Donald School Journal of Ultrasound in Obstetrics and Gynecology

Register      Login

VOLUME 16 , ISSUE 1 ( January-March, 2022 ) > List of Articles

REVIEW ARTICLE

Fetal Brain Structure and CNS Anomalies

Ritsuko K Pooh, Megumi Machida, Nana Matsuzawa

Keywords : Fetal brain, Molecular genetics, Three-dimensional neurosonography, Transvaginal ultrasound

Citation Information : Pooh RK, Machida M, Matsuzawa N. Fetal Brain Structure and CNS Anomalies. Donald School J Ultrasound Obstet Gynecol 2022; 16 (1):31-52.

DOI: 10.5005/jp-journals-10009-1921

License: CC BY-NC 4.0

Published Online: 22-04-2022

Copyright Statement:  Copyright © 2022; The Author(s).


Abstract

As the brain is an organ that must be understood as a three-dimensional (3D) structure, and because the fetal skull ossifies in late pregnancy, it is difficult to depict detailed structures in the brain using conventional horizontal cross-sectional images captured by transabdominal ultrasound. However, there are large spaces such as anterior/posterior fontanels and sagittal sutures in the fetal skull. By using these spaces as a window for ultrasound, it becomes easier to observe the brain structure. Transvaginal fetal 3D neurosonography and transvaginal ultrasound have made it possible to observe congenital brain structural abnormalities and cortical dysgenesis in more detail. Transvaginal 3D ultrasound imaging has been reported to be effective in the evaluation of fetal brain structure. Images of normal brain development, intracerebral vascular architecture, brain malformations, brain disorders such as intracerebral hemorrhage and stroke, and abnormalities in cortical development have gradually revealed the previously unknown development and pathology of the fetal brain. Fetal 3D neurosonography provides information on the orientation of the fetal brain, brain development during pregnancy, the exact location of brain lesions, and the inner structure of the lesions. Detailed neuroimaging is now available for diagnosis of the central nervous system, and genetic tests such as chromosomal microarrays, exome sequencing, and genome sequencing add information on genetic causative factors. The combination of detailed neurosonography and molecular genetics has established a new interdisciplinary field of fetal neurology called “neurosonogenetics,” which will enable accurate perinatal management and care in the future.


PDF Share
  1. Timor-Tritsch IE, Monteagudo A. Tansvaginal fetal neurosonography: standardization of the planes and sections by anatomic landmarks. UOG 1996;8(1):42–47. DOI: 10.1046/j.1469-0705.1996.08010042.x
  2. Timor-Tritsch IE, Monteagudo A, Mayberry P. Three-dimensional ultrasound evaluation of the fetal brain: the three horn view. Ultrasound Obstet Gynecol 2000;16(4):302–306. DOI: 10.1046/j.1469-0705.2000.00177.x
  3. Pooh RK. Contribution of transvaginal high-resolution ultrasound in fetal neurology. Donald Sch J Ultrasound Obstet Gynecol 2011:5(2):93–99. DOI: 10.5005/jp-journals-10009-1183
  4. Pooh RK. Recent fetal neurology: from neurosonography to neurosonogenetics. Donald Sch J Ultrasound Obs Gynecol. 2021;15(3):229–239. DOI: 10.5005/jp-journals-10009-1718
  5. 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(4):307–313. DOI: 10.1046/j.1469-0705.2000.00264.x
  6. Pooh RK, Kurjak A. 3D and 4D sonography and magnetic resonance in the assessment of normal and abnormal CNS development: alternative or complementary. J Perinat Med 2011;39(1):3–13. DOI: 10.1515/JPM.2010.118
  7. Pooh RK. Neuroimaging Published online 2012:45–53.
  8. Pooh RK, Machida M, Nakamura T, et al. Increased Sylvian fissure angle as early sonographic sign of malformation of cortical development. Ultrasound Obstet Gynecol 2019;54(2):199–206. DOI: 10.1002/uog.20171
  9. Poon LC, Sahota DS, Chaemsaithong P, et al. Transvaginal three-dimensional ultrasound assessment of Sylvian fissures at 18–30 weeks’ gestation. Ultrasound Obstet Gynecol 2019;54(2):190–198. DOI: 10.1002/uog.20172
  10. Pooh RK, Kurjak A. Three-dimensional ultrasound in detection of fetal anomalies. Donald Sch J Ultrasound Obstet Gynecol 2016;10(3):214–234. DOI: 10.5005/jp-journals-10009-1471
  11. Pooh RK. Three-dimensional evaluation of the fetal brain. Donald Sch J Ultrasound Obstet Gynecol 2017;11(4):268–275. DOI: 10.5005/jp-journals-10009-1532
  12. Pooh RK. Fetal brain imaging. Ultrasound Med Biol 2017. DOI: 10.1016/j.ultrasmedbio.2017.08.1416
  13. Pooh RK. 13-week pulmonary sonoangiogram by 3D HDlive flow. Donald Sch J Ultrasound Obstet Gynecol 2015;9(4):355–356. DOI: 10.5005/jp-journals-10009-1421
  14. Pooh RK. Sonoembryology by 3D HDlive silhouette ultrasound – what is added by the “see-through fashion”? J Perinat Med 2016;44(2):1. DOI: 10.1515/jpm-2016
  15. Pooh RK. ‘See-through fashion’ in prenatal diagnostic imaging. Donald Sch J Ultrasound Obstet Gynecol 2015;9(2):111. DOI: 10.5005/jp-journals-10009-1397
  16. Pooh RK. Fetal central nervous system: new insights with ultrasound. Donald School Textbook of Ultrasound in Obstetrics & Gynecology 2018. DOI: 10.5005/jp/books/13058_18
  17. Pooh RK. Recent advances in 3D ultrasound, silhouette ultrasound, and sonoangiogram in fetal neurology. Donald Sch J Ultrasound Obstet Gynecol 2016;10(2):193–200. DOI: 10.5005/jp-journals-10009-1468
  18. Pooh RK, Aono T. Transvaginal power doppler angiography of the fetal brain. Ultrasound Obstet Gynecol 1996;8(6):417–421. DOI: 10.1046/j.1469-0705.1997.08060417.x
  19. Pooh RK. The role of issmaging detection of congenital defects in the era of PGT-A and NIPT. J Perinat Med 2019;47(eA):92. DOI: 10.1515/jpm-2019-2501
  20. Pooh RK, Pooh K. Transvaginal 3D and doppler ultrasonography of the fetal brain. Semin Perinatol 2001;25(1):38–43. DOI: 10.1053/sper.2001.22895
  21. Pooh RK. Twenty-week brain vascularity by transvaginal 3D HDlive flow. Donald Sch J Ultrasound Obstet Gynecol 2016;10(3):203–204. DOI: 10.5005/jp-journals-10009-1469
  22. Copp AJ, Greene NDE. Genetics and development of neural tube defects. J Pathol 2010;220(2):217–230. DOI: 10.1002/path.2643
  23. Greene NDE, Copp AJ. Development of the vertebrate central nervous system: formation of the neural tube. Prenat Diagn 2009;29(4):303–311. DOI: 10.1002/pd.2206
  24. Rolo A, Galea GL, Savery D, et al. Novel mouse model of encephalocele: post-neurulation origin and relationship to open neural tube defects. Dis Model Mech 2019;12(11):dmm040683. DOI: 10.1242/dmm.040683
  25. Cohen MM. Perspectives on holoprosencephaly: part I. Epidemiology, genetics, and syndromology. Teratology 1989;40(3):211–235. DOI: 10.1002/tera.1420400304
  26. Matsunaga E, Shiota K. Holoprosencephaly in human embryos: epidemiologic studies of 150 cases. Teratology 1977;16(3):261–272. DOI: 10.1002/tera.1420160304
  27. Cohen MM. Holoprosencephaly: clinical, anatomic, and molecular dimensions. Birth Defects Res A Clin Mol Teratol 2006;76(9):658–673. DOI: 10.1002/bdra.20295
  28. Roessler E, Muenke M. The molecular genetics of holoprosencephaly. Am J Med Genet 2010;154C(1):52–61. DOI: 10.1002/ajmg.c.30236
  29. Robbins DJ, Nybakken KE, Kobayashi R, et al. Hedgehog elicits signal transduction by means of a large complex containing the kinesin-related protein costal2. Cell 1997;90(2):225–234. DOI: 10.1016/S0092-8674(00)80331-1
  30. Robbins DJ, Fei DL, Riobo NA. The hedgehog signal transduction network. Sci Signal 2012;5(246):re6. DOI: 10.1126/scisignal.2002906
  31. Blaas HGK. Holoprosencephaly. In: Obstetric Imaging: Fetal Diagnosis and Care, 2nd Edition.; 2017. DOI: 10.1016/B978-0-323-44548-1.00039-5
  32. Edwards TJ, Sherr EH, Barkovich AJ, et al. Clinical, genetic and imaging findings identify new causes for corpus callosum development syndromes. Brain 2014;137(Pt 6):1579–1613. DOI: 10.1093/brain/awt358
  33. O'Leary DDM, Chou SJ, Sahara S. Area patterning of the mammalian cortex. Neuron 2007;56(2):252–269. DOI: 10.1016/j.neuron.2007.10.010
  34. Hoerder-Suabedissen A, Hayashi S, Upton L, et al. Subset of cortical layer 6b neurons selectively innervates higher order thalamic nuclei in mice. Cereb Cortex 2018;28(5):1882-1897. DOI: 10.1093/cercor/bhy036
  35. Puthuran MJ, Rowland-Hill CA, Simpson J, et al. Chromosome 1q42 deletion and agenesis of the corpus callosum. Am J Med Genet 2005;138(1):68–69. DOI: 10.1002/ajmg.a.30888
  36. Filges I, Röthlisberger B, Boesch N, et al. Interstitial deletion 1q42 in a patient with agenesis of corpus callosum: phenotype-genotype comparison to the 1q41q42 microdeletion suggests a contiguous 1q4 syndrome. Am J Med Gene 2010;152A(4):987–993. DOI: 10.1002/ajmg.a.33330
  37. Righini A, Ciosci R, Selicorni A, et al. Brain magnetic resonance imaging in Wolf-Hirschhorn syndrome. Neuropediatrics 2007;38(1):25–28. DOI: 10.1055/s-2007-981685
  38. O'Driscoll MC, Black GC, Clayton-Smith J, et al. Identification of genomic loci contributing to agenesis of the corpus callosum. Am J Med Genet A 2010;152A(9):2145–2159. DOI: 10.1002/ajmg.a.33558
  39. Heide S, Keren B, Billette de Villemeur T, et al. Copy number variations found in patients with a corpus callosum abnormality and intellectual disability. J Pediatr 2017;185:160–166.e1. DOI: 10.1016/j.jpeds.2017.02.023
  40. Schell-Apacik CC, Wagner K, Bihler M, et al. Agenesis and dysgenesis of the corpus callosum: clinical, genetic and neuroimaging findings in a series of 41 patients. Am J Med Genet 2008;146A(19):2501–2511. DOI: 10.1002/ajmg.a.32476
  41. Chen CP, Chang TY, Guo WY, et al. Chromosome 17p13.3 deletion syndrome: ACGH characterization, prenatal findings and diagnosis, and literature review. Gene 2013;532(1):152–159. DOI: 10.1016/j.gene.2013.09.044
  42. Chen CP, Chien SC. Prenatal sonographic features of Miller-Dieker syndrome. J Med Ultrasound 2010;18(4):147–152. DOI: 10.1016/j.jmu.2010.11.002
  43. Kitamura K, Yanazawa M, Sugiyama N, et al. Mutation of ARX causes abnormal development of forebrain and testes in mice and X-linked lissencephaly with abnormal genitalia in humans. Nat Genet 2002;32(3):359–369. DOI: 10.1038/ng1009
  44. Kato M, Das S, Petras K, et al. Mutations of ARX are associated with striking pleiotropy and consistent genotype-phenotype correlation. Hum Mutat 2004;23(2):147–159. DOI: 10.1002/humu.10310
  45. Dobyns WB, Berry-Kravis E, Havernick NJ, et al. X-linked lissencephaly with absent corpus callosum and ambiguous genitalia. Am J Med Genet 1999; DOI: 10.1002/(SICI)1096-8628(19991008)86:4<331::AID-AJMG7>3.0.CO;2-P
  46. Bonneau D, Toutain A, Laquerrière A, et al. X-linked lissencephaly with absent corpus callosum and ambiguous genitalia (XLAG): clinical, magnetic resonance imaging, and neuropathological findings. Ann Neurol 2002;51(3):340–349. DOI: 10.1002/ana.10119
  47. Fransen E, Vits L, Van Camp G, et al. The clinical spectrum of mutations in L1, a neuronal cell adhesion molecule. Am J Med Genet 1996;64(1):73–77. DOI: 10.1002/(SICI)1096-8628(19960712)64:1<73::AID-AJMG11>3.0.CO;2-P
  48. Aicardi J. Aicardi syndrome. Brain Dev 2005. DOI: 10.1016/j.braindev.2003.11.011
  49. Lund C, Bjørnvold M, Tuft M, et al. Aicardi syndrome: an epidemiologic and clinical study in Norway. Pediatr Neurol 2015;52(2):182–6.e3. DOI: 10.1016/j.pediatrneurol.2014.10.022
  50. Parrini E, Conti V, Dobyns WB, et al. Genetic basis of brain malformations. Mol Syndromol 2016;7(4):220–233. DOI: 10.1159/000448639
  51. Guerrini R, Dobyns WB. Malformations of cortical development: clinical features and genetic causes. Lancet Neurol 2014;13(7):710–726. DOI: 10.1016/S1474-4422(14)70040-7
  52. Desikan RS, Barkovich AJ. Malformations of cortical development. Ann Neurol 2016;80(6):797–810. DOI: 10.1002/ana.24793
  53. Barkovich J. Complication begets clarification in classification. Brain 2013;136(2):368–370. DOI: 10.1093/brain/awt001
  54. Severino M, Geraldo AF, Utz N, et al. Definitions and classification of malformations of cortical development: practical guidelines. Brain 2020;143(10):2874–2894. DOI: 10.1093/brain/awaa174
  55. Gilmore EC, Walsh CA. Genetic causes of microcephaly and lessons for neuronal development. Wiley Interdiscip Rev Dev Biol 2013;2(4):461–478. DOI: 10.1002/wdev.89
  56. Yu TW, Mochida GH, Tischfield DJ, et al. Mutations in WDR62, encoding a centrosome-associated protein, cause microcephaly with simplified gyri and abnormal cortical architecture. Nat Genet 2010;42(11):1015–1020. DOI: 10.1038/ng.683
  57. Jackson AP, Eastwood H, Bell SM, et al. Identification of microcephalin, a protein implicated in determining the size of the human brain. Am J Hum Genet 2002;71(1):136–142. DOI: 10.1086/341283
  58. Nicholas AK, Khurshid M, Désir J, et al. WDR62 is associated with the spindle pole and is mutated in human microcephaly. Nat Genet 2010;42(11):1010–1014. DOI: 10.1038/ng.682
  59. Trimborn M, Bell SM, Felix C, et al. Mutations in microcephalin cause aberrant regulation of chromosome condensation. Am J Hum Genet 2004;75(2):261–266. DOI: 10.1086/422855
  60. Brunk K, Vernay B, Griffith E, et al. Microcephalin coordinates mitosis in the syncytial Drosophila embryo. J Cell Sci 2007;120(Pt 20):3578–3588. DOI: 10.1242/jcs.014290
  61. Bond J, Roberts E, Mochida GH, et al. ASPM is a major determinant of cerebral cortical size. Nat Genet 2002;32(2):316–320. DOI: 10.1038/ng995
  62. Bond J, Roberts E, Springell K, et al. A centrosomal mechanism involving CDK5RAP2 and CENPJ controls brain size. Nat Genet 2005;37(4):353–355. DOI: 10.1038/ng1539
  63. Kumar A, Girimaji SC, Duvvari MR, et al. Mutations in STIL, encoding a pericentriolar and centrosomal protein, cause primary microcephaly. Am J Hum Genet 2008;84(2):286–290. DOI: 10.1016/j.ajhg.2009.01.017
  64. Bilgüvar K, Öztürk AK, Louvi A, et al. Whole-exome sequencing identifies recessive WDR62 mutations in severe brain malformations. Nature 2010;467(7312):207–210. DOI: 10.1038/nature09327
  65. Kaya B, Ali Kemal O, Angeliki L, et al. Whole-exome sequencing identifies recessive WDR62 mutations in severe brain malformations. Nature 2011. DOI: 10.1038/nature09327
  66. Guernsey DL, Jiang H, Hussin J, et al. Mutations in centrosomal protein CEP152 in primary microcephaly families linked to MCPH4. Am J Hum Genet 2010. DOI: 10.1016/j.ajhg.2010.06.003
  67. Toi A, Lister WS, Fong KW. How early are fetal cerebral sulci visible at prenatal ultrasound and what is the normal pattern of early fetal sulcal development?. Ultrasound Obstet Gynecol 2004;24(7):706–715. DOI: 10.1002/uog.1802
  68. Namburete AI, Stebbing RV, Kemp B, et al. Learning-based prediction of gestational age from ultrasound images of the fetal brain. Med Image Anal 2015;21(1):72–86. DOI: 10.1016/j.media.2014.12.006
  69. Chen X, Li SL, Luo GY, et al. Ultrasonographic characteristics of cortical sulcus development in the human fetus between 18 and 41 weeks of gestation. Chin Med J (Engl) 2017;130(8):920–928. DOI: 10.4103/0366-6999.204114
  70. Di Donato N, Chiari S, Mirzaa GM, et al. Lissencephaly: expanded imaging and clinical classification. Am J Med Genet 2017;173(6):1473–1488. DOI: 10.1002/ajmg.a.38245
  71. Pooh RK. Fetal neuroimaging of neural migration disorder. Ultrasound Clin 2008;3(4):541–552. DOI: 10.1016/j.cult.2008.09.007
  72. McGahan JP, Grix A, Gerscovich EO. Prenatal diagnosis of lissencephaly: Miller-Dieker syndrome. J Clin Ultrasound 1994. DOI: 10.1002/jcu.1870220908
  73. Greco P, Resta M, Vimercati A, et al. Antenatal diagnosis of isolated lissencephaly by ultrasound and magnetic resonance imaging. Ultrasound Obstet Gynecol 1998;12(4):276–279. DOI: 10.1046/j.1469-0705.1998.12040276.x
  74. Kojima K, Suzuki Y, Seki K, et al. Prenatal diagnosis of lissencephaly (type II) by ultrasound and fast magnetic resonance imaging. Fetal Diagn Ther 2002;17(1):34–36. DOI: 10.1159/000048003
  75. Fong KW, Ghai S, Toi A, et al. Prenatal ultrasound findings of lissencephaly associated with Miller-Dieker syndrome and comparison with pre-and postnatal magnetic resonance imaging. Ultrasound Obstet Gynecol 2004;24(7):716–723. DOI: 10.1002/uog.1777
  76. Gha S, Fong KW, Toi A, et al. Prenatal US and MR imaging findings of lissencephaly: review of fetal cerebral sulcal development. Radiographics 2006;26(2):389–405. DOI: 10.1148/rg.262055059
  77. Yoshida A, Kobayashi K, Manya H, et al. Muscular dystrophy and neuronal migration disorder caused by mutations in a glycosyltransferase, POMGnT1. Dev Cell 2001;1(5):717–724. DOI: 10.1016/S1534-5807(01)00070-3
  78. Hehr U, Uyanik G, Gross C, et al. Novel POMGnT1 mutations define broader phenotypic spectrum of muscle-eye-brain disease. Neurogenetics 2007;8(4):279–288. DOI: 10.1007/s10048-007-0096-y
  79. Godfrey C, Clement E, Mein R, et al. Refining genotype phenotype correlations in muscular dystrophies with defective glycosylation of dystroglycan. Brain 2007;130(Pt 10):2725–2735. DOI: 10.1093/brain/awm212
  80. Kobayashi K, Nakahori Y, Miyake M, et al. An ancient retrotransposal insertion causes Fukuyama-type congenital muscular dystrophy. Nature 1998;394(6691):388–392. DOI: 10.1038/28653
  81. Toda T, Kobayashi K, Kondo-Iida E, et al. The Fukuyama congenital muscular dystrophy story. Neuromuscul Disord 2000;10(3):153–159. DOI: 10.1016/S0960-8966(99)00109-1
  82. Takeda S. Fukutin is required for maintenance of muscle integrity, cortical histiogenesis and normal eye development. Hum Mol Genet 2003;12(12):1449–1459. DOI: 10.1093/hmg/ddg153
  83. Friocourt G, Kanatani S, Tabata H, et al. Cell-autonomous roles of ARX in cell proliferation and neuronal migration during corticogenesis. J Neurosci 2008;28(22): 5794–5805. DOI: 10.1523/JNEUROSCI.1067-08.2008
  84. Friocourt G, Poirier K, Rakić S, et al. The role of ARX in cortical development. Eur J Neurosci 2006;23(4):869–876. DOI: 10.1111/j.1460-9568.2006.04629.x
  85. Sherr EH. The ARX story (epilepsy, mental retardation, autism, and cerebral malformations): one gene leads to many phenotypes. Curr Opin Pediatr 2003;15(6):567–571. DOI: 10.1097/00008480-200312000-00004
  86. Colasante G, Simonet JC, Calogero R, et al. ARX regulates cortical intermediate progenitor cell expansion and upper layer neuron formation through repression of Cdkn1c. Cereb Cortex 2015;25(2):322–335. DOI: 10.1093/cercor/bht222
  87. Folsom TD, Fatemi SH. The involvement of Reelin in neurodevelopmental disorders. Neuropharmacology 2013;68:122–135. DOI: 10.1016/j.neuropharm.2012.08.015
  88. Tissir F, Goffinet AM. Reelin and brain development. Nat Rev Neurosci 2003;4(6):496–505. DOI: 10.1038/nrn1113
  89. Chen Y, Beffert U, Ertunc M, et al. Reelin modulates NMDA receptor activity in cortical neurons. J Neurosci 2005;25(36):8209–8216. DOI: 10.1523/JNEUROSCI.1951-05.2005
  90. Kato M. Genotype-phenotype correlation in neuronal migration disorders and cortical dysplasias. Front Neurosci 2015;9:181. DOI: 10.3389/fnins.2015.00181
  91. Fallet-Bianco C, Laquerrière A, Poirier K, et al. Mutations in tubulin genes are frequent causes of various foetal malformations of cortical development including microlissencephaly. Acta Neuropathol Commun 2014;2:69. DOI: 10.1186/2051-5960-2-69
  92. Laquerriere A, Gonzales M, Saillour Y, et al. De novo TUBB2B mutation causes fetal akinesia deformation sequence with microlissencephaly: An unusual presentation of tubulinopathy. Eur J Med Genet 2016;59(4):249–256. DOI: 10.1016/j.ejmg.2015.12.007
  93. Harding BN, Moccia A, Drunat S, et al. Mutations in citron kinase cause recessive microlissencephaly with multinucleated neurons. Am J Hum Genet 2016;99(2):511–520. DOI: 10.1016/j.ajhg.2016.07.003
  94. Barkovich AJ, Ferriero DM, Barr RM, et al. Microlissencephaly: A heterogeneous malformation of cortical development. Neuropediatrics 1998;29(3):113–119. DOI: 10.1055/s-2007-973545
  95. Poirier K, Martinovic J, Laquerrière A, et al. Rare ACTG1 variants in fetal microlissencephaly. Eur J Med Genet 2015;58(8):416–418. DOI: 10.1016/j.ejmg.2015.06.006
  96. Pooh RK, Machida M, Imoto I, et al. Fetal megalencephaly with cortical dysplasia at 18 gestational weeks related to paternal UPD mosaicism with PTEN mutation. Genes (Basel) 2021;12(3):358. DOI: 10.3390/genes12030358
  97. Manzini MC, Walsh CA. The Genetics of Brain Malformations. The Genetics of Neurodevelopmental Disorders 2015. DOI: 10.1002/9781118524947.ch7
  98. Smigiel R, Cabala M, Jakubiak A, et al. Novel COL4A1 mutation in an infant with severe dysmorphic syndrome with schizencephaly, periventricular calcifications, and cataract resembling congenital infection. Birth Defects Res A Clin Mol Teratol 2016;106(4):304–307. DOI: 10.1002/bdra.23488
  99. Watanabe J, Okamoto K, Ohashi T, et al. Malignant hyperthermia and cerebral venous sinus thrombosis after ventriculoperitoneal shunt in infant with schizencephaly and COL4A1 mutation. World Neurosurg 2019;127:446–450. DOI: 10.1016/j.wneu.2019.04.156
  100. Errata to Intracranial hemorrhage and tortuosity of veins detected on susceptibility-weighted imaging of a child with a type IV collagen α1 mutation and schizencephaly(Singapore Med J Magn Reson Med Sci 14,3 223–226, 2014 10.2463/mrms.2014–0060). 2015. DOI: 10.2463/mrms.2014-0060er
  101. Leventer RJ, Jansen A, Pilz DT, et al. Clinical and imaging heterogeneity of polymicrogyria: a study of 328 patients. Brain 2010;133(Pt 5):1415–1427. DOI: 10.1093/brain/awq078
  102. Stutterd CA, Leventer RJ. Polymicrogyria: a common and heterogeneous malformation of cortical development. Am J Med Genet Part C Semin Med Genet 2014;166C(2):227–239. DOI: 10.1002/ajmg.c.31399
  103. Salomon LJ, Bernard JP, Ville Y. Reference ranges for fetal ventricular width: a non-normal approach. Ultrasound Obstet Gynecol 2007;30(1):61–66. DOI: 10.1002/uog.4026
  104. Heaphy-Henault KJ, Guimaraes C V., Mehollin-Ray AR, et al. Congenital aqueductal stenosis: findings at fetal MRI that accurately predict a postnatal diagnosis. Am J Neuroradiol 2018;39(5):942–948. DOI: 10.3174/ajnr.A5590
  105. Norton ME, Fox NS, Monteagudo A, et al. Fetal ventriculomegaly. Am J Obstet Gynecol 2020;223(6):B30–B33. DOI: 10.1016/j.ajog.2020.08.182
  106. Huang RN, Chen JY, Pan H, et al. Correlation between mild fetal ventriculomegaly, chromosomal abnormalities, and copy number variations. J Matern Neonatal Med 2020;0(0):1–9. DOI: 10.1080/14767058.2020.1863941
  107. Etchegaray A, Juarez-Peñalva S, Petracchi F, Igarzabal L. Prenatal genetic considerations in congenital ventriculomegaly and hydrocephalus. Child's Nerv Syst 2020;36(8):1645–1660. DOI: 10.1007/s00381-020-04526-5
  108. Putbrese B, Kennedy A. Findings and differential diagnosis of fetal intracranial haemorrhage and fetal ischaemic brain injury: What is the role of fetal MRI?. Br J Radiol 2017;90((1070)). DOI: 10.1259/bjr.20160253
  109. Melchiorre K, Bhide A, Gika AD, et al. Counseling in isolated mild fetal ventriculomegaly. Ultrasound Obstet Gynecol 2009;34(2):212–224. DOI: 10.1002/uog.7307
  110. Fox NS, Monteagudo A, Kuller JA, et al. Mild fetal ventriculomegaly: diagnosis, evaluation, and management. Am J Obstet Gynecol 2018;219(1):B2–B9. DOI: 10.1016/j.ajog.2018.04.039
  111. Cardoza JD, Goldstein RB, Filly RA. Exclusion of fetal ventriculomegaly with a single measurement: the width of the lateral ventricular atrium. Radiology 1988;169(3):711–714. DOI: doi.org/10.1148/radiology.169.3.3055034
  112. Almog B, Gamzu R, Achiron R, et al. Fetal lateral ventricular width: what should be its upper limit? J Ultrasound Med 2003;22(1):39–43. DOI: 10.7863/jum.2003.22.1.39
  113. Malinger G, Paladini D, Haratz KK, et al. ISUOG practice guidelines (updated): sonographic examination of the fetal central nervous system. Part 1: performance of screening examination and indications for targeted neurosonography. Ultrasound Obstet Gynecol 2020;56(3):476–484. DOI: 10.1002/uog.22145
  114. Cardoza JD, Goldstein RB, Filly RA. Exclusion of fetal ventriculomegaly with a single measurement: the width of the lateral ventricular atrium. Radiology 1988;169(3):711–714. DOI: 10.1148/radiology.169.3.3055034
  115. Gaglioti P, Danelon D, Bontempo S, et al. Fetal cerebral ventriculomegaly: outcome in 176 cases. Ultrasound Obstet Gynecol 2005;25(4):372–377. DOI: 10.1002/uog.1857
  116. Chu N, Zhang Y, Yan Y, et al. Fetal ventriculomegaly: pregnancy outcomes and follow-ups in ten years. Biosci Trends 2016;10(2):125–132. DOI: 10.5582/bst.2016.01046
  117. Pagani G, Thilaganathan B, Prefumo F. Neurodevelopmental outcome in isolated mild fetal ventriculomegaly: systematic review and meta-analysis. Ultrasound Obstet Gynecol 2014;44(3):254–260. DOI: 10.1002/uog.13364
  118. Scelsa B, Rustico M, Righini A, et al. Mild ventriculomegaly from fetal consultation to neurodevelopmental assessment: a single center experience and review of the literature. Eur J Paediatr Neurol 2018;22(6):919–928. DOI: 10.1016/j.ejpn.2018.04.001
  119. Carta S, Kealin Agten A, Belcaro C, et al. Outcome of fetuses with prenatal diagnosis of isolated severe bilateral ventriculomegaly: systematic review and meta-analysis. Ultrasound Obstet Gynecol 2018;52(2):165–173. DOI: 10.1002/uog.19038
  120. Hannon T, Tennant PWG, Rankin J, Robson SC. Epidemiology, natural history, progression, and postnatal outcome of severe fetal ventriculomegaly. Obstet Gynecol 2012;120(6):1345–1353. DOI: 10.1097/AOG.0b013e3182732b53
  121. Shaheen R, Sebai MA, Patel N, et al. The genetic landscape of familial congenital hydrocephalus. Ann Neurol 2017;81(6):890–897. DOI: 10.1002/ana.24964
  122. Ekici AB, Hilfinger D, Jatzwauk M, et al. Disturbed Wnt signalling due to a mutation in CCDC88C causes an autosomal recessive non-syndromic hydrocephalus with medial diverticulum. Mol Syndromol 2010;1(3):99–112. DOI: 10.1159/000319859
  123. Al-Dosari MS, Al-Owain M, Tulbah M, et al. Mutation in MPDZ causes severe congenital hydrocephalus. J Med Genet 2013;50(1):54–58. DOI: 10.1136/jmedgenet-2012-101294
  124. Kousi M, Katsanis N. The genetic basis of hydrocephalus. Annu Rev Neurosci 2016;39:409–435. DOI: 10.1146/annurev-neuro-070815-014023
  125. Yamasaki M, Thompson P, Lemmon V. CRASH syndrome: mutations in L1CAM correlate with severity of the disease. Neuropediatrics 1997;28(3):175–178. DOI: 10.1055/s-2007-973696
  126. Itoh K, Fushiki S. The role of L1cam in murine corticogenesis, and the pathogenesis of hydrocephalus. Pathol Int 2015;65(2):58–66. DOI: 10.1111/pin.12245
  127. Takahashi S, Makita Y, Okamoto N, et al. L1CAM mutation in a Japanese family with X-linked hydrocephalus: a study for genetic counseling. Brain Dev 1997;19(8):559–562. DOI: 10.1016/S0387-7604(97)00079-X
  128. Jouet M, Rosenthal A, Armstrong G, et al. X–linked spastic paraplegia (SPG1), MASA syndrome and X–linked hydrocephalus result from mutations in the L1 gene. Nat Genet 1994;(3):402–407. DOI: 10.1038/ng0794-402
  129. Adle-Biassette H, Saugier-Veber P, Fallet-Bianco C, et al. Neuropathological review of 138 cases genetically tested for X-linked hydrocephalus: evidence for closely related clinical entities of unknown molecular bases. Acta Neuropathol 2013;126(3):427–442. DOI: 10.1007/s00401-013-1146-1
  130. Rachel RA, Yamamoto EA, Dewanjee MK, et al. CEP290 alleles in mice disrupt tissue-specific cilia biogenesis and recapitulate features of syndromic ciliopathies. Hum Mol Genet 2015;24(13):3775–3791. DOI: 10.1093/hmg/ddv123
  131. Iannicelli M, Brancati F, Mougou-Zerelli S, et al. Novel TMEM67 mutations and genotype-phenotype correlates in meckelin-related ciliopathies. Hum Mutat 2010;31(5):E1319–1331. DOI: 10.1002/humu.21239
  132. Abdelhamed ZA, Natarajan S, Wheway G, et al. The Meckel-Gruber syndrome protein TMEM67 controls basal body positioning and epithelial branching morphogenesis in mice via the non-canonical Wnt pathway. DMM Dis Model Mech 2015;8(6):527–541. DOI: 10.1242/dmm.019083
  133. Leightner AC, Hommerding CJ, Peng Y, et al. The Meckel syndrome protein meckelin (TMEM67) is a key regulator of cilia function but is not required for tissue planar polarity. Hum Mol Genet 2013;22(10):2024–2040. DOI: 10.1093/hmg/ddt054
  134. Xiao D, Lv C, Zhang Z, et al. Novel CC2D2A compound heterozygous mutations cause Joubert syndrome. Mol Med Rep 2017;15(1):305–308. DOI: 10.3892/mmr.2016.6007
  135. Johnson K, Bertoli M, Phillips L, et al. Detection of variants in dystroglycanopathy-associated genes through the application of targeted whole-exome sequencing analysis to a large cohort of patients with unexplained limb-girdle muscle weakness. Skelet Muscle 2018;8(1):1–12. DOI: 10.1186/s13395-018-0170-1
  136. Mirzaa GM, Rivière JB, Dobyns WB. Megalencephaly syndromes and activating mutations in the PI3K-AKT pathway: MPPH and MCAP. Am J Med Genet C Semin Med Genet 2013;163C(2):122–130. DOI: 10.1002/ajmg.c.31361
  137. Itoh K, Pooh R, Kanemura Y, et al. Brain malformation with loss of normal FGFR3 expression in thanatophoric dysplasia type I. Neuropathology 2013;33(6):663–666. DOI: 10.1111/neup.12036
  138. Dicuonzo F, Palma M, Fiume M, et al. Cerebrovascular disorders in the prenatal period. J Child Neurol 2008;23(11):1260-1266. DOI: 10.1177/0883073808318054
  139. Özduman K, Pober BR, Barnes P, et al. Fetal stroke. Pediatr Neurol 2004;30(3):151–162. DOI: 10.1016/j.pediatrneurol.2003.08.004
  140. Elchalal U, Yagel S, Gomori JM, et al. Fetal intracranial hemorrhage (fetal stroke): does grade matter? Ultrasound Obstet Gynecol 2005;26(3):233–243. DOI: 10.1002/uog.1969
  141. Huang YF, Chen WC, Tseng JJ, et al. Fetal intracranial hemorrhage (fetal stroke): report of four antenatally diagnosed cases and review of the literature. Taiwan J Obstet Gyneco 2006;45(2):135–141. DOI: 10.1016/S1028-4559(09)60211-4
  142. Kutuk MS, Yikilmaz A, Ozgun MT, et al. Prenatal diagnosis and postnatal outcome of fetal intracranial hemorrhage. Child's Nerv Syst 014;30(3):411–418. DOI: 10.1007/s00381-013-2243-0
  143. Sims ME, Turkel SB, Halterman G, et al. Brain injury and intrauterine death. Am J Obstet Gynecol 1985;151(6):721–723. DOI: 10.1016/0002-9378(85)90503-4
  144. Shannon P, Hum C, Parks T, et al. Brain and placental pathology in fetal COL4A1 related disease. Pediatr Dev Pathol 2021;24(3):175–186. DOI: 10.1177/1093526620984083
  145. Itai T, Miyatake S, Taguri M, et al. Prenatal clinical manifestations in individuals with COL4A1/2 variants. Neurogenetics 2020;0:1–9. DOI: 10.1136/individuals
  146. Nakamura Y, Okanishi T, Yamada H, et al. Progressive cerebral atrophies in three children with COL4A1 mutations. Brain Dev 2021;43(10):1033–1038. DOI: 10.1016/j.braindev.2021.06.008
  147. Papile LA, Burstein J, Burstein R, et al. Incidence and evolution of subependymal and intraventricular hemorrhage: a study of infants with birth weights less than 1,500 gm. J Pediatr 1978;92(4):529–534. DOI: 10.1016/S0022-3476(78)80282-0
PDF Share
PDF Share

© Jaypee Brothers Medical Publishers (P) LTD.