Advertisement

Clinical and Pathological Features of Selected Human Retinal Degenerative Diseases

  • Michael C. Hogden
  • Stephen Tsang
Chapter
Part of the Stem Cell Biology and Regenerative Medicine book series (STEMCELL)

Abstract

The following chapter provides an overview of several important retinal degenerative conditions, with a focus on phenotypic description and correlation with the genetic basis as currently understood. The conditions selected for this chapter have been subdivided into those associated with either a generalized retinal degeneration, such as retinitis pigmentosa, Leber congenital amaurosis, and choroideremia, or those causing degeneration primarily affecting the macula, including age-related macular degeneration, ABCA4 retinal dystrophy, and Best disease. For each condition, coverage is also given to important investigative findings with optical coherence tomography, fundus autofluorescence, retinal angiography, and electrodiagnostic testing in addition to a description of their characteristic clinical features. It is hoped this chapter will enhance the reader’s understanding of the clinical aspects of these conditions and provide a practical link to current research in the field of cell-based therapy.

Keywords

Retinitis pigmentosa Leber congenital amaurosis Choroideremia Age-related macular degeneration ABCA4 retinal dystrophy Best disease 

References

  1. 1.
    Gregory-Evans KPM, Weleber RG. In: Ryan SJ, editor. Retinitis pigmentosa and allied disorders. 5th ed. London: Elsevier; 2013.Google Scholar
  2. 2.
    Hu DN. Genetic aspects of retinitis pigmentosa in China. Am J Med Genet. 1982;12(1):51–6.PubMedCrossRefGoogle Scholar
  3. 3.
    Merin S, Auerbach E. Retinitis pigmentosa. Surv Ophthalmol. 1976;20(5):303–46.PubMedCrossRefGoogle Scholar
  4. 4.
    Bunker CH, Berson EL, Bromley WC, Hayes RP, Roderick TH. Prevalence of retinitis pigmentosa in Maine. Am J Ophthalmol. 1984;97(3):357–65.PubMedCrossRefGoogle Scholar
  5. 5.
    Ammann F, Klein D, Franceschetti A. Genetic and epidemiological investigations on pigmentary degeneration of the retina and allied disorders in Switzerland. J Neurol Sci. 1965;2(2):183–96.PubMedCrossRefGoogle Scholar
  6. 6.
    Ffytche TJ. Cystoid maculopathy in retinitis pigmentosa. Trans Ophthalmol Soc U K. 1972;92:265–83.PubMedGoogle Scholar
  7. 7.
    Hansen RI, Friedman AH, Gartner S, Henkind P. The association of retinitis pigmentosa with preretinal macular gliosis. Br J Ophthalmol. 1977;61(9):597–600.PubMedPubMedCentralCrossRefGoogle Scholar
  8. 8.
    Hamel C. Retinitis pigmentosa. Orphanet J Rare Dis. 2006;1:40.PubMedPubMedCentralCrossRefGoogle Scholar
  9. 9.
    Jay M. On the heredity of retinitis pigmentosa. Br J Ophthalmol. 1982;66(7):405–16.PubMedPubMedCentralCrossRefGoogle Scholar
  10. 10.
    North V, Gelman R, Tsang SH. Juvenile-onset macular degeneration and allied disorders. Dev Ophthalmol. 2014;53:44–52.PubMedPubMedCentralCrossRefGoogle Scholar
  11. 11.
    Rivolta C, Sharon D, DeAngelis MM, Dryja TP. Retinitis pigmentosa and allied diseases: numerous diseases, genes, and inheritance patterns. Hum Mol Genet. 2002;11(10):1219–27.PubMedCrossRefGoogle Scholar
  12. 12.
    Karpe G. The basis of clinical electroretinography. Acta Ophthalmol. 1945;23(Suppl):1–114.Google Scholar
  13. 13.
    Berson EL, Sandberg MA, Rosner B, Birch DG, Hanson AH. Natural course of retinitis pigmentosa over a three-year interval. Am J Ophthalmol. 1985;99(3):240–51.PubMedCrossRefGoogle Scholar
  14. 14.
    von Ruckmann A, Fitzke FW, Bird AC. Distribution of fundus autofluorescence with a scanning laser ophthalmoscope. Br J Ophthalmol. 1995;79(5):407–12.CrossRefGoogle Scholar
  15. 15.
    Robson AG, Michaelides M, Saihan Z, Bird AC, Webster AR, Moore AT, et al. Functional characteristics of patients with retinal dystrophy that manifest abnormal parafoveal annuli of high density fundus autofluorescence; a review and update. Doc Ophthalmol. 2008;116(2):79–89.PubMedCrossRefGoogle Scholar
  16. 16.
    Fleckenstein M, Charbel Issa P, Fuchs HA, Finger RP, Helb HM, Scholl HP, et al. Discrete arcs of increased fundus autofluorescence in retinal dystrophies and functional correlate on microperimetry. Eye (Lond). 2009;23(3):567–75.CrossRefGoogle Scholar
  17. 17.
    Robson AG, Tufail A, Fitzke F, Bird AC, Moore AT, Holder GE, et al. Serial imaging and structure-function correlates of high-density rings of fundus autofluorescence in retinitis pigmentosa. Retina. 2011;31(8):1670–9.PubMedCrossRefGoogle Scholar
  18. 18.
    Lima LH, Cella W, Greenstein VC, Wang NK, Busuioc M, Smith RT, et al. Structural assessment of hyperautofluorescent ring in patients with retinitis pigmentosa. Retina. 2009;29(7):1025–31.PubMedPubMedCentralCrossRefGoogle Scholar
  19. 19.
    Newsome DA. Retinal fluorescein leakage in retinitis pigmentosa. Am J Ophthalmol. 1986;101(3):354–60.PubMedCrossRefGoogle Scholar
  20. 20.
    Lupo S, Grenga PL, Vingolo EM. Fourier-domain optical coherence tomography and microperimetry findings in retinitis pigmentosa. Am J Ophthalmol. 2011;151(1):106–11.PubMedCrossRefGoogle Scholar
  21. 21.
    Wolsley CJ, Silvestri G, O’Neill J, Saunders KJ, Anderson RS. The association between multifocal electroretinograms and OCT retinal thickness in retinitis pigmentosa patients with good visual acuity. Eye (Lond). 2009;23(7):1524–31.CrossRefGoogle Scholar
  22. 22.
    Hajali M, Fishman GA, Anderson RJ. The prevalence of cystoid macular oedema in retinitis pigmentosa patients determined by optical coherence tomography. Br J Ophthalmol. 2008;92(8):1065–8.PubMedCrossRefGoogle Scholar
  23. 23.
    de Paula Freitas B, de Oliveira Dias JR, Prazeres J, et al. Ocular findings in infants with microcephaly associated with presumed Zika virus congenital infection in Salvador, Brazil. JAMA Ophthalmol. 2016;  https://doi.org/10.1001/jamaophthalmol.2016.0267.CrossRefGoogle Scholar
  24. 24.
    Koenekoop R. Leber congental amaurosis. In: Heckenlively JR, Arden GB, editors. Principles and practice of clinical electrophysiology of vision. 2nd ed. Cambridge: MIT Press; 2006. p. 745.Google Scholar
  25. 25.
    Leber T. Uber retinitis pigmentosa und angeborene amaurose. Graefes Arch Klin Ophthalmol. 1869:1–25.Google Scholar
  26. 26.
    Franceschetti A, Dieterlé P. Rubeola pendant la grossesse et cataracte congenitale chez l’enfant, accompagnee du phenomene digito-oculaire. Ophthalmologica. 1947;114:332–9.CrossRefGoogle Scholar
  27. 27.
    Schuil J, Meire FM, Delleman JW. Mental retardation in amaurosis congenita of Leber. Neuropediatrics. 1998;29(6):294–7.PubMedCrossRefGoogle Scholar
  28. 28.
    Casteels I, Spileers W, Demaerel P, Casaer P, De Cock P, Dralands L, et al. Leber congenital amaurosis—differential diagnosis, ophthalmological and neuroradiological report of 18 patients. Neuropediatrics. 1996;27(4):189–93.PubMedCrossRefGoogle Scholar
  29. 29.
    Scholl HP, Chong NH, Robson AG, Holder GE, Moore AT, Bird AC. Fundus autofluorescence in patients with leber congenital amaurosis. Invest Ophthalmol Vis Sci. 2004;45(8):2747–52.PubMedCrossRefGoogle Scholar
  30. 30.
    Bowne SJ, Sullivan LS, Mortimer SE, Hedstrom L, Zhu J, Spellicy CJ, et al. Spectrum and frequency of mutations in IMPDH1 associated with autosomal dominant retinitis pigmentosa and leber congenital amaurosis. Invest Ophthalmol Vis Sci. 2006;47(1):34–42.PubMedPubMedCentralCrossRefGoogle Scholar
  31. 31.
    Nichols LL 2nd, Alur RP, Boobalan E, Sergeev YV, Caruso RC, Stone EM, et al. Two novel CRX mutant proteins causing autosomal dominant Leber congenital amaurosis interact differently with NRL. Hum Mutat. 2010;31(6):E1472–83.PubMedPubMedCentralCrossRefGoogle Scholar
  32. 32.
    Edwards WC, Macdonald R Jr, Price WD. Congenital amaurosis of retinal origin (Leber). Am J Ophthalmol. 1971;72(4):724–8.PubMedCrossRefGoogle Scholar
  33. 33.
    Schroeder R, Mets MB, Maumenee IH. Leber’s congenital amaurosis. Retrospective review of 43 cases and a new fundus finding in two cases. Arch Ophthalmol. 1987;105(3):356–9.PubMedCrossRefGoogle Scholar
  34. 34.
    Flanders M, Lapointe ML, Brownstein S, Little JM. Keratoconus and Leber’s congenital amaurosis: a clinicopathological correlation. Can J Ophthalmol. 1984;19(7):310–4.PubMedGoogle Scholar
  35. 35.
    Lorenz B, Wabbels B, Wegscheider E, Hamel CP, Drexler W, Preising MN. Lack of fundus autofluorescence to 488 nanometers from childhood on in patients with early-onset severe retinal dystrophy associated with mutations in RPE65. Ophthalmology. 2004;111(8):1585–94.PubMedCrossRefGoogle Scholar
  36. 36.
    Franceschetti A, Dieterlé P. Importance diagnostique et pronostique de l’electroretinopgramme dans le degenerescences tapeto-retiniennes avec retrecissement du champ visuel et hemeralopie. Confinia Neurol. 1954;114:184–6.CrossRefGoogle Scholar
  37. 37.
    Foxman SG, Heckenlively JR, Bateman JB, Wirtschafter JD. Classification of congenital and early onset retinitis pigmentosa. Arch Ophthalmol. 1985;103(10):1502–6.PubMedCrossRefGoogle Scholar
  38. 38.
    Koenekoop RK. An overview of Leber congenital amaurosis: a model to understand human retinal development. Surv Ophthalmol. 2004;49(4):379–98.PubMedCrossRefGoogle Scholar
  39. 39.
    Weleber RG, Tongue AC. Congenital stationary night blindness presenting as Leber’s congenital amaurosis. Arch Ophthalmol. 1987;105(3):360–5.PubMedCrossRefGoogle Scholar
  40. 40.
    Weleber RG. The dystrophic retina in multisystem disorders: the electroretinogram in neuronal ceroid lipofuscinoses. Eye. 1998;12(Pt 3b):580–90.PubMedCrossRefGoogle Scholar
  41. 41.
    Loken AC, Hanssen O, Halvorsen S, Jolster NJ. Hereditary renal dysplasia and blindness. Acta Paediatr. 1961;50:177–84.PubMedCrossRefGoogle Scholar
  42. 42.
    Mauthner L. Ein fall von chorioideremie. Berl natur-med ver Innsbruck. 1872;2:191.Google Scholar
  43. 43.
    McCulloch C, McCulloch R. A hereditary and clinical study of choroideremia. Trans Am Acad Ophthalmol Otolaryngol. 1948;52:160–90.PubMedGoogle Scholar
  44. 44.
    MacDonald IM, Sereda C, McTaggart K, Mah D. Choroideremia gene testing. Expert Rev Mol Diagn. 2004;4(4):478–84.PubMedCrossRefGoogle Scholar
  45. 45.
    Roberts MF, Fishman GA, Roberts DK, Heckenlively JR, Weleber RG, Anderson RJ, et al. Retrospective, longitudinal, and cross sectional study of visual acuity impairment in choroideraemia. Br J Ophthalmol. 2002;86(6):658–62.PubMedPubMedCentralCrossRefGoogle Scholar
  46. 46.
    Lewis RA, Nussbaum RL, Ferrell R. Mapping X-linked ophthalmic diseases. Provisional assignment of the locus for choroideremia to Xq13-q24. Ophthalmology. 1985;92(6):800–6.PubMedCrossRefGoogle Scholar
  47. 47.
    Nussbaum RL, Lewis RA, Lesko JG, Ferrell R. Mapping X-linked ophthalmic diseases: II. Linkage relationship of X-linked retinitis pigmentosa to X chromosomal short arm markers. Hum Genet. 1985;70(1):45–50.PubMedCrossRefGoogle Scholar
  48. 48.
    Seabra MC, Brown MS, Slaughter CA, Sudhof TC, Goldstein JL. Purification of component A of Rab geranylgeranyl transferase: possible identity with the choroideremia gene product. Cell. 1992;70(6):1049–57.PubMedCrossRefGoogle Scholar
  49. 49.
    Renner AB, Kellner U, Cropp E, Preising MN, MacDonald IM, van den Hurk JA, et al. Choroideremia: variability of clinical and electrophysiological characteristics and first report of a negative electroretinogram. Ophthalmology. 2006;113(11):2066.e1–10.CrossRefGoogle Scholar
  50. 50.
    Preising MN, Wegscheider E, Friedburg C, Poloschek CM, Wabbels BK, Lorenz B. Fundus autofluorescence in carriers of choroideremia and correlation with electrophysiologic and psychophysical data. Ophthalmology. 2009;116(6):1201-9.e1-2.PubMedCrossRefGoogle Scholar
  51. 51.
    Noble KG, Carr RE, Siegel IM. Fluorescein angiography of the hereditary choroidal dystrophies. Br J Ophthalmol. 1977;61(1):43–53.PubMedPubMedCentralCrossRefGoogle Scholar
  52. 52.
    Xue K, Oldani M, Jolly JK, Edwards TL, Groppe M, Downes SM, et al. Correlation of optical coherence tomography and autofluorescence in the outer retina and choroid of patients with choroideremia. Invest Ophthalmol Vis Sci. 2016;57(8):3674–84.PubMedPubMedCentralCrossRefGoogle Scholar
  53. 53.
    Francis PJ, Fishman GA, Trzupek KM, MacDonald IM, Stone EM, Weleber RG. Stop mutations in exon 6 of the choroideremia gene, CHM, associated with preservation of the electroretinogram. Arch Ophthalmol. 2005;123(8):1146–9.PubMedCrossRefGoogle Scholar
  54. 54.
    Lim LS, Mitchell P, Seddon JM, Holz FG, Wong TY. Age-related macular degeneration. Lancet. 2012;379(9827):1728–38.PubMedCrossRefGoogle Scholar
  55. 55.
    Rudnicka AR, Jarrar Z, Wormald R, Cook DG, Fletcher A, Owen CG. Age and gender variations in age-related macular degeneration prevalence in populations of European ancestry: a meta-analysis. Ophthalmology. 2012;119(3):571–80.PubMedCrossRefGoogle Scholar
  56. 56.
    Saksens NT, Fleckenstein M, Schmitz-Valckenberg S, Holz FG, den Hollander AI, Keunen JE, et al. Macular dystrophies mimicking age-related macular degeneration. Prog Retin Eye Res. 2014;39:23–57.PubMedCrossRefGoogle Scholar
  57. 57.
    Klein RJ, Zeiss C, Chew EY, Tsai JY, Sackler RS, Haynes C, et al. Complement factor H polymorphism in age-related macular degeneration. Science. 2005;308(5720):385–9.PubMedPubMedCentralCrossRefGoogle Scholar
  58. 58.
    Hageman GS, Anderson DH, Johnson LV, Hancox LS, Taiber AJ, Hardisty LI, et al. A common haplotype in the complement regulatory gene factor H (HF1/CFH) predisposes individuals to age-related macular degeneration. Proc Natl Acad Sci U S A. 2005;102(20):7227–32.PubMedPubMedCentralCrossRefGoogle Scholar
  59. 59.
    Haines JL, Hauser MA, Schmidt S, Scott WK, Olson LM, Gallins P, et al. Complement factor H variant increases the risk of age-related macular degeneration. Science. 2005;308(5720):419–21.PubMedPubMedCentralCrossRefGoogle Scholar
  60. 60.
    Edwards AO, Ritter R 3rd, Abel KJ, Manning A, Panhuysen C, Farrer LA. Complement factor H polymorphism and age-related macular degeneration. Science. 2005;308(5720):421–4.PubMedPubMedCentralCrossRefGoogle Scholar
  61. 61.
    Gold B, Merriam JE, Zernant J, Hancox LS, Taiber AJ, Gehrs K, et al. Variation in factor B (BF) and complement component 2 (C2) genes is associated with age-related macular degeneration. Nat Genet. 2006;38(4):458–62.PubMedPubMedCentralCrossRefGoogle Scholar
  62. 62.
    Maller JB, Fagerness JA, Reynolds RC, Neale BM, Daly MJ, Seddon JM. Variation in complement factor 3 is associated with risk of age-related macular degeneration. Nat Genet. 2007;39(10):1200–1.PubMedCrossRefGoogle Scholar
  63. 63.
    Jakobsdottir J, Conley YP, Weeks DE, Mah TS, Ferrell RE, Gorin MB. Susceptibility genes for age-related maculopathy on chromosome 10q26. Am J Hum Genet. 2005;77(3):389–407.PubMedPubMedCentralCrossRefGoogle Scholar
  64. 64.
    Rivera A, Fisher SA, Fritsche LG, Keilhauer CN, Lichtner P, Meitinger T, et al. Hypothetical LOC387715 is a second major susceptibility gene for age-related macular degeneration, contributing independently of complement factor H to disease risk. Hum Mol Genet. 2005;14(21):3227–36.PubMedCrossRefGoogle Scholar
  65. 65.
    Wang L, Clark ME, Crossman DK, Kojima K, Messinger JD, Mobley JA, et al. Abundant lipid and protein components of drusen. PLoS One. 2010;5(4):e10329.PubMedPubMedCentralCrossRefGoogle Scholar
  66. 66.
    Gass’ AA. Atlas of macular diseases. 5th ed. Nashville: Elsevier; 2012.Google Scholar
  67. 67.
    van de Ven JP, Boon CJ, Fauser S, Hoefsloot LH, Smailhodzic D, Schoenmaker-Koller F, et al. Clinical evaluation of 3 families with basal laminar drusen caused by novel mutations in the complement factor H gene. Arch Ophthalmol. 2012;130(8):1038–47.PubMedGoogle Scholar
  68. 68.
    Spaide RF, Curcio CA. Drusen characterization with multimodal imaging. Retina. 2010;30(9):1441–54.  https://doi.org/10.1097/IAE.0b013e3181ee5ce8.CrossRefPubMedPubMedCentralGoogle Scholar
  69. 69.
    Klein R, Davis MD, Magli YL, Segal P, Klein BE, Hubbard L. The Wisconsin age-related maculopathy grading system. Ophthalmology. 1991;98(7):1128–34.PubMedCrossRefGoogle Scholar
  70. 70.
    Mimoun G, Soubrane G, Coscas G. Macular drusen. J Fr Ophtalmol. 1990;13(10):511–30.PubMedGoogle Scholar
  71. 71.
    Klein R, Meuer SM, Knudtson MD, Iyengar SK, Klein BE. The epidemiology of retinal reticular drusen. Am J Ophthalmol. 2008;145(2):317–26.PubMedCrossRefGoogle Scholar
  72. 72.
    Knudtson MD, Klein R, Klein BE, Lee KE, Meuer SM, Tomany SC. Location of lesions associated with age-related maculopathy over a 10-year period: the beaver dam eye study. Invest Ophthalmol Vis Sci. 2004;45(7):2135–42.PubMedCrossRefGoogle Scholar
  73. 73.
    Greferath U, Guymer RH, Vessey KA, Brassington K, Fletcher EL. Correlation of histologic features with in vivo imaging of reticular Pseudodrusen. Ophthalmology. 2016;123(6):1320–31.PubMedCrossRefGoogle Scholar
  74. 74.
    Curcio CA, Messinger JD, Sloan KR, McGwin G, Medeiros NE, Spaide RF. Subretinal drusenoid deposits in non-neovascular age-related macular degeneration: morphology, prevalence, topography, and biogenesis model. Retina. 2013;33(2):265–76.  https://doi.org/10.1097/IAE.0b013e31827e25e0.CrossRefPubMedGoogle Scholar
  75. 75.
    Grossniklaus HE, Miskala PH, Green WR, Bressler SB, Hawkins BS, Toth C, et al. Histopathologic and ultrastructural features of surgically excised subfoveal choroidal neovascular lesions: submacular surgery trials report no. 7. Arch Ophthalmol. 2005;123(7):914–21.PubMedCrossRefGoogle Scholar
  76. 76.
    Pauleikhoff D, Zuels S, Sheraidah GS, Marshall J, Wessing A, Bird AC. Correlation between biochemical composition and fluorescein binding of deposits in Bruch’s membrane. Ophthalmology. 1992;99(10):1548–53.PubMedCrossRefGoogle Scholar
  77. 77.
    Schmitz-Valckenberg S, Fleckenstein M, Gobel AP, Hohman TC, Holz FG. Optical coherence tomography and autofluorescence findings in areas with geographic atrophy due to age-related macular degeneration. Invest Ophthalmol Vis Sci. 2011;52(1):1–6.PubMedCrossRefGoogle Scholar
  78. 78.
    Forte R, Querques G, Querques L, Massamba N, Le Tien V, Souied EH. Multimodal imaging of dry age-related macular degeneration. Acta Ophthalmol. 2012;90(4):e281–7.  https://doi.org/10.1111/j.1755-3768.2011.02331.x.CrossRefPubMedGoogle Scholar
  79. 79.
    McBain VA, Townend J, Lois N. Fundus autofluorescence in exudative age-related macular degeneration. Br J Ophthalmol. 2007;91(4):491–6.PubMedCrossRefGoogle Scholar
  80. 80.
    Warrow DJ, Hoang QV, Freund KB. Pachychoroid pigment epitheliopathy. Retina. 2013;33(8):1659–72.CrossRefPubMedGoogle Scholar
  81. 81.
    Wiszniewski W, Zaremba CM, Yatsenko AN, Jamrich M, Wensel TG, Lewis RA, et al. ABCA4 mutations causing mislocalization are found frequently in patients with severe retinal dystrophies. Hum Mol Genet. 2005;14(19):2769–78.PubMedCrossRefGoogle Scholar
  82. 82.
    Allikmets R. A photoreceptor cell-specific ATP-binding transporter gene (ABCR) is mutated in recessive Stargardt macular dystrophy. Nat Genet. 1997;17(1):122.PubMedGoogle Scholar
  83. 83.
    Quazi F, Lenevich S, Molday RS. ABCA4 is an N-retinylidene-phosphatidylethanolamine and phosphatidylethanolamine importer. Nat Commun. 2012;3:925.PubMedPubMedCentralCrossRefGoogle Scholar
  84. 84.
    Radu RA, Mata NL, Bagla A, Travis GH. Light exposure stimulates formation of A2E oxiranes in a mouse model of Stargardt’s macular degeneration. Proc Natl Acad Sci U S A. 2004;101(16):5928–33.PubMedPubMedCentralCrossRefGoogle Scholar
  85. 85.
    Sparrow JR, Vollmer-Snarr HR, Zhou J, Jang YP, Jockusch S, Itagaki Y, et al. A2E-epoxides damage DNA in retinal pigment epithelial cells. Vitamin E and other antioxidants inhibit A2E-epoxide formation. J Biol Chem. 2003;278(20):18207–13.PubMedCrossRefGoogle Scholar
  86. 86.
    Burke TR, Tsang SH. Allelic and phenotypic heterogeneity in ABCA4 mutations. Ophthalmic Genet. 2011;32(3):165–74.PubMedPubMedCentralCrossRefGoogle Scholar
  87. 87.
    Fishman GA. Fundus flavimaculatus. A clinical classification. Arch Ophthalmol. 1976;94(12):2061–7.PubMedCrossRefGoogle Scholar
  88. 88.
    Westeneng-van Haaften SC, Boon CJ, Cremers FP, Hoefsloot LH, den Hollander AI, Hoyng CB. Clinical and genetic characteristics of late-onset Stargardt’s disease. Ophthalmology. 2012;119(6):1199–210.PubMedCrossRefGoogle Scholar
  89. 89.
    Ergun E, Hermann B, Wirtitsch M, Unterhuber A, Ko TH, Sattmann H, et al. Assessment of central visual function in Stargardt’s disease/fundus flavimaculatus with ultrahigh-resolution optical coherence tomography. Invest Ophthalmol Vis Sci. 2005;46(1):310–6.PubMedCrossRefGoogle Scholar
  90. 90.
    Oh KT, Weleber RG, Stone EM, Oh DM, Rosenow J, Billingslea AM. Electroretinographic findings in patients with Stargardt disease and fundus flavimaculatus. Retina. 2004;24(6):920–8.PubMedCrossRefGoogle Scholar
  91. 91.
    Mohler CW, Fine SL. Long-term evaluation of patients with Best’s vitelliform dystrophy. Ophthalmology. 1981;88(7):688–92.PubMedCrossRefGoogle Scholar
  92. 92.
    Chung MM, Oh KT, Streb LM, Kimura AE, Stone EM. Visual outcome following subretinal hemorrhage in best disease. Retina. 2001;21(6):575–80.PubMedCrossRefGoogle Scholar
  93. 93.
    Clemett R. Vitelliform dystrophy: long-term observations on New Zealand pedigrees. Aust N Z J Ophthalmol. 1991;19(3):221–7.PubMedCrossRefGoogle Scholar
  94. 94.
    Hartzell HC, Qu Z, Yu K, Xiao Q, Chien LT. Molecular physiology of bestrophins: multifunctional membrane proteins linked to best disease and other retinopathies. Physiol Rev. 2008;88(2):639–72.PubMedPubMedCentralCrossRefGoogle Scholar
  95. 95.
    Stuck MW, Conley SM, Naash MI. RDS functional domains and dysfunction in disease. Adv Exp Med Biol. 2016;854:217–22.  https://doi.org/10.1007/978-3-319-17121-0_29.CrossRefPubMedGoogle Scholar
  96. 96.
    Spaide RF, Noble K, Morgan A, Freund KB. Vitelliform macular dystrophy. Ophthalmology. 2006;113(8):1392–400.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Michael C. Hogden
    • 1
  • Stephen Tsang
    • 2
    • 3
  1. 1.Princess Alexandra Hospital, University of QueenslandBrisbaneAustralia
  2. 2.Institute for Genomic MedicineColumbia UniversityNew YorkUSA
  3. 3.Edward S. Harkness Eye Institute, Columbia University Department of OphthalmologyNew YorkUSA

Personalised recommendations