Prenatal Diagnosis of Lissencephaly Type 2 using Three-dimensional Ultrasound and Fetal MRI: Case Report and Review of the Literature

Abstract

Lissencephaly is a genetic heterogeneous autosomal recessive disorder characterized by the classical triad: brain malformations, eye anomalies, and congenital muscular dystrophy. Prenatal diagnosis is feasible by demonstrating abnormal development of sulci and gyri. Magnetic resonance imaging (MRI) may enhance detection of developmental cortical disorders as well as ocular anomalies. We describe a case of early diagnosis of lissencephaly type 2 detected at the time of routine second trimester scan by three-dimensional ultrasound and fetal MRI. Gross pathology confirmed the accuracy of the prenatal diagnosis while histology showed the typical feature of cobblestone cortex. As the disease is associated with poor perinatal prognosis, early and accurate prenatal diagnosis is important for genetic counseling and antenatal care.

Resumo

Lissencefalia são doenças genéticas autossômicas recessivas heterogêneas caracterizadas pela tríade clássica: malformações do cérebro, anomalias oculares e distrofia muscular congênita. Diagnóstico pré-natal é factível pela demonstração do desenvolvimento anormal de sulcos e giros. Ressonância magnética (RM) melhora a detecção de distúrbios do desenvolvimento cortical, bem como as anomalias oculares. Descrevemos um caso de diagnóstico precoce de lisencefalia tipo 2 detectado no momento do ultrassom morfológico de segundo trimestre pela ultrassonografia tridimensional e RM fetal. A macroscopia confirmou a acurácia do diagnóstico pré-natal, enquanto que a microscopia mostrou a típica característica de córtex em cobblestone. Como a doença está associada à um pobre prognóstico perinatal, o precoce e acurado diagnóstico pré-natal é importante para o aconselhamento genético e seguimento da gestação.

Keywords

lissencephaly - cobblestone cortex - genetic counseling - magnetic resonance imaging - pathology - prenatal diagnosis - three-dimensional ultrasound

Palavras-chave

lisencefalia - cobblestone córtex - aconselhamento genético - ressonância magnética - patologia - diagnóstico pré-natal - ultrassom tridimensional

Note

Study performed at the Dipartimento di Ostetricia e Ginecologia, Ospedale Civile di Guastalla, AUSL Reggio Emilia, Reggio Emilia, Italy.

• References

• 1 Vajsar J, Schachter H. Walker-Warburg syndrome. Orphanet J Rare Dis 2006; 1: 29
• 2 Walker W. Lissencephaly. Arch Neurol Psychiatry 1942; 48 (1) 13-29
• 3 Monteagudo A, Alayón A, Mayberry P. Walker-Warburg syndrome: case report and review of the literature. J Ultrasound Med 2001; 20 (4) 419-426
• 4 Blin G, Rabbé A, Ansquer Y, Meghdiche S, Floch-Tudal C, Mandelbrot L. First-trimester ultrasound diagnosis in a recurrent case of Walker-Warburg syndrome. Ultrasound Obstet Gynecol 2005; 26 (3) 297-299
• 5 Vuillaumier-Barrot S, Bouchet-Séraphin C, Chelbi M , et al. Identification of mutations in TMEM5 and ISPD as a cause of severe cobblestone lissencephaly. Am J Hum Genet 2012; 91 (6) 1135-1143
• 6 Hansen DV, Lui JH, Parker PR, Kriegstein AR. Neurogenic radial glia in the outer subventricular zone of human neocortex. Nature 2010; 464 (7288) 554-561
• 7 Siegenthaler JA, Pleasure SJ. We have got you ‘covered’: how the meninges control brain development. Curr Opin Genet Dev 2011; 21 (3) 249-255
• 8 Labelle-Dumais C, Dilworth DJ, Harrington EP , et al. COL4A1 mutations cause ocular dysgenesis, neuronal localization defects, and myopathy in mice and Walker-Warburg syndrome in humans. PLoS Genet 2011; 7 (5) e1002062
• 9 Costell M, Gustafsson E, Aszódi A , et al. Perlecan maintains the integrity of cartilage and some basement membranes. J Cell Biol 1999; 147 (5) 1109-1122
• 10 Luo R, Jeong SJ, Jin Z, Strokes N, Li S, Piao X. G protein-coupled receptor 56 and collagen III, a receptor-ligand pair, regulates cortical development and lamination. Proc Natl Acad Sci U S A 2011; 108 (31) 12925-12930
• 11 Beltrán-Valero de Bernabé D, Currier S, Steinbrecher A , et al. Mutations in the O-mannosyltransferase gene POMT1 give rise to the severe neuronal migration disorder Walker-Warburg syndrome. Am J Hum Genet 2002; 71 (5) 1033-1043
• 12 van Reeuwijk J, Grewal PK, Salih MA , et al. Intragenic deletion in the LARGE gene causes Walker-Warburg syndrome. Hum Genet 2007; 121 (6) 685-690
• 13 Godfrey C, Escolar D, Brockington M , et al. Fukutin gene mutations in steroid-responsive limb girdle muscular dystrophy. Ann Neurol 2006; 60 (5) 603-610
• 14 Lee J, Gross JM. Laminin beta1 and gamma1 containing laminins are essential for basement membrane integrity in the zebrafish eye. Invest Ophthalmol Vis Sci 2007; 48 (6) 2483-2490
• 15 Radmanesh F, Caglayan AO, Silhavy JL , et al. Mutations in LAMB1 cause cobblestone brain malformation without muscular or ocular abnormalities. Am J Hum Genet 2013; 92 (3) 468-474
• 16 Cohen-Sacher B, Lerman-Sagie T, Lev D, Malinger G. Sonographic developmental milestones of the fetal cerebral cortex: a longitudinal study. Ultrasound Obstet Gynecol 2006; 27 (5) 494-502
• 17 Rolo LC, Araujo Júnior E, Nardozza LM, de Oliveira PS, Ajzen SA, Moron AF. Development of fetal brain sulci and gyri: assessment through two and three-dimensional ultrasound and magnetic resonance imaging. Arch Gynecol Obstet 2011; 283 (2) 149-158
• 18 van der Knaap MS, Valk J. Classification of congenital abnormalities of the CNS. AJNR Am J Neuroradiol 1988; 9 (2) 315-326
• 19 Fong KW, Ghai S, Toi A, Blaser S, Winsor EJ, Chitayat D. 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
• 20 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
• 21 Allias F, Buenerd A, Bouvier R , et al. The spectrum of type III lissencephaly: a clinicopathological update. Fetal Pediatr Pathol 2004; 23 (5–6) 305-317
• 22 Crowe C, Jassani M, Dickerman L. The prenatal diagnosis of the Walker-Warburg syndrome. Prenat Diagn 1986; 6 (3) 177-185
• 23 Rodgers BL, Vanner LV, Pai GS, Sens MA. Walker-Warburg syndrome: report of three affected sibs. Am J Med Genet 1994; 49 (2) 198-201
• 24 Chitayat D, Toi A, Babul R , et al. Prenatal diagnosis of retinal nonattachment in the Walker-Warburg syndrome. Am J Med Genet 1995; 56 (4) 351-358
• 25 Gasser B, Lindner V, Dreyfus M , et al. Prenatal diagnosis of Walker-Warburg syndrome in three sibs. Am J Med Genet 1998; 76 (2) 107-110
• 26 Malinger G, Kidron D, Schreiber L , et al. Prenatal diagnosis of malformations of cortical development by dedicated neurosonography. Ultrasound Obstet Gynecol 2007; 29 (2) 178-191
• 27 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
• 28 Strigini F, Valleriani A, Cecchi M , et al. Prenatal ultrasound and magnetic resonance imaging features in a fetus with Walker-Warburg syndrome. Ultrasound Obstet Gynecol 2009; 33 (3) 363-365
• 29 Tonni G, Grisolia G. Dilated intracranial translucency and Blake's pouch cyst: first-trimester ultrasound markers of occipital cephalocele diagnosed using novel three-dimensional reslicing technique. J Clin Ultrasound 2014; 42 (3) 157-161
• 30 Tonni G, Grisolia G, Sepulveda W. Second trimester fetal neurosonography: reconstructing cerebral midline anatomy and anomalies using a novel three-dimensional ultrasound technique. Prenat Diagn 2014; 34 (1) 75-83
• 31 Haratz KK, Oliveira PS, Rolo LC , et al. Fetal cerebral ventricle volumetry: comparison between 3D ultrasound and magnetic resonance imaging in fetuses with ventriculomegaly. J Matern Fetal Neonatal Med 2011; 24 (11) 1384-1391
• 32 Abe S, Takagi K, Yamamoto T, Okuhata Y, Kato T. Assessment of cortical gyrus and sulcus formation using MR images in normal fetuses. Prenat Diagn 2003; 23 (3) 225-231
• 33 Ghai S, Fong KW, Toi A, Chitayat D, Pantazi S, Blaser S. Prenatal US and MR imaging findings of lissencephaly: review of fetal cerebral sulcal development. Radiographics 2006; 26 (2) 389-405
• 34 Hoffman JD, Park JJ, Schreiber-Agus N , et al. The Ashkenazi Jewish carrier screening panel: evolution, status quo, and disparities. Prenat Diagn 2014; 34 (12) 1161-1167
• 35 Lacalm A, Nadaud B, Massoud M, Putoux A, Gaucherand P, Guibaud L. Prenatal diagnosis of cobblestone lissencephaly associated with Walker-Warburg syndrome based on a specific sonographic pattern. Ultrasound Obstet Gynecol 2016; 47 (1) 117-122
• 36 Harwood-Nash DC, Fitz CR. Neuroradiology in Infants and Children. St. Louis: Mosby; 1976
• 37 Tonni G, Grisolia G. Ultrasound diagnosis of central nervous system anomalies (bifid choroid plexus, ventriculomegaly, Dandy-Walker malformation) associated with multicystic dysplastic kidney disease in a trisomy 9 fetus: case report with literature review. J Clin Ultrasound 2013; 41 (7) 441-447
• 38 Dattani MT, Martinez-Barbera JP, Thomas PQ , et al. Mutations in the homeobox gene HESX1/Hesx1 associated with septo-optic dysplasia in human and mouse. Nat Genet 1998; 19 (2) 125-133