Correlation analysis between grading of diabetic retinopathy and retinal ischemia_Chinese Journal of Ocular Fundus Diseases

Authors：

Fu Mei ,  Chen Changzheng , Jiang Jingwen , Sun Gongpeng , Wang Xiaoling , Yi Zuohuizi

Eye Center, Renmin Hospital of Wuhan University, Wuhan 430060, China;

Corresponding?author：

Chen Changzheng, Email: whuchenchzh@163.com

Keywords：

Diabetic retinopathy; Fluorescein angiography; Ischemic index

DOI：

10.3760/cma.j.cn511434-20210218-00083

Video：

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Objective To observe and preliminarily discuss the distribution characteristics of the non-perfusion area (NP) of the retina in different stages of diabetic retinopathy (DR) and its changes with the progression of DR. Methods A retrospective clinical study. From October 2018 to December 2020, 118 cases of 175 eyes of DR patients diagnosed in Eye Center of Renmin Hospital of Wuhan University were included in the study. Among them, there were 64 males with 93 eyes and 54 females with 82 eyes; the average age was 56.61±8.99 years old. There were 95 eyes of non-proliferative DR (NPDR), of which 25, 47, and 23 eyes were mild, moderate, and severe; 80 eyes were proliferative DR (PDR). Ultra-wide-angle fluorescein fundus angiography was performed with the British Optos 200Tx imaging system, and the fundus image was divided into posterior, middle, and distal parts with Image J software, and the ischemic index (ISI) was calculated. The difference of the retina in different DR staging groups and the difference of ISI were compared in the same area. The Kruskal-Wallis test was used to compare the ISI between the different DR staging groups and the Kruskal-Wallis one-way analysis of variance was used for the pairwise comparison between the groups. Results The ISI of the posterior pole of the eyes in the moderate NPDR group, severe NPDR group, and PDR group were significantly greater than that in the distal periphery, and the difference was statistically significant (χ²=6.551, 3.540, 6.614; P=0.000, 0.002, 0.000). In severe NPDR group and PDR group, the ISI of the middle and peripheral parts of the eyes was significantly greater than that of the distal parts, and the difference was statistically significant (χ²=3.027, 3.429; P=0.015, 0.004). In the moderate NPDR group, there was no significant difference in ISI between the peripheral and distal parts of the eye (χ²=2.597, P=0.057). The ISI of the posterior pole of the eyes in the moderate NPDR group and the PDR group was significantly greater than that in the middle periphery, and the difference was statistically significant (χ²=3.955, 3.184; P=0.000, 0.009). In the severe NPDR group, there was no significant difference in ISI between the posterior pole and the middle periphery of the eye (χ²=0.514, P=1.000). Compared with the mild NPDR group and the moderate NPDR group, the ISI of the whole retina, posterior pole, middle and distal parts of the PDR group was larger, and the difference was statistically significant (χ²=－7.064, －6.349,－6.999, －5.869, －6.695, －6.723, －3.459, －4.098; P=0.000, 0.000, 0.000, 0.000, 0.000, 0.000, 0.003, 0.000). Conclusion The NP of the eyes with different DR stages is mainly distributed in the posterior pole and the middle periphery. The higher the severity of DR, the greater the NP in the posterior and middle periphery.

Citation： Fu Mei, Chen Changzheng, Jiang Jingwen, Sun Gongpeng, Wang Xiaoling, Yi Zuohuizi. Correlation analysis between grading of diabetic retinopathy and retinal ischemia. Chinese Journal of Ocular Fundus Diseases, 2021, 37(10): 784-789. doi: 10.3760/cma.j.cn511434-20210218-00083 Copy

1.	Antonetti DA, Klein R, Gardner TW. Diabetic retinopathy[J]. N Engl J Med, 2012, 366(13): 1227-1239. DOI: 10.1056/NEJMra1005073.
2.	陳長征, 許阿敏. 提升超廣角熒光素眼底血管造影技術應用水平, 深化周邊眼底特征觀察及臨床意義研究[J]. 中華眼底病雜志, 2017, 33(1): 7-9. DOI: 10.3760/cma.j.issn.1005-1015.2017.01.003.Chen CZ, Xu AM. Improve our understanding of ocular fundus diseases with ultra-wide-field fluorescein angiography[J]. Chin J Ocul Fundus Dis, 2017, 33(1): 7-9. DOI: 10.3760/cma.j.issn.1005-1015.2017.01.003.
3.	Singer M, Tan CS, Bell D, et al. Area of peripheral retinal nonperfusion and treatment response in branch and central retinal vein occlusion[J]. Retina, 2014, 34(9): 1736-1742. DOI: 10.1097/IAE.0000000000000148.
4.	Nicholson L, Vazquez-Alfageme C, Patrao NV, et al. Retinal nonperfusion in the posterior pole is associated with increased risk of neovascularization in central retinal vein occlusion[J]. Am J Ophthalmol, 2017, 182(10): 118-125. DOI: 10.1016/j.ajo.2017.07.015.
5.	Fan W, Wang K, Ghasemi Falavarjani K, et al. Distribution of nonperfusion area on ultra-widefield fluorescein angiography in eyes with diabetic macular edema: DAVE study[J]. Am J Ophthalmol, 2017, 180(8): 110-116. DOI: 10.1016/j.ajo.2017.05.024.
6.	中華醫學會眼科學會眼底病學組. 我國糖尿病視網膜病變臨床診療指南(2014年)[J]. 中華眼科雜志, 2014, 50(11): 851-865. DOI: 10.3760/cma.j.issn.0412-4081.2014.11.014.Fundus Ophthalmology Group of Chinese Medical Association Ophthalmology Society. The clinical diagnosis and treatment guidelines for diabetic retinopathy in China (2014)[J]. Chin J Ophthalmol, 2014, 50(11): 851-865. DOI: 10.3760/cma.j.issn.0412-4081.2014.11.014.
7.	Fan W, Nittala MG, Velaga SB, et al. Distribution of nonperfusion and neovascularization on ultrawide-field fluorescein angiography in proliferative diabetic retinopathy (RECOVERY Study): report 1[J]. Am J Ophthalmol, 2019, 206(10): 154-160. DOI: 10.1016/j.ajo.2019.04.023.
8.	Wang W, Lo ACY. Diabetic retinopathy: pathophysiology and treatments[J/OL]. Int J Mol Sci, 2018, 19(6): 1816[2018-06-20]. https://pubmed.ncbi.nlm.nih.gov/29925789/. DOI: 10.3390/ijms19061816.
9.	Niki T, Muraoka K, Shimizu K. Distribution of capillary nonperfusion in early-stage diabetic retinopathy[J]. Ophthalmology, 1984, 91(12): 1431-1439. DOI: 10.1016/s0161-6420(84)34126-4.
10.	許阿敏, 陳長征, 易佐慧子, 等. 糖尿病視網膜病變超廣角熒光素眼底血管造影檢查與標準7視野檢查結果的對比分析[J]. 中華眼底病雜志, 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.
11.	Nicholson L, Ramu J, Chan EW, et al. Retinal nonperfusion characteristics on ultra-widefield angiography in eyes with severe nonproliferative diabetic retinopathy and proliferative diabetic retinopathy[J]. JAMA Ophthalmol, 2019, 137(6): 626-631. DOI: 10.1001/jamaophthalmol.2019.0440.
12.	Lange J, Hadziahmetovic M, Zhang J, et al. Region-specific ischemia, neovascularization and macular oedema in treatment-na?ve proliferative diabetic retinopathy[J]. Clin Exp Ophthalmol, 2018, 46(7): 757-766. DOI: 10.1111/ceo.13168.
13.	Akiba J, Arzabe CW, Trempe CL. Posterior vitreous detachment and neovascularization in diabetic retinopathy[J]. Ophthalmology, 1990, 97(7): 889-891. DOI: 10.1016/s0161-6420(90)32486-7.
14.	Antaki F, Coussa RG, Mikhail M, et al. The prognostic value of peripheral retinal nonperfusion in diabetic retinopathy using ultra-widefield fluorescein angiography[J]. Graefe's Arch Clin Exp Ophthalmol, 2020, 258(12): 2681-2690. DOI: 10.1007/s00417-020-04847-w.
15.	Kristinsson JK, Gottfredsdóttir MS, Stefánsson E. Retinal vessel dilatation and elongation precedes diabetic macular oedema[J]. Br J Ophthalmol, 1997, 81(4): 274-278. DOI: 10.1136/bjo.81.4.274.
16.	Curcio CA, Sloan KR, Kalina RE, et al. Human photoreceptor topography[J]. J Comp Neurol, 1990, 292(4): 497-523. DOI: 10.1002/cne.902920402.
17.	Wang X, Xu A, Yi Z, et al. Observation of the far peripheral retina of normal eyes by ultra-wide field fluorescein angiography[J]. Eur J Ophthalmol, 2020, 26(5): 1-8. DOI: 10.1177/1120672120926453.
18.	陳長征, 王曉玲. 正確分析周邊部視網膜超廣角熒光素眼底血管造影特征[J]. 中華實驗眼科雜志, 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.
19.	Silva PS, Cavallerano JD, Haddad NM, et al. Peripheral lesions identified on ultrawide field imaging predict increased risk of diabetic retinopathy progression over 4 years[J]. Ophthalmology, 2015, 122(5): 949-956. DOI: 10.1016/j.ophtha.2015.01.008.
20.	Sagong M, van Hemert J, Olmos de Koo LC, et al. Assessment of accuracy and precision of quantification of ultra-widefield images[J]. Ophthalmology, 2015, 122(4): 864-866. DOI: 10.1016/j.ophtha.2014.11.016.

1. Antonetti DA, Klein R, Gardner TW. Diabetic retinopathy[J]. N Engl J Med, 2012, 366(13): 1227-1239. DOI: 10.1056/NEJMra1005073.
2. 陳長征, 許阿敏. 提升超廣角熒光素眼底血管造影技術應用水平, 深化周邊眼底特征觀察及臨床意義研究[J]. 中華眼底病雜志, 2017, 33(1): 7-9. DOI: 10.3760/cma.j.issn.1005-1015.2017.01.003.Chen CZ, Xu AM. Improve our understanding of ocular fundus diseases with ultra-wide-field fluorescein angiography[J]. Chin J Ocul Fundus Dis, 2017, 33(1): 7-9. DOI: 10.3760/cma.j.issn.1005-1015.2017.01.003.
3. Singer M, Tan CS, Bell D, et al. Area of peripheral retinal nonperfusion and treatment response in branch and central retinal vein occlusion[J]. Retina, 2014, 34(9): 1736-1742. DOI: 10.1097/IAE.0000000000000148.
4. Nicholson L, Vazquez-Alfageme C, Patrao NV, et al. Retinal nonperfusion in the posterior pole is associated with increased risk of neovascularization in central retinal vein occlusion[J]. Am J Ophthalmol, 2017, 182(10): 118-125. DOI: 10.1016/j.ajo.2017.07.015.
5. Fan W, Wang K, Ghasemi Falavarjani K, et al. Distribution of nonperfusion area on ultra-widefield fluorescein angiography in eyes with diabetic macular edema: DAVE study[J]. Am J Ophthalmol, 2017, 180(8): 110-116. DOI: 10.1016/j.ajo.2017.05.024.
6. 中華醫學會眼科學會眼底病學組. 我國糖尿病視網膜病變臨床診療指南(2014年)[J]. 中華眼科雜志, 2014, 50(11): 851-865. DOI: 10.3760/cma.j.issn.0412-4081.2014.11.014.Fundus Ophthalmology Group of Chinese Medical Association Ophthalmology Society. The clinical diagnosis and treatment guidelines for diabetic retinopathy in China (2014)[J]. Chin J Ophthalmol, 2014, 50(11): 851-865. DOI: 10.3760/cma.j.issn.0412-4081.2014.11.014.
7. Fan W, Nittala MG, Velaga SB, et al. Distribution of nonperfusion and neovascularization on ultrawide-field fluorescein angiography in proliferative diabetic retinopathy (RECOVERY Study): report 1[J]. Am J Ophthalmol, 2019, 206(10): 154-160. DOI: 10.1016/j.ajo.2019.04.023.
8. Wang W, Lo ACY. Diabetic retinopathy: pathophysiology and treatments[J/OL]. Int J Mol Sci, 2018, 19(6): 1816[2018-06-20]. https://pubmed.ncbi.nlm.nih.gov/29925789/. DOI: 10.3390/ijms19061816.
9. Niki T, Muraoka K, Shimizu K. Distribution of capillary nonperfusion in early-stage diabetic retinopathy[J]. Ophthalmology, 1984, 91(12): 1431-1439. DOI: 10.1016/s0161-6420(84)34126-4.
10. 許阿敏, 陳長征, 易佐慧子, 等. 糖尿病視網膜病變超廣角熒光素眼底血管造影檢查與標準7視野檢查結果的對比分析[J]. 中華眼底病雜志, 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.
11. Nicholson L, Ramu J, Chan EW, et al. Retinal nonperfusion characteristics on ultra-widefield angiography in eyes with severe nonproliferative diabetic retinopathy and proliferative diabetic retinopathy[J]. JAMA Ophthalmol, 2019, 137(6): 626-631. DOI: 10.1001/jamaophthalmol.2019.0440.
12. Lange J, Hadziahmetovic M, Zhang J, et al. Region-specific ischemia, neovascularization and macular oedema in treatment-na?ve proliferative diabetic retinopathy[J]. Clin Exp Ophthalmol, 2018, 46(7): 757-766. DOI: 10.1111/ceo.13168.
13. Akiba J, Arzabe CW, Trempe CL. Posterior vitreous detachment and neovascularization in diabetic retinopathy[J]. Ophthalmology, 1990, 97(7): 889-891. DOI: 10.1016/s0161-6420(90)32486-7.
14. Antaki F, Coussa RG, Mikhail M, et al. The prognostic value of peripheral retinal nonperfusion in diabetic retinopathy using ultra-widefield fluorescein angiography[J]. Graefe's Arch Clin Exp Ophthalmol, 2020, 258(12): 2681-2690. DOI: 10.1007/s00417-020-04847-w.
15. Kristinsson JK, Gottfredsdóttir MS, Stefánsson E. Retinal vessel dilatation and elongation precedes diabetic macular oedema[J]. Br J Ophthalmol, 1997, 81(4): 274-278. DOI: 10.1136/bjo.81.4.274.
16. Curcio CA, Sloan KR, Kalina RE, et al. Human photoreceptor topography[J]. J Comp Neurol, 1990, 292(4): 497-523. DOI: 10.1002/cne.902920402.
17. Wang X, Xu A, Yi Z, et al. Observation of the far peripheral retina of normal eyes by ultra-wide field fluorescein angiography[J]. Eur J Ophthalmol, 2020, 26(5): 1-8. DOI: 10.1177/1120672120926453.
18. 陳長征, 王曉玲. 正確分析周邊部視網膜超廣角熒光素眼底血管造影特征[J]. 中華實驗眼科雜志, 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.
19. Silva PS, Cavallerano JD, Haddad NM, et al. Peripheral lesions identified on ultrawide field imaging predict increased risk of diabetic retinopathy progression over 4 years[J]. Ophthalmology, 2015, 122(5): 949-956. DOI: 10.1016/j.ophtha.2015.01.008.
20. Sagong M, van Hemert J, Olmos de Koo LC, et al. Assessment of accuracy and precision of quantification of ultra-widefield images[J]. Ophthalmology, 2015, 122(4): 864-866. DOI: 10.1016/j.ophtha.2014.11.016.

Chinese Journal of Ocular Fundus Diseases

Correlation analysis between grading of diabetic retinopathy and retinal ischemia

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