Fundus Autofluorescence and Clinical Applications

Abstract

Fundus autofluorescence (FAF) has allowed in vivo mapping of retinal metabolic derangements and structural changes not possible with conventional color imaging. Incident light is absorbed by molecules in the fundus, which are excited and in turn emit photons of specific wavelengths that are captured and processed by a sensor to create a metabolic map of the fundus. Studies on the growing number of FAF platforms has shown each may be suited to certain clinical scenarios. Scanning laser ophthalmoscopes, fundus cameras, and modifications of these each have benefits and drawbacks that must be considered before and after imaging to properly interpret the images. Emerging clinical evidence has demonstrated the usefulness of FAF in diagnosis and management of an increasing number of chorioretinal conditions, such as agerelated macular degeneration, central serous chorioretinopathy, retinal drug toxicities, and inherited retinal degenerations such as retinitis pigmentosa and Stargardt disease. This article reviews commercial imaging platforms, imaging techniques, and clinical applications of FAF.

Keywords:

Fundus Autofluorescence, Fundus Camera, Near-infrared Autofluorescence, Retinitis Pigmentosa, Scanning Laser Ophthalmoscope, Short-wave Autofluorescence

References
1. Delori FC, Dorey CK, Staurenghi G, Arend O, Goger DG, Weiter JJ. In vivo fluorescence of the ocular fundus exhibits retinal pigment epithelium lipofuscin characteristics. Invest Ophthalmol Vis Sci 1995;36:718– 729.

2. Calvo-Maroto AM, Esteve-Taboada JJ, Domínguez-Vicent A, Pérez-Cambrodí RJ, Cerviño A. Confocal scanning laser ophthalmoscopy versus modified conventional fundus camera for fundus autofluorescence. Expert Rev Med Devices 2016;13:965–978.

3. Yakovleva MA, Radchenko AS, Feldman TB, Kostyukov AA, Arbukhanova PM, Borzenok SA, et al. Fluorescence characteristics of lipofuscin fluorophores from human retinal pigment epithelium. Photochem Photobiol Sci Off J Eur Photochem Assoc Eur Soc Photobiol 2020;19:920–930.

4. Boyer NP, Higbee D, Currin MB, Blakeley LR, Chen C, Ablonczy Z, et al. Lipofuscin and N-retinylidene-Nretinylethanolamine (A2E) accumulate in retinal pigment epithelium in absence of light exposure: their origin is 11- cis-retinal. J Biol Chem 2012;287:22276–22286.

5. Eldred GE, Lasky MR. Retinal age pigments generated by self-assembling lysosomotropic detergents. Nature 1993;361:724–726.

6. Maeda A, Golczak M, Chen Y, Okano K, Kohno H, Shiose S, et al. Primary amines protect against retinal degeneration in mouse models of retinopathies. Nat Chem Biol 2011;8:170–178.

7. Roberts JE, Kukielczak BM, Hu D-N, Miller DS, Bilski P, Sik RH, et al. The role of A2E in prevention or enhancement of light damage in human retinal pigment epithelial cells. Photochem Photobiol 2002;75:184–190.

8. Van Schaik HJ, Alkemade C, Swart W, Van Best JA. Autofluorescence of the diabetic and healthy human cornea in vivo at different excitation wavelengths. Exp Eye Res 1999;68:1–8.

9. Schmitz-Valckenberg S, Pfau M, Fleckenstein M, Fleckenstein M, Staurenghi G, Sparrow JR, et al. Fundus autofluorescence imaging. Prog Retin Eye Res 2021;8:100893.

10. Sparrow JR, Gregory-Roberts E, Yamamoto K, Blonska A, Ghosh SK, Ueda K, et al. The bisretinoids of retinal pigment epithelium. Prog Retin Eye Res 2012;31:121–135.

11. Kim HJ, Sparrow JR. Novel bisretinoids of human retina are lyso alkyl ether glycerophosphoethanolamine-bearing A2PE species. J Lipid Res 2018;59:1620–1629.

12. Eldred GE, Katz ML. Fluorophores of the human retinal pigment epithelium: separation and spectral characterization. Exp Eye Res 1988;47:71–86.

13. Ng K-P, Gugiu B, Renganathan K, Davies MW, Gu X, Crabb JS, et al. Retinal pigment epithelium lipofuscin proteomics. Mol Cell Proteomics MCP 2008;7:1397–1405.

14. Eldred GE, Miller GV, Stark WS, Feeney-Burns L. Lipofuscin: resolution of discrepant fluorescence data. Science 1982;216:757–759.

15. Eldred GE, Katz ML. Fluorophores of the human retinal pigment epithelium: separation and spectral characterization. Exp Eye Res 1988;47:71–86.

16. Eldred GE, Katz ML. The lipid peroxidation theory of lipofuscinogenesis cannot yet be confirmed. Free Radic Biol Med 1991;10:445–447.

17. Sparrow JR, Wu Y, Nagasaki T, Yoon KD, Yamamoto K, Zhou J. Fundus autofluorescence and the bisretinoids of retina. Photochem Photobiol Sci 2010;9:1480–1489.

18. Fishkin NE, Sparrow JR, Allikmets R, Nakanishi K. Isolation and characterization of a retinal pigment epithelial cell fluorophore: an all-trans-retinal dimer conjugate. Proc Natl Acad Sci 2005;102:7091–7096.

19. Parish CA, Hashimoto M, Nakanishi K, Dillon J, Sparrow J. Isolation and one-step preparation of A2E and iso-A2E, fluorophores from human retinal pigment epithelium. Proc Natl Acad Sci USA. 1998;95:14609–14613.

20. Sparrow JR, Parish CA, Hashimoto M, Nakanishi K. A2E, a lipofuscin fluorophore, in human retinal pigmented epithelial cells in culture. Invest Ophthalmol Vis Sci 1999;40:2988–2995.

21. Snodderly DM, Brown PK, Delori FC, Auran JD. The macular pigment. I. Absorbance spectra, localization, and discrimination from other yellow pigments in primate retinas. Invest Ophthalmol Vis Sci 1984;25:660–673.

22. Cardillo Piccolino F, Borgia L, Zinicola E, Iester M, Torrielli S. Pre-injection fluorescence in indocyanine green angiography. Ophthalmology 1996;103:1837–1845.

23. Keilhauer CN, Delori FC. Near-infrared autofluorescence imaging of the fundus: visualization of ocular melanin. Invest Ophthalmol Vis Sci 2006;47:3556–3564.

24. Skondra D, Papakostas TD, Hunter R, Vavvas DG. Near infrared autofluorescence imaging of retinal diseases. Semin Ophthalmol 2012;27:202–208.

25. Bonnin P, Passot, Triolaire-Cotten T. [Autofluorescence of papillary drusen in the diagnosis of false papillary edema]. Bull Soc Dophtalmologie Fr 1976;76:331–335.

26. Schatz H, Burton TC, Yannuzzi LA, Rabb MF. Preinjection fluorescence. Disc leak. In: Interpretation of Fundus Fluorescein Angiography. 1978. p. 251–259.

27. Eagle RC, Lucier AC, Bernardino VB, Yanoff M. Retinal pigment epithelial abnormalities in fundus flavimmaculatus: a light and electron microscopic study. Ophthalmology 1980;87:1189–1200.

28. Bloom SM, Spaide RF. Autofluorescence and yellowing subhyaloid blood with proliferative diabetic retinopathy. Retin Cases Brief Rep 2020;Online ahead of print.

29. von Rückmann A. In vivo fundus autofluorescence in macular dystrophies. Arch Ophthalmol 1997;115:609.

30. Miller SA. Fluorescence in Best’s vitelliform dystrophy, lipofuscin, and fundus flavimaculatus. Br J Ophthalmol 1978;62:256–260.

31. Paavo M, Lee W, Allikmets R, Tsang S, Sparrow JR. Photoreceptor cells as a source of fundus autofluorescence in recessive Stargardt disease. J Neurosci Res 2019;97:98–106.

32. Theelen T, Berendschot TTJM, Boon CJF, Hoyng CB, Klevering BJ. Analysis of visual pigment by fundus autofluorescence. Exp Eye Res 2008;86:296–304.

33. Morgan JIW, Pugh EN. Scanning laser ophthalmoscope measurement of local fundus reflectance and autofluorescence changes arising from rhodopsin bleaching and regeneration. Invest Ophthalmol Vis Sci 2013;54:2048–2059.

34. Zelentsova EA, Yanshole LV, Fursova AZh, Tsentalovich YP. Optical properties of the human lens constituents. J Photochem Photobiol B 2017;173:318–324.

35. Ranjan M, Beedu SR. Spectroscopic and biochemical correlations during the course of human lens aging. BMC Ophthalmol 2006;6:10.

36. Gaillard ER, Zheng L, Merriam JC, Dillon J. Age-related changes in the absorption characteristics of the primate lens. Invest Ophthalmol Vis Sci 2000;41:1454–1459.

37. Delori F, Greenberg JP, Woods RL, Fischer J, Duncker T, Sparrow J, et al. Quantitative measurements of autofluorescence with the scanning laser ophthalmoscope. Invest Ophthalmol Vis Sci 2011;52:9379–9390.

38. Greenberg JP, Duncker T, Woods RL, Smith RT, Sparrow JR, Delori FC. Quantitative fundus autofluorescence in healthy eyes. Invest Ophthalmol Vis Sci 2013;54:5684–5693.

39. Borrelli E, Battista M, Zuccaro B, Sacconi R, Brambati M, Querques L, et al. Spectrally resolved fundus autofluorescence in healthy eyes: repeatability and topographical analysis of the green-emitting fluorophores. J Clin Med 2020;9:2388.

40. Dysli C, Wolf S, Berezin MY, Sauer L, Hammer M, Zinkernagel MS. Fluorescence lifetime imaging ophthalmoscopy. Prog Retin Eye Res 2017;60:120–143.

41. Digman MA, Caiolfa VR, Zamai M, Gratton E. The phasor approach to fluorescence lifetime imaging analysis. Biophys J 2008;94:L14–L16.

42. Dysli C, Quellec G, Abegg M, Menke MN, Wolf- Schnurrbusch U, Kowal J, et al. Quantitative analysis of fluorescence lifetime measurements of the macula using the fluorescence lifetime imaging ophthalmoscope in healthy subjects. Invest Ophthalmol Vis Sci 2014;55:2106– 2113.

43. Sauer L, Andersen KM, Li B, Gensure RH, Hammer M, Bernstein PS. Fluorescence lifetime imaging ophthalmoscopy (FLIO) of macular pigment. Invest Ophthalmol Vis Sci 2018;59:3094–3103.

44. Sauer L, Gensure RH, Andersen KM, Kreilkamp L, Hageman GS, Hammer M, et al. Patterns of fundus autofluorescence lifetimes in eyes of individuals with nonexudative age-related macular degeneration. Invest Ophthalmol Vis Sci 2018;59:AMD65–AMD77.

45. Sauer L, Gensure RH, Hammer M, Bernstein PS. Fluorescence lifetime imaging ophthalmoscopy: a novel way to assess macular telangiectasia type 2. Ophthalmol Retina 2018;2:587–598.

46. Dysli C, Wolf S, Hatz K, Zinkernagel MS. Fluorescence lifetime imaging in Stargardt disease: potential marker for disease progression. Invest Ophthalmol Vis Sci 2016;57:832–841.

47. Sauer L, Calvo CM, Vitale AS, Henrie N, Milliken CM, Bernstein PS. Imaging of hydroxychloroquine toxicity with fluorescence lifetime imaging ophthalmoscopy. Ophthalmol Retina 2019;3:814–825.

48. Dysli C, Wolf S, Tran HV, Zinkernagel MS. Autofluorescence lifetimes in patients with choroideremia identify photoreceptors in areas with retinal pigment epithelium atrophy. Invest Ophthalmol Vis Sci 2016;57:6714–6721.

49. Webb RH, Hughes GW, Pomerantzeff O. Flying spot TV ophthalmoscope. Appl Opt 1980;19:2991–2997.

50. Fischer J, Otto T, Delori F, Pace L, Staurenghi G. Scanning laser ophthalmoscopy (SLO). In: Bille JF, editor. High resolution imaging in microscopy and ophthalmology: new frontiers in biomedical optics. Springer; 2019 [cited 2020 November 19]. Available from: http://www.ncbi.nlm. nih.gov/books/NBK554043/

51. Webb RH, Hughes GW, Delori FC. Confocal scanning laser ophthalmoscope. Appl Opt 1987;26:1492–1499.

52. Heidelberg Engineering. Heidelberg HRA 2 retina angiograph - operation manual. Germany: Heidelberg Engineering GmbH; 2003. Available from: http://www.frankshospitalworkshop.com/ equipment/documents/ophthalmology/user_manuals/ Heidelberg%20HRA%202%20Retina%20Angiograph% 20-%20Operation%20manual.pdf

53. Heidelberg Engineering. SPECTRALIS [Internet,cited 2020 December 17]. Available from: https://businesslounge. heidelbergengineering.com/us/en/products/ spectralis/spectralis/

54. Acton JH, Cubbidge RP, King H, Galsworthy P, Gibson JM. Drusen detection in retro-mode imaging by a scanning laser ophthalmoscope. Acta Ophthalmol 2011;89:e404–e411.

55. Muñoz JM, Coco RM, Sanabria MR, Cuadrado R, Blanco E. Autofluorescence images with Carl Zeiss versus Topcon Eye Fundus Camera: a comparative study. J Ophthalmol 2013;2013:1–4.

56. Schmitz-Valckenberg S, Fleckenstein M, Göbel AP, Sehmi K, Fitzke FW, Holz FG, et al. Evaluation of autofluorescence imaging with the scanning laser ophthalmoscope and the fundus camera in age-related geographic atrophy. Am J Ophthalmol 2008;146:183–192.

57. Spaide R. Autofluorescence from the outer retina and subretinal space: hypothesis and review. Retina 2008;28:5–35.

58. Ziess. Zeiss Clarus 500 fundus camera - medical technology [Internet,cited 2021 January 27]. ZEISS United States. Available from: https://www.zeiss.com/meditec/us/ products/ophthalmology-optometry/retina/diagnostics/ fundus-imaging/clarus-500.html

59. Optos. Optos-california [Internet,cited 2020 December 17]. Available from: https://www.optos.com/globalassets/ www.optos.com/products/california/optos-california.pdf

60. Reznicek L, Dabov S, Haritoglou C, Kampik A, Kernt M, Neubauer AS. Green-light fundus autofluorescence in diabetic macular edema. Int J Ophthalmol 2013;6:75–80.

61. Tan CS, Chew MC, van Hemert J, Singer MA, Bell D, Sadda SR. Measuring the precise area of peripheral retinal nonperfusion using ultra-widefield imaging and its correlation with the ischaemic index. Br J Ophthalmol 2016;100:235– 239.

62. Bourne RRA, Stevens GA, White RA, Smith JL, Flaxman SR, Price H, et al. Causes of vision loss worldwide, 1990–2010: a systematic analysis. Lancet Glob Health 2013;1:e339– e349.

63. Bindewald A, Bird AC, Dandekar SS, Dolar-Szczasny J, Dreyhaupt J, Fitzke FW, et al. Classification of fundus autofluorescence patterns in early age-related macular disease. Invest Ophthalmol Vis Sci 2005;46:3309–3314.

64. Delori FC, Fleckner MR, Goger DG, Weiter JJ, Dorey CK. Autofluorescence distribution associated with drusen in age-related macular degeneration. Invest Ophthalmol Vis Sci 2000;41:496–504.

65. Göbel AP, Fleckenstein M, Heeren TFC, Holz FG, Schmitz- Valckenberg S. In-vivo mapping of drusen by fundus autofluorescence and spectral-domain optical coherence tomography imaging. Graefes Arch Clin Exp Ophthalmol 2016;254:59–67.

66. Klein R, Meuer SM, Knudtson MD, Iyengar SK, Klein BEK. The epidemiology of retinal reticular drusen. Am J Ophthalmol 2008;145:317–326.

67. Smith RT, Sohrab MA, Busuioc M, Barile G. Reticular macular disease. Am J Ophthalmol 2009;148:733–743.e2.

68. Zweifel SA, Spaide RF, Curcio CA, Malek G, Imamura Y. Reticular pseudodrusen are subretinal drusenoid deposits. Ophthalmology 2010;117:303–312.e1.

69. Schmitz-Valckenberg S, Steinberg JS, Fleckenstein M, Visvalingam S, Brinkmann CK, Holz FG. Combined confocal scanning laser ophthalmoscopy and spectraldomain optical coherence tomography imaging of reticular drusen associated with age-related macular degeneration. Ophthalmology 2010;117:1169–1176.

70. Paavo M, Lee W, Merriam J, Bearelly S, Tsang S, Chang S, et al. Intraretinal correlates of reticular pseudodrusen revealed by autofluorescence and en face OCT. Invest Ophthalmol Vis Sci 2017;58:4769–4777.

71. Schmitz-Valckenberg S, Alten F, Steinberg JS, Jaffe GJ, Fleckenstein M, Mukesh BN, et al. Reticular drusen associated with geographic atrophy in age-related macular degeneration. Invest Ophthalmol Vis Sci 2011;52:5009–5015.

72. Domalpally A, Agron E, Pak JW, Keenan TD, Ferris FL 3rd, Clemons TE, et al. Prevalence, risk and genetic association of reticular pseudodrusen in age-related macular degeneration. AREDS2 Report 21. Ophthalmology 2019;126:1659–1666.

73. Holz FG, Bindewald-Wittich A, Fleckenstein M, Dreyhaupt J, Scholl HPN, Schmitz-Valckenberg S. Progression of geographic atrophy and impact of fundus autofluorescence patterns in age-related macular degeneration. Am J Ophthalmol 2007;143:463–472.e2.

74. Holz FG, Bellman C, Staudt S, Schütt F, Völcher HE. Fundus autofluorescence and development of geographic atrophy in age-related macular degeneration. Am J Ophthalmol 2002;133:304.

75. Fleckenstein M, Mitchell P, Freund KB, Sadda S, Holz FG, Brittain C, et al. The progression of geographic atrophy secondary to age-related macular degeneration. Ophthalmology 2018;125:369–390.

76. Sato T, Suzuki M, Ooto S, Spaide RF. Multimodal imaging findings and multimodal vision testing in neovascular agerelated macular degeneration. Retina 2015;35:1292–1302.

77. Parodi MB, Iacono P, Papayannis A, Alto G, Buzzotta A, Arrigo A, et al. Near-infrared fundus autofluorescence in early age-related macular degeneration. Eur J Ophthalmol 2020;30:1448–1453.

78. Kellner U, Kellner S, Weinitz S. Fundus autofluorescence (488 NM) and near-infrared autofluorescence (787 NM) visualize different retinal pigment epithelium alterations in patients with age-related macular degeneration. Retina 2010;30:6–15.

79. Pilotto E, Vujosevic S, Melis R, Convento E, Sportiello P, Alemany-Rubio E, et al. Short wavelength fundus autofluorescence versus near-infrared fundus autofluorescence, with microperimetric correspondence, in patients with geographic atrophy due to age-related macular degeneration. Br J Ophthalmol 2011;95:1140– 1144.

80. Sadda SR, Guymer R, Holz FG, Schmitz-Valckenberg S, Curcio CA, Bird AC, et al. Consensus definition for atrophy associated with age-related macular degeneration on OCT: classification of atrophy report 3. Ophthalmology 2018;125:537–548.

81. Wolf-Schnurrbusch UEK, Wittwer VV, Ghanem R, Niederhaeuser M, Enzmann V, Framme C, et al. Bluelight versus green-light autofluorescence: lesion size of areas of geographic atrophy. Invest Ophthalmol Vis Sci 2011;52:9497–9502.

82. Pfau M, Goerdt L, Schmitz-Valckenberg S, Mauschitz MM, Mishra DK, Holz FG, et al. Green-light autofluorescence versus combined blue-light autofluorescence and nearinfrared reflectance imaging in geographic atrophy secondary to age-related macular degeneration. Invest Ophthalmol Vis Sci 2017;58:BIO121–BIO130.

83. Wu Z, Luu CD, Ayton LN, Goh JK, Lucci LM, Hubbard WC, et al. Optical coherence tomography–defined changes preceding the development of drusen-associated atrophy in age-related macular degeneration. Ophthalmology 2014;121:2415–2422.

84. Sawa M, Ober MD, Spaide RF. Autofluorescence and retinal pigment epithelial atrophy after subretinal hemorrhage. Retina 2006;26:119–120.

85. Vaclavik V, Vujosevic S, Dandekar SS, Bunce C, Peto T, Bird AC. Autofluorescence imaging in agerelated macular degeneration complicated by choroidal neovascularization: a prospective study. Ophthalmology 2008;115:342–346.

86. McBain VA, Townend J, Lois N. Fundus autofluorescence in exudative age-related macular degeneration. Br J Ophthalmol 2007;91:491–496.

87. Camacho N, Barteselli G, Nezgoda JT, El-Emam S, Cheng L, Bartsch DU, et al. Significance of the hyperautofluorescent ring associated with choroidal neovascularisation in eyes undergoing anti-VEGF therapy for wet age-related macular degeneration. Br J Ophthalmol 2015;99:1277–1283.

88. Heimes B, Lommatzsch A, Zeimer M, Gutfleisch M, Spital G, Bird AC, et al. Foveal RPE autofluorescence as a prognostic factor for anti-VEGF therapy in exudative AMD. Graefes Arch Clin Exp Ophthalmol 2008;246:1229.

89. Gass JD. Pathogenesis of tears of the retinal pigment epithelium. Br J Ophthalmol 1984;68:513–519.

90. Sarraf D, Joseph A, Rahimy E. Retinal pigment epithelial tears in the era of intravitreal pharmacotherapy: risk factors, pathogenesis, prognosis and treatment (an American Ophthalmological Society thesis). Trans Am Ophthalmol Soc 2014;112:142–159.

91. Mitchell P, Rodríguez FJ, Joussen AM, Koh A, Eter N, Wong DT, et al. Management of retinal pigment epithelium tear during anti-VEGF therapy. Retina 2021;41:671–678.

92. Nagiel A, Freund KB, Spaide RF, Munch IC, Larsen M, Sarraf D. Mechanism of retinal pigment epithelium tear formation following intravitreal anti–vascular endothelial growth factor therapy revealed by spectral-domain optical coherence tomography. Am J Ophthalmol 2013;156:981–988.e2.

93. Mendis R, Lois N. Fundus autofluorescence in patients with retinal pigment epithelial (RPE) tears: an in-vivo evaluation of RPE resurfacing. Graefes Arch Clin Exp Ophthalmol 2014;252:1059–1063.

94. Sarraf D, Reddy S, Chiang A, Yu F, Jain A. A new grading system for retinal pigment epithelial tears. Retina 2010;30:1039–1045.

95. Cunningham ET, Feiner L, Chung C, Tuomi L, Ehrlich JS. Incidence of retinal pigment epithelial tears after intravitreal ranibizumab injection for neovascular age-related macular degeneration. Ophthalmology 2011;118:2447–2452.

96. Clemens CR, Alten F, Baumgart C, Heiduschka P, Eter N. Quantification of retinal pigment epithelium tear area in age-related macular degeneration. Retina 2014;34:24–31.

97. Saksens NTM, Fleckenstein M, Schmitz-Valckenberg S, Holz FG, den HollanderAI, Keunen JEE, et al. Macular dystrophies mimicking age-related macular degeneration. Prog Retin Eye Res 2014;39:23–57.

98. WHO. Diabetes [Internet,cited 2021 March 7]. Available from: https://www.who.int/westernpacific/health-topics/ diabetes

99. Yau JWY, Rogers SL, Kawasaki R, Lamoureux EL, Kowalski JW, Bek T, et al. Global prevalence and major risk factors of diabetic retinopathy. Diabetes Care 2012;35:556–564.

100. Cicinelli MV, Cavalleri M, Brambati M, Lattanzio R, Bandello F. New imaging systems in diabetic retinopathy. Acta Diabetol 2019;56:981–994.

101. Schweitzer D, Schenke S, Hammer M, Schweitzer F, Jentsch S, Birckner E, et al. Towards metabolic mapping of the human retina. Microsc Res Tech 2007;70:410–419.

102. Field MG, Elner VM, Puro DG, Feuerman JM, Musch DC, Pop-Busui R, et al. Rapid, noninvasive detection of diabetes-induced retinal metabolic stress. Arch Ophthalmol 2008;126:934–938.

103. Calvo-Maroto AM, Esteve-Taboada JJ, Pérez-Cambrodí RJ, Madrid-Costa D, Cerviño A. Pilot study on visual function and fundus autofluorescence assessment in diabetic patients. J Ophthalmol 2016;2016.

104. Özmen S, Ağca S, Doğan E, Aksoy NÖ, Çakır B, Sonalcan V, et al. Evaluation of fundus autofluorescence imaging of diabetic patients without retinopathy. Arq Bras Oftalmol 2019;82:412–416.

105. Schmidt J, Peters S, Sauer L, Schweitzer D, Klemm M, Augsten R, et al. Fundus autofluorescence lifetimes are increased in non-proliferative diabetic retinopathy. Acta Ophthalmol 2017;95:33–40.

106. Schweitzer D, Deutsch L, Klemm M, Jentsch S, Hammer M, Peters S, et al. Fluorescence lifetime imaging ophthalmoscopy in type 2 diabetic patients who have no signs of diabetic retinopathy. J Biomed Opt 2015;20:061106.

107. Pece A, Isola V, Holz F, Milani P, Brancato R. Autofluorescence imaging of cystoid macular edema in diabetic retinopathy. Ophthalmologica 2010;224:230– 235.

108. Bessho K, Gomi F, Harino S, Sawa M, Sayanagi K, Tsujikawa M, et al. Macular autofluorescence in eyes with cystoid macula edema, detected with 488 nm-excitation but not with 580 nm-excitation. Graefes Arch Clin Exp Ophthalmol 2009;247:729–734.

109. Chung H, Park B, Shin HJ, Kim HC. Correlation of fundus autofluorescence with spectral-domain optical coherence tomography and vision in diabetic macular edema. Ophthalmology 2012;119:1056–1065.

110. Vujosevic S, Casciano M, Pilotto E, Boccassini B, Varano M, Midena E. Diabetic macular edema: fundus autofluorescence and functional correlations. Invest Ophthalmol Vis Sci 2011;52:442–448.

111. Xu H, Chen M, Manivannan A, Lois N, Forrester JV. Age-dependent accumulation of lipofuscin in perivascular and subretinal microglia in experimental mice. Aging Cell 2008;7:58–68.

112. Yoshitake S, Murakami T, Horii T, Uji A, Ogino K, Unoki N, et al. Qualitative and quantitative characteristics of near-infrared autofluorescence in diabetic macular edema. Ophthalmology 2014;121:1036–1044.

113. Haimovici R, Gragoudas ES, Duker JS, Sjaarda RN, Eliott D. Central serous chorioretinopathy associated with inhaled or intranasal corticosteroids. Ophthalmology 1997;104:1653–1660.

114. Wu CY, Riangwiwat T, Rattanawong P, Nesmith BLW, Deobhakta A. Association of obstructive sleep apnea with central serous chorioretinopathy and choroidal thickness: a systematic review and meta-analysis. Retina 2018;38:1642–1651.

115. Yannuzzi LA. Type-A behavior and central serous chorioretinopathy. Retina 1987;7:111–131.

116. Setrouk E, Hubault B, Vankemmel F, Zambrowski O, Nazeyrollas P, Delemer B, et al. Circadian disturbance and idiopathic central serous chorioretinopathy. Graefes Arch Clin Exp Ophthalmol 2016;254:2175–2181.

117. von Rückmann A, Fitzke FW, Fan J, Halfyard A, Bird AC. Abnormalities of fundus autofluorescence in central serous retinopathy. Am J Ophthalmol 2002;133:780–786.

118. Zhang P, Wang H-Y, Zhang Z-F, Sun D-J, Zhu JT, Li J, et al. Fundus autofluorescence in central serous chorioretinopathy: Association with spectraldomain optical coherence tomography and fluorescein angiography. Int J Ophthalmol 2015;8:1003–1007.

119. Pang CE, Shah VP, Sarraf D, Freund KB. Ultra-widefield imaging with autofluorescence and indocyanine green angiography in central serous chorioretinopathy. Am J Ophthalmol 2014;158:362–371.e2.

120. Iacono P, Battaglia PM, Papayannis A, La Spina C, Varano M, Bandello F. Acute central serous chorioretinopathy: a correlation study between fundus autofluorescence and spectral-domain OCT. Graefes Arch Clin Exp Ophthalmol 2015;253:1889–1897.

121. Singh SR, Matet A, van Dijk EHC, Daruich A, Fauser S, Yzer S, et al. Discrepancy in current central serous chorioretinopathy classification. Br J Ophthalmol 2019;103:737–742.

122. Han J, Cho NS, Kim K, Kim ES, Kim DG, Kim, JM, et al. Fundus autofluorescence patterns in central serous chorioretinopathy. Retina 2020;40:1387–1394.

123. Mrejen S, Balaratnasingam C, Kaden TR, Bottini A, Dansingani K, Bhavsar KV, et al. Long-term visual outcomes and causes of vision loss in chronic central serous chorioretinopathy. Ophthalmology 2019;126:576–588.

124. Imamura Y, Fujiwara T, Spaide RF. Fundus autofluorescence and visual acuity in central serous chorioretinopathy. Ophthalmology 2011;118:700–705.

125. Eandi CM, Piccolino FC, Alovisi C, Tridico F, Giacomello D, Grignolo FM. Correlation between fundus autofluorescence and central visual function in chronic central serous chorioretinopathy. Am J Ophthalmol 2015;159:652–658.e1.

126. Iovino C, Chhablani J, Parameswarappa DC, Pellegrini M, Giannaccare G, Peiretti E. Retinal pigment epithelium apertures as a late complication of longstanding serous pigment epithelium detachments in chronic central serous chorioretinopathy. Eye 2019;33:1871–1876.

127. Lois N, Halfyard AS, Bird AC, Holder GE, Fitzke FW. Fundus autofluorescence in stargardt macular dystrophy– fundus flavimaculatus. Am J Ophthalmol 2004;138:55–63.

128. Parodi MB, Iacono P, Campa C, Del Turco C, Bandello F. Fundus autofluorescence patterns in best vitelliform macular dystrophy. Am J Ophthalmol 2014;158:1086– 1092.e2.

129. Robson AG, Egan C, Holder GE, Bird AC, Fitzke FW. Comparing rod and cone function with fundus autofluorescence images in retinitis pigmentosa. Adv Exp Med Biol 2003;533:41–47.

130. Boon CJF, Klevering BJ, Cremers FPM, Zonneveld- Vrieling MN, Theelen T, Den Hollander AI, et al. Central areolar choroidal dystrophy. Ophthalmology 2009;116:771–782.e1.

131. Parodi MB, Iacono P, Pedio M, Pece A, Isola V, Fachin A, et al. Autofluorescence in adult-onset foveomacular vitelliform dystrophy. Retina 2008;28:801–807.

132. Miere A, Le Meur T, Bitton K, Pallone C, Semoun O, Capuano V, et al. Deep learning-based classification of inherited retinal diseases using fundus autofluorescence. J Clin Med 2020;9:3303.

133. Trichonas G, Traboulsi EI, Ehlers JP. Correlation of ultra-widefield fundus autofluorescence patterns with the underlying genotype in retinal dystrophies and retinitis pigmentosa. Ophthalmic Genet 2017;38:320–324.

134. Hafler BP. Clinical progress in inherited retinal degenerations: gene therapy clinical trials and advances in genetic sequencing. Retina 2017;37:417–423.

135. Georgiou M, Kane T, Tanna P, Bouzia Z, Singh N, Kalitzeos A, et al. Prospective cohort study of childhood-onset Stargardt disease: fundus autofluorescence imaging, progression, comparison with adult-onset disease, and disease symmetry. Am J Ophthalmol 2020;211:159–175.

136. Strauss RW, Kong X, Ho A, Jha A, West S, Ip M, et al. Progression of Stargardt disease as determined by fundus autofluorescence over a 12-month period: progstar report no. 11. JAMA Ophthalmol 2019;137:1134–1145.

137. Stargardt K. Über familiäre, progressive degeneration in der maculagegend des auges. Albrecht Von Graefes Arch Für Ophthalmol 1909;71:534–550.

138. Delori FC, Staurenghi G, Arend O, Dorey CK, Goger DG, Weiter JJ. In vivo measurement of lipofuscin in Stargardt’s disease–Fundus flavimaculatus. Invest Ophthalmol Vis Sci 1995;36:2327–2331.

139. Yi J, Li S, Jia X, Xiao X, Wang P, Guo X, et al. Evaluation of the ELOVL4, PRPH2 and ABCA4 genes in patients with Stargardt macular degeneration. Mol Med Rep 2012;6:1045–1049.

140. Zhang K, Kniazeva M, Han M, Li W, Yu Z, Yang Z, et al. A 5- bp deletion in ELOVL4 is associated with two related forms of autosomal dominant macular dystrophy. Nat Genet 2001;27:89–93.

141. Müller PL, Gliem M, McGuinnes M, Birtel J, Holz FG, Charbel Issa P. Quantitative fundus autofluorescence in ABCA4-related retinopathy -functional relevance and genotype-phenotype correlation. Am J Ophthalmol 2021;222:340–350.

142. Burke TR, Duncker T, Woods RL, Greenberg JP, Zernant J, Tsang SH, et al. Quantitative fundus autofluorescence in recessive Stargardt disease. Invest Ophthalmol Vis Sci 2014;55:2841–2852.

143. Marsiglia M, Lee W, Mahajan VB, Zernant J, Delori FC, Tsang SH, et al. Quantitative autofluorescence as a clinical tool for expedited differential diagnosis of retinal degeneration. JAMA Ophthalmol 2015;133:219.

144. Cicinelli MV, Rabiolo A, Brambati M, Viganò C, Bandello F, Battaglia Parodi M. Factors influencing retinal pigment epithelium-atrophy progression rate in Stargardt disease. Transl Vis Sci Technol 2020;9:33.

145. Klufas MA, Tsui I, Sadda SR, Hosseini H, Schwartz SD. Ultrawidefield autofluoresence in ABCA4 Stargardt disease. Retina 2018;38:403–415.

146. Bakall B, Radu RA, Stanton JB, Burke JM, McKay BS, Wadelius C, et al. Enhanced accumulation of A2E in individuals homozygous or heterozygous for mutations in BEST1 (VMD2). Exp Eye Res 2007;85:34–43.

147. Rosenthal R, Bakall B, Kinnick T, Peachey N, Wimmers S, Wadelius C, et al. Expression of bestrophin-1, the product of the VMD2 gene, modulates voltage-dependent Ca2+ channels in retinal pigment epithelial cells. FASEB J 2006;20:178–180.

148. Lima de Carvalho JR, Paavo M, Chen L, Chiang J, Tsang SH, Sparrow JR. Multimodal imaging in best vitelliform macular dystrophy. Invest Ophthalmol Vis Sci 2019;60:2012–2022.

149. Querques G, Zerbib J, Georges A, Massamba N, Forte R, Querques L, et al. Multimodal analysis of the progression of Best vitelliform macular dystrophy. Mol Vis 2014;20:575–592.

150. Parodi MB, Arrigo A, Calamuneri A, Aragona E, Bandello F. Multimodal imaging in subclinical best vitelliform macular dystrophy. Br J Ophthalmol 2020. Available from: 10.1136/bjophthalmol-2020-317635

151. Duncker T, Greenberg JP, Ramachandran R, Hood DC, Smith RT, Hirose T, et al. Quantitative fundus autofluorescence and optical coherence tomography in best vitelliform macular dystrophy. Invest Ophthalmol Vis Sci 2014;55:1471–1482.

152. Casalino G, Khan KN, Armengol M, Wright G, Pontikos N, Georgiou M, et al. Autosomal recessive bestrophinopathy: clinical features, natural history, and genetic findings in preparation for clinical trials. Ophthalmology 2020;5:706–718.

153. Barbazetto I, Dansingani KK, Dolz-Marco R, Giovannini A, Piccolino FC, Agarwal A, et al. Idiopathic acute exudative polymorphous vitelliform maculopathy: clinical spectrum and multimodal imaging characteristics. Ophthalmology 2018;125:75–88.

154. Grajewski RS, Schuler-Thurner B, Mauch C, et al. Ocular diseases in metastatic cutaneous melanoma: review of 108 consecutive patients in two German tertiary centers. Graefes Arch Clin Exp Ophthalmol 2014;252:679–685.

155. Vaclavik V. Autofluorescence findings in acute exudative polymorphous vitelliform maculopathy. Arch Ophthalmol 2007;125:274.

156. Crane ER, Bass SJ. Case series: multimodal imaging reveals the spectrum of pattern dystrophies of the retinal pigment epithelium. Optom Vis Sci 2019;96:314–321.

157. Farjo R, Naash MI. The role of Rds in outer segment morphogenesis and human retinal disease. Ophthalmic Genet 2006;27:117–122.

158. Boon CJF, van Schooneveld MJ, den Hollander AI, van Lith-Verhoeven JJC, Zonneveld-Vrieling MN, Theelen T, et al. Mutations in the peripherin/RDS gene are an important cause of multifocal pattern dystrophy simulating STGD1/fundus flavimaculatus. Br J Ophthalmol 2007;91:1504–1511.

159. Kumar V, Kumawat D. Multimodal imaging in a case of butterfly pattern dystrophy of retinal pigment epithelium. Int Ophthalmol 2018;38:775–779.

160. Zerbib J, Querques G, Massamba N, Puche N, Tilleul J, Lalloum F, et al. Reticular pattern dystrophy of the retina: a spectral-domain optical coherence tomography analysis. Am J Ophthalmol 2013;156:1228–1237.

161. Roy R, Saurabh K, Shah D. Multimodal imaging in a case of fundus pulverulentus. Retina 2018;38:e55.

162. Hoyng CB, Heutink P, Testers L, Pinckers A, Deutman AF, Oostra BA. Autosomal dominant central areolar choroidal dystrophy caused by a mutation in codon 142 in the Peripherin/RDS Gene. Am J Ophthalmol 1996;121:623– 629.

163. Klevering BJ, Blankenagel A, Maugeri A, Cremers FPM, Hoyng CB, Rohrschneider K. Phenotypic spectrum of autosomal recessive cone–rod dystrophies caused by mutations in the ABCA4 (ABCR) gene. Invest Ophthalmol Vis Sci 2002;43:1980–1985.

164. Smailhodzic D, Fleckenstein M, Theelen T, Boon CJF, van Huet RAC, van de Ven JPH, et al. Central areolar choroidal dystrophy (CACD) and age-related macular degeneration (AMD): differentiating characteristics in multimodal imaging. Invest Ophthalmol Vis Sci 2011;52:8908–8918.

165. Bunker CH, Berson EL, Bromley WC, Hayes RP, Roderick TH. Prevalence of retinitis pigmentosa in maine. Am J Ophthalmol 1984;97:357–365.

166. Murakami T, Akimoto M, Ooto S, Suzuki T, Ikeda H, Kawagoe N, et al. Association between abnormal autofluorescence and photoreceptor disorganization in retinitis pigmentosa. Am J Ophthalmol 2008;145:687–694.

167. Robson AG. Functional characterisation and serial imaging of abnormal fundus autofluorescence in patients with retinitis pigmentosa and normal visual acuity. Br J Ophthalmol 2006;90:472–479.

168. Robson AG, Egan CA, Luong VA, Bird AC, Holder GE, Fitzke FW. Comparison of fundus autofluorescence with photopic and scotopic fine-matrix mapping in patients with retinitis pigmentosa and normal visual acuity. Invest Opthalmol Vis Sci 2004;45:4119.

169. Robson AG, Lenassi E, Saihan Z, Luong VA, Fitzke FW, Holder GE, et al. Comparison of fundus autofluorescence with photopic and scotopic fine matrix mapping in patients with retinitis pigmentosa: 4- to 8-year follow-up. Invest Opthalmol Vis Sci 2012;53:6187.

170. Schuerch K, Woods RL, Lee W, Duncker T, Delori FC, Allikmets R, et al. Quantifying fundus autofluorescence in patients with retinitis pigmentosa. Invest Opthalmol Vis Sci 2017;58:1843.

171. Lima LH, Burke T, Greenstein VC, Chou CL, Cella W, Yannuzzi LA, et al. Progressive constriction of the hyperautofluorescent ring in retinitis pigmentosa. Am J Ophthalmol 2012;153:718–727.e2.

172. Lenassi E, Troeger E, Wilke R, Hawlina M. Correlation between macular morphology and sensitivity in patients with retinitis pigmentosa and hyperautofluorescent ring. Invest Opthalmol Vis Sci 2012;53:47.

173. Robson AG, El-Amir A, Bailey C, Egan CA, Fitzke FW, Webster AR, et al. Pattern ERG correlates of abnormal fundus autofluorescence in patients with retinitis pigmentosa and normal visual acuity. Invest Opthalmol Vis Sci 2003;44:3544.

174. Down-Schoeman TJ, Rosenbloom J, Ameri H. Patterns of autofluorescence in common genotypes of retinitis pigmentosa. Ophthalmic Surg Lasers Imag Retina 2021; In Press.

175. Oishi A, Ogino K, Makiyama Y, Nakagawa S, Kurimoto M, Yoshimura N. Wide-field fundus autofluorescence imaging of retinitis pigmentosa. Ophthalmology 2013;120:1827–1834.

176. Duncker T, Tabacaru MR, Lee W, Tsang SH, Sparrow JR, Greenstein VC. Comparison of near-infrared and shortwavelength autofluorescence in retinitis pigmentosa. Invest Opthalmol Vis Sci 2013;54:585.

177. Dysli C, Schuerch K, Escher P, Wolf S, Zinkernagel MS. Fundus autofluorescence lifetime patterns in retinitis pigmentosa. Invest Opthalmol Vis Sci 2018;59:1769.

178. Fleckenstein M, Charbel Issa P, Fuchs HA, Finger RP, Helb H-M, Scholl HPN, et al. Discrete arcs of increased fundus autofluorescence in retinal dystrophies and functional correlate on microperimetry. Eye 2009;23:567–575.

179. Scholl HPN, Chong NHV, Robson AG, Holder GE, Moore AT, Bird AC. Fundus autofluorescence in patients with leber congenital amaurosis. Invest Ophthalmol Vis Sci 2004;45:2747–2752.

180. 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;116:79–89.

181. Ogura S, Yasukawa T, Kato A, Usui H, Hirano Y, Yoshida M, et al. Wide-field fundus autofluorescence imaging to evaluate retinal function in patients with retinitis pigmentosa. Am J Ophthalmol 2014;158:1093–1098.e3.

182. Lenassi E, Troeger E, Wilke R, Hawlina M. Correlation between macular morphology and sensitivity in patients with retinitis pigmentosa and hyperautofluorescent ring. Invest Ophthalmol Vis Sci 2012;53:47–52.

183. Greenstein VC, Duncker T, Holopigian K, Carr RE, Greenberg JP, Tsang SH, et al. Structural and functional changes associated with normal and abnormal fundus autofluorescence in patients with retinitis pigmentosa. Retina 2012;32:349–357.

184. Wegscheider E, Preising MN, Lorenz B. Fundus autofluorescence in carriers of X-linked recessive retinitis pigmentosa associated with mutations in RPGR, and correlation with electrophysiological and psychophysical data. Graefes Arch Clin Exp Ophthalmol 2004;242:501–511.

185. Ogino K, Oishi M, Oishi A, Morooka S, Sugahara M, Gotoh N, et al. Radial fundus autofluorescence in the periphery in patients with X-linked retinitis pigmentosa. Clin Ophthalmol 2015;9:1467–1474.

186. Duncker T, Lee W, Tsang SH, et al. Distinct characteristics of inferonasal fundus autofluorescence patterns in Stargardt disease and retinitis pigmentosa. Invest Opthalmol Vis Sci 2013;54:6820.

187. Li A, Jiao X, Munier FL, Greenberg JP, Zernant J, Allikmets R, et al. Bietti crystalline corneoretinal dystrophy is caused by mutations in the novel gene CYP4V2. Am J Hum Genet 2004;74:817–826.

188. Li Q, Li Y, Zhang X, Xu Z, Zhu X, Ma K, et al. Utilization of fundus autofluorescence, spectral domain optical coherence tomography, and enhanced depth imaging in the characterization of bietti crystalline dystrophy in different stages. Retina 2015;35:2074–2084.

189. Fuerst NM, Serrano L, Han G, Morgan JIW, Maguire AM, Leroy BP, et al. Detailed functional and structural phenotype of Bietti crystalline dystrophy associated with mutations in CYP4V2 complicated by choroidal neovascularization. Ophthalmic Genet 2016;37:445–452.

190. Ameri H, Su E, Dowd-Schoeman TJ. Autofluorescence of choroidal vessels in Bietti’s crystalline dystrophy. BMJ Open Ophthalmol 2020;5:e000592.

191. Oishi A, Oishi M, Miyata M, Hirashima T, Hasegawa T, Numa S, et al. Multimodal imaging for differential diagnosis of bietti crystalline dystrophy. Ophthalmol Retina 2018;2:1071–1077.

192. Talib M, Schooneveld MJ van, Wijnholds J, van Genderen MM, Schalij-Delfos NE, Talsma HE, et al. Defining inclusion criteria and endpoints for clinical trials: a prospective cross-sectional study in CRB1-associated retinal dystrophies. Acta Ophthalmol 2021;99:3.

193. Corvi F, Juhn A, Corradetti G, Nguyen TV, Fawzi AA, Sarraf D, et al. Multimodal imaging of CRB1 retinitis pigmentosa with a peripheral retinal tumor. Retin Cases Brief Rep 2021;Online ahead of print.

194. Huang H-B, Zhang Y-X. Pigmented paravenous retinochoroidal atrophy (Review). Exp Ther Med 2014;7:1439–1445.

195. Ranjan R, M AJ, Verghese S, Manayath GJ, Narendran V. Multimodal imaging of pigmented paravenous retinochoroidal atrophy. Eur J Ophthalmol 2020;1120672120965489.

196. Kumar V, Kumawat D, Tewari R, Venkatesh P. Ultra-wide field imaging of pigmented para-venous retino-choroidal atrophy. Eur J Ophthalmol 2019;29:444–452.

197. Escher P, Tran HV, Vaclavik V, Borruat FX, Schorderet DF, Munier FL. Double concentric autofluorescence ring in NR2E3-p.G56R-linked autosomal dominant retinitis pigmentosa. Invest Ophthalmol Vis Sci 2012;53:4754– 4764.

198. Fakin A, Šuštar M, Brecelj J, Bonnet C, Petit C, Zupan A, et al. Double hyperautofluorescent rings in patients with USH2A-retinopathy. Genes 2019;10:956.

199. Trichonas G, Traboulsi EI, Ehlers JP. Correlation of ultra-widefield fundus autofluorescence patterns with the underlying genotype in retinal dystrophies and retinitis pigmentosa. Ophthalmic Genet 2017;38:320–324.

200. Melles RB, Marmor MF. The risk of toxic retinopathy in patients on long-term hydroxychloroquine therapy. JAMA Ophthalmol 2014;132:1453.

201. Marmor MF, Kellner U, Lai TYY, Melles RB, Mieler WF. Recommendations on screening for chloroquine and hydroxychloroquine retinopathy (2016 revision). Ophthalmology 2016;123:1386–1394.

202. Kellner U, Renner AB, Tillack H. Fundus autofluorescence and mfERG for early detection of retinal alterations in patients using chloroquine/hydroxychloroquine. Invest Ophthalmol Vis Sci 2006;47:3531–3538.

203. Melles RB, Marmor MF. Pericentral retinopathy and racial differences in hydroxychloroquine toxicity. Ophthalmology 2015;122:110–116.

204. Greenstein VC, Lima de Carvalho JR, Parmann R, Amaro- QuirezL a, Lee W, Hood DC, et al. Quantitative fundus autofluorescence in HCQ retinopathy. Invest Ophthalmol Vis Sci 2020;61:41.

205. Sauer L, Calvo CM, Vitale AS, Henrie N, Milliken CM, Bernstein PS. Imaging of hydroxychloroquine toxicity with fluorescence lifetime imaging ophthalmoscopy. Ophthalmol Retina 2019;3:814–825.

206. Jauregui R, Parmann R, Nuzbrokh Y, Tsang SH, Sparrow JR. Spectral-domain optical coherence tomography is more sensitive for hydroxychloroquine-related structural abnormalities than short-wavelength and near-infrared autofluorescence. Transl Vis Sci Technol 2020;9:8.

207. Pearce WA, Chen R, Jain N. Pigmentary maculopathy associated with chronic exposure to pentosan polysulfate sodium. Ophthalmology 2018;125:1793–1802.

208. Hanif AM, Armenti ST, Taylor SC, Shah RA, Igelman AD, Jayasundera KT, et al. Phenotypic spectrum of pentosan polysulfate sodium–associated maculopathy. JAMA Ophthalmol 2019;137:1275–1282.

209. Wang D, Au A, Gunnemann F, Hilely A, Scharf J, Tran K, et al. Pentosan-associated maculopathy: prevalence, screening guidelines, and spectrum of findings based on prospective multimodal analysis. Can J Ophthalmol 2020;55:116–125.

210. Hadad A, Helmy O, Leeman S, Schaal S. A novel multimethod image analysis to quantify pentosan polysulfate sodium retinal toxicity. Ophthalmology 2020;127:429–431.

211. Hanif AM, Shah R, Yan J, Varghese JS, Patel SA, Cribbs BE,et al. Strength of association between pentosan polysulfate and a novel maculopathy. Ophthalmology 2019;126:1464–1466.

212. Haimovici R, D’Amico DJ, Gragoudas ES, Sokol S. The expanded clinical spectrum of deferoxamine retinopathy. Ophthalmology 2002;109:164–171.

213. Viola F, Barteselli G, Dell’arti L, Vezzola D, Villani E, Mapelli C, et al. Abnormal fundus autofluorescence results of patients in long-term treatment with deferoxamine. Ophthalmology 2012;119:1693–1700.

214. Viola F, Barteselli G, Dell’Arti L, Laura MD, Vezzola, D, Mapelli, C, et al. Multimodal imaging in deferoxamine retinopathy. Retina 2014;34:1428–1438.

215. Bergen AA, Plomp AS, Schuurman EJ, Terry S, Breuning M, Dauwerse H, et al. Mutations in ABCC6 cause pseudoxanthoma elasticum. Nat Genet 2000;25:228– 231.

216. Zweifel SA, Imamura Y, Freund KB, Spaide RF. Multimodal fundus imaging of pseudoxanthoma elasticum. Retina 2011;31:482–491.

217. Gliem M, Müller PL, Birtel J, McGuinness MB, Finger RP, Herrmann P, et al. Quantitative fundus autofluorescence in pseudoxanthoma elasticum. Invest Ophthalmol Vis Sci 2017;58:6159–6165.

218. Murro V, Mucciolo DP, Giorgio D, Sodi A, Boraldi F, Quaglino D, et al. Pattern dystrophy-like changes and coquille d’oeuf atrophy in elderly patients affected by pseudoxanthoma elasticum. Graefes Arch Clin Exp Ophthalmol 2020;258:1881–1892.

219. Marchese A, Rabiolo A, Corbelli E, Carnevali A, Cicinelli MV, Giuffrè C, et al. Ultra-widefield imaging in patients with angioid streaks secondary to pseudoxanthoma elasticum. Ophthalmol Retina 2017;1:137–144.

220. Gass JDM, Blodi BA. Idiopathic juxtafoveolar retinal telangiectasis: update of classification and follow-up study. Ophthalmology 1993;100:1536–1546.

221. Helb H-M, Charbel Issa P, van Der Veen RLP, Berendschot TTJM, Scholl HPN, Holz FG. Abnormal macular pigment distribution in type 2 idiopathic macular telangiectasia. Retina 2008;28:808–816.

222. Solberg Y, Dysli C, Wolf S, Zinkernagel MS. Fluorescence lifetime patterns in macular telangiectasia type 2. Retina 2020;40:99–108.

223. Balaskas K, Leung I, Sallo FB, Clemons TE, Bird AC, Peto T. Associations between autofluorescence abnormalities and visual acuity in idiopathic macular telangiectasia type 2: mactel project report number 5. Retina 2014;34:1630–1636.

224. Govindahari V, Fraser-Bell S, Ayachit AG, Invernizzi A, Nair U, Nair DV,et al. Multicolor imaging in macular telangiectasia—a comparison with fundus autofluorescence. Graefes Arch Clin Exp Ophthalmol 2020;258:2379–2387.

225. Wong WT, Forooghian F, Majumdar Z, Bonner RF, Cunningham D, Chew EY. Fundus autofluorescence in type 2 idiopathic macular telangiectasia: correlation with optical coherence tomography and microperimetry. Am J Ophthalmol 2009;148:573–583.

226. Witmer MT, Cho M, Favarone G, Paul Chan RV, D’Amico DJ, Kiss S. Ultra-wide-field autofluorescence imaging in non-traumatic rhegmatogenous retinal detachment. Eye 2012;26:1209–1216.

227. Salvanos P, Navaratnam J, Ma J, Bragadóttir R, Moe MC. Ultra-widefield autofluorescence imaging in the evaluation of scleral buckling surgery for retinal detachment. Retina 2013;33:1421–1427.

228. Navaratnam J, Salvanos P, Vavvas DG, Bragadóttir R. Ultra-widefield autofluorescence imaging findings in retinoschisis, rhegmatogenous retinal detachment and combined retinoschisis retinal detachment. Acta Ophthalmol.

229. Francone A, Kothari N, Farajzadeh M, Hosseini H, Prasad P, Schwartz S, et al. Detection of neurosensory retinal detachment complicating degenerative retinoschisis by ultra-widefield fundus autofluorescence imaging. Retina 2020;40:819–824.