebral MRI for diagnosis of structural anomalies. Prenat Diagn 29(4):420–433
Guibaud L (2009) Fetal cerebral ventricular measurement and ventriculomegaly: time for procedure standardization. Ultrasound Obstet Gynecol 34(2):127–130
Habas PA, Kim K, Corbett-Detig JM, Rousseau F, Glenn OA, Barkovich AJ, Studholme C (2010) A spatiotemporal atlas of MR intensity, tissue probability and shape of the fetal brain with application to segmentation. Neuroimage 53(2):460–470
Habas PA, Kim K, Rousseau F, Glenn OA, Barkovich AJ, Studholme C (2010) Atlas-based segmentation of developing tissues in the human brain with quantitative validation in young fetuses. Hum Brain Mapp 31(9):1348–1358
Habas PA, Rajagopalan V, Scott JA, Kim K, Roosta A, Rousseau F, Barkovich AJ, Glenn OA, Studholme C (2011) Detection and mapping of delays in early cortical folding derived from in utero MRI. In: Medical Imaging 2011: Image Processing, Proceedings of SPIE, vol 7962, 79,624D
Habas PA, Scott JA, Roosta A, Rajagopalan V, Kim K, Rousseau F, Barkovich AJ, Glenn OA, Studholme C (2012) Early folding patterns and asymmetries of the normal human brain detected from in utero MRI. Cereb Cortex 22(1):13–25
Kanekar S, Gent M (2011) Malformations of cortical development. Semin Ultrasound CT MR 32(3):211–227
Kazan-Tannus JF, Dialani V, Kataoka ML, Chiang G, Feldman HA, Brown JS, Levine D (2007) MR volumetry of brain and CSF in fetuses referred for ventriculomegaly. AJR Am J Roentgenol 189(1):145–151
Kim K, Habas PA, Rousseau F, Glenn OA, Barkovich AJ, Studholme C (2010) Intersection based motion correction of multislice MRI for 3-D in utero fetal brain image formation. IEEE Trans Med Imaging 29(1):146–158
Li Y, Estroff JA, Mehta TS, Robertson RL, Robson CD, Poussaint TY, Feldman HA, Ware J, Levine D (2011) Ultrasound and MRI of fetuses with ventriculomegaly: can cortical development be used to predict postnatal outcome? AJR Am J Roentgenol 196(6):1457–1467
Lopes A, Brodlie K (2003) The robustness and accuracy of the marching cubes algorithm for isosurfacing. IEEE Transact Visualiz Comput Graph 9(1):16–29
Melchiorre K, Bhide A, Gika AD, Pilu G, Papageorghiou AT (2009) Counseling in isolated mild fetal ventriculomegaly. Ultrasound Obstet Gynecol 34(2):212–224
Nichols TE, Holmes AP (2002) Nonparametric permutation tests for functional neuroimaging: a primer with examples. Hum Brain Mapp 15(1):1–25
Ouahba J, Luton D, Vuillard E, Garel C, Gressens P, Blanc N, Elmaleh M, Evrard P, Oury JF (2006) Prenatal isolated mild ventriculomegaly: outcome in 167 cases. BJOG 113(9):1072–1079
Rajagopalan V, Scott J, Habas PA, Kim K, Corbett-Detig J, Rousseau F, Barkovich AJ, Glenn OA, Studholme C (2011) Local tissue growth patterns underlying normal fetal human brain gyrification quantified in utero. J Neurosci 31(8):2878–2287
Scott JA, Habas PA, Kim K, Rajagopalan V, Hamzelou KS, Corbett-Detig JM, Barkovich AJ, Glenn OA, Studholme C (2011) Growth trajectories of the human fetal brain tissues estimated from 3D reconstructed in utero MRI. Int J Dev Neurosci 29(5):529–536
Senapati GM, Levine D, Smith C, Estroff JA, Barnewolt CE, Robertson RL, Poussaint TY, Mehta TS, Werdich XQ, Pier D, Feldman HA, Robson CD (2010) Frequency and cause of disagreements in imaging diagnosis in children with ventriculomegaly diagnosed prenatally. Ultrasound Obstet Gynecol 36(5):582–595
Signorelli M, Tiberti A, Valseriati D, Molin E, Cerri V, Groli C, Bianchi UA (2004) Width of the fetal lateral ventricular atrium between 10 and 12 mm: a simple variation of the norm? Ultrasound Obstet Gynecol 23(1):14–18
Studholme C, Cardenas V (2004) A template free approach to volumetric spatial normalization of brain anatomy. Pattern Recogn Lett 25(10):1191–1202
Wax JR, Bookman L, Cartin A, Pinette MG, Blackstone J (2003) Mild fetal cerebral ventriculomegaly: diagnosis, clinical associations, and outcomes. Obstet Gynecol Surv 58(6):407–414
Weichert J, Hartge D, Krapp M, Germer U, Gembruch U, Axt-Fliedner R (2010) Prevalence, characteristics and perinatal outcome of fetal ventriculomegaly in 29,000 pregnancies followed at a single institution. Fetal Diagn Ther 27(3):142–148
Acknowledgements
This research was funded by the National Institutes of Health through the National Institute of Neurological Disorders and Stroke (R01 NS 061957 and R01 NS 055064); National Center for Research Resources to UCSF-CTSI (UL1 RR024131); and award to O.A.G. (K23 NS52506-03).
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Scott, J.A., Habas, P.A., Rajagopalan, V. et al. Volumetric and surface-based 3D MRI analyses of fetal isolated mild ventriculomegaly. Brain Struct Funct 218, 645–655 (2013). https://doi.org/10.1007/s00429-012-0418-1
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DOI: https://doi.org/10.1007/s00429-012-0418-1