Systemic factors associated with treatment response in patients with diabetic macular edema_Chinese Journal of Ocular Fundus Diseases

Authors：

Yao Jie ^1,2 , Cao Dan ¹ , Zeng Yunkao ^1,2 , Zhuang Xuenan ^1,2 ,  Zhang Liang ¹

1. Department of Ophthalmology, Guangdong Provincial People’s Hospital, Guangdong Academy of Medical Sciences, Guangdong Eye Institute, Guangzhou 510080, China;
2. Shantou University Medical College, Shantou 515041, China;

Corresponding author：

Zhang Liang, Email: zhangliang5413@163.com

Keywords：

Diabetic retinopathy; Macular edema; Therapy; Prognosis; Review

DOI：

10.3760/cma.j.cn511434-20200526-00244

Video：

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Diabetic macular edema (DME) is the main cause of vision loss and even blindness in patients with diabetic retinopathy. Intravitreal anti-vascular endothelial factor therapy has become the gold standard management of DME. However, not all eyes response optimally to common management of DME, which could be due to the differences of individual factors. Increasing age could be the predictive factors for poor outcome. The influence of glycemic control, hypertension, dyslipidemia, chronic kidney disease and relative factors on treatment response require further investigation. Identifying the systemic factors that influence the treatment response of DME can provide the evidence to predict the prognosis of DME, and improve the efficacy of clinical treatment.

Citation： Yao Jie, Cao Dan, Zeng Yunkao, Zhuang Xuenan, Zhang Liang. Systemic factors associated with treatment response in patients with diabetic macular edema. Chinese Journal of Ocular Fundus Diseases, 2022, 38(3): 253-256. doi: 10.3760/cma.j.cn511434-20200526-00244 Copy

1.	Tan GS, Cheung N, Simó R, et al. Diabetic macular oedema[J]. Lancet Diabetes Endocrinol, 2017, 5(2): 143-155. DOI: 10.1016/S2213-8587(16)30052-3.
2.	Lee R, Wong TY, Sabanayagam C. Epidemiology of diabetic retinopathy, diabetic macular edema and related vision loss[J]. Eye Vis (Lond), 2015, 2: 17. DOI: 10.1186/s40662-015-0026-2.
3.	Virgili G, Parravano M, Evans JR, et al. Anti-vascular endothelial growth factor for diabetic macular oedema: a network meta-analysis[J/OL]. Cochrane Database Syst Rev, 2018, 10(10): CD007419[2018-10-16]. https://pubmed.ncbi.nlm.nih.gov/30325017/.DOI: 10.1002/14651858.CD007419.pub6.
4.	Bressler NM, Beaulieu WT, Glassman AR, et al. Persistent macular thickening following intravitreous aflibercept, bevacizumab, or ranibizumab for central-involved diabetic macular edema with vision impairment: a secondary analysis of a randomized clinical trial[J]. JAMA Ophthalmol, 2018, 136(3): 257-269. DOI: 10.1001/jamaophthalmol.2017.6565.
5.	Hermenean A, Trotta MC, Gharbia S, et al. Changes in retinal structure and ultrastructure in the aged mice correlate with differences in the expression of selected retinal miRNAs[J/OL]. Front Pharmacol, 2021, 11: 593514[2021-03-15]. https://pubmed.ncbi.nlm.nih.gov/33519453/. DOI: 10.3389/fphar.2020.593514.
6.	Singh RP, Habbu K, Ehlers JP, et al. The impact of systemic factors on clinical response to ranibizumab for diabetic macular edema[J]. Ophthalmology, 2016, 123(7): 1581-1587. DOI: 10.1016/j.ophtha.2016.03.038.
7.	Bressler SB, Odia I, Maguire MG, et al. Factors associated with visual acuity and central subfield thickness changes when treating diabetic macular edema with anti-vascular endothelial growth factor therapy: an exploratory analysis of the protocol T randomized clinical trial[J]. JAMA Ophthalmol, 2019, 137(4): 382-389. DOI: 10.1001/jamaophthalmol.2018.6786.
8.	Ozsaygili C, Duru Z, Cicek A, et al. The effect of age on aflibercept (EYLEA) response in diabetic macular edema[J]. Retina, 2020, 40(6): 1038-1043. DOI: 10.1097/IAE.0000000000002504.
9.	Zhang X, Lai TYY. Baseline predictors of visual acuity outcome in patients with wet age-related macular degeneration[J/OL]. Biomed Res Int, 2018, 2018: 9640131[2018-02-26]. https://pubmed.ncbi.nlm.nih.gov/29682574/. DOI: 10.1155/2018/9640131.
10.	Edelhauser HF, Rowe-Rendleman CL, Robinson MR, et al. Ophthalmic drug delivery systems for the treatment of retinal diseases: basic research to clinical applications[J]. Invest Ophthalmol Vis Sci, 2010, 51(11): 5403-5420. DOI: 10.1167/iovs.10-5392.
11.	Sophie R, Lu N, Campochiaro PA. Predictors of functional and anatomic outcomes in patients with diabetic macular edema treated with ranibizumab[J]. Ophthalmology, 2015, 122(7): 1395-1401. DOI: 10.1016/j.ophtha.2015.02.036.
12.	Diabetes Control and Complications Trial (DCCT)/Epidemiology of Diabetes Interventions and Complications (EDIC) Research Group, Lachin JM, White NH, et al. Effect of intensive diabetes therapy on the progression of diabetic retinopathy in patients with type 1 diabetes: 18 years of follow-up in the DCCT/EDIC[J]. Diabetes, 2015, 64(2): 631-642. DOI: 10.2337/db14-0930.
13.	Ting DS, Cheung GC, Wong TY. Diabetic retinopathy: global prevalence, major risk factors, screening practices and public health challenges: a review[J]. Clin Exp Ophthalmol, 2016, 44(4): 260-277. DOI: 10.1111/ceo.12696.
14.	Warid Al-Laftah FA, Elshafie M, Alhashimi M, et al. Pretreatment clinical variables associated with the response to intravitreal bevacizumab (Avastin) injection in patients with persistent diabetic macular edema[J]. Saudi J Ophthalmol, 2010, 24(4): 133-138. DOI: 10.1016/j.sjopt.2010.05.001.
15.	Wong WM, Chee C, Bhargava M, et al. Systemic factors associated with treatment response in diabetic macular edema[J/OL]. J Ophthalmol, 2020, 2020: 1875860[2020-03-19]. https://pubmed.ncbi.nlm.nih.gov/32280516/. DOI: 10.1155/2020/1875860.
16.	Do DV, Shah SM, Sung JU, et al. Persistent diabetic macular edema is associated with elevated hemoglobin A1c[J]. Am J Ophthalmol, 2005, 139(4): 620-623. DOI: 10.1016/j.ajo.2004.10.063.
17.	Dhoot DS, Baker K, Saroj N, et al. Baseline factors affecting changes in diabetic retinopathy severity scale score after intravitreal aflibercept or laser for diabetic macular edema: post hoc analyses from VISTA and VIVID[J]. Ophthalmology, 2018, 125(1): 51-56. DOI: 10.1016/j.ophtha.2017.06.029.
18.	Singh RP, Wykoff CC, Brown DM, et al. Outcomes of diabetic macular edema patients by baseline hemoglobin A1c: analyses from VISTA and VIVID[J]. Ophthalmol Retina, 2017, 1(5): 382-388. DOI: 10.1016/j.oret.2017.02.003.
19.	Fong DS, Ferris FL 3rd, Davis MD, et al. Causes of severe visual loss in the early treatment diabetic retinopathy study: ETDRS report no. 24. early treatment diabetic retinopathy study research group[J]. Am J Ophthalmol, 1999, 127(2): 137-141. DOI: 10.1016/s0002-9394(98)00309-2.
20.	Romero-Aroca P, Baget-Bernaldiz M, Pareja-Rios A, et al. Diabetic macular edema pathophysiology: vasogenic versus inflammatory[J/OL]. J Diabetes Res, 2016, 2016: 2156273[2016-09-28]. https://pubmed.ncbi.nlm.nih.gov/27761468/. DOI: 10.1155/2016/2156273.
21.	Flaxel CJ, Adelman RA, Bailey ST, et al. Diabetic retinopathy preferred practice pattern®[J]. Ophthalmology, 2020, 127(1): P66-P145. DOI: 10.1016/j.ophtha.2019.09.025.
22.	Do DV, Wang X, Vedula SS, et al. Blood pressure control for diabetic retinopathy[J/OL]. Cochrane Database Syst Rev, 2015, 1: CD006127[2015-01-31]. https://pubmed.ncbi.nlm.nih.gov/25637717/. DOI: 10.1002/14651858.CD006127.pub2.
23.	Joshi L, Bar A, Tomkins-Netzer O, et al. Intravitreal bevacizumab injections for diabetic macular edema-predictors of response: a retrospective study[J]. Clin Ophthalmol, 2016, 10: 2093-2098. DOI: 10.2147/OPTH.S109809.
24.	Bezzina AD, Carbonaro F. Factors predicting treatment response in anti-vascular endothelial growth factor naïve diabetic macular edema patients treated with intravitreal bevacizumab[J]. J Ocul Pharmacol Ther, 2019, 35(10): 551-557. DOI: 10.1089/jop.2018.0112.
25.	Yoon YH, Boyer DS, Maturi RK, et al. Natural history of diabetic macular edema and factors predicting outcomes in sham-treated patients (MEAD study)[J]. Graefe's Arch Clin Exp Ophthalmol, 2019, 257(12): 2639-2653. DOI: 10.1007/s00417-019-04464-2.
26.	Das R, Kerr R, Chakravarthy U, et al. Dyslipidemia and diabetic macular edema: a systematic review and meta-analysis[J]. Ophthalmology, 2015, 122(9): 1820-1827. DOI: 10.1016/j.ophtha.2015.05.011.
27.	Chung YR, Park SW, Choi SY, et al. Association of statin use and hypertriglyceridemia with diabetic macular edema in patients with type 2 diabetes and diabetic retinopathy[J]. Cardiovasc Diabetol, 2017, 16(1): 4. DOI: 10.1186/s12933-016-0486-2.
28.	Kang EY, Chen TH, Garg SJ, et al. Association of statin therapy with prevention of vision-threatening diabetic retinopathy[J]. JAMA Ophthalmol, 2019, 137(4): 363-371. DOI: 10.1001/jamaophthalmol.2018.6399.
29.	Keech AC, Mitchell P, Summanen PA, et al. Effect of fenofibrate on the need for laser treatment for diabetic retinopathy (FIELD study): a randomised controlled trial[J]. Lancet, 2007, 370(9600): 1687-1697. DOI: 10.1016/S0140-6736(07)61607-9.
30.	Pearsall EA, Cheng R, Matsuzaki S, et al. Neuroprotective effects of PPARα in retinopathy of type 1 diabetes[J/OL]. PLoS One, 2019, 14(2): e0208399[2019-02-04]. https://pubmed.ncbi.nlm.nih.gov/30716067/. DOI: 10.1371/journal.pone.0208399.
31.	Srinivasan S, Hande P, Shetty J, et al. Efficiency of fenofibrate in facilitating the reduction of central macular thickness in diabetic macular edema[J]. Indian J Ophthalmol, 2018, 66(1): 98-105. DOI: 10.4103/ijo.IJO_566_17.
32.	Barrett EJ, Liu Z, Khamaisi M, et al. Diabetic microvascular disease: an endocrine society scientific statement[J]. J Clin Endocrinol Metab, 2017, 102(12): 4343-4410. DOI: 10.1210/jc.2017-01922.
33.	Martín-Merino E, Fortuny J, Rivero-Ferrer E, et al. Risk factors for diabetic macular oedema in type 2 diabetes: a case-control study in a United Kingdom primary care setting[J]. Prim Care Diabetes, 2017, 11(3): 288-296. DOI: 10.1016/j.pcd.2017.03.002.
34.	Zhuang X, Cao D, Yang D, et al. Association of diabetic retinopathy and diabetic macular oedema with renal function in southern Chinese patients with type 2 diabetes mellitus: a single-centre observational study[J/OL]. BMJ Open, 2019, 9(9): e031194[2019-09-06]. https://pubmed.ncbi.nlm.nih.gov/31494622/. DOI: 10.1136/bmjopen-2019-031194.
35.	Hsieh YT, Tsai MJ, Tu ST, et al. Association of abnormal renal profiles and proliferative diabetic retinopathy and diabetic macular edema in an Asian population with type 2 diabetes[J]. JAMA Ophthalmol, 2018, 136(1): 68-74. DOI: 10.1001/jamaophthalmol.2017.5202.
36.	Theodossiadis PG, Theodoropoulou S, Neamonitou G, et al. Hemodialysis-induced alterations in macular thickness measured by optical coherence tomography in diabetic patients with end-stage renal disease[J]. Ophthalmologica, 2012, 227(2): 90-94. DOI: 10.1159/000331321.
37.	Takamura Y, Matsumura T, Ohkoshi K, et al. Functional and anatomical changes in diabetic macular edema after hemodialysis initiation: one-year follow-up multicenter study[J/OL]. Sci Rep, 2020, 10(1): 7788[2020-05-08]. https://pubmed.ncbi.nlm.nih.gov/32385333/. DOI: 10.1038/s41598-020-64798-4.
38.	Samanta R, Puthalath AS, Saraswat N, et al. Rapidly reversing bilateral macular edema associated with fluid overload in a young type 1 diabetic[J]. Indian J Ophthalmol, 2019, 67(7): 1221-1223. DOI: 10.4103/ijo.IJO_1805_18.
39.	Kahtani ES. Diabetic glomerulosclerosis can be the pathogenesis of refractory diabetic macular edema[J]. Clin Ophthalmol, 2015, 9: 929-933. DOI: 10.2147/OPTH.S80850.

1. Tan GS, Cheung N, Simó R, et al. Diabetic macular oedema[J]. Lancet Diabetes Endocrinol, 2017, 5(2): 143-155. DOI: 10.1016/S2213-8587(16)30052-3.
2. Lee R, Wong TY, Sabanayagam C. Epidemiology of diabetic retinopathy, diabetic macular edema and related vision loss[J]. Eye Vis (Lond), 2015, 2: 17. DOI: 10.1186/s40662-015-0026-2.
3. Virgili G, Parravano M, Evans JR, et al. Anti-vascular endothelial growth factor for diabetic macular oedema: a network meta-analysis[J/OL]. Cochrane Database Syst Rev, 2018, 10(10): CD007419[2018-10-16]. https://pubmed.ncbi.nlm.nih.gov/30325017/.DOI: 10.1002/14651858.CD007419.pub6.
4. Bressler NM, Beaulieu WT, Glassman AR, et al. Persistent macular thickening following intravitreous aflibercept, bevacizumab, or ranibizumab for central-involved diabetic macular edema with vision impairment: a secondary analysis of a randomized clinical trial[J]. JAMA Ophthalmol, 2018, 136(3): 257-269. DOI: 10.1001/jamaophthalmol.2017.6565.
5. Hermenean A, Trotta MC, Gharbia S, et al. Changes in retinal structure and ultrastructure in the aged mice correlate with differences in the expression of selected retinal miRNAs[J/OL]. Front Pharmacol, 2021, 11: 593514[2021-03-15]. https://pubmed.ncbi.nlm.nih.gov/33519453/. DOI: 10.3389/fphar.2020.593514.
6. Singh RP, Habbu K, Ehlers JP, et al. The impact of systemic factors on clinical response to ranibizumab for diabetic macular edema[J]. Ophthalmology, 2016, 123(7): 1581-1587. DOI: 10.1016/j.ophtha.2016.03.038.
7. Bressler SB, Odia I, Maguire MG, et al. Factors associated with visual acuity and central subfield thickness changes when treating diabetic macular edema with anti-vascular endothelial growth factor therapy: an exploratory analysis of the protocol T randomized clinical trial[J]. JAMA Ophthalmol, 2019, 137(4): 382-389. DOI: 10.1001/jamaophthalmol.2018.6786.
8. Ozsaygili C, Duru Z, Cicek A, et al. The effect of age on aflibercept (EYLEA) response in diabetic macular edema[J]. Retina, 2020, 40(6): 1038-1043. DOI: 10.1097/IAE.0000000000002504.
9. Zhang X, Lai TYY. Baseline predictors of visual acuity outcome in patients with wet age-related macular degeneration[J/OL]. Biomed Res Int, 2018, 2018: 9640131[2018-02-26]. https://pubmed.ncbi.nlm.nih.gov/29682574/. DOI: 10.1155/2018/9640131.
10. Edelhauser HF, Rowe-Rendleman CL, Robinson MR, et al. Ophthalmic drug delivery systems for the treatment of retinal diseases: basic research to clinical applications[J]. Invest Ophthalmol Vis Sci, 2010, 51(11): 5403-5420. DOI: 10.1167/iovs.10-5392.
11. Sophie R, Lu N, Campochiaro PA. Predictors of functional and anatomic outcomes in patients with diabetic macular edema treated with ranibizumab[J]. Ophthalmology, 2015, 122(7): 1395-1401. DOI: 10.1016/j.ophtha.2015.02.036.
12. Diabetes Control and Complications Trial (DCCT)/Epidemiology of Diabetes Interventions and Complications (EDIC) Research Group, Lachin JM, White NH, et al. Effect of intensive diabetes therapy on the progression of diabetic retinopathy in patients with type 1 diabetes: 18 years of follow-up in the DCCT/EDIC[J]. Diabetes, 2015, 64(2): 631-642. DOI: 10.2337/db14-0930.
13. Ting DS, Cheung GC, Wong TY. Diabetic retinopathy: global prevalence, major risk factors, screening practices and public health challenges: a review[J]. Clin Exp Ophthalmol, 2016, 44(4): 260-277. DOI: 10.1111/ceo.12696.
14. Warid Al-Laftah FA, Elshafie M, Alhashimi M, et al. Pretreatment clinical variables associated with the response to intravitreal bevacizumab (Avastin) injection in patients with persistent diabetic macular edema[J]. Saudi J Ophthalmol, 2010, 24(4): 133-138. DOI: 10.1016/j.sjopt.2010.05.001.
15. Wong WM, Chee C, Bhargava M, et al. Systemic factors associated with treatment response in diabetic macular edema[J/OL]. J Ophthalmol, 2020, 2020: 1875860[2020-03-19]. https://pubmed.ncbi.nlm.nih.gov/32280516/. DOI: 10.1155/2020/1875860.
16. Do DV, Shah SM, Sung JU, et al. Persistent diabetic macular edema is associated with elevated hemoglobin A1c[J]. Am J Ophthalmol, 2005, 139(4): 620-623. DOI: 10.1016/j.ajo.2004.10.063.
17. Dhoot DS, Baker K, Saroj N, et al. Baseline factors affecting changes in diabetic retinopathy severity scale score after intravitreal aflibercept or laser for diabetic macular edema: post hoc analyses from VISTA and VIVID[J]. Ophthalmology, 2018, 125(1): 51-56. DOI: 10.1016/j.ophtha.2017.06.029.
18. Singh RP, Wykoff CC, Brown DM, et al. Outcomes of diabetic macular edema patients by baseline hemoglobin A1c: analyses from VISTA and VIVID[J]. Ophthalmol Retina, 2017, 1(5): 382-388. DOI: 10.1016/j.oret.2017.02.003.
19. Fong DS, Ferris FL 3rd, Davis MD, et al. Causes of severe visual loss in the early treatment diabetic retinopathy study: ETDRS report no. 24. early treatment diabetic retinopathy study research group[J]. Am J Ophthalmol, 1999, 127(2): 137-141. DOI: 10.1016/s0002-9394(98)00309-2.
20. Romero-Aroca P, Baget-Bernaldiz M, Pareja-Rios A, et al. Diabetic macular edema pathophysiology: vasogenic versus inflammatory[J/OL]. J Diabetes Res, 2016, 2016: 2156273[2016-09-28]. https://pubmed.ncbi.nlm.nih.gov/27761468/. DOI: 10.1155/2016/2156273.
21. Flaxel CJ, Adelman RA, Bailey ST, et al. Diabetic retinopathy preferred practice pattern®[J]. Ophthalmology, 2020, 127(1): P66-P145. DOI: 10.1016/j.ophtha.2019.09.025.
22. Do DV, Wang X, Vedula SS, et al. Blood pressure control for diabetic retinopathy[J/OL]. Cochrane Database Syst Rev, 2015, 1: CD006127[2015-01-31]. https://pubmed.ncbi.nlm.nih.gov/25637717/. DOI: 10.1002/14651858.CD006127.pub2.
23. Joshi L, Bar A, Tomkins-Netzer O, et al. Intravitreal bevacizumab injections for diabetic macular edema-predictors of response: a retrospective study[J]. Clin Ophthalmol, 2016, 10: 2093-2098. DOI: 10.2147/OPTH.S109809.
24. Bezzina AD, Carbonaro F. Factors predicting treatment response in anti-vascular endothelial growth factor naïve diabetic macular edema patients treated with intravitreal bevacizumab[J]. J Ocul Pharmacol Ther, 2019, 35(10): 551-557. DOI: 10.1089/jop.2018.0112.
25. Yoon YH, Boyer DS, Maturi RK, et al. Natural history of diabetic macular edema and factors predicting outcomes in sham-treated patients (MEAD study)[J]. Graefe's Arch Clin Exp Ophthalmol, 2019, 257(12): 2639-2653. DOI: 10.1007/s00417-019-04464-2.
26. Das R, Kerr R, Chakravarthy U, et al. Dyslipidemia and diabetic macular edema: a systematic review and meta-analysis[J]. Ophthalmology, 2015, 122(9): 1820-1827. DOI: 10.1016/j.ophtha.2015.05.011.
27. Chung YR, Park SW, Choi SY, et al. Association of statin use and hypertriglyceridemia with diabetic macular edema in patients with type 2 diabetes and diabetic retinopathy[J]. Cardiovasc Diabetol, 2017, 16(1): 4. DOI: 10.1186/s12933-016-0486-2.
28. Kang EY, Chen TH, Garg SJ, et al. Association of statin therapy with prevention of vision-threatening diabetic retinopathy[J]. JAMA Ophthalmol, 2019, 137(4): 363-371. DOI: 10.1001/jamaophthalmol.2018.6399.
29. Keech AC, Mitchell P, Summanen PA, et al. Effect of fenofibrate on the need for laser treatment for diabetic retinopathy (FIELD study): a randomised controlled trial[J]. Lancet, 2007, 370(9600): 1687-1697. DOI: 10.1016/S0140-6736(07)61607-9.
30. Pearsall EA, Cheng R, Matsuzaki S, et al. Neuroprotective effects of PPARα in retinopathy of type 1 diabetes[J/OL]. PLoS One, 2019, 14(2): e0208399[2019-02-04]. https://pubmed.ncbi.nlm.nih.gov/30716067/. DOI: 10.1371/journal.pone.0208399.
31. Srinivasan S, Hande P, Shetty J, et al. Efficiency of fenofibrate in facilitating the reduction of central macular thickness in diabetic macular edema[J]. Indian J Ophthalmol, 2018, 66(1): 98-105. DOI: 10.4103/ijo.IJO_566_17.
32. Barrett EJ, Liu Z, Khamaisi M, et al. Diabetic microvascular disease: an endocrine society scientific statement[J]. J Clin Endocrinol Metab, 2017, 102(12): 4343-4410. DOI: 10.1210/jc.2017-01922.
33. Martín-Merino E, Fortuny J, Rivero-Ferrer E, et al. Risk factors for diabetic macular oedema in type 2 diabetes: a case-control study in a United Kingdom primary care setting[J]. Prim Care Diabetes, 2017, 11(3): 288-296. DOI: 10.1016/j.pcd.2017.03.002.
34. Zhuang X, Cao D, Yang D, et al. Association of diabetic retinopathy and diabetic macular oedema with renal function in southern Chinese patients with type 2 diabetes mellitus: a single-centre observational study[J/OL]. BMJ Open, 2019, 9(9): e031194[2019-09-06]. https://pubmed.ncbi.nlm.nih.gov/31494622/. DOI: 10.1136/bmjopen-2019-031194.
35. Hsieh YT, Tsai MJ, Tu ST, et al. Association of abnormal renal profiles and proliferative diabetic retinopathy and diabetic macular edema in an Asian population with type 2 diabetes[J]. JAMA Ophthalmol, 2018, 136(1): 68-74. DOI: 10.1001/jamaophthalmol.2017.5202.
36. Theodossiadis PG, Theodoropoulou S, Neamonitou G, et al. Hemodialysis-induced alterations in macular thickness measured by optical coherence tomography in diabetic patients with end-stage renal disease[J]. Ophthalmologica, 2012, 227(2): 90-94. DOI: 10.1159/000331321.
37. Takamura Y, Matsumura T, Ohkoshi K, et al. Functional and anatomical changes in diabetic macular edema after hemodialysis initiation: one-year follow-up multicenter study[J/OL]. Sci Rep, 2020, 10(1): 7788[2020-05-08]. https://pubmed.ncbi.nlm.nih.gov/32385333/. DOI: 10.1038/s41598-020-64798-4.
38. Samanta R, Puthalath AS, Saraswat N, et al. Rapidly reversing bilateral macular edema associated with fluid overload in a young type 1 diabetic[J]. Indian J Ophthalmol, 2019, 67(7): 1221-1223. DOI: 10.4103/ijo.IJO_1805_18.
39. Kahtani ES. Diabetic glomerulosclerosis can be the pathogenesis of refractory diabetic macular edema[J]. Clin Ophthalmol, 2015, 9: 929-933. DOI: 10.2147/OPTH.S80850.

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