Case Report of Proliferative Peripheral Retinopathy in Two Familial Lissencephaly Infants with Miller–Dieker Syndrome

Abstract

A complete ophthalmic examination is not routinely performed on infants with Miller–Dieker syndrome (MDS, chromosome 17p13.3 microdeletion). The authors present the cases of four cousins with MDS who also carried a 16p13.3 microduplication (not associated with Rubinstein–Taybi syndrome). Retinopathy of prematurity-like proliferative peripheral retinopathy (PPR) was detected in two male first cousins, but was not detected in the female half-cousins. PPR in the first infant resolved by 4 months, but the second infant's PPR progressed, requiring photocoagulation followed by lens-sparing vitrectomy. While ocular abnormalities are more prevalent and severe in other lissencephalopathies, the PPR in these MDS infants underscores the sight-saving potential of performing an ophthalmologic exam with early molecular testing for all lissencephaly infants.

Keywords

agyria - LIS1 gene - pediatric - PDIA2 - retina - SERPINF1

Availability of Data and Materials

All the data supporting the findings of this study are available from the LSU Health, Shreveport, but restrictions apply to the availability of these data, which were used under the Internal Review Board (IRB) approval for the current study, and so are not publicly available. However, data are available upon reasonable request from the author(s) and with permission of the LSU Health, Shreveport IRB.

Authors' Contributions

O.S.: Patient interaction, literature research, and initial drafting of the manuscript. A.B.R.: Patient interaction, patient diagnosis, literature research, critical revision, and language editing. L.A.P.: Literature research, evaluated the gene analysis, and made critical revision. J.H.: Patient interaction and patient diagnosis. W.R.S.: Operated on the patient, consented, and took the fundus photographs. M.P.L.: Literature research, critical revision, language editing, drafting, and submission of the manuscript. All authors have read and approved the final manuscript.

Note

Written informed consent was obtained from the parents for publication of the accompanying deidentified images.

Ethics Approval and Consent to Participate

This study was approved by the Ethics Committee of the LSU Health Sciences Center, Shreveport (FWA 00000653), and adheres to the tenets of the Declaration of Helsinki.

• References

• 1 Spalice A, Parisi P, Nicita F, Pizzardi G, Del Balzo F, Iannetti P. Neuronal migration disorders: clinical, neuroradiologic and genetics aspects. Acta Paediatr 2009; 98 (03) 421-433
• 2 Banna M, Malabarey T. Lissencephaly and pachygyria. Can Assoc Radiol J 1989; 40 (03) 156-158
• 3 Dobyns WB, Das S. LIS1-associated lissencephaly/subcortical band heterotopia. 2009 Mar 3. In: Pagon RA, Adam MP, Ardinger HH. , et al, eds. GeneReviews® [Internet]. Seattle, WA: University of Washington, Seattle; 1993. –2014. Available at: http://www.ncbi.nlm.nih.gov/books/NBK5189/ . Accessed March 2015
• 4 De Wilde G, Hansens M, Govaert P. The Walker-Warburg syndrome. Bull Soc Belge Ophtalmol 1992; 243: 129-138
• 5 Nabi NU, Mezer E, Blaser SI, Levin AA, Buncic JR. Ocular findings in lissencephaly. J AAPOS 2003; 7 (03) 178-184
• 6 Bosch DG, Boonstra FN, Reijnders MR, Pfundt R, Cremers FP, de Vries BB. Chromosomal aberrations in cerebral visual impairment. Eur J Paediatr Neurol 2014; 18 (06) 677-684
• 7 Marqués-Fernández VE, Sánchez-Tocino H, Escudero-Caro MT, Cancho-Candela R, García-Zamora M. Visual impairment due to lissencephaly. Neuroophthalmology 2016; 40 (05) 229-233
• 8 Di Donato N, Chiari S, Mirzaa GM. , et al. Lissencephaly: expanded imaging and clinical classification. Am J Med Genet A 2017; 173 (06) 1473-1488
• 9 Verloes A, Elmaleh M, Gonzales M, Laquerrière A, Gressens P. Genetic and clinical aspects of lissencephaly [in French]. Rev Neurol (Paris) 2007; 163 (05) 533-547
• 10 Dobyns WB, McCluggage CW. Computed tomographic appearance of lissencephaly syndromes. Am J Neuroradiol 1985; 6 (04) 545-550
• 11 Dobyns WB, Reiner O, Carrozzo R, Ledbetter DH. Lissencephaly. A human brain malformation associated with deletion of the LIS1 gene located at chromosome 17p13. JAMA 1993; 270 (23) 2838-2842
• 12 Cardoso C, Leventer RJ, Dowling JJ. , et al. Clinical and molecular basis of classical lissencephaly: mutations in the LIS1 gene (PAFAH1B1). Hum Mutat 2002; 19 (01) 4-15
• 13 Noor A, Bogatan S, Watkins N, Meschino WS, Stavropoulos DJ. Disruption of YWHAE gene at 17p13.3 causes learning disabilities and brain abnormalities. Clin Genet 2018; 93 (02) 365-367
• 14 Pilz DT, Matsumoto N, Minnerath S. , et al. LIS1 and XLIS (DCX) mutations cause most classical lissencephaly, but different patterns of malformation. Hum Mol Genet 1998; 7 (13) 2029-2037
• 15 Cardoso C, Leventer RJ, Ward HL. , et al. Refinement of a 400-kb critical region allows genotypic differentiation between isolated lissencephaly, Miller-Dieker syndrome, and other phenotypes secondary to deletions of 17p13.3. Am J Hum Genet 2003; 72 (04) 918-930
• 16 Kato M. Genotype-phenotype correlation in neuronal migration disorders and cortical dysplasias. Front Neurosci 2015; 9: 181
• 17 Dobyns WB, Truwit CL. Lissencephaly and other malformations of cortical development: 1995 update. Neuropediatrics 1995; 26 (03) 132-147
• 18 Mano N, Mitsutsuji T, Yoshikawa Y. , et al. Optical coherence tomography in an infant with Walker-Warburg Syndrome. Case Rep Ophthalmol 2015; 6 (02) 210-215
• 19 Hodgkins PR, Kriss A, Boyd S. , et al. A study of EEG, electroretinogram, visual evoked potential, and eye movements in classical lissencephaly. Dev Med Child Neurol 2000; 42 (01) 48-52
• 20 Kim SR, Kim HJ, Kim YJ, Kwon JY, Kim JW, Kim SH. Cryptic microdeletion of the CREBBP gene from t(1;16) (p36.2;p13.3) as a novel genetic defect causing Rubinstein-Taybi syndrome. Ann Clin Lab Sci 2013; 43 (04) 450-456
• 21 de Rijk-van Andel JF, Arts WF, Hofman A, Staal A, Niermeijer MF. Epidemiology of lissencephaly type I. Neuroepidemiology 1991; 10 (04) 200-204
• 22 de Wit MC, de Rijk-van Andel J, Halley DJ. , et al. Long-term follow-up of type 1 lissencephaly: survival is related to neuroimaging abnormalities. Dev Med Child Neurol 2011; 53 (05) 417-421
• 23 Tombran-Tink J, Barnstable CJ. PEDF: a multifaceted neurotrophic factor. Nat Rev Neurosci 2003; 4 (08) 628-636
• 24 Dawson DW, Volpert OV, Gillis P. , et al. Pigment epithelium-derived factor: a potent inhibitor of angiogenesis. Science 1999; 285 (5425): 245-248
• 25 Tombran-Tink J. PEDF in angiogenic eye diseases. Curr Mol Med 2010; 10 (03) 267-278
• 26 Peña E, Arderiu G, Badimon L. Protein disulphide-isomerase A2 regulated intracellular tissue factor mobilisation in migrating human vascular smooth muscle cells. Thromb Haemost 2015; 113 (04) 891-902
• 27 Civelek M, Lusis AJ. Systems genetics approaches to understand complex traits. Nat Rev Genet 2014; 15 (01) 34-48
• 28 Rosenfeld JA, Patel A. Chromosomal microarrays: understanding genetics of neurodevelopmental disorders and congenital anomalies. J Pediatr Genet 2017; 6 (01) 42-50