Advertisement

Syndromic Disorders

  • Alfonso Senatore
  • Wajiha Jurdi Kheir
  • Minzhong YuEmail author
  • Alessandro Racioppi
  • Roberto Gattegna
  • Donnell Creel
  • Alessandro Iannaccone
Chapter
  • 99 Downloads

Abstract

This chapter summarizes the application of visual electrophysiology in syndromic disorders involving the retina. The characteristics of electroretinogram (ERG) and/or electrooculogram (EOG) and/or visual evoked potential (VEP) are described in Usher syndrome, Refsum disease, Wolfram syndrome, Kearns–Sayre syndrome, neuropathy–ataxia–retinitis pigmentosa syndrome, maternally inherited diabetes and deafness syndrome (MIDD), Bardet–Biedl syndrome, Alström syndrome, Cohen syndrome, Cockayne syndrome, Alagille syndrome, Senior–Loken syndrome, Joubert syndrome, abetalipoproteinemia (Bassen–Kornzweig syndrome), neuronal ceroid lipofuscinoses (Batten’s disease), and mucopolysaccharidosis.

Keywords

Electroretinogram Electrooculogram Usher syndrome Refsum disease Wolfram syndrome Kearns–Sayre syndrome Neuropathy–ataxia–retinitis pigmentosa syndrome Maternally inherited diabetes and Deafness syndrome Bardet–Biedl syndrome Alström syndrome Cohen syndrome Cockayne syndrome Alagille syndrome Senior–Loken Syndrome Joubert syndrome Abetalipoproteinemia (Bassen-Kornzweig syndrome) Neuronal ceroid lipofuscinoses (Batten’s disease) Mucopolysaccharidosis 

References

  1. 1.
    Iannaccone A, Berdia J. Retinitis pigmentosa. Danbury: National Organization for Rare Disorder; 2017. Review No. 21.Google Scholar
  2. 2.
    Smith RJ, et al. Clinical diagnosis of the Usher syndromes. Usher Syndrome Consortium. Am J Med Genet. 1994;50(1):32–8.PubMedGoogle Scholar
  3. 3.
    Iannaccone A, et al. Clinical and immunohistochemical evidence for an X linked retinitis pigmentosa syndrome with recurrent infections and hearing loss in association with an RPGR mutation. J Med Genet. 2003;40(11):e118.PubMedPubMedCentralGoogle Scholar
  4. 4.
    Iannaccone A, et al. Retinal phenotype of an X-linked pseudo-Usher syndrome in association with the G173R mutation in the RPGR gene. Adv Exp Med Biol. 2008;613:221–7.PubMedGoogle Scholar
  5. 5.
    Edwards A, et al. Visual acuity and visual field impairment in Usher syndrome. Arch Ophthalmol. 1998;116(2):165–8.PubMedGoogle Scholar
  6. 6.
    Fishman GA, et al. Prevalence of foveal lesions in type 1 and type 2 Usher’s syndrome. Arch Ophthalmol. 1995;113:770–3.PubMedGoogle Scholar
  7. 7.
    Iannaccone A. Usher syndrome: correlation between visual field size and maximal ERG response b-wave amplitude. In: LaVail MM, Hollyfield JG, Anderson RE, editors. Retinal degenerations: mechanisms and experimental therapy. New York: Plenum Publishers; 2003. p. 123–31.Google Scholar
  8. 8.
    Iannaccone A, et al. Kinetics of visual field loss in Usher syndrome Type II. Invest Ophthalmol Vis Sci. 2004;45(3):784–92.PubMedGoogle Scholar
  9. 9.
    Herrera W, et al. Retinal disease in Usher syndrome III caused by mutations in the clarin-1 gene. Invest Ophthalmol Vis Sci. 2008;49(6):2651–60.PubMedGoogle Scholar
  10. 10.
    Refsum S, Salomonsen L, Skatvedt M. Heredopathia atactica polyneuritiformis in children. J Pediatr. 1949;35:335–43.PubMedGoogle Scholar
  11. 11.
    Wanders RJA, Waterham HR, Leroy BP. Refsum disease. In: Adam MP, et al., editors. GeneReviews(R). University of Washington, Seattle; 1993.Google Scholar
  12. 12.
    Gibberd FB, et al. Heredopathia atactica polyneuritiformis (refsum’s disease) treated by diet and plasma-exchange. Lancet. 1979;1(8116):575–8.PubMedGoogle Scholar
  13. 13.
    Strom TM, et al. Diabetes insipidus, diabetes mellitus, optic atrophy and deafness (DIDMOAD) caused by mutations in a novel gene (wolframin) coding for a predicted transmembrane protein. Hum Mol Genet. 1998;7(13):2021–8.PubMedGoogle Scholar
  14. 14.
    Inoue H, et al. A gene encoding a transmembrane protein is mutated in patients with diabetes mellitus and optic atrophy (Wolfram syndrome). Nat Genet. 1998;20:143–8.PubMedGoogle Scholar
  15. 15.
    Mozzillo E, et al. A novel CISD2 intragenic deletion, optic neuropathy and platelet aggregation defect in Wolfram syndrome type 2. BMC Med Genet. 2014;15:88.PubMedPubMedCentralGoogle Scholar
  16. 16.
    Amr S, et al. A homozygous mutation in a novel zinc-finger protein, ERIS, is responsible for Wolfram syndrome 2. Am J Hum Genet. 2007;81(4):673–83.PubMedPubMedCentralGoogle Scholar
  17. 17.
    Lucariello A, et al. Modulation of wolframin expression in human placenta during pregnancy: comparison among physiological and pathological states. Biomed Res Int. 2014;2014:985478.PubMedPubMedCentralGoogle Scholar
  18. 18.
    De Falco M, et al. Localization and distribution of wolframin in human tissues. Front Biosci (Elite Ed). 2012;4:1986–98.Google Scholar
  19. 19.
    Borgna-Pignatti C, et al. Thiamine-responsive anemia in DIDMOAD syndrome. J Pediatr. 1989;114(3):405–10.PubMedGoogle Scholar
  20. 20.
    Kozak I, et al. New observations regarding the retinopathy of genetically confirmed Kearns-Sayre syndrome. Retin Cases Brief Rep. 2018 Fall;12(4):349–58.PubMedGoogle Scholar
  21. 21.
    Proto F, et al. Kearns-Sayre syndrome (KSS): case report and review of the literature [Italian]. Ann Ottalmol Clin Ocul. 1994;120:149–54.Google Scholar
  22. 22.
    Ohkoshi K, et al. Corneal endothelium in a case of mitochondrial encephalomyopathy (Kearns-Sayre syndrome). Cornea. 1989;8(3):210–4.PubMedGoogle Scholar
  23. 23.
    Finsterer J, Zarrouk-Mahjoub S. Corneal involvement in Kearns-Sayre syndrome responsive to coenzyme-Q? Cornea. 2016;35(12):e39.PubMedGoogle Scholar
  24. 24.
    Kim J, et al. Coenzyme Q10 in the treatment of corneal edema in Kearns-Sayre: is there an application in fuchs endothelial corneal dystrophy? Cornea. 2016;35(9):1250–4.PubMedGoogle Scholar
  25. 25.
    Ota I, Miyake Y, Awaya S. Studies of ocular fundus and visual functions in Kearns-Sayre syndrome – with special reference to the new stage classification. Nippon Ganka Gakkai Zasshi. 1989;93(3):329–38.PubMedGoogle Scholar
  26. 26.
    Holt IJ, et al. A new mitochondrial disease associated with mitochondrial DNA heteroplasmy. Am J Hum Genet. 1990;46(3):428–33.PubMedPubMedCentralGoogle Scholar
  27. 27.
    Chowers I, et al. Cone and rod dysfunction in the NARP syndrome. Br J Ophthalmol. 1999;83(2):190–3.PubMedPubMedCentralGoogle Scholar
  28. 28.
    Fryer A, et al. Mitochondrial DNA 8993 (NARP) mutation presenting with a heterogeneous phenotype including ‘cerebral palsy’. Arch Dis Child. 1994;71(5):419–22.PubMedPubMedCentralGoogle Scholar
  29. 29.
    Lemoine S, et al. Renal involvement in neuropathy, ataxia, retinitis pigmentosa (NARP) syndrome: a case report. Am J Kidney Dis. 2018;71(5):754–7.PubMedGoogle Scholar
  30. 30.
    Reardon W, et al. Diabetes mellitus associated with a pathogenic point mutation in mitochondrial DNA. Lancet. 1992;340(8832):1376–9.PubMedGoogle Scholar
  31. 31.
    Ballinger SW, et al. Maternally transmitted diabetes and deafness associated with a 10.4 kb mitochondrial DNA deletion. Nat Genet. 1992;1(1):11–5.PubMedGoogle Scholar
  32. 32.
    Guillausseau PJ, et al. Maternally inherited diabetes and deafness: a multicenter study. Ann Intern Med. 2001;134(9 Pt 1):721–8.PubMedGoogle Scholar
  33. 33.
    Massin P, et al. Prevalence of macular pattern dystrophy in maternally inherited diabetes and deafness. GEDIAM Group. Ophthalmology. 1999;106(9):1821–7.PubMedGoogle Scholar
  34. 34.
    Ogun O, Sheldon C, Barton JJ. Pearls & oy-sters: maternally inherited diabetes and deafness presenting with ptosis and macular pattern dystrophy. Neurology. 2012;79(6):e54–6.PubMedPubMedCentralGoogle Scholar
  35. 35.
    Feigl B, Morris CP. Visual function and risk genotypes in maternally inherited diabetes and deafness. Can J Ophthalmol. 2013;48(5):e111–4.PubMedGoogle Scholar
  36. 36.
    Rath PP, et al. Characterisation of the macular dystrophy in patients with the A3243G mitochondrial DNA point mutation with fundus autofluorescence. Br J Ophthalmol. 2008;92(5):623–9.PubMedPubMedCentralGoogle Scholar
  37. 37.
    Strauss DS, Freund KB. Diagnosis of maternally inherited diabetes and deafness (mitochondrial A3243G mutation) based on funduscopic appearance in an asymptomatic patient. Br J Ophthalmol. 2012;96(4):604.PubMedGoogle Scholar
  38. 38.
    Bellmann C, et al. Localized retinal electrophysiological and fundus autofluorescence imaging abnormalities in maternal inherited diabetes and deafness. Invest Ophthalmol Vis Sci. 2004;45(7):2355–60.PubMedGoogle Scholar
  39. 39.
    Iannaccone A. The genetics of hereditary retinopathies and optic neuropathies. Comp Ophthalmol Update. 2005;5:39–62.Google Scholar
  40. 40.
    Iannaccone A, et al. Clinical evidence of decreased olfaction in Bardet-Biedl syndrome caused by a deletion in the BBS4 gene. Am J Med Genet A. 2005;132(4):343–6.Google Scholar
  41. 41.
    Barnett S, et al. Behavioural phenotype of Bardet-Biedl syndrome. J Med Genet. 2002;39(12):e76.PubMedPubMedCentralGoogle Scholar
  42. 42.
    Adams NA, Awadein A, Toma HS. The retinal ciliopathies. Ophthalmic Genet. 2007;28(3):113–25.PubMedGoogle Scholar
  43. 43.
    RetNet – Retinal Information Network., https://sph.uth.edu/retnet/home.htm. 2019.
  44. 44.
    Iannaccone A, et al. Electroretinographic alterations in the Laurence-Moon-Bardet-Biedl phenotype. Acta Ophthalmol Scand. 1996;74:8–13.PubMedGoogle Scholar
  45. 45.
    Iannaccone A, et al. The ocular phenotype of the Bardet-Biedl syndrome. Comparison to non-syndromic retinitis pigmentosa. Ophthalmic Genet. 1997;18:13–26.PubMedGoogle Scholar
  46. 46.
    Cox KF, et al. Phenotypic expression of Bardet-Biedl syndrome in patients homozygous for the common M390R mutation in the BBS1 gene. Vision Res. 2012;75:77–87.PubMedGoogle Scholar
  47. 47.
    Praidou A, et al. Multifocal electroretinogram contributes to differentiation of various clinical pictures within a family with Bardet-Biedl syndrome. Eye (Lond). 2014;28(9):1136–42.Google Scholar
  48. 48.
    Forte R, et al. The optic nerve in patients with the Laurence-Moon-Bardet-Biedl phenotype: a clinical and functional study. [Italian]. Boll Ocul. 1996;75(Suppl 4):115–24.Google Scholar
  49. 49.
    Marshall JD, et al. Spectrum of ALMS1 variants and evaluation of genotype-phenotype correlations in Alstrom syndrome. Hum Mutat. 2007;28(11):1114–23.PubMedGoogle Scholar
  50. 50.
    Marshall JD, et al. Alstrom syndrome: genetics and clinical overview. Curr Genomics. 2011;12(3):225–35.PubMedPubMedCentralGoogle Scholar
  51. 51.
    Marshall JD, et al. Alstrom syndrome. Eur J Hum Genet. 2007;15(12):1193–202.PubMedGoogle Scholar
  52. 52.
    Hearn T. ALMS1 and Alstrom syndrome: a recessive form of metabolic, neurosensory and cardiac deficits. J Mol Med (Berl). 2019;97(1):1–17.Google Scholar
  53. 53.
    Collin GB, et al. Alms1-disrupted mice recapitulate human Alstrom syndrome. Hum Mol Genet. 2005;14(16):2323–33.PubMedPubMedCentralGoogle Scholar
  54. 54.
    Katagiri S, et al. Whole-exome sequencing identifies a novel ALMS1 mutation (p.Q2051X) in two Japanese brothers with Alstrom syndrome. Mol Vis. 2013;19:2393–406.PubMedPubMedCentralGoogle Scholar
  55. 55.
    Karska-Basta I, et al. Alstrom syndrome – a case report and literature review. Klin Ocz. 2008;110(4–6):188–92.Google Scholar
  56. 56.
    Malm E, et al. Full-field electroretinography and marked variability in clinical phenotype of Alstrom syndrome. Arch Ophthalmol. 2008;126(1):51–7.PubMedGoogle Scholar
  57. 57.
    Sadowski B, et al. Onset of bilateral blindness in the first year of life. Alstrom syndrome. Ophthalmologe. 2004;101(3):298–300.PubMedGoogle Scholar
  58. 58.
    Hung YJ, et al. Alstrom syndrome in two siblings. J Formos Med Assoc. 2001;100(1):45–9.PubMedGoogle Scholar
  59. 59.
    Russell-Eggitt IM, et al. Alstrom syndrome. Report of 22 cases and literature review. Ophthalmology. 1998;105(7):1274–80.PubMedGoogle Scholar
  60. 60.
    Michaud JL, et al. Natural history of Alstrom syndrome in early childhood: onset with dilated cardiomyopathy. J Pediatr. 1996;128(2):225–9.PubMedGoogle Scholar
  61. 61.
    Tremblay F, et al. Longitudinal study of the early electroretinographic changes in Alstrom’s syndrome. Am J Ophthalmol. 1993;115(5):657–65.PubMedGoogle Scholar
  62. 62.
    Sheck L, et al. Alstrom syndrome – an uncommon cause of early childhood retinal dystrophy. BMJ Case Rep. 2011;2011.Google Scholar
  63. 63.
    Chandler KE, et al. Diagnostic criteria, clinical characteristics, and natural history of Cohen syndrome. J Med Genet. 2003;40(4):1–3.PubMedPubMedCentralGoogle Scholar
  64. 64.
    Kolehmainen J, et al. Cohen syndrome is caused by mutations in a novel gene, COH1, encoding a transmembrane protein with a presumed role in vesicle-mediated sorting and intracellular protein transport. Am J Hum Genet. 2003;72(6):1359–69.PubMedPubMedCentralGoogle Scholar
  65. 65.
    Wang H, et al. Cohen syndrome. In: Pagon RA, et al., editors. GeneReviews(R). University of Washington, Seattle; 1993.Google Scholar
  66. 66.
    Dastan J, et al. Exome sequencing identifies pathogenic variants of VPS13B in a patient with familial 16p11.2 duplication. BMC Med Genet. 2016;17(1):78.PubMedPubMedCentralGoogle Scholar
  67. 67.
    Gillentine MA, Schaaf CP, Patel A. The importance of phase analysis in multiexon copy number variation detected by aCGH in autosomal recessive disorder loci. Am J Med Genet A. 2017;173(9):2485–8.PubMedPubMedCentralGoogle Scholar
  68. 68.
    Rodrigues JM, et al. Cohen syndrome: review of the literature. Cureus. 2018;10(9):e3330.PubMedPubMedCentralGoogle Scholar
  69. 69.
    Parri V, et al. High frequency of COH1 intragenic deletions and duplications detected by MLPA in patients with Cohen syndrome. Eur J Hum Genet. 2010;18(10):1133–40.PubMedPubMedCentralGoogle Scholar
  70. 70.
    Yang C, et al. Gene analysis: a rare gene disease of intellectual deficiency-Cohen syndrome. Int J Dev Neurosci. 2018;68:83–8.PubMedGoogle Scholar
  71. 71.
    Chandler KE, et al. The ophthalmic findings in Cohen syndrome. Br J Ophthalmol. 2002;86(12):1395–8.PubMedPubMedCentralGoogle Scholar
  72. 72.
    Hennies HC, et al. Allelic heterogeneity in the COH1 gene explains clinical variability in Cohen syndrome. Am J Hum Genet. 2004;75(1):138–45.PubMedPubMedCentralGoogle Scholar
  73. 73.
    Hanawalt PC, DNA r. The bases for Cockayne syndrome. Nature. 2000;405(6785):415–6.PubMedGoogle Scholar
  74. 74.
    Friedberg EC. Cockayne syndrome – a primary defect in DNA repair, transcription, both or neither? BioEssays. 1996;18(9):731–8.PubMedGoogle Scholar
  75. 75.
    Venema J, et al. The genetic defect in Cockayne syndrome is associated with a defect in repair of UV-induced DNA damage in transcriptionally active DNA. Proc Natl Acad Sci U S A. 1990;87(12):4707–11.PubMedPubMedCentralGoogle Scholar
  76. 76.
    Stefanini M, et al. Genetic analysis of twenty-two patients with Cockayne syndrome. Hum Genet. 1996;97(4):418–23.PubMedGoogle Scholar
  77. 77.
    Ozdirim E, et al. Cockayne syndrome: review of 25 cases. Pediatr Neurol. 1996;15(4):312–6.PubMedGoogle Scholar
  78. 78.
    Dollfus H, et al. Ocular manifestations in the inherited DNA repair disorders. Surv Ophthalmol. 2003;48(1):107–22.PubMedGoogle Scholar
  79. 79.
    Scaioli V, D’Arrigo S, Pantaleoni C. Unusual neurophysiological features in Cockayne’s syndrome: a report of two cases as a contribution to diagnosis and classification. Brain and Development. 2004;26(4):273–80.PubMedGoogle Scholar
  80. 80.
    Ikeda N, et al. Nondetectable cone and rod electroretinographic responses in a patient with Cockayne syndrome. Jpn J Ophthalmol. 1995;39(4):420–3.PubMedGoogle Scholar
  81. 81.
    Schalk A, et al. Deep intronic variation in splicing regulatory element of the ERCC8 gene associated with severe but long-term survival Cockayne syndrome. Eur J Hum Genet. 2018;26(4):527–36.PubMedPubMedCentralGoogle Scholar
  82. 82.
    Alagille D, et al. Hepatic ductular hypoplasia associated with characteristic facies, vertebral malformations, retarded physical, mental, and sexual development, and cardiac murmur. J Pediatr. 1975;86(1):63–71.PubMedGoogle Scholar
  83. 83.
    Oda T, et al. Mutations in the human Jagged1 gene are responsible for Alagille syndrome. Nat Genet. 1997;16(3):235–42.PubMedGoogle Scholar
  84. 84.
    Kamath BM, et al. NOTCH2 mutations in Alagille syndrome. J Med Genet. 2012;49(2):138–44.PubMedGoogle Scholar
  85. 85.
    Grochowski CM, Loomes KM, Spinner NB. Jagged1 (JAG1): structure, expression, and disease associations. Gene. 2016;576(1 Pt 3):381–4.PubMedGoogle Scholar
  86. 86.
    Emerick KM, et al. Features of Alagille syndrome in 92 patients: frequency and relation to prognosis. Hepatology. 1999;29(3):822–9.PubMedGoogle Scholar
  87. 87.
    Kamath BM, et al. Facial features in Alagille syndrome: specific or cholestasis facies? Am J Med Genet. 2002;112(2):163–70.PubMedGoogle Scholar
  88. 88.
    Puklin JE, et al. Anterior segment and retinal pigmentary abnormalities in arteriohepatic dysplasia. Ophthalmology. 1981;88(4):337–47.PubMedGoogle Scholar
  89. 89.
    Romanchuk KG, Judisch GF, LaBrecque DR. Ocular findings in arteriohepatic dysplasia (Alagille’s syndrome). Can J Ophthalmol. 1981;16(2):94–9.PubMedGoogle Scholar
  90. 90.
    Mayer U, Grosse KP. [Clinical picture and inheritance of ocular symptoms in arteriohepatic dysplasia (author’s transl)]. Klin Monatsbl Augenheilkd. 1982;180(4):290–3.PubMedGoogle Scholar
  91. 91.
    Hingorani M, et al. Ocular abnormalities in Alagille syndrome. Ophthalmology. 1999;106(2):330–7.PubMedGoogle Scholar
  92. 92.
    Tanino T, et al. Electrophysiological findings in a family with congenital arteriohepatic dysplasia (Alagille syndrome). Doc Ophthalmol. 1986;63(1):83–9.PubMedGoogle Scholar
  93. 93.
    Alvarez F, et al. Nervous and ocular disorders in children with cholestasis and vitamin A and E deficiencies. Hepatology. 1983;3(3):410–4.PubMedGoogle Scholar
  94. 94.
    Senior B, Friedmann AI, Braudo JL. Juvenile familial nephropathy with tapetoretinal degeneration. A new oculorenal dystrophy. Am J Ophthalmol. 1961;52:625–33.PubMedGoogle Scholar
  95. 95.
    Loken AC, et al. Hereditary renal dysplasia and blindness. Acta Paediatr. 1961;50:177–84.PubMedGoogle Scholar
  96. 96.
    Ronquillo CC, Bernstein PS, Baehr W. Senior-Loken syndrome: a syndromic form of retinal dystrophy associated with nephronophthisis. Vision Res. 2012;75:88–97.PubMedPubMedCentralGoogle Scholar
  97. 97.
    Shimada H, et al. In vitro modeling using ciliopathy-patient-derived cells reveals distinct cilia dysfunctions caused by CEP290 mutations. Cell Rep. 2017;20(2):384–96.PubMedPubMedCentralGoogle Scholar
  98. 98.
    Boye SE, et al. Natural history of cone disease in the murine model of Leber congenital amaurosis due to CEP290 mutation: determining the timing and expectation of therapy. PLoS One. 2014;9(3):e92928.PubMedPubMedCentralGoogle Scholar
  99. 99.
    Jacobson SG, et al. Outcome measures for clinical trials of Leber congenital amaurosis caused by the intronic mutation in the CEP290 gene. Invest Ophthalmol Vis Sci. 2017;58(5):2609–22.PubMedGoogle Scholar
  100. 100.
    Cideciyan AV, et al. Cone photoreceptors are the main targets for gene therapy of NPHP5 (IQCB1) or NPHP6 (CEP290) blindness: generation of an all-cone Nphp6 hypomorph mouse that mimics the human retinal ciliopathy. Hum Mol Genet. 2011;20(7):1411–23.PubMedPubMedCentralGoogle Scholar
  101. 101.
    Stone EM, et al. Variations in NPHP5 in patients with nonsyndromic leber congenital amaurosis and Senior-Loken syndrome. Arch Ophthalmol. 2011;129(1):81–7.PubMedPubMedCentralGoogle Scholar
  102. 102.
    Cideciyan AV, et al. Effect of an intravitreal antisense oligonucleotide on vision in Leber congenital amaurosis due to a photoreceptor cilium defect. Nat Med. 2019;25(2):225–8.PubMedGoogle Scholar
  103. 103.
    Joubert M, et al. Familial agenesis of the cerebellar vermis. A syndrome of episodic hyperpnea, abnormal eye movements, ataxia, and retardation. Neurology. 1969;19(9):813–25.PubMedGoogle Scholar
  104. 104.
    Wang SF, et al. Review of ocular manifestations of Joubert syndrome. Genes (Basel). 2018;9:12.Google Scholar
  105. 105.
    Brancati F, Dallapiccola B, Valente EM. Joubert syndrome and related disorders. Orphanet J Rare Dis. 2010;5:20.PubMedPubMedCentralGoogle Scholar
  106. 106.
    Parisi MA. Clinical and molecular features of Joubert syndrome and related disorders. Am J Med Genet C Semin Med Genet. 2009;151C(4):326–40.PubMedPubMedCentralGoogle Scholar
  107. 107.
    Bassen FA, Kornzweig AL. Malformation of the erythrocytes in a case of atypical retinitis pigmentosa. Blood. 1950;5(4):381–7.PubMedGoogle Scholar
  108. 108.
    Benayoun L, et al. Abetalipoproteinemia in Israel: evidence for a founder mutation in the Ashkenazi Jewish population and a contiguous gene deletion in an Arab patient. Mol Genet Metab. 2007;90(4):453–7.PubMedGoogle Scholar
  109. 109.
    Shoulders CC, et al. Abetalipoproteinemia is caused by defects of the gene encoding the 97 kDa subunit of a microsomal triglyceride transfer protein. Hum Mol Genet. 1993;2(12):2109–16.PubMedGoogle Scholar
  110. 110.
    Wang J, Hegele RA. Microsomal triglyceride transfer protein (MTP) gene mutations in Canadian subjects with abetalipoproteinemia. Hum Mutat. 2000;15(3):294–5.PubMedGoogle Scholar
  111. 111.
    Burnett JR, Hooper AJ, Hegele RA. Abetalipoproteinemia. In: Adam MP, et al., editors. GeneReviews(R). Seattle: University of Washington; 1993.Google Scholar
  112. 112.
    Harcourt B, Hopkins D. Tapetoretinal degeneration in childhood presenting as a disturbance of behaviour. Br Med J. 1972;1(5794):202–5.PubMedPubMedCentralGoogle Scholar
  113. 113.
    Bishara S, et al. Combined vitamin A and E therapy prevents retinal electrophysiological deterioration in abetalipoproteinaemia. Br J Ophthalmol. 1982;66(12):767–70.PubMedPubMedCentralGoogle Scholar
  114. 114.
    Brin MF, et al. Electrophysiologic features of abetalipoproteinemia: functional consequences of vitamin E deficiency. Neurology. 1986;36(5):669–73.PubMedGoogle Scholar
  115. 115.
    Grant CA, Berson EL. Treatable forms of retinitis pigmentosa associated with systemic neurological disorders. Int Ophthalmol Clin. 2001;41(1):103–10.PubMedGoogle Scholar
  116. 116.
    Berson EL, et al. A randomized trial of vitamin A and vitamin E supplementation for retinitis pigmentosa. Arch Ophthalmol. 1993;111:761–72.PubMedGoogle Scholar
  117. 117.
    Bennett MJ, Hofmann SL. The neuronal ceroid-lipofuscinoses (Batten disease): a new class of lysosomal storage diseases. J Inherit Metab Dis. 1999;22(4):535–44.PubMedGoogle Scholar
  118. 118.
    Anderson GW, Goebel HH, Simonati A. Human pathology in NCL. Biochim Biophys Acta. 2013;1832(11):1807–26.PubMedGoogle Scholar
  119. 119.
    Dolisca SB, et al. Batten disease: clinical aspects, molecular mechanisms, translational science, and future directions. J Child Neurol. 2013;28(9):1074–100.PubMedPubMedCentralGoogle Scholar
  120. 120.
    Preising MN, et al. Ocular morphology and function in juvenile neuronal ceroid lipofuscinosis (CLN3) in the first decade of life. Ophthalmic Genet. 2017;38(3):252–9.PubMedGoogle Scholar
  121. 121.
    Santavuori P, et al. Infantile neuronal ceroid-lipofuscinosis (INCL): diagnostic criteria. J Inherit Metab Dis. 1993;16(2):227–9.PubMedGoogle Scholar
  122. 122.
    Lu JY, Verkruyse LA, Hofmann SL. Lipid thioesters derived from acylated proteins accumulate in infantile neuronal ceroid lipofuscinosis: correction of the defect in lymphoblasts by recombinant palmitoyl-protein thioesterase. Proc Natl Acad Sci U S A. 1996;93(19):10046–50.PubMedPubMedCentralGoogle Scholar
  123. 123.
    Weleber RG, et al. Electroretinographic and clinicopathologic correlations of retinal dysfunction in infantile neuronal ceroid lipofuscinosis (infantile Batten disease). Mol Genet Metab. 2004;83(1–2):128–37.PubMedGoogle Scholar
  124. 124.
    Johnson TB, et al. Therapeutic landscape for Batten disease: current treatments and future prospects. Nat Rev Neurol. 2019;15(3):161–78.PubMedPubMedCentralGoogle Scholar
  125. 125.
    Dawson WW, et al. Disease-specific electrophysiological findings in adult ceroid-lipofuscinosis (Kufs disease). Doc Ophthalmol. 1985;60(2):163–71.PubMedGoogle Scholar
  126. 126.
    Safary A, et al. Targeted enzyme delivery systems in lysosomal disorders: an innovative form of therapy for mucopolysaccharidosis. Cell Mol Life Sci. 2019;76:3363.PubMedGoogle Scholar
  127. 127.
    Scott HS, et al. A common mutation for mucopolysaccharidosis type I associated with a severe Hurler syndrome phenotype. Hum Mutat. 1992;1(2):103–8.PubMedGoogle Scholar
  128. 128.
    Sornalingam K, et al. Variability in the ocular phenotype in mucopolysaccharidosis. Br J Ophthalmol. 2019;103(4):504–10.PubMedGoogle Scholar
  129. 129.
    Mack HG, Symons RCA, de Jong G. Bull’s eye maculopathy and subfoveal deposition in two mucopolysaccharidosis type I patients on long-term enzyme replacement therapy. Am J Ophthalmol Case Rep. 2018;9:1–6.PubMedGoogle Scholar
  130. 130.
    Lin HY, et al. Ophthalmologic manifestations in Taiwanese patients with mucopolysaccharidoses. Mol Genet Genomic Med. 2019;7(5):e00617.PubMedPubMedCentralGoogle Scholar
  131. 131.
    Muenzer J, et al. Multidisciplinary management of Hunter syndrome. Pediatrics. 2009;124(6):e1228–39.PubMedGoogle Scholar
  132. 132.
    Salvucci IDM, et al. Multimodal image analysis of the retina in Hunter syndrome (mucopolysaccharidosis type II): case report. Ophthalmic Genet. 2018;39(1):103–7.PubMedGoogle Scholar
  133. 133.
    Wilkin J, et al. Characterization of a case of pigmentary retinopathy in Sanfilippo syndrome type IIIA associated with compound heterozygous mutations in the SGSH gene. Ophthalmic Genet. 2016;37(2):217–27.PubMedGoogle Scholar
  134. 134.
    Wicker G, et al. Mucopolysaccharidosis VI (Maroteaux-Lamy syndrome). An intermediate clinical phenotype caused by substitution of valine for glycine at position 137 of arylsulfatase B. J Biol Chem. 1991;266(32):21386–91.PubMedGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Alfonso Senatore
    • 1
  • Wajiha Jurdi Kheir
    • 1
  • Minzhong Yu
    • 2
    Email author
  • Alessandro Racioppi
    • 1
    • 3
  • Roberto Gattegna
    • 1
    • 4
  • Donnell Creel
    • 5
  • Alessandro Iannaccone
    • 1
  1. 1.Center for Retinal Degenerations and Ophthalmic Genetic Diseases, Duke University School of Medicine, Duke Eye Center, Department of OphthalmologyDurhamUSA
  2. 2.Department of OphthalmologyUniversity Hospitals Eye InstituteClevelandUSA
  3. 3.University of North CarolinaChapel HillUSA
  4. 4.Retina Service, Israelitic HospitalRomeItaly
  5. 5.Moran Eye Center, University of Utah School of MedicineSalt Lake CityUSA

Personalised recommendations