Published date: Nov 24 2022

Journal Title: Journal of Ophthalmic and Vision Research

Issue title: Oct–Dec 2022, Volume 17, Issue 4

Pages: 551–573

DOI: 10.18502/jovr.v17i4.12321

Haniah Zaheerhaz61@pitt.eduDepartment of Ophthalmology, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA

Deepika ParameswarappaL.V. Prasad Eye Institute, Hyderabad, Telangana, India

Myra ZaheerSchool of Medicine and Health Sciences, George Washington University, Washington DC, USA

Jay ChhablaniUPMC Eye Center, University of Pittsburgh, Pittsburgh, PA, USA

Preeti Patil-ChhablaniUPMC Eye Center, University of Pittsburgh, Pittsburgh, PA, USA

(SNHL) can have a large impact on the outcome and treatment of pediatric patients. Due to the common co-incidence of ocular manifestations and SNHL in children, both ophthalmologic and hearing loss screening and routine examinations must be conducted to minimize adverse outcomes and worsening of pathology. Early evaluation and diagnosis is imperative for intervention and further development of the patient. Coincidence requires a thorough evaluation that includes a comprehensive history, examination, and diagnostic testing. In this article, a literature review was conducted to analyze the presentations of various diseases and syndromes, such as Alport Syndrome, Waardenburg Syndrome, Norrie Disease, Usher Disease, Stickler Syndrome, Marfan Syndrome, Congenital Rubella, and Hereditary Optic Neuropathies. We divided the various ocular pathologies into anterior and posterior segment presentations and associated systemic findings for better understanding. Additionally, this review aims to include an update on the management of patients with both ocular and hearing loss manifestations.

Keywords: Developmental Effects, Neuro-ophthalmology, Ocular Manifestations, Pediatric Ophthalmology, Sensorineural Hearing Loss

1. Keeffe J. Childhood vision impairment. Br J Ophthalmol 2004;88:728–729.

2. Litovsky R. Development of the auditory system. Handb Clin Neurol 2015;129:55–72.

3. Nye C. A child’s vision. Pediatr Clin North Am 2014;61:495– 503.

4. Shojaei E, Jafari Z, Gholami M. Effect of early intervention on language development in hearing-impaired children. Iran J Otorhinolaryngol 2016;28:13–21.

5. Grasland A, Pouchot J, Hachulla E, Blétry O, Papo T, Vinceneux P, et al. Typical and atypical Cogan’s syndrome: 32 cases and review of the literature. Rheumatology 2004;43:1007–1015.

6. Bonnet C, El-Amraoui A. Usher syndrome (sensorineural deafness and retinitis pigmentosa): pathogenesis, molecular diagnosis and therapeutic approaches. Curr Opin Neurol 2012;25:42–49.

7. Zhang Y, Ding J. Renal, auricular, and ocular outcomes of Alport syndrome and their current management. Pediatr Nephrol 2018;33:1309–1316.

8. Hogewind BF, Pennings RJ, Hol FA, Kunst HP, Hoefsloot EH, Cruysberg JR, et al. Autosomal dominant optic neuropathy and sensorineual hearing loss associated with a novel mutation of WFS1. Mol Vis 2010;16:26–35.

9. Payne M, Yang Z, Katz BJ, Warner JEA, Weight CJ, Zhao Y, et al. Dominant optic atrophy, sensorineural hearing loss, ptosis, and ophthalmoplegia: A syndrome caused by a missense mutation in OPA1. Am J Ophthalmol 2004;138:749–755.

10. Kashtan CE, Ding J, Garosi G, Heidet L, Massella L, Nakanishi K, et al. Alport syndrome: A unified classification of genetic disorders of collagen IV alpha345: A position paper of the Alport Syndrome Classification Working Group. Kidney Int 2018;93:1045–1051.

11. Robin NH, Moran RT, Ala-Kokko L. Stickler syndrome. In: Adam MP, et al., editors. GeneReviews. Volume R. Seattle (WA); 1993.

12. Shanker V, Gupta M, Prashar A. Keratitis-Ichthyosis- Deafness syndrome: A rare congenital disorder. Indian Dermatol Online J 2012;3:48–50.

13. Abdollahi A, Hallaji Z, Esmaili N, Valikhani M, Barzegari M, Akhyani M, et al. KID syndrome. Dermatol Online J 2007;13:11.

14. Skinner BA, Greist MC, Norins AL. The keratitis, ichthyosis, and deafness (KID) syndrome. Arch Dermatol 1981;117:285–289.

15. Grob JJ, Breton A, Bonafe JL, Sauvan-Ferdani M, Bonerandi JJ. Keratitis, ichthyosis, and deafness (KID) Syndrome: Vertical transmission and death from multiple squamous cell carcinomas. Arch Dermatol 1987;123:777– 782.

16. Nazzaro V, Blanchet-Bardon C, Lorette G, Civatte J. Familial occurrence of KID (keratitis, ichthyosis, deafness) syndrome. Case reports of a mother and daughter. J Am Acad Dermatol 1990;23:385–388.

17. Messmer EM, Kenyon KR, Rittinger O, Janecke AR, Kampik A. Ocular manifestations of keratitis-ichthyosis-deafness (KID) syndrome. Ophthalmology 2005;112:e1–6.

18. Langer K, Konrad K, Wolff K. Keratitis, ichthyosis and deafness (KID)-syndrome: Report of three cases and a review of the literature. Br J Dermatol 1990;122:689–697.

19. Maintz L, Betz RC, Allam JP, Wenzel J, Jaksche A, Friedrichs N, et al. Keratitis-ichthyosis-deafness syndrome in association with follicular occlusion triad. Eur J Dermatol 2005;15:347–352.

20. Bettoli V, Forconi R, Pezzini I, Martinello R, Scuderi V, Zedde P, et al. KID Syndrome and Hidradenitis Suppurativa: A rare association responding to surgical treatment. Skin Appendage Disord 2021;7:21–24.

21. Natsuga K, Akiyama M, Shimizu H. Malignant skin tumours in patients with inherited ichthyosis. Br J Dermatol 2011;165:263–268.

22. Al Fahaad H. Keratitis-ichthyosis-deafness syndrome: First affected family reported in the Middle East. Int Med Case Rep J 2014;7:63–66.

23. Sharif Z, Sharif W. Corneal neovascularization: Updates on pathophysiology, investigations & management. Rom J Ophthalmol 2019;63:15–22.

24. Feizi S, Azari AA, Safapour S. Therapeutic approaches for corneal neovascularization. Eye Vis 2017;4:28.

25. Smyth CM, Sinnathuray AR, Hughes AE, Toner JG. Cochlear implantation in keratitis-ichthyosis-deafness syndrome: 10-year follow-up of two patients. Cochlear Implants Int 2012;13:54–59.

26. Barker EJ, Briggs RJ. Cochlear implantation in children with keratitis-ichthyosis-deafness (KID) syndrome: Outcomes in three cases. Cochlear Implants Int 2009;10:166–173.

27. Patel V, Sun G, Dickman M, Khuu P, Teng JMC. Treatment of keratitis-ichthyosis- deafness (KID) syndrome in children: A case report and review of the literature. Dermatol Ther 2015;28:89–93.

28. Boughman JA, Vernon M, Shaver KA. Usher syndrome: Definition and estimate of prevalence from two high-risk populations. J Chronic Dis 1983;36:595–603.

29. Kimberling WJ, Hildebrand MS, Shearer AE, Jensen ML, Halder JA, Cohn ES, et al. Frequency of Usher syndrome in two pediatric populations: Implications for genetic screening of deaf and hard of hearing children. Genet Med 2010;12:512–516.

30. Toms M, Pagarkar W, Moosajee M. Usher syndrome: Clinical features, molecular genetics and advancing therapeutics. Ther Adv Ophthalmol 2020;12:2515841420952194.

31. Koenekoop R, FARVO, Arriaga M, Trzupek KM, Lentz J. Usher Syndrome Type II. In: Adam MP et al, editors. GeneReviews. Volume R. Seattle (WA); 1993.

32. Smith RJ, Berlin CI, Hejtmancik JF, Keats BJ, Kimberling WJ, Lewis RA, et al. Clinical diagnosis of the Usher syndromes. Usher Syndrome Consortium. Am J Med Genet 1994;50:32–38.

33. Yang J, Sadaf N. Usher Syndrome: Genes, proteins, models, molecular mechanisms, and therapies. Hearing Loss; 2012. p. 293–328.

34. Waters AM, Beales PL. Ciliopathies: An expanding disease spectrum. Pediatr Nephrol 2011;26: 1039–1056.

35. Hildebrandt F, Benzing T, Katsanis N. Ciliopathies. N Engl J Med 2011;364:1533–1543.

36. Fuster-García C, García-Bohórquez B, Rodríguez-Muñoz A, Aller E, Jaijo T, Millán JM, et al. Usher Syndrome: Genetics of a human ciliopathy. Int J Mol Sci 2021 Jun;22(13):6723.

37. Keats BJ, Corey DP. The usher syndromes. Am J Med Genet 1999 Sep;89:158–166.

38. Fishman GA, Kumar A, Joseph ME, Torok N, Anderson RJ. Usher’s syndrome. Ophthalmic and neuro-otologic findings suggesting genetic heterogeneity. Arch Ophthalmol 1983;101:1367–1374.

39. Edwards A, Fishman GA, Anderson RJ, Grover S, Derlacki DJ. Visual acuity and visual field impairment in Usher syndrome. Arch Ophthalmol 1998;116:165–168.

40. Liu XZ, Angeli SI, Rajput K, Yan D, Hodges AV, Eshraghi A, et al. Cochlear implantation in individuals with Usher type 1 syndrome. Int J Pediatr Otorhinolaryngol 2008;72:841– 847.

41. Hartel BP, Agterberg MJH, Snik AF, Kunst HPM, van Opstal AJ, Bosman AJ, et al. Hearing aid fitting for visual and hearing impaired patients with Usher syndrome type IIa. Clin Otolaryngol 2017;42:805–814.

42. Abdelkader E, Enani L, Schatz P, Safiehd L. Severe retinal degeneration at an early age in Usher syndrome type 1B associated with homozygous splice site mutations in MYO7A gene. Saudi J Ophthalmol 2018;32:119–125.

43. Walia S, Fishman GA, Hajali M. Prevalence of cystic macular lesions in patients with Usher II syndrome. Eye 2009;23:1206–1209.

44. Galli-Resta L, Placidi G, Campagna F, Ziccardi L, Piccardi M, Minnella A, et al. Central retina functional damage in Usher Syndrome Type 2: 22 years of focal macular ERG analysis in a patient population from Central and Southern Italy. Invest Ophthalmol Vis Sci 2018;59:3827–3835.

45. Herrera W, Aleman TS, Cideciyan AV, Roman AJ, Banin E, Ben-Yosef T, et al. Retinal disease in Usher syndrome III caused by mutations in the clarin-1 gene. Invest Ophthalmol Vis Sci 2008;49:2651–2660.

46. Dean G, Orford A, Staines R, McGee A, Smith KJ. Psychosocial well-being and health-related quality of life in a UK population with Usher syndrome. BMJ Open 2017;7:e013261.

47. Arcous M, Putois O, Dalle-Nazébi S, Kerbourch S, Cariou A, Aissa IB, et al. Psychosocial determinants associated with quality of life in people with usher syndrome. A scoping review. Disabil Rehabil 2020;42:2809–2820.

48. Delettre C, Lenaers G, Pelloquin L, Belenguer P, Hamel CP. OPA1 (Kjer type) dominant optic atrophy: A novel mitochondrial disease. Mol Genet Metab 2002;75:97–107.

49. Chun BY, Rizzo JF. 3rd, Dominant optic atrophy: Updates on the pathophysiology and clinical manifestations of the optic atrophy 1 mutation. Curr Opin Ophthalmol 2016;27:475–480.

50. Votruba M, Fitzke FW, Holder GE, Carter A, Bhattacharya SS, Moore AT. Clinical features in affected individuals from 21 pedigrees with dominant optic atrophy. Arch Ophthalmol 1998;116:351–358.

51. Kline LB, Glaser JS. Dominant optic atrophy. The clinical profile. Arch Ophthalmol 1979;7:1680–1686.

52. Fournier AV, Damji KF, Epstein DL, Pollock SC. Disc excavation in dominant optic atrophy: Differentiation from normal tension glaucoma. Ophthalmology 2001;108:1595–1602.

53. Votruba M, Thiselton D, Bhattacharya SS. Optic disc morphology of patients with OPA1 autosomal dominant optic atrophy. Br J Ophthalmol 2003;87:48–53.

54. Yu-Wai-Man P, Votruba M, Burté F, La Morgia C, Barboni P, Carelli V. A neurodegenerative perspective on mitochondrial optic neuropathies. Acta Neuropathologica 2016;132:789–806.

55. Amati-Bonneau P, Guichet A, Olichon A, Chevrollier A, Viala F, Miot S, et al. OPA1 R445H mutation in optic atrophy associated with sensorineural deafness. Ann Neurol 2005;58:958–963.

56. Horga A, Bugiardini E, Manole A, Bremner F, Jaunmuktane Z, Dankwa L, et al. Autosomal dominant optic atrophy and cataract ”plus” phenotype including axonal neuropathy. Neurol Genet 2019;5:e322.

57. Leruez S, Milea D, Defoort-Dhellemmes S, Colin E, Crochet M, Procaccio V, et al. Sensorineural hearing loss in OPA1- linked disorders. Brain 2013;136:e236.

58. Amore G, Romagnoli M, Carbonelli M, Barboni P, Carelli V, La Morgia C. Therapeutic options in hereditary optic neuropathies. Drugs 2021;81:57–86.

59. Romagnoli M, La Morgia C, Carbonelli M, Di Vito L, Amore G, Zenesini C, et al. Idebenone increases chance of stabilization/recovery of visual acuity in OPA1-dominant optic atrophy. Ann Clin Transl Neurol 2020;7:590–594.

60. Smith TG, Seto S, Ganne P, Votruba M. A randomized, placebo-controlled trial of the benzoquinone idebenone in a mouse model of OPA1-related dominant optic atrophy reveals a limited therapeutic effect on retinal ganglion cell dendropathy and visual function. Neuroscience 2016;319:92–106.

61. Santarelli R, La Morgia C, Valentino M, Barboni P, Monteleone A, Scimemi P, et al. Hearing dysfunction in a large family affected by dominant optic atrophy (OPA8-Related DOA): A human model of hidden auditory neuropathy. Front Neurosci 2019;13:501.

62. Boutzios G, Livadas S, Marinakis E, Opie N, Economou F, Diamanti-Kandarakis E. Endocrine and metabolic aspects of the Wolfram syndrome. Endocrine 2011;40:10–13.

63. Cremers CW, Wijdeveld PG, Pinckers AJ. Juvenile diabetes mellitus, optic atrophy, hearing loss, diabetes insipidus, atonia of the urinary tract and bladder, and other abnormalities (Wolfram syndrome). A review of 88 cases from the literature with personal observations on 3 new patients. Acta Paediatr Scand Suppl 1977:1–16.

64. de Heredia ML, Cleries R, Nunes V. Genotypic classification of patients with Wolfram syndrome: Insights into the natural history of the disease and correlation with phenotype. Genet Med 2013;15:497–506.

65. Eller P, Foger B, Gander R, Sauper T, Lechleitner M, Finkenstedt G, et al. Wolfram syndrome: A clinical and molecular genetic analysis. J Med Genet 2001;38:e37.

66. Lauenborg J, Grarup N, Damm P, Borch-Johnsen K, Jørgensen T, Pedersen O, et al. Common type 2 diabetes risk gene variants associate with gestational diabetes. J Clin Endocrinol Metab 2009;94:145–150.

67. Rendtorff ND, Lodahl M, Boulahbel H, Johansen IR, Pandya A, Welch KO, et al. Identification of p.A684V missense mutation in the WFS1 gene as a frequent cause of autosomal dominant optic atrophy and hearing impairment. Am J Med Genet A 2011;155A:1298–1313.

68. Bespalova IN, Van Camp G, Bom SJ, Brown DJ, Cryns K, DeWan AT, et al. Mutations in the Wolfram syndrome 1 gene (WFS1) are a common cause of low frequency sensorineural hearing loss. Hum Mol Genet 2001;10:2501–2508.

69. Barrett TG, Bundey SE, Macleod AF. Neurodegeneration and diabetes: UK nationwide study of Wolfram (DIDMOAD) syndrome. Lancet 1995;346:1458–1463.

70. Wolfram H. [Comment on the letter by M. Gress-Heister regarding the contribution by H. Wolfram and J. Pausch. On the value of the brief psychological performance test for detection of acquired impairments. Exemplified by the Lehrl and Fischer c. I. Test]. Nervenarzt 1995;66:479.

71. Barrett TG, Bundey SE, Fielder AR, Good PA. Optic atrophy in Wolfram (DIDMOAD) syndrome. Eye 1997;11:882–888.

72. Niemeyer G, Marquardt JL. Retinal function in an unique syndrome of optic atrophy, juvenile diabetes mellitus, diabetes insipidus, neurosensory hearing loss, autonomic dysfunction, and hyperalanineuria. Invest Ophthalmol 1972;11:617–624.

73. Al-Till M, Jarrah NS, Ajlouni KM. Ophthalmologic findings in fifteen patients with Wolfram syndrome. Eur J Ophthalmol 2002;12:84–88.

74. Wu J, Asanad S, Ross-Cisneros FN, Sadun AA. Insight into Wolfram Syndrome pathophysiology using optical coherence tomography-angiography. Invest Ophthalmol Vis Sci 2018;59:2831.

75. Hardy C, Khanim F, Torres R, Scott-Brown M, Seller A, Poulton J, et al. Clinical and molecular genetic analysis of 19 Wolfram syndrome kindreds demonstrating a wide spectrum of mutations in WFS1. Am J Hum Genet 1999;65:1279–1290.

76. Pallotta MT, Tascini G, Crispoldi R, Orabona C, Mondanelli G, Grohmann U, et al. Wolfram syndrome, a rare neurodegenerative disease: From pathogenesis to future treatment perspectives. J Transl Med 2019;17:238.

77. Karzon R, Narayanan A, Chen L, Lieu JEC, Hershey T. Longitudinal hearing loss in Wolfram syndrome. Orphanet J Rare Dis 2018;13:102.

78. Urano F. Wolfram Syndrome: Diagnosis, management, and treatment. Curr Diab Rep 2016;16:6.

79. Howell N. Leber hereditary optic neuropathy: Mitochondrial mutations and degeneration of the optic nerve. Vision Res 1997;37:3495–3507.

80. Howell N. Leber hereditary optic neuropathy: How do mitochondrial DNA mutations cause degeneration of the optic nerve? J Bioenerg Biomembr 1997;29:165–173.

81. Manickam AH, Michael MJ, Ramasamy S. Mitochondrial genetics and therapeutic overview of Leber’s hereditary optic neuropathy. Indian J Ophthalmol 2017;65:1087– 1092.

82. Rance G, Kearns LS, Tan J, Gravina A, Rosenfeld L, Henley L, et al. Auditory function in individuals within Leber’s hereditary optic neuropathy pedigrees. J Neurol 2012;259:542–550.

83. Beretta S, Mattavelli L, Sala G, Tremolizzo L, Schapira AHV, Martinuzzi A, et al. Leber hereditary optic neuropathy mtDNA mutations disrupt glutamate transport in cybrid cell lines. Brain 2004;127:2183–2192.

84. Yu-Wai-Man P, Chinnery PF. Leber hereditary optic neuropathy. In: Adam MP, et al, editors. GeneReviews. Seattle: University of Washington; 1993.

85. Kirkman MA, Yu-Wai-Man P, Korsten A, Leonhardt M, Dimitriadis K, De Coo IF, et al. Gene-environment interactions in Leber hereditary optic neuropathy. Brain 2009;132:2317–2326.

86. Prado RC, Moura FC. Leber hereditary optic neuropathy with interval of visual loss greater than 12 months. Neuroophthalmology 2016;40:243–246.

87. Newman NJ, Carelli V, Taiel M, Yu-Wai-Man P. Visual outcomes in Leber hereditary optic neuropathy patients with the m.11778G>A (MTND4) mitochondrial DNA mutation. J Neuroophthalmol 2020;40:547–557.

88. Bingöl Kızıltunç P, Tüntaş Bilen F, Atilla H. Optical coherence tomography angiography findings in long-term follow-up of Leber’s hereditary optic neuropathy: Report of two cases. Turk J Ophthalmol 2020;50:313–316.

89. Iorga RE, Moraru A, Ozturk MR, Costin D. The role of optical coherence tomography in optic neuropathies. Rom J Ophthalmol 2018;62:3–14.

90. Nikoskelainen EK, Marttila RJ, Huoponen K, Juvonen V, Lamminen T, Sonninen P, et al. Leber’s ”plus”: Neurological abnormalities in patients with Leber’s hereditary optic neuropathy. J Neurol Neurosurg Psychiatry 1995;59:160–164.

91. Matthews L, Lucy M, Enzinger C, Fazekas F, Rovira A, Ciccarelli O, et al. MRI in Leber’s hereditary optic neuropathy: The relationship to multiple sclerosis. J Neurol Neurosurg Psychiatry 2015;86:537–542.

92. Klopstock T, Yu-Wai-Man P, Dimitriadis K, Rouleau J, Heck S, Bailie M, et al. A randomized placebo-controlled trial of idebenone in Leber’s hereditary optic neuropathy. Brain 2011;134:2677–2686.

93. Carelli V, La Morgia C, Valentino ML, Rizzo G, Carbonelli M, De Negri AM, et al. Idebenone treatment in Leber’s hereditary optic neuropathy. Brain 2011;134:e188.

94. Sahel JA, Newman NJ, Yu-Wai-Man P, Vignal-Clermont C, Carelli V, Biousse V, et al. Gene therapies for the treatment of Leber hereditary optic neuropathy. Int Ophthalmol Clin 2021;61:195–208.

95. Sahel JA, Vignal-Clermont C, Yu-Wai-Man P, Biousse V, Blouin L, Taiel M. Leber hereditary optic neuropathy: Bilateral improvement of visual acuity following gene therapy by unilateral injection. Med Sci 2021;37:712–715.

96. Dean JC. Marfan syndrome: Clinical diagnosis and management. Eur J Hum Genet 2007;15:724–733.

97. Pepe G, Giusti B, Sticchi E, Abbate R, Gensini GF, Nistri S. Marfan syndrome: Current perspectives. Appl Clin Genet 2016;9:55–65.

98. Hoffjan S. Genetic dissection of marfan syndrome and related connective tissue disorders: An update 2012. Mol Syndromol 2012;3:47–58.

99. Judge DP, Dietz HC. Marfan’s syndrome. Lancet 2005;366:1965–1976.

100. Pyeritz RE. The Marfan Syndrome. Ann Rev Med 2000;51:481–510.

101. Beighton P, de Paepe A, Danks D, Finidori G, Gedde-Dahl T, Goodman R, et al. International nosology of heritable disorders of connective tissue, Berlin, 1986. Am J Med Genet 1988;29:581–594.

102. Loeys BL, Dietz HC, Braverman AC, Callewaert BL, De Backer J, Devereux RB, et al. The revised Ghent nosology for the Marfan syndrome. J Med Genet 2010;47:476–485.

103. von Kodolitsch Y, De Backer J, Schüler H, Bannas P, Behzadi C, Bernhardt AM, et al. Perspectives on the revised Ghent criteria for the diagnosis of Marfan syndrome. Appl Clin Genet 2015;8:137–155.

104. Welder J, Nylen EL, Oetting TA. Marfan Syndrome. 2010; Available from: https://eyerounds.org/cases/110-Marfan.htm

105. Hamberis AO, Mehta CH, Valente TA, Dornhoffer JR, Nguyen SA, Meyer TA. The pattern and progression of hearing loss in Marfan Syndrome: A study of children and young adults. Int J Pediatr Otorhinolaryngol 2020;138:110207.

106. Child A, Rowntree J, Syndrome EA, editor. Diagnosis and management of Marfan Syndrome. Diagnosis and management of Marfan Syndrome. London: Springer; 2016.

107. Nemet AY, Assia EI, Apple DJ, Barequet IS. Current concepts of ocular manifestations in Marfan syndrome. Surv Ophthalmol 2006;51:561–575.

108. Maumenee IH. The eye in the Marfan syndrome. Trans Am Ophthalmol Soc 1981;79:684–733.

109. Siganos DS, Siganos CS, Popescu CN, Margaritis VN. Clear lens extraction and intraocular lens implantation in Marfan’s syndrome. J Cataract Refract Surg 2000;26:781–784.

110. Remulla JF, Tolentino FI. Retinal detachment in Marfan’s syndrome. Int Ophthalmol Clin 2001;41:235–240.

111. Abboud EB. Retinal detachment surgery in Marfan’s syndrome. Retina 1998;18:z405–409.

112. Holmes LB. Norrie’s disease: An X-linked syndrome of retinal malformation, mental retardation, and deafness. J Pediatr 1971;79:89–92.

113. Donnai D, Mountford RC, Read AP. Norrie disease resulting from a gene deletion: Clinical features and DNA studies. J Med Genet 1988;25:73–78.

114. Schuback DE, Chen ZY, Craig IW, Breakefield XO, Sims KB. Mutations in the Norrie disease gene. Hum Mutat 1995;5:285–292.

115. Dickinson JL, Sale MM, Passmore A, FitzGerald LM, Wheatley CM, Burdon KP, et al. Mutations in the NDP gene: contribution to Norrie disease, familial exudative vitreoretinopathy and retinopathy of prematurity. Clin Exp Ophthalmol 2006;34:682–688.

116. Braunger BM, Tamm ER. The different functions of Norrin. Adv Exp Med Biol 2012;723:679–683.

117. Ohlmann A, Tamm ER. Norrin: Molecular and functional properties of an angiogenic and neuroprotective growth factor. Prog Retin Eye Res 2012;31:243–257.

118. Drenser KA, Fecko A, Dailey W, Trese MT. A characteristic phenotypic retinal appearance in Norrie disease. Retina 2007;27:243–246.

119. Xu Q, Wang Y, Dabdoub A, Smallwood PM, Williams J, Woods C, et al. Vascular development in the retina and inner ear: Control by Norrin and Frizzled-4, a high-affinity ligand-receptor pair. Cell 2004;116:883–895.

120. Halpin C, Owen G, Gutiérrez-Espeleta GA, Sims K, Rehm HL. Audiologic features of Norrie disease. Ann Otol Rhinol Laryngol 2005;114:533–538.

121. Smith SE, Mullen TE, Graham D, Sims KB, Rehm HL. Norrie disease: Extraocular clinical manifestations in 56 patients. Am J Med Genet A 2012;158A:1909–1917.

122. Michaelides M, Luthert PJ, Cooling R, Firth H, Moore AT. Norrie disease and peripheral venous insufficiency. Br J Ophthalmol 2004;88:1475.

123. Walsh MK, Drenser KA, Capone Jr A, Trese MT. Early vitrectomy effective for Norrie disease. Arch Ophthalmol 2010;128:456–460.

124. Chow CC, Kiernan DF, Chau FY, Blair MP, Ticho BH, Galasso JM. Laser photocoagulation at birth prevents blindness in Norrie’s disease diagnosed using amniocentesis. Ophthalmology 2010;117:2402–2406.

125. Stickler GB, Belau PG, Farrell FJ, Jones JD, Pugh DG, Steinberg AG, et al. Hereditary progressive arthroophthalmopathy. Mayo Clin Proc 1965;40:433–455.

126. Snead M, Martin H, Bale P, Shenker N, Baguley D, Alexander P, et al. Therapeutic and diagnostic advances in Stickler syndrome. Ther Adv Rare Dis 2020;1:2633004020978661.

127. Snead MP, McNinch AM, Poulson AV, Bearcroft P, Silverman B, Gomersall P, et al. Stickler syndrome, ocular-only variants and a key diagnostic role for the ophthalmologist. Eye 2011;25:1389–1400.

128. Snead MP, Yates JR. Clinical and molecular genetics of Stickler syndrome. J Med Genet 1999;36:353–359.

129. Snead MP, Payne SJ, Barton DE, Yates JR, al-Imara L, Pope FM, et al. Stickler syndrome: Correlation between vitreoretinal phenotypes and linkage to COL 2A1. Eye 1994;8:609–614.

130. Rose PS, Levy HP, Liberfarb RM, Davis J, Szymko- Bennett Y, Rubin BI, et al. Stickler syndrome: Clinical characteristics and diagnostic criteria. Am J Med Genet A 2005;138A:199–207.

131. Snead MP (Taylor D, Hoyt C, editors). Retinal detachment in childhood. Oxford: Paediatric Ophthalmology and Strabismus Blackwell Scientific Publications; p. 2005595– 2005605.

132. Seery CM, Pruett RC, Liberfarb RM, Cohen BZ. Distinctive cataract in the Stickler syndrome. Am J Ophthalmol 1990;110:143–148.

133. Szymko-Bennett YM, Mastroianni MA, Shotland LI, Davis J, Ondrey FG, Balog JZ, et al. Auditory dysfunction in Stickler syndrome. Arch Otolaryngol Head Neck Surg 2001;127:1061–1068.

134. Knutsson J, Bagger-Sjoback D, von Unge M. Distribution of different collagen types in the rat’s tympanic membrane and its suspending structures. Otol Neurotol 2007;28:486–491.

135. Carroll C, Papaioannou D, Rees A, Kaltenthaler E. The clinical effectiveness and safety of prophylactic retinal interventions to reduce the risk of retinal detachment and subsequent vision loss in adults and children with Stickler syndrome: A systematic review. Health Technol Assess 2011;15:iii–xiv, 1–62.

136. Mechaussier S, Perrault I, Dollfus H, Bloch-Zupan A, Loundon N, Jonard L, et al. Heimler Syndrome. Adv Exp Med Biol 2020;1299:81–87.

137. Heimler A, Fox JE, Hershey JE, Crespi P. Sensorineural hearing loss, enamel hypoplasia, and nail abnormalities in sibs. Am J Med Genet 1991;39:192–195.

138. Lima LH, Barbazetto IA, Chen R, Yannuzzi LA, Tsang SH, Spaide RF. Macular dystrophy in Heimler syndrome. Ophthalmic Genet 2011;32:97–100.

139. Ratbi I, Falkenberg KD, Sommen M, Al-Sheqaih N, Guaoua S, Vandeweyer G, et al. Heimler syndrome is caused by hypomorphic mutations in the peroxisome-biogenesis genes PEX1 and PEX6. Am J Hum Genet 2015;97:535–545.

140. Ong KR, Visram S, McKaig S, Brueton LA. Sensorineural deafness, enamel abnormalities and nail abnormalities: A case report of Heimler syndrome in identical twin girls. Eur J Med Genet 2006;49:187–193.

141. Pollak C, Floy M, Say B. Sensorineural hearing loss and enamel hypoplasia with subtle nail findings: Another family with Heimler’s syndrome. Clin Dysmorphol 2003;12:55– 58.

142. O’Neal TB, Luther EE. Retinitis pigmentosa. Treasure Island, FL: StatPearls; 2022.

143. Öner A. Stem cell treatment in retinal diseases: Recent developments. Turk J Ophthalmol 2018;48:33–38.

144. Sharma A, Jaganathan BG. Stem cell therapy for retinal degeneration: The evidence to date. Biologics 2021;15:299–306.

145. Möhn M, Bulski JC, Krämer N, Rahman A, Schulz- Weidner N. Management of Amelogenesis Imperfecta in childhood: Two case reports. Int J Environ Res Public Health 2021;18:7204.

146. Haynes BF, Kaiser-Kupfer MI, Mason P, Fauci AS. Cogan syndrome: Studies in thirteen patients, long-term followup, and a review of the literature. Medicine 1980;59:426–441.

147. Kanski JJ, Bowling B, Nischal KK, Pearson A. Clinical ophthalmology: A systematic approach. Edinburgh, NY: Elsevier/Saunders; 2011.

148. Vollertsen RS, McDonald TJ, Younge BR, Banks PM, Stanson AW, Ilstrup DM. Cogan’s syndrome: 18 cases and a review of the literature. Mayo Clin Proc 1986;61:344–361.

149. Rodrigues-Barros S, Parreira S. Interstitial keratitis in Cogan’s syndrome. N Engl J Med 2018;378:852.

150. Shah P, Luqmani RA, Murray PI, Honan WP, Corridan PG, Emery P. Posterior scleritis–An unusual manifestation of Cogan’s syndrome. Br J Rheumatol 1994;33:774–775.

151. Greco A, Gallo A, Fusconi M, Magliulo G, Turchetta R, Marinelli C, et al. Cogan’s syndrome: An autoimmune inner ear disease. Autoimmun Rev 2013;12:396–400.

152. Morinaka S, Takano Y, Tsuboi H, Goto D, Sumida T. Familial HLA-B*52 vasculitis: Maternal, atypical Cogan’s syndrome with Takayasu Arteritis-mimicking Aortitis and Filial Takayasu Arteritis. Intern Med 2020;59:1899–1904.

153. Cochrane AD, Tatoulis J. Cogan’s syndrome with aortitis, aortic regurgitation, and aortic arch vessel stenoses. Ann Thorac Surg 1991;52:1166–1167.

154. Centers for Disease Control and Prevention (CDC). Elimination of rubella and congenital rubella syndrome— United States, 1969–2004. MMWR Morb Mortal Wkly Rep 2005;54:279–282.

155. Reef SE, Plotkin S, Cordero JF, Katz M, Cooper L, Schwartz B, et al. Preparing for elimination of congenital Rubella syndrome (CRS): Summary of a workshop on CRS elimination in the United States. Clin Infect Dis 2000;31:85–95.

156. Leung AKC, Hon KL, Leong KF. Rubella (German measles) revisited. Hong Kong Med J 2019;25:134–141.

157. Givens KT, Lee DA, Jones T, Ilstrup DM. Congenital rubella syndrome: Ophthalmic manifestations and associated systemic disorders. Br J Ophthalmol 1993;77:358–363.

158. Arnold J. Ocular manifestations of congenital rubella. Curr Opin Ophthalmol 1995;6:45–50.

159. Wild NJ, Sheppard S, Smithells RW, Holzel H, Jones G. Onset and severity of hearing loss due to congenital rubella infection. Arch Dis Child 1989;64:1280–1283.

160. Centers for Disease, C.a.P. Congenital Infectious Syndromes; 2020.

161. Yu Chan JY, Choy BNK, Ng ALK, Shum JWH. Review on the management of primary congenital glaucoma. J Curr Glaucoma Pract 2015;9:92–99.

162. Chen TC, Chen PP, Francis BA, Junk AK, Smith SD, Singh K, et al. Pediatric glaucoma surgery: A report by the American Academy Of Ophthalmology. Ophthalmology 2014;121:2107–2115.

163. Boye E, Mollet G, Forestier L, Cohen-Solal L, Heidet L, Cochat P, et al. Determination of the genomic structure of the COL4A4 gene and of novel mutations causing autosomal recessive Alport syndrome. Am J Hum Genet 1998;63:1329–1340.

164. Heidet L, Arrondel C, Forestier L, Cohen-Solal L, Mollet G, Gutierrez B. Structure of the human type IV collagen gene COL4A3 and mutations in autosomal Alport syndrome. J Am Soc Nephrol 2001;12:97–106.

165. Kashtan CE. Alport syndrome: Achieving early diagnosis and treatment. Am J Kidney Dis 2021;77:272–279.

166. Kashtan C, Fish AJ, Kleppel M, Yoshioka K, Michael AF. Nephritogenic antigen determinants in epidermal and renal basement membranes of kindreds with Alport-type familial nephritis. J Clin Invest 1986;78:1035–1044.

167. Savige J, Gregory M, Gross O, Kashtan C, Ding J, Flinter F. Expert guidelines for the management of Alport syndrome and thin basement membrane nephropathy. J Am Soc Nephrol 2013;24:364–375.

168. Colville DJ, Savige J. Alport syndrome. A review of the ocular manifestations. Ophthalmic Genet 1997;18:161–173.

169. Karki P, Shrestha JK. Alport syndrome. Nepal J Ophthalmol 2009;1:139–140.

170. Gubler M, Levy M, Broyer M, Naizot C, Gonzales G, Perrin D, et al. Alport’s syndrome. A report of 58 cases and a review of the literature. Am J Med 1981;70:493–505.

171. Savige J, Sheth S, Leys A, Nicholson A, Mack HG, Colville D. Ocular features in Alport syndrome: Pathogenesis and clinical significance. Clin J Am Soc Nephrol 2015;10:703–709.

172. Al-Mahmood AM, Al-Swailem SA, Al-Khalaf A, Al- Binali GY. Progressive posterior lenticonus in a patient with alport syndrome. Middle East Afr J Ophthalmol 2010;17:379–381.

173. Sonarkhan S, Ramappa M, Chaurasia S, Mulay K. Bilateral anterior lenticonus in a case of Alport syndrome: A clinical and histopathological correlation after successful clear lens extraction. BMJ Case Rep 2014;2014:bcr2013202036.

174. Savige J, Liu J, DeBuc DC, Handa JT, Hageman GS, Wang YY, et al. Retinal basement membrane abnormalities and the retinopathy of Alport syndrome. Invest Ophthalmol Vis Sci 2010;51:1621–1627.

175. Gross O, Licht C, Anders HJ, Hoppe B, Beck B, Tönshoff B, et al. Early angiotensin-converting enzyme inhibition in Alport syndrome delays renal failure and improves life expectancy. Kidney Int 2012;81:494–501.

176. Yoshioka K, Hino S, Takemura T, Maki S, Wieslander J, Takekoshi Y, et al. Type IV collagen alpha 5 chain. Normal distribution and abnormalities in X-linked Alport syndrome revealed by monoclonal antibody. Am J Pathol 1994;144:986–996.

177. Dourmishev AL, et al. Waardenburg syndrome. Int J Dermatol 1999;38:656–663.

178. Read AP. Waardenburg syndrome. Adv Otorhinolaryngol 2000;56:32–38.

179. Spritz RA. Piebaldism, Waardenburg syndrome, and related disorders of melanocyte development. Semin Cutan Med Surg 1997;16:15–23.

180. Alehabib E, Alinaghi S, Pourfatemi F, Darvish H. Incomplete penetrance of MITF gene c.943C>T mutation in an extended family with Waardenburg syndrome type II. Int J Pediatr Otorhinolaryngol 2020;135:110014.

181. Ahmed Jan N, Mui RK, Masood S. Waardenburg Syndrome. Treasure Island, FL: StatPearls; 2021.

182. Bist J, Adhikari P, Sharma AK. Waardenburg syndrome. Clin Exp Optom 2011;94:240–242.

183. Hoth CF, Milunsky A, Lipsky N, Sheffer R, Clarren SK, Baldwin CT. Mutations in the paired domain of the human PAX3 gene cause Klein-Waardenburg syndrome (WS-III) as well as Waardenburg syndrome type I (WS-I). Am J Hum Genet 1993;52:455–462.

184. Shah M, Patton E, Zedek D. Piebaldism. Treasure Island, FL: StatPearls; 2021.

185. Liu Y, Pan H, Wang J, Yao Q, Lin M, Ma B, et al. Ophthalmological features and treatments in five cases of Waardenburg syndrome. Exp Ther Med 2020;20:3072– 3077.

186. Ohno N, Kiyosawa M, Mori H, Wang WF, Takase H, Mochizuki M. Clinical findings in Japanese patients with Waardenburg syndrome type 2. Jpn J Ophthalmol 2003;47:77–84.

187. Gowda VK, Srinivas S, Srinivasan VM, Waardenburg syndrome type I. Indian J Pediatr 2020;87:244.

188. Astakhov YS, Tultseva SN, Lisochkina AB, Takhtaev YV, Astakhov SY, Shakhnazarova AA. Ophthalmologic manifestations of Waardenburg syndrome. Vestn Oftalmol 2019;135:91–99.

189. Polanski JF, Kochen AP, de Oliveira CA. Hearing and speech performance after cochlear implantation in children with Waardenburg syndrome. Codas 2020;32:e20180295.

190. Xu J-M, Zhang S-S, Zhang Q, Zhou Y-M, Zhu C-H, Jian Ge, et al. Ocular manifestations of Alport syndrome. Int J Ophthalmol 2010;3:149–151.

191. Gomez-Faina P, et al. Patient with severe corneal disease in KID syndrome. Arch Soc Esp Oftalmol 2006;81:225– 227.

192. Song J, Feng Y, Acke FR, Coucke P, Vleminckx K, Dhooge IJ. Hearing loss in Waardenburg syndrome: A systematic review. Clin Genet 2016;89:416–425.

193. Goodyear HM, Sonksen PM, McConachie H. Norrie’s disease: A prospective study of development. Arch Dis Child 1989;64:1587–1592.

194. Wu WC, Drenser K, Trese M, Capone Jr A, Dailey W. Retinal phenotype-genotype correlation of pediatric patients expressing mutations in the Norrie disease gene. Arch Ophthalmol 2007;125:225–230.

195. Scruggs BA, Reding MQ, Schimmenti LA. NDP-related retinopathies. In: Adam MP, et al, editors. Volume R. Seattle, WA: GeneReviews; 1993.

196. Zhou Y, Shapiro MJ, Burton BK, Mets MB, Kurup SP. Case report: A case of Norrie disease due to deletion of the entire coding region of NDP gene. Am J Ophthalmol Case Rep 2021;23:101151.

197. Daich Varela M, Jani P, Zein WM, D’Souza P, Wolfe L, Chisholm J, et al. The peroxisomal disorder spectrum and Heimler syndrome: Deep phenotyping and review of the literature. Am J Med Genet C Semin Med Genet 2020;184:618–630.

198. Ratbi I, Jaouad IC, Elorch H, Al-Sheqaih N, Elalloussi M, Lyahyai J, et al. Severe early onset retinitis pigmentosa in a Moroccan patient with Heimler syndrome due to novel homozygous mutation of PEX1 gene. Eur J Med Genet 2016;59:507–511.

199. Garcia Berrocal JR, Vargas JA, Vaquero M, Ramón y Cajal S, Ramírez-Camacho RA. Cogan’s syndrome: An oculoaudiovestibular disease. Postgrad Med J 1999;75:262–264.

200. Boothe M, Morris R, Robin N. Stickler syndrome: A review of clinical manifestations and the genetics evaluation. J Pers Med 2020;10:E105.

201. Lenaers G, Hamel C, Delettre C, Amati-Bonneau P, Procaccio V, Bonneau D, et al. Dominant optic atrophy. Orphanet J Rare Dis 2012;7:46.

202. Yuan SM, Jing H. Marfan’s syndrome: An overview. Sao Paulo Med J 2010;128:360–366.

203. Esfandiari H, Ansari S, Mohammad-Rabei H, Mets MB. Management strategies of ocular abnormalities in patients with Marfan syndrome: Current perspective. J Ophthalmic Vis Res 2019;14:71–77.