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Study | Type of study | Follow-up period | Type of diabetes | Aim of study | Basis for DR diagnosis/classification | Basis for DKD diagnosis | Study definition of DKD progression | Results | JBI score |
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Yamanouchi et al. [32] 2019, Japan (N = 232) | Retrospective | 5.7 years (median) | Type 2 | (1) To evaluate the association between clinical findings in the retina and pathological lesions in kidney biopsy specimens and (2) to quantify the risk for ESKD, according to the severity of diabetic retinopathy, in patients with type 2 diabetes and biopsy-proven DKD | Review of medical records on retinal/fundus Examination DR classification: ICDR scale | Biopsy-proven DKD | Progression to ESKD (defined as initiation of any hemodialysis, peritoneal dialysis, or renal transplantation, or death from uremia) | HR (95% CI) of ESKD risk for each DR stage, relative to no DR Mild NPDR: 1.35 (0.49–3.76) Moderate NPDR: 2.89 (1.42–5.86) Severe NPDR: 5.00 (2.63–9.52) PDR: 5.32 (2.89–9.78) | 10 |
Hsing et al. [33] 2020, Taiwan (N = 1329) | Retrospective | 1.97 years (mean) | Type 2 | To evaluate the renal disease progression (ESKD and CKD) in patients with type 2 diabetes and with/without DKD according to DR severity | Fundus photographs analysed by deep learning models and confirmed by ophthalmologist DR classification: ICDR scale | Presumed DKD | Progression to ESKD (defined as initiation of any hemodialysis, peritoneal dialysis, renal transplantation or death from uremia) | HR (95% CI) of ESKD risk for each DR stage, relative to no DR Mild NPDR: 2.35 (1.01–5.43) Moderate NPDR: 5.96 (2.99–11.89) Severe NPDR: 2.79 (1.16–6.75) PDR: 6.98 (2.22–21.94) | 9 |
HR (95% CI) of CKD for each DR stage, relative to no DR for subjects without CKD initially (n = 841): Mild NPDR: 3.46 (0.92–12.98) Moderate NPDR: 8.75 (2.74–27.92) Severe NPDR: 5.73 (1.64–20.04) PDR: 14.21 (1.55–130.67) |
Zhao et al. [34] 2020, China (N = 91) | Retrospective | 15 months (median) | Type 2 | (1) To classify DR as mild, moderate, or severe nonproliferative, or proliferative by artificial intelligence and an ophthalmologist, in Chinese patients with biopsy-confirmed DKD (2) To determine whether the severity of DR at the time of biopsy can predict progression to ESKD and (3) To characterize the relationship between DR and DKD in patients with DKD | Digital fundus photographs analysed by the lesion-aware deep learning system (RetinalNET) DR classification: early treatment diabetic retinopathy study severity scale (ETDRS) | Biopsy-proven DKD | Progression to ESKD (defined as eGFR<15 ml/min/1.73 m2, or the use of renal replacement therapy) | HR (95% CI) of ESKD risk for DR, relative to no DR: 2.23 (1.51–3.29) | 10 |
ESRD (n,%) for each stage of baseline DR: no DR: (0,0%), mild: (1, 9.1%), moderate: (13, 30.2%), severe: (6, 46.2%), PDR: (5, 55.6%) |
Mottl et al. [35] 2014, USA (N = 3210) | Prospective | 4 years (mean) | Type 2 | To evaluate specificity of DR for renal versus CV disease | Fundus photographs evaluated by trained graders DR classification: ETDRS final diabetic retinopathy severity scale | Presumed DKD | Progression to ESKD (defined as eGFR<15 ml/min/1.73m2 or if a participant was on dialysis or received renal transplantation) | HR (95% CI) of ESKD risk for moderate/severe DR, relative to no/mild DR: 1.05 (0.64, 1.73) | 10 |
Zhang et al. [36] 2018, China (N = 141) | Retrospective | 19 months (median) | Type 2 | To identify whether DR was associated with the progression of DKD in patients with T2DM and biopsy-proven DKD | Ophthalmoscopy, equivocal diagnosis was validated with optical coherence tomography and fundus colour photography DR classification: NR | Biopsy-proven DKD | Progression to ESKD (defined as eGFR<15 mL/min/1.73 m2 or the initiation of renal replacement therapy) | HR (95% CI) of ESKD risk for DR, relative to no DR: 2.264(1.309–3.917) | 10 |
Hung et al. [37] 2017, Taiwan (N = 1330) | Prospective | 2.9 years (median) | Types 1 and 2 | To study if longer diabetes duration, DR, and a diagnostic model were associated with less favourable renal outcomes, cardiovascular events and all-cause mortality in nonbiopsied patients with DKD | Fundoscopy/digital fundus photography examination DR classification: background, preproliferative, and proliferative changes | Presumed DKD | Progression to ESKD (defined as initiation of hemodialysis, peritoneal dialysis, or renal transplantation) | HR (95% CI) of ESKD risk for DR, relative to no DR: 2.56 (1.81–3.62) | 9 |
Alwakeel et al. [38] 2011, Saudi Arabia (N = 621) | Retrospective | 9.9 years (mean) | Type 2 | To evaluate the pattern and changes in GFR over time and investigate the potential risk factors associated with enhanced loss of renal function and all-cause mortality among Saudis with type 2 diabetes and nephropathy | NR | Presumed DKD | Drop in KDIGO GFR category | HR (95% CI) of CKD progression for DR, relative to no DR: 1.8 (1.3–2.3) | 10 |
Hong et al. [39] 2021, USA (N = 1759) | Retrospective | 14.2 years (median) | Types 1 and 2 | To examine the association between retinopathy and kidney disease in persons with diabetes in the community-based atherosclerosis risk in communities (ARIC) study | Fundus photographs assessed by masked graders. DR classification: early treatment diabetic retinopathy study severity scale | Presumed DKD | Incident ESKD [defined by linkage to the US renal data system (USRDS)] | HR (95% CI) of ESKD risk for DR, relative to no DR: 2.92 (2.00–4.26) | 9 |
Lin et al. [40] 2019, Singapore (N = 4050) | Prospective | <1 year | Types 1 and 2 | To evaluate the characteristics of CKD patients, with or without DR, and examine the relation between DR and its severity on the decline rate in the eGFR in stages 1–5 CKD patients | Dilated fundus examination and fluorescein angiography DR classification: no apparent signs of DR: normal; microaneurysms, hard exudates, intraretinal hemorrhages, venous beading, or prominent intraretinal microvascular abnormality: early stage, nonproliferative DR (NPDR); and retinal or optic disk neovascularization, vitreous hemorrhage, or preretinal hemorrhage: late stage, proliferative DR (PDR) | Presumed DKD | eGFR decline by more than 5 mL/min/1.73 m2/year | OR (95% CI) of DKD progression for DR, relative to no DR: 1.75 (1.48–2.07) | 10 |
Park et al. [41] 2019, Korea (N = 1592) | Retrospective | 5.6 years (mean) | Type 2 | To assess the value of DR severity to predict renal dysfunction and albuminuria progression in type 2 DM patients | Slit-lamp examination, indirect ophthalmoscopy and/or fluorescein angiography DR classification: no DR, NPDR and PDR | Presumed DKD | Decline in GFR category accompanied by ≥25% eGFR drop OR sustained decline in eGFR of more than 5 mL/min/1.73 m2/year | OR (95% CI) of DKD progression for DR, relative to no DR NPDR: 4.05 (2.993–5.488) PDR: 9.293 (6.569–13.146) | 10 |
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