Top

Graefe's Archive for Clinical and Experimental Ophthalmology

Published in:

21-06-2023 | Pigmentary Retinopathy | Review Article

Multidisciplinary approach to inherited causes of dual sensory impairment

Authors: Borja Arias-Peso, María Luisa Calero-Ramos, Cayetana López-Ladrón García de la Borbolla, Mireia López-Domínguez, María José Morillo-Sánchez, Silvia Méndez-Martínez, Serafin Sánchez-Gómez, Enrique Rodríguez-de-la-Rúa

Published in: Graefe's Archive for Clinical and Experimental Ophthalmology | Issue 3/2024

Abstract

Purpose

This article presents a review of the main causes of inherited dual sensory impairment (DSI) with an emphasis on the multidisciplinary approach.

Methods

A narrative review of English literature published before January 2023 was conducted using PubMed, Medline, and Scopus databases. The different causes of inherited DSI are discussed from a multidisciplinary perspective.

Results

There are a wide range of dual sensory impairment (DSI), commonly referred to as blindness and deafness. While Usher syndrome is the most frequent genetic cause, other genetic syndromes such as Alport syndrome or Stickler syndrome can also lead to DSI. Various retinal phenotypes, including pigmentary retinopathy as seen in Usher syndrome, vitreoretinopathy as in Stickler syndrome, and macular dystrophy as in Alport syndrome, along with type of hearing loss (sensorineural or conductive) and additional systemic symptoms can aid in diagnostic suspicion. A thorough ophthalmologic and otorhinolaryngologic examination can help guide diagnosis, which can then be confirmed with genetic studies, crucial for determining prognosis. Effective hearing rehabilitation measures, such as hearing implants, and visual rehabilitation measures, such as low vision optical devices, are crucial for maintaining social interaction and proper development in these patients.

Conclusions

While Usher syndrome is the primary cause of inherited dual sensory impairment (DSI), other genetic syndromes can also lead to this condition. A proper diagnostic approach based on retinal phenotypes and types of hearing loss can aid in ruling out alternative causes. Multidisciplinary approaches can assist in reaching a definitive diagnosis, which has significant prognostic implications.

Dammeyer J (2014) Deafblindness: a review of the literature. Scand J Public Health 42:554–562. https://doi.org/10.1177/1403494814544399CrossRefPubMed

Smith SL, Bennett LW, Wilson RH (2008) Prevalence and characteristics of dual sensory impairment (hearing and vision) in a veteran population. J Rehabil Res Dev 45:597–610. https://doi.org/10.1682/JRRD.2007.02.0023CrossRefPubMed

World Federation of the Deafblind (WFDB) (2018) WFDB Global Report 2018 – WFDB. At risk of exclusion from CRPD and SDGS implementation: inequality and persons with deafblindness. https://wfdb.eu/wfdb-report-2018/. Accessed 5 Jan 2023

Minhas R, Jaiswal A, Chan S et al (2022) Prevalence of individuals with deafblindness and age-related dual-sensory loss. J Vis Impair Blind 116:36–47. https://doi.org/10.1177/0145482X211072541CrossRef

Wittich W, Watanabe DH, Gagné JP (2012) Sensory and demographic characteristics of deafblindness rehabilitation clients in Montréal, Canada. Ophthalmic and Physiological Optics 32:242–251. https://doi.org/10.1111/J.1475-1313.2012.00897.XCrossRefPubMed

Anthony TL (2016) Early Identification of Infants and Toddlers With Deafblindness. Am Ann Deaf 161:412–423. https://doi.org/10.1353/AAD.2016.0034CrossRefPubMed

Dammeyer J (2010) Prevalence and aetiology of congenitally deafblind people in Denmark. Int J Audiol 49:76–82. https://doi.org/10.3109/14992020903311388CrossRefPubMed

Bahena P, Daftarian N, Maroofian R et al (2022) Unraveling the genetic complexities of combined retinal dystrophy and hearing impairment. Hum Genet 141:785–803. https://doi.org/10.1007/S00439-021-02303-1CrossRefPubMed

Medina G, Perry J, Oza A, Kenna M (2021) Hiding in plain sight: genetic deaf-blindness is not always Usher syndrome. Cold Spring Harb Mol Case Stud 7:a006088. https://doi.org/10.1101/MCS.A006088/-/DC1CrossRefPubMedPubMedCentral

10.

Krinsky-McHale SJ, Jenkins EC, Zigman WB, Silverman W (2012) Ophthalmic disorders in adults with Down syndrome. Curr Gerontol Geriatr Res 2012:1. https://doi.org/10.1155/2012/974253CrossRef

11.

Kreicher KL, Weir FW, Nguyen SA, Meyer TA (2018) Characteristics and progression of hearing loss in children with Down syndrome. J Pediatr 193:27–33.e2. https://doi.org/10.1016/J.JPEDS.2017.09.053CrossRefPubMed

12.

Mirmohammadsadeghi A, Akbari MR, Malekpoor A (2017) Ocular manifestations in Edward’s syndrome, a case report and literature review. J Curr Ophthalmol 29:329. https://doi.org/10.1016/J.JOCO.2017.06.005CrossRefPubMedPubMedCentral

13.

Cereda A, Carey JC (2012) The trisomy 18 syndrome. Orphanet J Rare Dis 7:81. https://doi.org/10.1186/1750-1172-7-81CrossRefPubMedPubMedCentral

14.

Yu-Wai-Man P, Griffiths PG, Gorman GS et al (2010) Multi-system neurological disease is common in patients with OPA1 mutations. Brain 133:771–786. https://doi.org/10.1093/BRAIN/AWQ007CrossRefPubMedPubMedCentral

15.

Chang CC, Steinbacher DM (2012) Treacher Collins syndrome. Semin Plast Surg 26:83–90. https://doi.org/10.1055/S-0032-1320066CrossRefPubMed

16.

Pedrosa AL, Bitencourt L, Paranhos RM et al (2021) Alport syndrome: a comprehensive review on genetics, pathophysiology, histology, clinical and therapeutic perspectives. Curr Med Chem 28:5602–5624. https://doi.org/10.2174/0929867328666210108113500CrossRefPubMed

17.

Nguyen XTA, Almushattat H, Strubbe I et al (2021) The phenotypic spectrum of patients with PHARC syndrome due to variants in ABHD12: an ophthalmic perspective. Genes (Basel) 12:1404. https://doi.org/10.3390/GENES12091404CrossRefPubMed

18.

Weihbrecht K, Goar WA, Pak T et al (2017) Keeping an eye on Bardet-Biedl syndrome: a comprehensive review of the role of Bardet-Biedl syndrome genes in the eye. Med Res Arch 5:9. https://doi.org/10.18103/MRA.V5I9.1526CrossRef

19.

Ascaso FJ, Lopez-Gallardo E, del Prado E et al (2010) Macular lesion resembling adult-onset vitelliform macular dystrophy in Kearns-Sayre syndrome with multiple mtDNA deletions. Clin Exp Ophthalmol 38:812–816. https://doi.org/10.1111/J.1442-9071.2010.02335.XCrossRefPubMed

20.

Lindsey S, Brewer C, Stakhovskaya O et al (2017) Auditory and otologic profile of Alström syndrome: comprehensive single center data on 38 patients. Am J Med Genet A 173:2210–2218. https://doi.org/10.1002/AJMG.A.38316CrossRefPubMedPubMedCentral

21.

Castiglione A, Möller C (2022) Usher syndrome. Audiol Res 12:42–65. https://doi.org/10.3390/AUDIOLRES12010005CrossRefPubMedPubMedCentral

22.

Fuster-García C, García-Bohórquez B, Rodríguez-Muñoz A et al (2021) Usher syndrome: genetics of a human ciliopathy. Int J Mol Sci 22:6723. https://doi.org/10.3390/IJMS22136723/S1CrossRefPubMedPubMedCentral

23.

Khan SA, Muhammad N, Khan MA et al (2016) Genetics of human Bardet-Biedl syndrome, an updates. Clin Genet 90:3–15. https://doi.org/10.1111/CGE.12737CrossRefPubMed

24.

Marshall D, Maffei P, Collin B, Naggert K (2011) Alström syndrome: genetics and clinical overview. Curr Genomics 12:225. https://doi.org/10.2174/138920211795677912CrossRefPubMedPubMedCentral

25.

Pingault V, Ente D, Dastot-Le Moal F et al (2010) Review and update of mutations causing Waardenburg syndrome. Hum Mutat 31:391–406. https://doi.org/10.1002/HUMU.21211CrossRefPubMed

26.

Saldaña-Martínez A, de Lourdes Muñoz M, Pérez-Ramírez G et al (2019) Whole sequence of the mitochondrial DNA genome of Kearns Sayre syndrome patients: identification of deletions and variants. Gene 688:171–181. https://doi.org/10.1016/J.GENE.2018.11.085CrossRefPubMed

27.

Laugel V (2013) Cockayne syndrome: the expanding clinical and mutational spectrum. Mech Ageing Dev 134:161–170. https://doi.org/10.1016/J.MAD.2013.02.006CrossRefPubMed

28.

Fiskerstrand T, H’Mida-Ben Brahim D, Johansson S et al (2010) Mutations in ABHD12 cause the neurodegenerative disease PHARC: an inborn error of endocannabinoid metabolism. Am J Hum Genet 87:410. https://doi.org/10.1016/J.AJHG.2010.08.002CrossRefPubMedPubMedCentral

29.

Yahalom C, Volovelsky O, Macarov M et al (2021) Senior-Løken syndrome: a case series and review of the renoretinal phenotype and advances of molecular diagnosis. Retina 41:2179–2187. https://doi.org/10.1097/IAE.0000000000003138CrossRefPubMed

30.

Boothe M, Morris R, Robin N (2020) Stickler syndrome: a review of clinical manifestations and the genetics evaluation. J Pers Med 10:1–8. https://doi.org/10.3390/JPM10030105CrossRef

31.

Dickinson JL, Sale MM, Passmore A et al (2006) Mutations in the NDP gene: contribution to Norrie disease, familial exudative vitreoretinopathy and retinopathy of prematurity. Clin Exp Ophthalmol 34:682–688. https://doi.org/10.1111/J.1442-9071.2006.01314.XCrossRefPubMed

32.

Bergman JEH, Janssen N, Hoefsloot LH et al (2011) CHD7 mutations and CHARGE syndrome: the clinical implications of an expanding phenotype. J Med Genet 48:334–342. https://doi.org/10.1136/JMG.2010.087106CrossRefPubMed

33.

Tekin M, Chioza BA, Matsumoto Y et al (2013) SLITRK6 mutations cause myopia and deafness in humans and mice. J Clin Invest 123:2094–2102. https://doi.org/10.1172/JCI65853CrossRefPubMedPubMedCentral

34.

Naing A, Kenchaiah M, Krishnan B et al (2014) Maternally inherited diabetes and deafness (MIDD): diagnosis and management. J Diabetes Complications 28:542–546. https://doi.org/10.1016/J.JDIACOMP.2014.03.006CrossRefPubMed

35.

Gao FJ, Hu FY, Xu P et al (2019) Expanding the clinical and genetic spectrum of Heimler syndrome. Orphanet J Rare Dis 14:1–12. https://doi.org/10.1186/S13023-019-1243-XCrossRef

36.

37.

Delmaghani S, El-Amraoui A (2022) The genetic and phenotypic landscapes of Usher syndrome: from disease mechanisms to a new classification. Hum Genet 141:709–735. https://doi.org/10.1007/S00439-022-02448-7CrossRefPubMedPubMedCentral

38.

Géléoc GGS, El-Amraoui A (2020) Disease mechanisms and gene therapy for Usher syndrome. Hear Res 394:107932. https://doi.org/10.1016/J.HEARES.2020.107932CrossRefPubMed

39.

Hildebrandt F, Benzing T, Katsanis N (2011) Ciliopathies. N Engl J Med 364:1533. https://doi.org/10.1056/NEJMRA1010172CrossRefPubMedPubMedCentral

40.

Schulz Y, Wehner P, Opitz L et al (2014) CHD7, the gene mutated in CHARGE syndrome, regulates genes involved in neural crest cell guidance. Hum Genet 133:997–1009. https://doi.org/10.1007/S00439-014-1444-2CrossRefPubMed

41.

Tagra S, Talwar A, Walia RL, Sidhu P (2006) Waardenburg syndrome. Indian J Dermatol Venereol Leprol 72:326. https://doi.org/10.4103/0378-6323.26718CrossRefPubMed

42.

Varela MD, Jani P, Zein WM et al (2020) The peroxisomal disorder spectrum and Heimler syndrome: deep phenotyping and review of the literature. Am J Med Genet C Semin Med Genet 184:618. https://doi.org/10.1002/AJMG.C.31823CrossRefPubMedCentral

43.

Khobta A, Epe B (2013) Repair of oxidatively generated DNA damage in Cockayne syndrome. Mech Ageing Dev 134:253–260. https://doi.org/10.1016/J.MAD.2013.03.001CrossRefPubMed

44.

Núñez-Batalla F, Jáudenes-Casaubón C, Sequí-Canet JM et al (2021) New-born hearing screening programmes in 2020: CODEPEH recommendations. Acta Otorrinolaringol Esp 72:312–323. https://doi.org/10.1016/j.otoeng.2020.06.009CrossRef

45.

Toms M, Pagarkar W, Moosajee M (2020) Usher syndrome: clinical features, molecular genetics and advancing therapeutics. Ther Adv Ophthalmol 12:251584142095219. https://doi.org/10.1177/2515841420952194CrossRef

46.

Suppiej A, Marino S, Reffo ME et al (2019) Early onset retinal dystrophies: clinical clues to diagnosis for pediatricians. Ital J Pediatr 45:1–5. https://doi.org/10.1186/S13052-019-0760-5CrossRef

47.

Varela MD, de Guimaraes TAC, Georgiou M, Michaelides M (2022) Leber congenital amaurosis/early-onset severe retinal dystrophy: current management and clinical trials. Br J Ophthalmol 106:445–451. https://doi.org/10.1136/BJOPHTHALMOL-2020-318483CrossRef

48.

Domínguez-Serrano FD, Jiménez-López E, Jiménez MR et al (2019) Importance of ocular electrophysiology in the diagnosis of retinal dystrophies. Arch Soc Esp Oftalmol 94:160–164. https://doi.org/10.1016/J.OFTAL.2018.12.009CrossRefPubMed

49.

Pickett BP, Ahlstrom K (1999) Clinical evaluation of the hearing-impaired infant. Otolaryngol Clin North Am 32:1019–1035. https://doi.org/10.1016/S0030-6665(05)70192-4CrossRefPubMed

50.

van Beeck Calkoen EA, Engel MSD, van de Kamp JM et al (2019) The etiological evaluation of sensorineural hearing loss in children. Eur J Pediatr 178:1195–1205. https://doi.org/10.1007/S00431-019-03379-8CrossRefPubMedPubMedCentral

51.

Núñez F, Jáudenes C, Sequí JM et al (2021) Sordera infantil con discapacidad asociada (DA+): recomendaciones CODEPEH 2021. FIAPAS: Confederación Española de Familias de Personas Sordas 178:1–19

52.

Magliulo G, Iannella G, Gagliardi S et al (2017) Usher’s syndrome type II: a comparative study of genetic mutations and vestibular system evaluation. Otolaryngology - Head and Neck Surgery (United States) 157:853–860. https://doi.org/10.1177/0194599817715235/ASSET/IMAGES/LARGE/10.1177_0194599817715235-FIG1.JPEGCrossRef

53.

Bayram A, Kalkan M, Ünsal N et al (2018) Does blindness affect ocular vestibular evoked myogenic potentials? Am J Otolaryngol 39:290–292. https://doi.org/10.1016/J.AMJOTO.2018.03.010CrossRefPubMed

54.

Gori M, Sandini G, Martinoli C, Burr DC (2014) Impairment of auditory spatial localization in congenitally blind human subjects. Brain 137:288–293. https://doi.org/10.1093/BRAIN/AWT311CrossRefPubMed

55.

Simon M, Campbell E, Genest F et al (2020) The impact of early deafness on brain plasticity: a systematic review of the white and gray matter changes. Front Neurosci 14:206. https://doi.org/10.3389/FNINS.2020.00206CrossRefPubMedPubMedCentral

56.

Lambert SR (2007) Congenital rubella syndrome: the end is in sight. Br J Ophthalmol 91:1418. https://doi.org/10.1136/BJO.2007.117960CrossRefPubMedPubMedCentral

57.

Espinoza GM, Wheeler J, Temprano KK, Keller AP (2020) Cogan’s syndrome: clinical presentations and update on treatment. Curr Allergy Asthma Rep 20:1–6. https://doi.org/10.1007/S11882-020-00945-1CrossRef

58.

Matsunaga T (2021) Clinical genetics, practice, and research of deafblindness: from uncollected experiences to the national registry in Japan. Auris Nasus Larynx 48:185–193. https://doi.org/10.1016/J.ANL.2020.08.017CrossRefPubMed

59.

Saunders GH, Echt K, v. (2007) An overview of dual sensory impairment in older adults: perspectives for rehabilitation. Trends Amplif 11:243–258. https://doi.org/10.1177/1084713807308365CrossRefPubMedPubMedCentral

60.

Marsella P, Scorpecci A, Pacifico C, Tieri L (2011) Bone-anchored hearing aid (Baha) in patients with Treacher Collins syndrome: tips and pitfalls. Int J Pediatr Otorhinolaryngol 75:1308–1312. https://doi.org/10.1016/J.IJPORL.2011.07.020CrossRefPubMed

61.

Wang YB, Chen XW, Wang P et al (2017) Clinical diagnosis of Treacher Collins syndrome and the efficacy of using BAHA. Lin Chung Er Bi Yan Hou Tou Jing Wai Ke Za Zhi 31:577–582. https://doi.org/10.13201/J.ISSN.1001-1781.2017.08.002CrossRef

62.

Davies C, Bergman J, Misztal C et al (2021) The outcomes of cochlear implantation in Usher syndrome: a systematic review. J Clin Med 10:2915. https://doi.org/10.3390/JCM10132915CrossRefPubMedPubMedCentral

63.

Arndt S, Laszig R, Beck R et al (2010) Spectrum of hearing disorders and their management in children with CHARGE syndrome. Otol Neurotol 31:67–73. https://doi.org/10.1097/MAO.0B013E3181C0E972CrossRefPubMed

64.

Birman CS, Brew JA, Gibson WPR, Elliott EJ (2015) CHARGE syndrome and Cochlear implantation: difficulties and outcomes in the paediatric population. Int J Pediatr Otorhinolaryngol 79:487–492. https://doi.org/10.1016/J.IJPORL.2015.01.004CrossRefPubMed

65.

de Joya EM, Colbert BM, Tang PC et al (2021) Usher syndrome in the inner ear: etiologies and advances in gene therapy. Int J Mol Sci 22:3910. https://doi.org/10.3390/IJMS22083910CrossRefPubMedPubMedCentral

66.

Hendriks M, Verhoeven VJM, Buitendijk GHS et al (2017) Development of refractive errors-what can we learn from inherited retinal dystrophies? Am J Ophthalmol 182:81–89. https://doi.org/10.1016/J.AJO.2017.07.008CrossRefPubMed

67.

Barker L, Thomas R, Rubin G, Dahlmann-Noor A (2015) Optical reading aids for children and young people with low vision, vol 3. Cochrane Database of Systematic Reviews. https://doi.org/10.1002/14651858.CD010987CrossRef

68.

Kaur K, Gurnani B (2022) Low Vision Aids. StatPearls

69.

Chen C, Liu X, Peng X (2022) Management of cystoid macular edema in retinitis pigmentosa: a systematic review and meta-analysis. Front Med (Lausanne) 9:1197. https://doi.org/10.3389/FMED.2022.895208CrossRef

70.

Chatterjee S, Agrawal D, Agrawal D et al (2021) Cataract surgery in retinitis pigmentosa. Indian J Ophthalmol 69:1753–1757. https://doi.org/10.4103/IJO.IJO_2916_20CrossRefPubMedPubMedCentral

71.

Jouret G, Poirsier C, Spodenkiewicz M et al (2019) Genetics of Usher syndrome: new insights from a meta-analysis. Otol Neurotol 40:121–129. https://doi.org/10.1097/MAO.0000000000002054CrossRefPubMed

72.

French LS, Mellough CB, Chen FK, Carvalho LS (2020) A review of gene, drug and cell-based therapies for Usher syndrome. Front Cell Neurosci 14:183. https://doi.org/10.3389/FNCEL.2020.00183CrossRefPubMedPubMedCentral

73.

Pan B, Askew C, Galvin A et al (2017) Gene therapy restores auditory and vestibular function in a mouse model of Usher syndrome type 1c. Nat Biotechnol 35:264–272. https://doi.org/10.1038/NBT.3801CrossRefPubMedPubMedCentral

74.

Prado DA, Acosta-Acero M, Maldonado RS (2020) Gene therapy beyond luxturna: a new horizon of the treatment for inherited retinal disease. Curr Opin Ophthalmol 31:147–154. https://doi.org/10.1097/ICU.0000000000000660CrossRefPubMed

75.

Dinculescu A, Link BA, Saperstein DA (2021) Retinal gene therapy for Usher syndrome: current developments, challenges, and perspectives. Int Ophthalmol Clin 61:109. https://doi.org/10.1097/IIO.0000000000000378CrossRefPubMedPubMedCentral

76.

Audo I, Birch DG, Thiran Jayasundera K et al (2022) QR-421a RNA therapy in retinitis pigmentosa due to mutations in USH2A: Stellar trial phase[AP1] 1b/2 interim results. Acta Ophthalmol 100:1. https://doi.org/10.1111/J.1755-3768.2022.205CrossRef

77.

Dammeyer J (2012) Identification of congenital deafblindness. British Journal of Visual Impairment 30:101–107. https://doi.org/10.1177/0264619612443882CrossRef

78.

Ruiz González M (2016) La sordoceguera, su tratamiento normativo y atención a las personas que la presentan. Siglo Cero Revista Española sobre Discapacidad Intelectual 47:29–54. https://doi.org/10.14201/SCERO20164732945CrossRef

Title: Multidisciplinary approach to inherited causes of dual sensory impairment
Authors: Borja Arias-Peso
María Luisa Calero-Ramos
Cayetana López-Ladrón García de la Borbolla
Mireia López-Domínguez
María José Morillo-Sánchez
Silvia Méndez-Martínez
Serafin Sánchez-Gómez
Enrique Rodríguez-de-la-Rúa
Publication date: 21-06-2023
Publisher: Springer Berlin Heidelberg
Keywords: Pigmentary Retinopathy
Alport Syndrome
Alport Syndrome
Published in: Graefe's Archive for Clinical and Experimental Ophthalmology / Issue 3/2024
Print ISSN: 0721-832X
Electronic ISSN: 1435-702X
DOI: https://doi.org/10.1007/s00417-023-06153-7

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Multidisciplinary approach to inherited causes of dual sensory impairment

Abstract

Purpose

Methods

Results

Conclusions

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Purpose

Methods

Results

Conclusions

Please log in to get access to this content

Other articles of this Issue 3/2024

Nanopore sequencing method for CTG18.1 expansion in TCF4 in late-onset Fuchs endothelial corneal dystrophy and a comparison of the structural features of cornea with first-degree relatives

Proliferative vitreoretinopathy: an update on the current and emerging treatment options

Nicotinamide mononucleotide, a potential future treatment in ocular diseases

Workforce separation among ophthalmologists before and during the COVID-19 pandemic

Enhanced morphological assessment based on interocular asymmetry analysis for keratoconus detection

Clinical study on femtosecond laser restoration of accommodation