Donald School Journal of Ultrasound in Obstetrics and Gynecology

Register      Login

VOLUME 15 , ISSUE 3 ( July-September, 2021 ) > List of Articles

REVIEW ARTICLE

Recent Fetal Neurology: From Neurosonography to Neurosonogenetics

Ritsuko K Pooh

Keywords : Brain damage, Exome sequencing, Fetus, Malformations of cortical development, Migration, Neurology, Neurulation, Proliferation, Prosencephalic, Single gene mutation

Citation Information : Pooh RK. Recent Fetal Neurology: From Neurosonography to Neurosonogenetics. Donald School J Ultrasound Obstet Gynecol 2021; 15 (3):229-239.

DOI: 10.5005/jp-journals-10009-1718

License: CC BY-NC 4.0

Published Online: 30-09-2021

Copyright Statement:  Copyright © 2021; Jaypee Brothers Medical Publishers (P) Ltd.


Abstract

Among various congenital central nervous system (CNS) malformations, only cranial bifidum, spinal bifidum, and holoprosencephaly can be diagnosed during the early embryonic/fetal stage. Other CNS dysmorphic diseases occur after 13 weeks of gestation because CNS is formed through several developmental stages, including cell proliferation, neuronal migration, and post-migrational phases, after three gestational months. The recent significant advance of three-dimensional (3D) sonographic technology has accelerated fetal neuroimaging. Since the introduction of transvaginal, transfontanelle neuroimaging technique introduced in clinical practice, combined with 3D technology, has enabled us to conduct systematic neuroimaging analyses. Recently, congenital brain abnormalities have been classified not only by their morphological features but causal genetic factors. In this article, the author describes prenatal neuroimaging diagnoses and genetic causes, and fetal CNS disorders.


PDF Share
  1. Pooh RK, Kurjak A. 3D/4D sonography moved prenatal diagnosis of fetal anomalies from the second to the first trimester of pregnancy. J Matern Fetal Neonatal Med 2012;25(5):433–455. DOI: 10.15386/cjmed-437.
  2. Pooh RK, Shiota K, Kurjak A. Imaging of the human embryo with magnetic resonance imaging microscopy and high-resolution transvaginal 3-dimensional sonography: human embryology in the 21st century. Am J Obstet Gynecol 2011;204(1):77.e1-16. DOI: 10.1016/j.ajog.2010.07.028.
  3. Pooh RK. Sonoembryology by 3D HDlive silhouette ultrasound - what is added by the “see-through fashion”? J Perinat Med 2016;44(2):139–148. DOI: 10.1515/jpm-2016-0008.
  4. Copp AJ, Greene NDE. Genetics and development of neural tube defects. J Pathol. 2010;220(2):217–230. DOI: 10.1002/path.2643.
  5. 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.
  6. Rolo A, Galea GL, Savery D, et al. Novel mouse model of encephalocele: post-neurulation origin and relationship to open neural tube defects. DMM Dis Model Mech. 2019;12(11):dmm040683. DOI: 10.1242/dmm.040683.
  7. Cohen MM. Perspectives on holoprosencephaly: part I. Epidemiology, genetics, and syndromology. Teratology 1989;40(3):211–235. DOI: 10.1002/tera.1420400304.
  8. Matsunaga E, Shiota K. Holoprosencephaly in human embryos: epidemiologic studies of 150 cases. Teratology 1977;16(3):261–272. DOI: 10.1002/tera.1420160304.
  9. Cohen MM. Holoprosencephaly: clinical, anatomic, and molecular dimensions. Birth Defects Res Part A - Clin Mol Teratol 2006;76(9):658–673. DOI: 10.1002/bdra.20295.
  10. Roessler E, Muenke M. The molecular genetics of holoprosencephaly. Am J Med Genet Part C Semin Med Genet 2010;154C(1):52–61. DOI: 10.1002/ajmg.c.30236.
  11. 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.
  12. Robbins DJ, Fei DL, Riobo NA. The hedgehog signal transduction network. Sci Signal. 2012;5(246):re6. DOI: 10.1126/scisignal.2002906.
  13. Blaas HGK. Holoprosencephaly. In: Obstetric imaging: fetal diagnosis and care. 2nd ed., 2017. pp. 190–204.e1. DOI: 10.1016/B978-0-323-44548-1.00039-5.
  14. 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.
  15. 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.
  16. 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.
  17. Puthuran MJ, Rowland-Hill CA, Simpson J, et al. Chromosome 1q42 deletion and agenesis of the corpus callosum [3]. Am J Med Genet. 2005;138(1):68–69. DOI: 10.1002/ajmg.a.30888.
  18. 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 Genet Part A 2010;152A(4):987–993. DOI: 10.1002/ajmg.a.33330.
  19. 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.
  20. O’Driscoll MC, Black GCM, Clayton-Smith J, et al. Identification of genomic loci contributing to agenesis of the corpus callosum. Am J Med Genet Part A. 2010;152A(9):2145–2159. DOI: 10.1002/ajmg.a.33558.
  21. 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.
  22. 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 Part A 2008;146A(19):2501–2511. DOI: 10.1002/ajmg.a.32476.
  23. 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.
  24. 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.
  25. 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.
  26. 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.
  27. Dobyns WB, Berry-Kravis E, Havernick NJ, et al. X-linked lissencephaly with absent corpus callosum and ambiguous genitalia. Am J Med Genet 1999;86(4):331–337. DOI: 10.1002/(SICI)1096-8628(19991008)86:4<331::AID-AJMG7>3.0.CO;2-P.
  28. 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.
  29. 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.
  30. Aicardi J. Aicardi syndrome. Brain and development 2005;27(3):164–171. DOI: 10.1016/j.braindev.2003.11.011.
  31. Lund C, Bjørnvold M, Tuft M, et al. Aicardi syndrome: an epidemiologic and clinical study in Norway. Pediatr Neurol. 2015;52(2):182–186.e3. DOI: 10.1016/j.pediatrneurol.2014.10.022.
  32. Parrini E, Conti V, Dobyns WB, et al. Genetic basis of brain malformations. Mol Syndromol 2016;7(4):220–233. DOI: 10.1159/000448639.
  33. 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.
  34. Desikan RS, Barkovich AJ. Malformations of cortical development. Ann Neurol 2016;80(6):797–810. DOI: 10.1002/ana.24793.
  35. Barkovich J. Complication begets clarification in classification. Brain 2013;136(2):368–370. DOI: 10.1093/brain/awt001.
  36. 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.
  37. 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.
  38. 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.
  39. 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.
  40. 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.
  41. 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.
  42. 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.
  43. 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.
  44. 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.
  45. 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.
  46. 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.
  47. 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;87(1):40–51. DOI: 10.1016/j.ajhg.2010.06.003.
  48. 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.
  49. 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.
  50. Pooh RK. The role of imaging detection of congenital defects in the era of PGT-A and NIPT. J Perinat Med. 2019;47(s1):eA1–eA125. https://doi.org/10.1515/jpm-2019-2500.
  51. Pooh RK. Fetal brain imaging. Ultrasound Med Biol. 2017;43(Supp. 1):S132. DOI: 10.1016/j.ultrasmedbio.2017.08.1416.
  52. Pooh RK. Fetal neuroimaging of neural migration disorder. Ultrasound Clin. 2008;3(4):541–552. DOI: 10.1016/j.cult.2008.09.007.
  53. 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.
  54. 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.
  55. 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.
  56. 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.
  57. 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.
  58. 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.
  59. 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.
  60. 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.
  61. 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.
  62. 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.
  63. 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.
  64. 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.
  65. Folsom TD, Fatemi SH. The involvement of reelin in neurodevelopmental disorders. Neuropharmacology 2013;68:122–135. DOI: 10.1016/j.neuropharm.2012.08.015.
  66. Tissir F, Goffinet AM. Reelin and brain development. Nat Rev Neurosci 2003;4(6):496–505. DOI: 10.1038/nrn1113.
  67. 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.
  68. Kato M. Genotype-phenotype correlation in neuronal migration disorders and cortical dysplasias. Front Neurosci. 2015;9:181. DOI: 10.3389/fnins.2015.00181.
  69. 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.
  70. 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.
  71. 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.
  72. 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.
  73. 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.
  74. Di Donato N, Chiari S, Mirzaa GM, et al. Lissencephaly: expanded imaging and clinical classification. Am J Med Genet Part A. 2017;173(6):1473–1488. DOI: 10.1002/ajmg.a.38245.
  75. McGahan JP, Grix A, Gerscovich EO. Prenatal diagnosis of lissencephaly: Miller‐Dieker syndrome. J Clin Ultrasound 1994;22(9):560–563. DOI: 10.1002/jcu.1870220908.
  76. 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.
  77. 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;17:34–36. DOI: 10.1159/000048003.
  78. 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.
  79. 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.
  80. 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.
  81. 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.
  82. Manzini MC, Walsh CA. The genetics of brain malformations. Genet Neurodevelop Disord 2015:129–153. DOI: 10.1002/9781118524947.ch7.
  83. 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.
  84. 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.
  85. 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 14,3 223-226, 2014 10.2463/mrms.2014-0060). Magn Reson Med Sci 2015;14(4):373. DOI: 10.2463/mrms.2014-0060er.
  86. 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.
  87. 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.
  88. 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.
  89. 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.
  90. Kousi M, Katsanis N. The genetic basis of hydrocephalus. Annu Rev Neurosci. 2016;39:409–435. DOI: 10.1146/annurev-neuro-070815-014023.
  91. 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.
  92. 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.
  93. 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.
  94. 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;7(3):402–407. DOI: 10.1038/ng0794-402.
  95. 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.
  96. 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.
  97. 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–E1331. DOI: 10.1002/humu.21239.
  98. 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.
  99. 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.
  100. 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.
  101. 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.
  102. Mirzaa GM, Rivière JB, Dobyns WB. Megalencephaly syndromes and activating mutations in the PI3K-AKT pathway: MPPH and MCAP. Am J Med Genet Part C Semin Med Genet 2013(163C):122–130. DOI: 10.1002/ajmg.c.31361.
  103. 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.
  104. 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.
  105. 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.
  106. 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.
  107. 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 Gynecol 2006;45(2):135–141. DOI: 10.1016/S1028-4559(09)60211-4.
  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):20160253. DOI: 10.1259/bjr.20160253.
  109. Kutuk MS, Yikilmaz A, Ozgun MT, et al. Prenatal diagnosis and postnatal outcome of fetal intracranial hemorrhage. Child's Nerv Syst. 2014;30(3):411–418. DOI: 10.1007/s00381-013-2243-0.
  110. 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.
  111. Lichtenbelt KD, Pistorius LR, De Tollenaer SM, et al. Prenatal genetic confirmation of a COL4A1 mutation presenting with sonographic fetal intracranial hemorrhage. Ultrasound Obstet Gynecol 2012;39(6):726–727. DOI: 10.1002/uog.11070.
  112. Garel C, Rosenblatt J, Moutard ML, et al. Fetal intracerebral hemorrhage and COL4A1 mutation: promise and uncertainty. Ultrasound Obstet Gynecol 2013;41(2):228–230. DOI: 10.1002/uog.12268.
  113. Vermeulen RJ, Peeters-Scholte C, Van Vugt J, et al. Fetal origin of brain damage in 2 infants with a COL4A1 mutation: Fetal and eonatal MRI. Neuropediatrics 2011;42(1):1–3. DOI: 10.1055/s-0031-1284388.
  114. de Vries LS, Pistorius L, Lichtenbelt KD, et al. COL4A1 mutation: expansion of the phenotype. Pediatr Res 2011;70:181. DOI: 10.1038/pr.2011.406.
  115. Meuwissen MEC, Halley DJJ, Smit LS, et al. The expanding phenotype of COL4A1 and COL4A2 mutations: clinical data on 13 newly identified families and a review of the literature. Genet Med 2015;17(11):843–853. DOI: 10.1038/gim.2014.210.
  116. De Vries LS, Koopman C, Groenendaal F, et al. COL4A1 mutation in two preterm siblings with antenatal onset of parenchymal hemorrhage. Ann Neurol 2009;65(1):12–18. DOI: 10.1002/ana.21525.
  117. Colin E, Sentilhes L, Sarfati A, et al. Fetal intracerebral hemorrhage and cataract: think COL4A1. J Perinatol 2014;34(1):75–77. DOI: 10.1038/jp.2013.135.
  118. 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.
  119. Vergani P, Strobelt N, Locatelli A, et al. Clinical significance of fetal intracranial hemorrhage. Am J Obstet Gynecol. 1996;175(3 Pt 1):536–543. DOI: 10.1053/ob.1996.v175.a73598.
  120. Pooh RK, Kurjak A. Novel application of three-dimensional HDlive imaging in prenatal diagnosis from the first trimester. J Perinat Med 2015;43(2):147–158. DOI 10.1515/jpm-2014-0157.
  121. Pooh RK. Sonogenetics in fetal neurology. Semin Fetal Neonatal Med. 2012;17(6):353–359. DOI: 10.1016/j.siny.2012.07.005.
PDF Share
PDF Share

© Jaypee Brothers Medical Publishers (P) LTD.