Progress in the application of leakage index in retinal diseases_Chinese Journal of Ocular Fundus Diseases

Authors：

Cheng Yufang ,  Chen Changzheng

Department of Ophthalmology Renmin Hospital of Wuhan University, Wuhan 430060, China;

Corresponding author：

Chen Changzheng, Email: whuchenchzh@163.com

Keywords：

Leakage; Leakage index; Retinal disease; Review

DOI：

10.3760/cma.j.cn511434-20210308-00125

Video：

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Abstract Full text Figures/Tables Video References Cited by

Retinal leakage is not only a very common pathological phenomenon but also a common pathological feature of many retinal diseases, its pathogenesis is very complex. The application of ultra-wide-angle fluorescein angiography is one of the main means to observe and evaluate retinal leakage. Leakage index is a new index for evaluating retinal leakage. Studies have explored its correlation in diabetic retinopathy, retinal vein occlusion, uveitis and other diseases, evaluating treatment effects and predicting prognosis. However, the number of related studies is small and the conclusions are inconsistent. In the future, it is still necessary to further advance the quantitative analysis of leakage, the application of leakage in more diseases, and the clinical trials of leakage rate to explore its role in predicting and evaluating treatment effects in retinal diseases.

Citation： Cheng Yufang, Chen Changzheng. Progress in the application of leakage index in retinal diseases. Chinese Journal of Ocular Fundus Diseases, 2022, 38(7): 606-609. doi: 10.3760/cma.j.cn511434-20210308-00125 Copy

1.	Wang X, Sun G, Yi Z. Leakage index on ultra-widefield fluorescence angiography in different regions of retina and its correlation with cystoid macular edema in central retinal vein occlusion eyes[J]. Graefe's Arch Clin Exp Ophthalmol, 2021, 259(8): 2149-2156. DOI: 10.1007/s00417-021-05126-y.
2.	谷去非, 母林华. 葡萄膜炎42例眼底荧光造影特征分析[J]. 中国现代医药杂志, 2007, 9(6): 12. DOI: 10.3969/j.issn.1672-9463.2007.06.036.Gu QF, Mu LH. Analysis of the characteristics of fundus fluorescein angiography in 42 cases of uveitis[J]. Modern Medicine Journal of China, 2007, 9(6): 12. DOI: 10.3969/j.issn.1672-9463.2007.06.036.
3.	Early Treatment Diabetic Retinopathy Study Research Group. Grading diabetic retinopathy from stereoscopic color fundus photographs--an extension of the modified airlie house classification. ETDRS report number 10[J]. Ophthalmology, 1991, 98(5 Suppl): S786-806.
4.	Tsui I, Kaines A, Havunjian MA, et al. Ischemic index and neovascularization in central retinal vein occlusion[J]. Retina, 2011, 31(1): 105-110. DOI: 10.1097/IAE.0b013e3181e36c6d.
5.	Prasad PS, Oliver SC, Coffee RE, et al. Ultra wide-field angiographic characteristics of branch retinal and hemicentral retinal vein occlusion[J]. Ophthalmology, 2010, 117(4): 780-784. DOI: 10.1016/j.ophtha.2009.09.019.
6.	Wessel MM, Aaker GD, Parlitsis G, et al. Ultra-wide-field angiography improves the detection and classification of diabetic retinopathy[J]. Retina, 2012, 32(4): 785-791. DOI: 10.1097/IAE.0b013e3182278b64.
7.	Karampelas M, Sim DA, Chu C, et al. Quantitative analysis of peripheral vasculitis, ischemia, and vascular leakage in uveitis using ultra-widefield fluorescein angiography[J]. Am J Ophthalmol, 2015, 159(6): 1161-1168. DOI: 10.1016/j.ajo.2015.02.009.
8.	陈长征, 王晓玲. 正确分析周边部视网膜超广角荧光素眼底血管造影特征[J]. 中华实验眼科杂志, 2020, 38(7): 562-565. DOI: 10.3760/cma.j.cn115989-20190401-00158.Chen CZ, Wang XL. To correctly analyze ultra-wide field fluorescein angiography in peripheral retina[J]. Chin J Exp Ophthalmol, 2020, 38(7): 562-565. DOI: 10.3760/cma.j.cn115989-20190401-00158.
9.	Quinn N, Csincsik L, Flynn E, et al. The clinical relevance of visualising the peripheral retina[J]. Prog Retin Eye Res, 2019, 68: 83-109. DOI: 10.1016/j.preteyeres.2018.10.001.
10.	Bhagat N, Grigorian RA, Tutela A, et al. Diabetic macular edema: pathogenesis and treatment[J]. Surv Ophthalmol, 2009, 54(1): 1-32. DOI: 10.1016/j.survophthal.2008.10.001.
11.	Ehlers JP, Jiang AC, Boss JD, et al. Quantitative ultra-widefield angiography and diabetic retinopathy severity[J]. Ophthalmology, 2019, 126(11): 1527-1532. DOI: 10.1016/j.ophtha.2019.05.034.
12.	ValdezGuerrero AS, Quintana-Pérez JC, Arellano-Mendoza MG, et al. Diabetic retinopathy: important biochemical alterations and the main treatment strategies[J]. Can J Diabetes, 2021, 45(6): 504-511. DOI: 10.1016/j.jcjd.2020.10.009.
13.	Mitry D, Bunce C, Charteris D. Anti-vascular endothelial growth factor for macular oedema secondary to branch retinal vein occlusion[J/OL]. Cochrane Database Syst Rev, 2013(1): D9510[2013-01-31]. https://pubmed.ncbi.nlm.nih.gov/23440840/. DOI: 10.1002/14651858.CD009510.pub2.
14.	许阿敏, 陈长征, 易佐慧子, 等. 糖尿病视网膜病变超广角荧光素眼底血管造影检查与标准7视野检查结果的对比分析[J]. 中华眼底病杂志, 2017, 33(1): 23-26. DOI: 10.3760/cma.j.issn.1005-1015.2017.01.007.Xu AM, Chen CZ, Yi ZHZ, et al. Comparative analysis of ultra-wide-field fluorescein angiography and early treatment diabetic retinopathy study 7 standard field photography in diabetic retinopathy[J]. Chin J Ocul Fundus Dis, 2017, 33(1): 23-26. DOI: 10.3760/cma.j.issn.1005-1015.2017.01.007.
15.	Thomas AS, Thomas MK, Finn AP, et al. Use of the ischemic index on widefield fluorescein angiography to characterize a central retinal vein occlusion as ischemic or nonischemic[J]. Retina, 2019, 39(6): 1033-1038. DOI: 10.1097/IAE.0000000000002126.
16.	Price LD, Au S, Chong NV. Optomap ultrawide field imaging identifies additional retinal abnormalities in patients with diabetic retinopathy[J]. Clin Ophthalmol, 2015, 9: 527-531. DOI: 10.2147/OPTH.S79448.
17.	Oliver SC, Schwartz SD. Peripheral vessel leakage (PVL): a new angiographic finding in diabetic retinopathy identified with ultra wide-field fluorescein angiography[J]. Semin Ophthalmol, 2010, 25(1-2): 27-33. DOI: 10.3109/08820538.2010.481239.
18.	Sim DA, Keane PA, Rajendram R, et al. Patterns of peripheral retinal and central macula ischemia in diabetic retinopathy as evaluated by ultra-widefield fluorescein angiography[J]. Am J Ophthalmol, 2014, 158(1): 144-153. DOI: 10.1016/j.ajo.2014.03.009.
19.	Singer M, Sagong M, van Hemert J, et al. Ultra-widefield imaging of the peripheral retinal vasculature in normal subjects[J]. Ophthalmology, 2016, 123(5): 1053-1059. DOI: 10.1016/j.ophtha.2016.01.022.
20.	Ehlers JP, Wang K, Vasanji A, et al. Automated quantitative characterisation of retinal vascular leakage and microaneurysms in ultra-widefield fluorescein angiography[J]. Br J Ophthalmol, 2017, 101(6): 696-699. DOI: 10.1136/bjophthalmol-2016-310047.
21.	Silva PS, Dela CA, Ledesma MG, et al. Diabetic retinopathy severity and peripheral lesions are associated with nonperfusion on ultrawide field angiography[J]. Ophthalmology, 2015, 122(12): 2465-2472. DOI: 10.1016/j.ophtha.2015.07.034.
22.	Hajdu D, Sedova A, Datlinger F, et al. Association of macular perfusion status with microvascular parameters up to the far periphery in diabetic retinopathy using multimodal imaging[J]. Int J Retina Vitreous, 2020, 6(1): 50. DOI: 10.1186/s40942-020-00253-w.
23.	Hariprasad SM, Mieler WF, Grassi M, et al. Vision-related quality of life in patients with diabetic macular oedema[J]. Br J Ophthalmol, 2008, 92(1): 89-92. DOI: 10.1136/bjo.2007.122416.
24.	Jiang AC, Srivastava SK, Hu M, et al. Quantitative ultra-widefield angiographic features and associations with diabetic macular edema[J]. Ophthalmol Retina, 2020, 4(1): 49-56. DOI: 10.1016/j.oret.2019.08.008.
25.	Nguyen QD, Brown DM, Marcus DM, et al. Ranibizumab for diabetic macular edema: results from 2 phase Ⅲ randomized trials: RISE and RIDE[J]. Ophthalmology, 2012, 119(4): 789-801. DOI: 10.1016/j.ophtha.2011.12.039.
26.	Bonnin S, Dupas B, Lavia C, et al. Anti-vascular endothelial growth factor therapy can improve diabetic retinopathy score without change in retinal perfusion[J]. Retina, 2019, 39(3): 426-434. DOI: 10.1097/IAE.0000000000002422.
27.	Bressler SB, Liu D, Glassman AR, et al. Change in diabetic retinopathy through 2 years: secondary analysis of a randomized clinical trial comparing aflibercept, bevacizumab, and ranibizumab[J]. JAMA Ophthalmol, 2017, 135(6): 558-568. DOI: 10.1001/jamaophthalmol.2017.0821.
28.	Chandra S, Sheth J, Anantharaman G, et al. Ranibizumab-induced retinal reperfusion and regression of neovascularization in diabetic retinopathy: an angiographic illustration[J]. Am J Ophthalmol Case Rep, 2018, 9: 41-44. DOI: 10.1016/j.ajoc.2018.01.006.
29.	Gupta MP, Kiss S, Chan R. Reversal of retinal vascular leakage and arrest of progressive retinal nonperfusion with monthly anti-vascular endothelial growth factor therapy for proliferative diabetic retinopathy[J/OL]. Retina, 2018, 38(9): e74-e75[2018-09-01]. https://pubmed.ncbi.nlm.nih.gov/30005003/. DOI: 10.1097/IAE.0000000000002261.
30.	Levin AM, Rusu I, Orlin A, et al. Retinal reperfusion in diabetic retinopathy following treatment with anti-VEGF intravitreal injections[J]. Clin Ophthalmol, 2017, 11: 193-200. DOI: 10.2147/OPTH.S118807.
31.	Allingham MJ, Mukherjee D, Lally EB, et al. A quantitative approach to predict differential effects of anti-VEGF treatment on diffuse and focal leakage in patients with diabetic macular edema: a pilot study[J]. Transl Vis Sci Technol, 2017, 6(2): 7. DOI: 10.1167/tvst.6.2.7.
32.	Babiuch AS, Wykoff CC, Srivastava SK, et al. Retinal leakage index dynamics on ultra-widefield fluorescein angiography in eyes treated with intravitreal aflibercept for proliferative diabetic retinopathy in the recovery study[J]. Retina, 2020, 40(11): 2175-2183. DOI: 10.1097/IAE.0000000000002727.
33.	Yu HJ, Ehlers JP, Sevgi DD, et al. Real-time photographic- and fluorescein angiographic-guided management of diabetic retinopathy: randomized prime trial outcomes[J]. Am J Ophthalmol, 2021, 226: 126-136. DOI: 10.1016/j.ajo.2021.01.024.
34.	McIntosh RL, Rogers SL, Lim L, et al. Natural history of central retinal vein occlusion: an evidence-based systematic review[J]. Ophthalmology, 2010, 117(6): 1113-1123. DOI: 10.1016/j.ophtha.2010.01.060.
35.	Hayreh SS, Podhajsky PA, Zimmerman MB. Natural history of visual outcome in central retinal vein occlusion[J]. Ophthalmology, 2011, 118(1): 119-133. DOI: 10.1016/j.ophtha.2010.04.019.
36.	Manivannan A, Plskova J, Farrow A, et al. Ultra-wide-field fluorescein angiography of the ocular fundus[J]. Am J Ophthalmol, 2005, 140(3): 525-527. DOI: 10.1016/j.ajo.2005.02.055.
37.	Campbell JP, Leder HA, Sepah YJ, et al. Wide-field retinal imaging in the management of noninfectious posterior uveitis[J]. Am J Ophthalmol, 2012, 154(5): 908-911. DOI: 10.1016/j.ajo.2012.05.019.
38.	Fang M, Fan W, Shi Y, et al. Classification of regions of nonperfusion on ultra-widefield fluorescein angiography in patients with diabetic macular edema[J]. Am J Ophthalmol, 2019, 206: 74-81. DOI: 10.1016/j.ajo.2019.03.030.
39.	Rabiolo A, Cicinelli MV, Corbelli E, et al. Correlation analysis between foveal avascular zone and peripheral ischemic index in diabetic retinopathy: a pilot study[J]. Ophthalmol Retina, 2018, 2(1): 46-52. DOI: 10.1016/j.oret.2017.05.007.
40.	Sakimoto S, Kamei M, Suzuki M, et al. Relationship between grades of macular perfusion and foveal thickness in branch retinal vein occlusion[J]. Clin Ophthalmol, 2013, 7: 39-45. DOI: 10.2147/OPTH.S37185.

1. Wang X, Sun G, Yi Z. Leakage index on ultra-widefield fluorescence angiography in different regions of retina and its correlation with cystoid macular edema in central retinal vein occlusion eyes[J]. Graefe's Arch Clin Exp Ophthalmol, 2021, 259(8): 2149-2156. DOI: 10.1007/s00417-021-05126-y.
2. 谷去非, 母林华. 葡萄膜炎42例眼底荧光造影特征分析[J]. 中国现代医药杂志, 2007, 9(6): 12. DOI: 10.3969/j.issn.1672-9463.2007.06.036.Gu QF, Mu LH. Analysis of the characteristics of fundus fluorescein angiography in 42 cases of uveitis[J]. Modern Medicine Journal of China, 2007, 9(6): 12. DOI: 10.3969/j.issn.1672-9463.2007.06.036.
3. Early Treatment Diabetic Retinopathy Study Research Group. Grading diabetic retinopathy from stereoscopic color fundus photographs--an extension of the modified airlie house classification. ETDRS report number 10[J]. Ophthalmology, 1991, 98(5 Suppl): S786-806.
4. Tsui I, Kaines A, Havunjian MA, et al. Ischemic index and neovascularization in central retinal vein occlusion[J]. Retina, 2011, 31(1): 105-110. DOI: 10.1097/IAE.0b013e3181e36c6d.
5. Prasad PS, Oliver SC, Coffee RE, et al. Ultra wide-field angiographic characteristics of branch retinal and hemicentral retinal vein occlusion[J]. Ophthalmology, 2010, 117(4): 780-784. DOI: 10.1016/j.ophtha.2009.09.019.
6. Wessel MM, Aaker GD, Parlitsis G, et al. Ultra-wide-field angiography improves the detection and classification of diabetic retinopathy[J]. Retina, 2012, 32(4): 785-791. DOI: 10.1097/IAE.0b013e3182278b64.
7. Karampelas M, Sim DA, Chu C, et al. Quantitative analysis of peripheral vasculitis, ischemia, and vascular leakage in uveitis using ultra-widefield fluorescein angiography[J]. Am J Ophthalmol, 2015, 159(6): 1161-1168. DOI: 10.1016/j.ajo.2015.02.009.
8. 陈长征, 王晓玲. 正确分析周边部视网膜超广角荧光素眼底血管造影特征[J]. 中华实验眼科杂志, 2020, 38(7): 562-565. DOI: 10.3760/cma.j.cn115989-20190401-00158.Chen CZ, Wang XL. To correctly analyze ultra-wide field fluorescein angiography in peripheral retina[J]. Chin J Exp Ophthalmol, 2020, 38(7): 562-565. DOI: 10.3760/cma.j.cn115989-20190401-00158.
9. Quinn N, Csincsik L, Flynn E, et al. The clinical relevance of visualising the peripheral retina[J]. Prog Retin Eye Res, 2019, 68: 83-109. DOI: 10.1016/j.preteyeres.2018.10.001.
10. Bhagat N, Grigorian RA, Tutela A, et al. Diabetic macular edema: pathogenesis and treatment[J]. Surv Ophthalmol, 2009, 54(1): 1-32. DOI: 10.1016/j.survophthal.2008.10.001.
11. Ehlers JP, Jiang AC, Boss JD, et al. Quantitative ultra-widefield angiography and diabetic retinopathy severity[J]. Ophthalmology, 2019, 126(11): 1527-1532. DOI: 10.1016/j.ophtha.2019.05.034.
12. ValdezGuerrero AS, Quintana-Pérez JC, Arellano-Mendoza MG, et al. Diabetic retinopathy: important biochemical alterations and the main treatment strategies[J]. Can J Diabetes, 2021, 45(6): 504-511. DOI: 10.1016/j.jcjd.2020.10.009.
13. Mitry D, Bunce C, Charteris D. Anti-vascular endothelial growth factor for macular oedema secondary to branch retinal vein occlusion[J/OL]. Cochrane Database Syst Rev, 2013(1): D9510[2013-01-31]. https://pubmed.ncbi.nlm.nih.gov/23440840/. DOI: 10.1002/14651858.CD009510.pub2.
14. 许阿敏, 陈长征, 易佐慧子, 等. 糖尿病视网膜病变超广角荧光素眼底血管造影检查与标准7视野检查结果的对比分析[J]. 中华眼底病杂志, 2017, 33(1): 23-26. DOI: 10.3760/cma.j.issn.1005-1015.2017.01.007.Xu AM, Chen CZ, Yi ZHZ, et al. Comparative analysis of ultra-wide-field fluorescein angiography and early treatment diabetic retinopathy study 7 standard field photography in diabetic retinopathy[J]. Chin J Ocul Fundus Dis, 2017, 33(1): 23-26. DOI: 10.3760/cma.j.issn.1005-1015.2017.01.007.
15. Thomas AS, Thomas MK, Finn AP, et al. Use of the ischemic index on widefield fluorescein angiography to characterize a central retinal vein occlusion as ischemic or nonischemic[J]. Retina, 2019, 39(6): 1033-1038. DOI: 10.1097/IAE.0000000000002126.
16. Price LD, Au S, Chong NV. Optomap ultrawide field imaging identifies additional retinal abnormalities in patients with diabetic retinopathy[J]. Clin Ophthalmol, 2015, 9: 527-531. DOI: 10.2147/OPTH.S79448.
17. Oliver SC, Schwartz SD. Peripheral vessel leakage (PVL): a new angiographic finding in diabetic retinopathy identified with ultra wide-field fluorescein angiography[J]. Semin Ophthalmol, 2010, 25(1-2): 27-33. DOI: 10.3109/08820538.2010.481239.
18. Sim DA, Keane PA, Rajendram R, et al. Patterns of peripheral retinal and central macula ischemia in diabetic retinopathy as evaluated by ultra-widefield fluorescein angiography[J]. Am J Ophthalmol, 2014, 158(1): 144-153. DOI: 10.1016/j.ajo.2014.03.009.
19. Singer M, Sagong M, van Hemert J, et al. Ultra-widefield imaging of the peripheral retinal vasculature in normal subjects[J]. Ophthalmology, 2016, 123(5): 1053-1059. DOI: 10.1016/j.ophtha.2016.01.022.
20. Ehlers JP, Wang K, Vasanji A, et al. Automated quantitative characterisation of retinal vascular leakage and microaneurysms in ultra-widefield fluorescein angiography[J]. Br J Ophthalmol, 2017, 101(6): 696-699. DOI: 10.1136/bjophthalmol-2016-310047.
21. Silva PS, Dela CA, Ledesma MG, et al. Diabetic retinopathy severity and peripheral lesions are associated with nonperfusion on ultrawide field angiography[J]. Ophthalmology, 2015, 122(12): 2465-2472. DOI: 10.1016/j.ophtha.2015.07.034.
22. Hajdu D, Sedova A, Datlinger F, et al. Association of macular perfusion status with microvascular parameters up to the far periphery in diabetic retinopathy using multimodal imaging[J]. Int J Retina Vitreous, 2020, 6(1): 50. DOI: 10.1186/s40942-020-00253-w.
23. Hariprasad SM, Mieler WF, Grassi M, et al. Vision-related quality of life in patients with diabetic macular oedema[J]. Br J Ophthalmol, 2008, 92(1): 89-92. DOI: 10.1136/bjo.2007.122416.
24. Jiang AC, Srivastava SK, Hu M, et al. Quantitative ultra-widefield angiographic features and associations with diabetic macular edema[J]. Ophthalmol Retina, 2020, 4(1): 49-56. DOI: 10.1016/j.oret.2019.08.008.
25. Nguyen QD, Brown DM, Marcus DM, et al. Ranibizumab for diabetic macular edema: results from 2 phase Ⅲ randomized trials: RISE and RIDE[J]. Ophthalmology, 2012, 119(4): 789-801. DOI: 10.1016/j.ophtha.2011.12.039.
26. Bonnin S, Dupas B, Lavia C, et al. Anti-vascular endothelial growth factor therapy can improve diabetic retinopathy score without change in retinal perfusion[J]. Retina, 2019, 39(3): 426-434. DOI: 10.1097/IAE.0000000000002422.
27. Bressler SB, Liu D, Glassman AR, et al. Change in diabetic retinopathy through 2 years: secondary analysis of a randomized clinical trial comparing aflibercept, bevacizumab, and ranibizumab[J]. JAMA Ophthalmol, 2017, 135(6): 558-568. DOI: 10.1001/jamaophthalmol.2017.0821.
28. Chandra S, Sheth J, Anantharaman G, et al. Ranibizumab-induced retinal reperfusion and regression of neovascularization in diabetic retinopathy: an angiographic illustration[J]. Am J Ophthalmol Case Rep, 2018, 9: 41-44. DOI: 10.1016/j.ajoc.2018.01.006.
29. Gupta MP, Kiss S, Chan R. Reversal of retinal vascular leakage and arrest of progressive retinal nonperfusion with monthly anti-vascular endothelial growth factor therapy for proliferative diabetic retinopathy[J/OL]. Retina, 2018, 38(9): e74-e75[2018-09-01]. https://pubmed.ncbi.nlm.nih.gov/30005003/. DOI: 10.1097/IAE.0000000000002261.
30. Levin AM, Rusu I, Orlin A, et al. Retinal reperfusion in diabetic retinopathy following treatment with anti-VEGF intravitreal injections[J]. Clin Ophthalmol, 2017, 11: 193-200. DOI: 10.2147/OPTH.S118807.
31. Allingham MJ, Mukherjee D, Lally EB, et al. A quantitative approach to predict differential effects of anti-VEGF treatment on diffuse and focal leakage in patients with diabetic macular edema: a pilot study[J]. Transl Vis Sci Technol, 2017, 6(2): 7. DOI: 10.1167/tvst.6.2.7.
32. Babiuch AS, Wykoff CC, Srivastava SK, et al. Retinal leakage index dynamics on ultra-widefield fluorescein angiography in eyes treated with intravitreal aflibercept for proliferative diabetic retinopathy in the recovery study[J]. Retina, 2020, 40(11): 2175-2183. DOI: 10.1097/IAE.0000000000002727.
33. Yu HJ, Ehlers JP, Sevgi DD, et al. Real-time photographic- and fluorescein angiographic-guided management of diabetic retinopathy: randomized prime trial outcomes[J]. Am J Ophthalmol, 2021, 226: 126-136. DOI: 10.1016/j.ajo.2021.01.024.
34. McIntosh RL, Rogers SL, Lim L, et al. Natural history of central retinal vein occlusion: an evidence-based systematic review[J]. Ophthalmology, 2010, 117(6): 1113-1123. DOI: 10.1016/j.ophtha.2010.01.060.
35. Hayreh SS, Podhajsky PA, Zimmerman MB. Natural history of visual outcome in central retinal vein occlusion[J]. Ophthalmology, 2011, 118(1): 119-133. DOI: 10.1016/j.ophtha.2010.04.019.
36. Manivannan A, Plskova J, Farrow A, et al. Ultra-wide-field fluorescein angiography of the ocular fundus[J]. Am J Ophthalmol, 2005, 140(3): 525-527. DOI: 10.1016/j.ajo.2005.02.055.
37. Campbell JP, Leder HA, Sepah YJ, et al. Wide-field retinal imaging in the management of noninfectious posterior uveitis[J]. Am J Ophthalmol, 2012, 154(5): 908-911. DOI: 10.1016/j.ajo.2012.05.019.
38. Fang M, Fan W, Shi Y, et al. Classification of regions of nonperfusion on ultra-widefield fluorescein angiography in patients with diabetic macular edema[J]. Am J Ophthalmol, 2019, 206: 74-81. DOI: 10.1016/j.ajo.2019.03.030.
39. Rabiolo A, Cicinelli MV, Corbelli E, et al. Correlation analysis between foveal avascular zone and peripheral ischemic index in diabetic retinopathy: a pilot study[J]. Ophthalmol Retina, 2018, 2(1): 46-52. DOI: 10.1016/j.oret.2017.05.007.
40. Sakimoto S, Kamei M, Suzuki M, et al. Relationship between grades of macular perfusion and foveal thickness in branch retinal vein occlusion[J]. Clin Ophthalmol, 2013, 7: 39-45. DOI: 10.2147/OPTH.S37185.

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Progress in the application of leakage index in retinal diseases

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