Fundus autofluorescence and its applications in retinal diseases_Chinese Journal of Ocular Fundus Diseases

Authors：

HanRuoan ,  ChenYouxin

Department of Ophthalmology, Peking Union Medical College Hospital, Chinese Academy of Medical Science, Beijing 100730, China;

Corresponding author：

ChenYouxin, Email: chenyouxinpumch@163.com

Keywords：

Fluorescence; Retinal diseases/diagnosis; Diagnostic imaging; Review

DOI：

10.3760/cma.j.issn.1005-1015.2017.01.027

Video：

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Abstract Full text Figures/Tables Video References Cited by

Autofluorescence is produced by lipofuscin in retinal pigment epithelium (RPE) cells which is induced by exciting light and enables the visualization of lipofuscin changes in the RPE cells, thus showing the function of RPE and photoreceptor cells. Fundus autofluorescence (FAF) imaging is a non-invasive imaging technique providing information of RPE and photoreceptor cells, which is not obtainable with other imaging modalities. The scope of applications includes identification of diseased RPE in retinal diseases, elucidating pathophysiological mechanisms, estimating disease progression and prognosis, guiding treatment protocols. Common fundus diseases have different pathological types, levels and causes, so they can cause various damages of RPE and photoreceptor cells which induce complicated FAF. It is worth to further observing and investigating the common retinal diseases' FAF characteristics and clinical applications.

Citation： HanRuoan, ChenYouxin. Fundus autofluorescence and its applications in retinal diseases. Chinese Journal of Ocular Fundus Diseases, 2017, 33(1): 83-86. doi: 10.3760/cma.j.issn.1005-1015.2017.01.027 Copy

1.	Bui TV, Han Y, Radu RA, et al. Characterization of native retinal fluorophores involved in biosynthesis of A2E and lipofuscin-associated retinopathesis[J]. J Biol Chem, 2006, 281(26): 18112-18119. DOI: 10.1074/jbc.M601380200.
2.	Robson AG, Moreland JD, Pauleikhoff D, et al. Macular pigment density and distribution: comparison of fundus autofluorescence with minimum motion photometry[J]. Vision Res, 2003, 43(16): 1765-1775.
3.	Bindewald A, Bird AC, Dandekar SS, et al. Classification of fundus autofluorescence patterns in early age-related macular disease[J]. Invest Ophthalmol Vis Sci, 2005, 46(9): 3309-3314. DOI: 10.1167/iovs.04-0430.
4.	Lois N, Owens SL, Coco R, et al. Fundus autofluorescence in patients with age-related macular degeneration and high risk of visual loss[J]. Am J Ophthalmol, 2002, 133(3): 341-349.
5.	Arnold JJ, Sarks SH, Killingsworth MC, et al. Reticular pseudodrusen: a risk factor in age-related maculopathy[J]. Retina, 1995, 15(3): 183-191.
6.	Schmitz-Valckenberg S, Steinberg JS, Fleckenstein M, et al. Combined confocal scanning laser ophthalmoscopy and spectral-domain optical coherence tomography imaging of reticular drusen associated with age-related macular degeneration[J]. Ophthalmology, 2010, 117(6): 1169-1176. DOI: 10.1016/j.ophtha. 2009.10.044.
7.	Smith RT, Chan JK, Busuoic M, et al. Autofluorescence characteristics of early atrophic and high-risk fellow eyes in age-related macular degeneration[J]. Invest Ophthalmol Vis Sci, 2006, 47(12): 5495-5504. DOI: 10.1167/iovs.05-1318.
8.	Finger RP, Wu Z, Luu CD, et al. Reticular pseudodrusen: a risk factor for geographic atrophy in fellow eyes of individuals with unilateral choroidal neovascularization[J]. Ophthalmology, 2014, 121(6): 1252-1256. DOI: 10.1016/j.ophtha.2013.12.034.
9.	Pumariega NM, Smith RT, Sohrab MA, et al. A prospective study of reticular macular disease[J]. Ophthalmology, 2011, 118(8): 1619-1625. DOI: 10.1016/j.ophtha.2011.01.029.
10.	Schmitz-Valckenberg S, Bultmann S, Dreyhaupt J, et al. Fundus autofluorescence and fundus perimetry in the junctional zone of geographic atrophy in patients with age-related macular degeneration[J]. Invest Ophthalmol Vis Sci, 2004, 45(12): 4470-4476. DOI: 10.1167/iovs.03-1311.
11.	Pilotto E, Benetti E, Convento E, et al. Microperimetry, fundus autofluorescence, and retinal layer changes in progressing geographic atrophy[J]. Can J Ophthalmol, 2013, 48(5): 386-393. DOI: 10.1016/j.jcjo.2013.03.022.
12.	Fritsche LG, Fleckenstein M, Fiebig BS, et al. A subgroup of age-related macular degeneration is associated with mono-allelic sequence variants in the ABCA4 gene[J]. Invest Ophthalmol Vis Sci, 2012, 53(4): 2112-2118. DOI: 10.1167/iovs.11-8785.
13.	Holz FG, Bindewald-wittich A, Fleckestein M, et al. Progression of geographic atrophy and impact of fundus autofluorescence patterns in age-related macular degeneration[J]. Am J Ophthalmol, 2007, 143(3): 463-472. DOI: 10.1016/j.ajo.2006.11.041.
14.	Fleckenstein M, Schmitz-Valckenberg S, Lindner M, et al. The “diffuse-trickling” fundus autofluorescence phenotype in geographic atrophy[J]. Invest Ophthalmol Vis Sci, 2014, 55(5): 2911-2920. DOI: 10.1167/iovs.13-13409.
15.	Fleckenstein M, Charbel Issa P, Helb HM, et al. High-resolution spectral domain-OCT imaging in geographic atrophy associated with age-related macular degeneration[J]. Invest Ophthalmol Vis Sci, 2008, 49(9): 4137-4144. DOI: 10.1167/iovs.08-1967.
16.	Vaclavik V, Vujosevic S, Dandekar SS, et al. Autofluorescence imaging in age-related macular degeneration complicated by choroidal neovascularization: a prospective study[J]. Ophthalmology, 2008, 115(2): 342-346. DOI: 10.1016/ j.ophtha.2007.04.023.
17.	Kumar N, Mrejen S, Fung AT, et al. Retinal pigment epithelial cell loss assessed by fundus autofluorescence imaging in neovascular age-related macular degeneration[J]. Ophthalmology, 2013, 120(2): 334-341. DOI: 10.1016/j.ophtha.2012.07.076.
18.	Sparrow JR, Zhou J, Ben-Shabat S, et al. Involvement of oxidative mechanisms in blue-light-induced damage to A2E-laden RPE[J]. Invest Ophthalmol Vis Sci, 2002, 43(4): 1222-1227.
19.	Solbach U, Keilhauer C, Knabben H, et al. Imaging of retinal autofluorescence in patients with age-related macular degeneration[J]. Retina, 1997, 17(5): 385-389.
20.	Holz FG, Bellman C, Staudt S, et al. Fundus autofluorescence and development of geographic atrophy in age-related macular degeneration[J]. Invest Ophthalmol Vis Sci, 2001, 42(5): 1051-1056.
21.	Yannuzzi LA, Sorenson J, Spaide RF, et al. Idiopathic polypoidal choroidal vasculopathy (IPCV)[J]. Retina, 1990, 10: 1-8.
22.	Yamagishi T, Koizumi H, Yamazaki T, et al. Fundus autofluorescence in polypoidal choroidal vasculopathy[J]. Ophthalmology, 2012, 119(8):1650-1657. DOI: 10.1016/j.ophtha. 2012.02.016.
23.	Popović P, Jarc-Vidmar M, Hawlina M. Abnormal fundus autofluorescence in relation to retinal function in patients with retinitis pigmentosa[J]. Graefe’s Arch Clin Exp Ophthalmol, 2005, 243(10): 1018-1027. DOI: 10.1007/s00417-005-1186-x.
24.	Ogura S, Yasukawa T, Kato A, et al. Wide-field fundus autofluorescence imaging to evaluate retinal function in patients with retinitis pigmentosa[J]. Am J Ophthalmol, 2014, 158(5): 1093-1098. DOI: 10.1016/j.ajo.2014.07.021.
25.	Oishi A, Oishi M, Ogino K, et al. Wide-field fundus autofluorescence for retinitis pigmentosa and cone/cone-rod dystrophy[J]. Adv Exp Med Biol, 2016, 854: 307-313. DOI:10.1007/ 978-3-319-17121-0_41.
26.	Carsten F, Andress W, Bernhard G, et al. Fundus autofluorescence in acute and chronic-recurrent central serous chorioretinopathy[J]. Acta Ophthalmol Scand, 2005, 83(2): 161-167. DOI: 10.1111/j.1600-0420.2005.00442.x.
27.	Von Rückmann A, Fizke FW, Fan J, et al. Abnormalities of fundus autofluorescence in central serous retinopathy[J]. Am J Ophthalmol, 2002, 133(6): 780-786.
28.	Matsumoto H, Kishi S, Sato T, et al. Fundus autofluorescence of elongated photoreceptor outer segments in central serous chorioretinopathy[J]. Am J Ophthalmol, 2011, 151(4): 617-623. DOI: 10.1016/j.ajo.2010.09.031.
29.	Spaide RF, Klancnik JM Jr. Fundus autofluorescence and central serous chorioretinopathy[J]. Ophthalmology, 2005, 112(5): 825-833. DOI: 10.1016/j.ophtha.2005.01.003.
30.	Imamura Y, Fujiwara T, Spaide RF. Fundus autofluorescence and visual acuity in central serous chorioretinopathy[J]. Ophthalmology, 2011, 118(4): 700-705. DOI: 10.1016/j.ophtha.2010.08.017.
31.	Boon CJ, Klevering BJ, Keunen JE, et al. Fundus autoflorescence imaging of retinal dystrophies[J]. Vision Res, 2008, 48(26): 2569-2577. DOI: 10.1016/j.visres.2008.01.010.
32.	Parodi MB, Iacono P, Del Turco C, et al. Near-infrared fundus autofluorescence in subclinical best vitelliform macular dystrophy[J]. Am J Ophthalmol, 2014, 158(6): 1247-1252. DOI: 10.1016/j.ajo.2014.08.028.
33.	Sparrow JR, Zhou J, Ben-Shabat S, et al. Involvement of oxidative mechanisms in blue-light-induced damage to A2E-laden RPE[J]. Invest Ophthalmol Vis Sci, 2002, 43(4): 1222-1227.
34.	Taku W, Yasushi I, Kaorio S, et al. Fundus autofluorescence related to retinal morphological and functional changes in idiopathic macular holes[J]. Acta Ophthalmol, 2008, 86(8): 897-901. DOI: 10.1111/j.1755-3768.2007.01163.x.
35.	Kao TY, Yang CM, Yeh PT, et al. The value of combining autofluorescence and optical coherence tomography in predicting the visual prognosis of sealed macular hole[J]. Am J Ophthalmol, 2013, 156(1): 149-156. DOI: 10.1016/j.ajo.2013.02.005.
36.	Shields CL, Cater J, Shields JA, et al. Combination of clinical factor predictive of growth of small choroidal melanocytic tumors[J]. Arch Ophthalmol, 2000, 118(3): 360-364.
37.	Gündüz K, Pulido JS, Ezzat K, et al. Review of fundus autofluorescence in choroidal melanocytic lesions[J]. Eye, 2009, 23(3): 497-503. DOI: 10.1038/eye.2008.244.
38.	Gass JD. Acute zonal occult outer retinopathy. Donders lecture: The Netherlands Ophthalmological Society, Maastricht, Holland, June 19, 1992[J]. J Clin Neuroophthalmol, 1993, 13(2): 79-97.
39.	Gass JD. Are acute zonal occult outer retinopathy and the white spot syndromes (AZOOR complex) specific autoimmune diseases?[J]. Am J Ophthalmol, 2003, 135(3): 380-381.
40.	Bryan RG, Freund KB, Yannuzzi LA, et al. Multiple evanescent white dot syndrome in patients with multifocal choroiditis[J]. Retina, 2002, 22(3): 317-322.
41.	Taira K, Nakazawa M, Takano Y, et al. Acute zonal occult outer retinopathy in the fellow eye 5 years after pre- sentation of punctate inner choroidopathy[J]. Graefe’s Arch Clin Exp Ophthalmol, 2006, 244(7): 880-882. DOI: 10.1007/s00417-005-0172-7.
42.	Fine HF, Spaide RF, Ryan EH, et al. Acute zonal occult outer retinopathy in patients with multiple evanescent white dot syndrome[J]. Arch Ophthalmol, 2009, 127(1): 66-70. DOI: 10.1001/archophthalmol.2008.530.
43.	Mrejen S, Khan S, Galleogo-Pinazo, et al. Acute zonal occult outer retinopathy: a classification based on multimodal imaging[J]. JAMA Ophthalmol, 2014, 132(9): 1089-1098. DOI: 10.1001/jamaoph thalmol.2014.1683.
44.	Li M, Zhang X, Wen F. The fundus autofluorescence spectrum of punctate inner choroidopathy[J/OL]. J Ophthalmol, 2015, 2015: 202097[2015-07-22]. https://dx.doi.org/10.1155/2015/202097. DOI: 10.1155/2015/202097.

1. Bui TV, Han Y, Radu RA, et al. Characterization of native retinal fluorophores involved in biosynthesis of A2E and lipofuscin-associated retinopathesis[J]. J Biol Chem, 2006, 281(26): 18112-18119. DOI: 10.1074/jbc.M601380200.
2. Robson AG, Moreland JD, Pauleikhoff D, et al. Macular pigment density and distribution: comparison of fundus autofluorescence with minimum motion photometry[J]. Vision Res, 2003, 43(16): 1765-1775.
3. Bindewald A, Bird AC, Dandekar SS, et al. Classification of fundus autofluorescence patterns in early age-related macular disease[J]. Invest Ophthalmol Vis Sci, 2005, 46(9): 3309-3314. DOI: 10.1167/iovs.04-0430.
4. Lois N, Owens SL, Coco R, et al. Fundus autofluorescence in patients with age-related macular degeneration and high risk of visual loss[J]. Am J Ophthalmol, 2002, 133(3): 341-349.
5. Arnold JJ, Sarks SH, Killingsworth MC, et al. Reticular pseudodrusen: a risk factor in age-related maculopathy[J]. Retina, 1995, 15(3): 183-191.
6. Schmitz-Valckenberg S, Steinberg JS, Fleckenstein M, et al. Combined confocal scanning laser ophthalmoscopy and spectral-domain optical coherence tomography imaging of reticular drusen associated with age-related macular degeneration[J]. Ophthalmology, 2010, 117(6): 1169-1176. DOI: 10.1016/j.ophtha. 2009.10.044.
7. Smith RT, Chan JK, Busuoic M, et al. Autofluorescence characteristics of early atrophic and high-risk fellow eyes in age-related macular degeneration[J]. Invest Ophthalmol Vis Sci, 2006, 47(12): 5495-5504. DOI: 10.1167/iovs.05-1318.
8. Finger RP, Wu Z, Luu CD, et al. Reticular pseudodrusen: a risk factor for geographic atrophy in fellow eyes of individuals with unilateral choroidal neovascularization[J]. Ophthalmology, 2014, 121(6): 1252-1256. DOI: 10.1016/j.ophtha.2013.12.034.
9. Pumariega NM, Smith RT, Sohrab MA, et al. A prospective study of reticular macular disease[J]. Ophthalmology, 2011, 118(8): 1619-1625. DOI: 10.1016/j.ophtha.2011.01.029.
10. Schmitz-Valckenberg S, Bultmann S, Dreyhaupt J, et al. Fundus autofluorescence and fundus perimetry in the junctional zone of geographic atrophy in patients with age-related macular degeneration[J]. Invest Ophthalmol Vis Sci, 2004, 45(12): 4470-4476. DOI: 10.1167/iovs.03-1311.
11. Pilotto E, Benetti E, Convento E, et al. Microperimetry, fundus autofluorescence, and retinal layer changes in progressing geographic atrophy[J]. Can J Ophthalmol, 2013, 48(5): 386-393. DOI: 10.1016/j.jcjo.2013.03.022.
12. Fritsche LG, Fleckenstein M, Fiebig BS, et al. A subgroup of age-related macular degeneration is associated with mono-allelic sequence variants in the ABCA4 gene[J]. Invest Ophthalmol Vis Sci, 2012, 53(4): 2112-2118. DOI: 10.1167/iovs.11-8785.
13. Holz FG, Bindewald-wittich A, Fleckestein M, et al. Progression of geographic atrophy and impact of fundus autofluorescence patterns in age-related macular degeneration[J]. Am J Ophthalmol, 2007, 143(3): 463-472. DOI: 10.1016/j.ajo.2006.11.041.
14. Fleckenstein M, Schmitz-Valckenberg S, Lindner M, et al. The “diffuse-trickling” fundus autofluorescence phenotype in geographic atrophy[J]. Invest Ophthalmol Vis Sci, 2014, 55(5): 2911-2920. DOI: 10.1167/iovs.13-13409.
15. Fleckenstein M, Charbel Issa P, Helb HM, et al. High-resolution spectral domain-OCT imaging in geographic atrophy associated with age-related macular degeneration[J]. Invest Ophthalmol Vis Sci, 2008, 49(9): 4137-4144. DOI: 10.1167/iovs.08-1967.
16. Vaclavik V, Vujosevic S, Dandekar SS, et al. Autofluorescence imaging in age-related macular degeneration complicated by choroidal neovascularization: a prospective study[J]. Ophthalmology, 2008, 115(2): 342-346. DOI: 10.1016/ j.ophtha.2007.04.023.
17. Kumar N, Mrejen S, Fung AT, et al. Retinal pigment epithelial cell loss assessed by fundus autofluorescence imaging in neovascular age-related macular degeneration[J]. Ophthalmology, 2013, 120(2): 334-341. DOI: 10.1016/j.ophtha.2012.07.076.
18. Sparrow JR, Zhou J, Ben-Shabat S, et al. Involvement of oxidative mechanisms in blue-light-induced damage to A2E-laden RPE[J]. Invest Ophthalmol Vis Sci, 2002, 43(4): 1222-1227.
19. Solbach U, Keilhauer C, Knabben H, et al. Imaging of retinal autofluorescence in patients with age-related macular degeneration[J]. Retina, 1997, 17(5): 385-389.
20. Holz FG, Bellman C, Staudt S, et al. Fundus autofluorescence and development of geographic atrophy in age-related macular degeneration[J]. Invest Ophthalmol Vis Sci, 2001, 42(5): 1051-1056.
21. Yannuzzi LA, Sorenson J, Spaide RF, et al. Idiopathic polypoidal choroidal vasculopathy (IPCV)[J]. Retina, 1990, 10: 1-8.
22. Yamagishi T, Koizumi H, Yamazaki T, et al. Fundus autofluorescence in polypoidal choroidal vasculopathy[J]. Ophthalmology, 2012, 119(8):1650-1657. DOI: 10.1016/j.ophtha. 2012.02.016.
23. Popović P, Jarc-Vidmar M, Hawlina M. Abnormal fundus autofluorescence in relation to retinal function in patients with retinitis pigmentosa[J]. Graefe’s Arch Clin Exp Ophthalmol, 2005, 243(10): 1018-1027. DOI: 10.1007/s00417-005-1186-x.
24. Ogura S, Yasukawa T, Kato A, et al. Wide-field fundus autofluorescence imaging to evaluate retinal function in patients with retinitis pigmentosa[J]. Am J Ophthalmol, 2014, 158(5): 1093-1098. DOI: 10.1016/j.ajo.2014.07.021.
25. Oishi A, Oishi M, Ogino K, et al. Wide-field fundus autofluorescence for retinitis pigmentosa and cone/cone-rod dystrophy[J]. Adv Exp Med Biol, 2016, 854: 307-313. DOI:10.1007/ 978-3-319-17121-0_41.
26. Carsten F, Andress W, Bernhard G, et al. Fundus autofluorescence in acute and chronic-recurrent central serous chorioretinopathy[J]. Acta Ophthalmol Scand, 2005, 83(2): 161-167. DOI: 10.1111/j.1600-0420.2005.00442.x.
27. Von Rückmann A, Fizke FW, Fan J, et al. Abnormalities of fundus autofluorescence in central serous retinopathy[J]. Am J Ophthalmol, 2002, 133(6): 780-786.
28. Matsumoto H, Kishi S, Sato T, et al. Fundus autofluorescence of elongated photoreceptor outer segments in central serous chorioretinopathy[J]. Am J Ophthalmol, 2011, 151(4): 617-623. DOI: 10.1016/j.ajo.2010.09.031.
29. Spaide RF, Klancnik JM Jr. Fundus autofluorescence and central serous chorioretinopathy[J]. Ophthalmology, 2005, 112(5): 825-833. DOI: 10.1016/j.ophtha.2005.01.003.
30. Imamura Y, Fujiwara T, Spaide RF. Fundus autofluorescence and visual acuity in central serous chorioretinopathy[J]. Ophthalmology, 2011, 118(4): 700-705. DOI: 10.1016/j.ophtha.2010.08.017.
31. Boon CJ, Klevering BJ, Keunen JE, et al. Fundus autoflorescence imaging of retinal dystrophies[J]. Vision Res, 2008, 48(26): 2569-2577. DOI: 10.1016/j.visres.2008.01.010.
32. Parodi MB, Iacono P, Del Turco C, et al. Near-infrared fundus autofluorescence in subclinical best vitelliform macular dystrophy[J]. Am J Ophthalmol, 2014, 158(6): 1247-1252. DOI: 10.1016/j.ajo.2014.08.028.
33. Sparrow JR, Zhou J, Ben-Shabat S, et al. Involvement of oxidative mechanisms in blue-light-induced damage to A2E-laden RPE[J]. Invest Ophthalmol Vis Sci, 2002, 43(4): 1222-1227.
34. Taku W, Yasushi I, Kaorio S, et al. Fundus autofluorescence related to retinal morphological and functional changes in idiopathic macular holes[J]. Acta Ophthalmol, 2008, 86(8): 897-901. DOI: 10.1111/j.1755-3768.2007.01163.x.
35. Kao TY, Yang CM, Yeh PT, et al. The value of combining autofluorescence and optical coherence tomography in predicting the visual prognosis of sealed macular hole[J]. Am J Ophthalmol, 2013, 156(1): 149-156. DOI: 10.1016/j.ajo.2013.02.005.
36. Shields CL, Cater J, Shields JA, et al. Combination of clinical factor predictive of growth of small choroidal melanocytic tumors[J]. Arch Ophthalmol, 2000, 118(3): 360-364.
37. Gündüz K, Pulido JS, Ezzat K, et al. Review of fundus autofluorescence in choroidal melanocytic lesions[J]. Eye, 2009, 23(3): 497-503. DOI: 10.1038/eye.2008.244.
38. Gass JD. Acute zonal occult outer retinopathy. Donders lecture: The Netherlands Ophthalmological Society, Maastricht, Holland, June 19, 1992[J]. J Clin Neuroophthalmol, 1993, 13(2): 79-97.
39. Gass JD. Are acute zonal occult outer retinopathy and the white spot syndromes (AZOOR complex) specific autoimmune diseases?[J]. Am J Ophthalmol, 2003, 135(3): 380-381.
40. Bryan RG, Freund KB, Yannuzzi LA, et al. Multiple evanescent white dot syndrome in patients with multifocal choroiditis[J]. Retina, 2002, 22(3): 317-322.
41. Taira K, Nakazawa M, Takano Y, et al. Acute zonal occult outer retinopathy in the fellow eye 5 years after pre- sentation of punctate inner choroidopathy[J]. Graefe’s Arch Clin Exp Ophthalmol, 2006, 244(7): 880-882. DOI: 10.1007/s00417-005-0172-7.
42. Fine HF, Spaide RF, Ryan EH, et al. Acute zonal occult outer retinopathy in patients with multiple evanescent white dot syndrome[J]. Arch Ophthalmol, 2009, 127(1): 66-70. DOI: 10.1001/archophthalmol.2008.530.
43. Mrejen S, Khan S, Galleogo-Pinazo, et al. Acute zonal occult outer retinopathy: a classification based on multimodal imaging[J]. JAMA Ophthalmol, 2014, 132(9): 1089-1098. DOI: 10.1001/jamaoph thalmol.2014.1683.
44. Li M, Zhang X, Wen F. The fundus autofluorescence spectrum of punctate inner choroidopathy[J/OL]. J Ophthalmol, 2015, 2015: 202097[2015-07-22]. 10.1155/2015/202097">https://dx.doi.org/10.1155/2015/202097. DOI: 10.1155/2015/202097.

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