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Published in: BMC Cardiovascular Disorders 1/2020

Open Access 01-12-2020 | Diabetic Retinopathy | Research article

Diabetic retinopathy predicts cardiovascular mortality in diabetes: a meta-analysis

Authors: Xiao-Hong Xu, Bo Sun, Shan Zhong, Dong-Dong Wei, Ze Hong, Ai-Qiang Dong

Published in: BMC Cardiovascular Disorders | Issue 1/2020

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Abstract

Background

The prognostic significance of diabetic retinopathy (DR) for cardiovascular diseases (CVD) remained unclear. Therefore, we performed this meta-analysis to assess whether DR predicted CVD mortality in diabetic patients.

Methods

We searched PubMed, Embase, Web of Science and Cochrane Library for cohort studies reporting the association of DR and CVD mortality. Then we pooled the data for analysis.

Results

After screening the literature, 10 eligible studies with 11,239 diabetic subjects were finally included in quantitative synthesis. The pooled risk ratio (RR) of DR, mild DR, and severe DR for CVD mortality was 1.83 (95% confidence interval (CI): 1.42, 2.36; p < 0.001), 1.13 (95% CI 0.81, 1.59; p = 0.46), and 2.26 (1.31, 3.91; p = 0.003), respectively, compared to those without DR. In type 2 DM, the patients with DR had a significantly higher CVD mortality (RR: 1.69; 95% CI 1.27, 2.24; p < 0.001). Subgroup analysis also showed a significantly higher CVD mortality in DR according to various regions, study design, data source, and follow-up period (all RR > 1; all P values < 0.05). Data from 2 studies showed no significant correlation of DR and CVD mortality in diabetic patients receiving cardiovascular surgery (RR: 2.40; 95% CI 0.63, 9.18; P = 0.200).

Conclusions

DR is a risk marker of cardiovascular death, and severe DR predicts a doubled mortality of CVD in diabetes. These findings indicate the importance of early identification and management of diabetic patients with DR to reduce the risk of death.
Literature
1.
go back to reference Zimmet P, Alberti KG, Magliano DJ, Bennett PH. Diabetes mellitus statistics on prevalence and mortality: facts and fallacies. Nat Rev Endocrinol. 2016;12(10):616–22.CrossRefPubMed Zimmet P, Alberti KG, Magliano DJ, Bennett PH. Diabetes mellitus statistics on prevalence and mortality: facts and fallacies. Nat Rev Endocrinol. 2016;12(10):616–22.CrossRefPubMed
3.
go back to reference Zheng Y, Ley SH, Hu FB. Global aetiology and epidemiology of type 2 diabetes mellitus and its complications. Nat Rev Endocrinol. 2018;14(2):88–98.CrossRefPubMed Zheng Y, Ley SH, Hu FB. Global aetiology and epidemiology of type 2 diabetes mellitus and its complications. Nat Rev Endocrinol. 2018;14(2):88–98.CrossRefPubMed
5.
go back to reference Klein R. Epidemiology of diabetic retinopathy. In: Diabetic Retinopathy. Duh E, ed. Totowa: Humana Press. 2008. Klein R. Epidemiology of diabetic retinopathy. In: Diabetic Retinopathy. Duh E, ed. Totowa: Humana Press. 2008.
6.
go back to reference Varma R. From a population to patients: the Wisconsin epidemiologic study of diabetic retinopathy. Ophthalmology. 2008;115:1857–8.CrossRefPubMed Varma R. From a population to patients: the Wisconsin epidemiologic study of diabetic retinopathy. Ophthalmology. 2008;115:1857–8.CrossRefPubMed
7.
go back to reference Klein R, Klein BE, Moss SE, Cruickshanks KJ. Association of ocular disease and mortality in a diabetic population. Arch Ophthalmol. 1999;117(11):1487–95.CrossRefPubMed Klein R, Klein BE, Moss SE, Cruickshanks KJ. Association of ocular disease and mortality in a diabetic population. Arch Ophthalmol. 1999;117(11):1487–95.CrossRefPubMed
8.
go back to reference Klein BE, Klein R, McBride PE, Cruickshanks KJ, Palta M, Knudtson MD, et al. Cardiovascular disease, mortality, and retinal microvascular characteristics in type 1 diabetes: Wisconsin epidemiologic study of diabetic retinopathy. Arch Intern Med. 2004;164(17):1917–24.CrossRefPubMed Klein BE, Klein R, McBride PE, Cruickshanks KJ, Palta M, Knudtson MD, et al. Cardiovascular disease, mortality, and retinal microvascular characteristics in type 1 diabetes: Wisconsin epidemiologic study of diabetic retinopathy. Arch Intern Med. 2004;164(17):1917–24.CrossRefPubMed
9.
go back to reference Kramer CK, Rodrigues TC, Canani LH, Gross JL, Azevedo MJ. Diabetic retinopathy predicts all-cause mortality and cardiovascular events in both type 1 and 2 diabetes: meta-analysis of observational studies. Diabetes Care. 2011;34(5):1238–44.CrossRefPubMedPubMedCentral Kramer CK, Rodrigues TC, Canani LH, Gross JL, Azevedo MJ. Diabetic retinopathy predicts all-cause mortality and cardiovascular events in both type 1 and 2 diabetes: meta-analysis of observational studies. Diabetes Care. 2011;34(5):1238–44.CrossRefPubMedPubMedCentral
10.
go back to reference von Elm E, Altman DG, Egger M, Pocock SJ, Gøtzsche PC, Vandenbroucke JP; STROBE Initiative. The strengthening the reporting of observational studies in epidemiology (STROBE) statement: guidelines for reporting observational studies. PLoS Med. 2007; 4:e296. von Elm E, Altman DG, Egger M, Pocock SJ, Gøtzsche PC, Vandenbroucke JP; STROBE Initiative. The strengthening the reporting of observational studies in epidemiology (STROBE) statement: guidelines for reporting observational studies. PLoS Med. 2007; 4:e296.
11.
go back to reference Sabanayagam C, Chee ML, Banu R, Cheng CY, Lim SC, Tai ES, et al. Association of diabetic retinopathy and diabetic kidney disease with all-cause and cardiovascular mortality in a multiethnic Asian population. JAMA Netw Open. 2019;2(3):e191540.CrossRefPubMedPubMedCentral Sabanayagam C, Chee ML, Banu R, Cheng CY, Lim SC, Tai ES, et al. Association of diabetic retinopathy and diabetic kidney disease with all-cause and cardiovascular mortality in a multiethnic Asian population. JAMA Netw Open. 2019;2(3):e191540.CrossRefPubMedPubMedCentral
12.
go back to reference Takao T, Suka M, Yanagisawa H, Kasuga M. Combined effect of diabetic retinopathy and diabetic kidney disease on all-cause, cancer, vascular and non-cancer non-vascular mortality in patients with type 2 diabetes: A real-world longitudinal study. J Diabetes Investig. 2020. Epub ahead of print. Takao T, Suka M, Yanagisawa H, Kasuga M. Combined effect of diabetic retinopathy and diabetic kidney disease on all-cause, cancer, vascular and non-cancer non-vascular mortality in patients with type 2 diabetes: A real-world longitudinal study. J Diabetes Investig. 2020. Epub ahead of print.
13.
go back to reference Kim YH, Hong MK, Song JM, Han KH, Kang DH, Song JK, et al. Diabetic retinopathy as a predictor of late clinical events following percutaneous coronary intervention. J Invasive Cardiol. 2002;14(10):599–602.PubMed Kim YH, Hong MK, Song JM, Han KH, Kang DH, Song JK, et al. Diabetic retinopathy as a predictor of late clinical events following percutaneous coronary intervention. J Invasive Cardiol. 2002;14(10):599–602.PubMed
14.
go back to reference Rajala U, Pajunpää H, Koskela P, Keinänen-Kiukaanniemi S. High cardiovascular disease mortality in subjects with visual impairment caused by diabetic retinopathy. Diabetes Care. 2000;23(7):957–61.CrossRefPubMed Rajala U, Pajunpää H, Koskela P, Keinänen-Kiukaanniemi S. High cardiovascular disease mortality in subjects with visual impairment caused by diabetic retinopathy. Diabetes Care. 2000;23(7):957–61.CrossRefPubMed
15.
go back to reference Hsieh YM, Lee WJ, Sheu WH, Li YH, Lin SY, Lee IT. Inpatient screening for albuminuria and retinopathy to predict long-term mortality in type 2 diabetic patients: a retrospective cohort study. Diabetol Metab Syndr. 2017;9:29.CrossRefPubMedPubMedCentral Hsieh YM, Lee WJ, Sheu WH, Li YH, Lin SY, Lee IT. Inpatient screening for albuminuria and retinopathy to predict long-term mortality in type 2 diabetic patients: a retrospective cohort study. Diabetol Metab Syndr. 2017;9:29.CrossRefPubMedPubMedCentral
16.
go back to reference Juutilainen A, Lehto S, Rönnemaa T, Pyörälä K, Laakso M. Retinopathy predicts cardiovascular mortality in type 2 diabetic men and women. Diabetes Care. 2007;30(2):292–9.CrossRefPubMed Juutilainen A, Lehto S, Rönnemaa T, Pyörälä K, Laakso M. Retinopathy predicts cardiovascular mortality in type 2 diabetic men and women. Diabetes Care. 2007;30(2):292–9.CrossRefPubMed
17.
go back to reference Liew G, Wong TY, Mitchell P, Cheung N, Wang JJ. Retinopathy predicts coronary heart disease mortality. Heart. 2009;95(5):391–4.CrossRefPubMed Liew G, Wong TY, Mitchell P, Cheung N, Wang JJ. Retinopathy predicts coronary heart disease mortality. Heart. 2009;95(5):391–4.CrossRefPubMed
18.
go back to reference Lövestam-Adrian M, Hansson-Lundblad C, Torffvit O. Sight-threatening retinopathy is associated with lower mortality in type 2 diabetic subjects: a 10-year observation study. Diabetes Res Clin Pract. 2007;77(1):141–7.CrossRefPubMed Lövestam-Adrian M, Hansson-Lundblad C, Torffvit O. Sight-threatening retinopathy is associated with lower mortality in type 2 diabetic subjects: a 10-year observation study. Diabetes Res Clin Pract. 2007;77(1):141–7.CrossRefPubMed
19.
go back to reference Mottl AK, Pajewski N, Fonseca V, Ismail-Beigi F, Chew E, Ambrosius WT, et al. The degree of retinopathy is equally predictive for renal and macrovascular outcomes in the ACCORD Trial. J Diabetes Complications. 2014;28(6):874–9.CrossRefPubMedPubMedCentral Mottl AK, Pajewski N, Fonseca V, Ismail-Beigi F, Chew E, Ambrosius WT, et al. The degree of retinopathy is equally predictive for renal and macrovascular outcomes in the ACCORD Trial. J Diabetes Complications. 2014;28(6):874–9.CrossRefPubMedPubMedCentral
20.
go back to reference Ono T, Kobayashi J, Sasako Y, Bando K, Tagusari O, Niwaya K, et al. The impact of diabetic retinopathy on long-term outcome following coronary artery bypass graft surgery. J Am Coll Cardiol. 2002; 40(3):428–36. Ono T, Kobayashi J, Sasako Y, Bando K, Tagusari O, Niwaya K, et al. The impact of diabetic retinopathy on long-term outcome following coronary artery bypass graft surgery. J Am Coll Cardiol. 2002; 40(3):428–36.
21.
go back to reference Miettinen H, Haffner SM, Lehto S, Rönnemaa T, Pyörälà K, Laakso M. Retinopathy predicts coronary heart disease events in NIDDM patients. Diabetes Care. 1996;19(12):1445–8.CrossRefPubMed Miettinen H, Haffner SM, Lehto S, Rönnemaa T, Pyörälà K, Laakso M. Retinopathy predicts coronary heart disease events in NIDDM patients. Diabetes Care. 1996;19(12):1445–8.CrossRefPubMed
22.
go back to reference Drinkwater JJ, Davis TME, Hellbusch V, Turner AW, Bruce DG, Davis WA. Retinopathy predicts stroke but not myocardial infarction in type 2 diabetes: the Fremantle Diabetes Study Phase II. Cardiovasc Diabetol. 2020;19(1):43.CrossRefPubMedPubMedCentral Drinkwater JJ, Davis TME, Hellbusch V, Turner AW, Bruce DG, Davis WA. Retinopathy predicts stroke but not myocardial infarction in type 2 diabetes: the Fremantle Diabetes Study Phase II. Cardiovasc Diabetol. 2020;19(1):43.CrossRefPubMedPubMedCentral
23.
go back to reference Fisher DE, Jonasson F, Klein R, Jonsson PV, Eiriksdottir G, Launer LJ, et al. Mortality in older persons with retinopathy and concomitant health conditions: the age. Gene/Environ Suscep Reykjavik Stud Ophthalmol. 2016;123(7):1570–80. Fisher DE, Jonasson F, Klein R, Jonsson PV, Eiriksdottir G, Launer LJ, et al. Mortality in older persons with retinopathy and concomitant health conditions: the age. Gene/Environ Suscep Reykjavik Stud Ophthalmol. 2016;123(7):1570–80.
24.
go back to reference Fuller JH, Stevens LK, Wang SL. Risk factors for cardiovascular mortality and morbidity: the WHO Mutinational Study of Vascular Disease in Diabetes. Diabetologia. 2001;44(Suppl 2):S54-64.CrossRefPubMed Fuller JH, Stevens LK, Wang SL. Risk factors for cardiovascular mortality and morbidity: the WHO Mutinational Study of Vascular Disease in Diabetes. Diabetologia. 2001;44(Suppl 2):S54-64.CrossRefPubMed
25.
go back to reference Landers J, Liu E, Estevez J, Henderson T, Craig JE. Presence of diabetic retinopathy is associated with worse 10-year mortality among Indigenous Australians in Central Australia: The Central Australian ocular health study. Clin Exp Ophthalmol. 2019;47(2):226–32.CrossRefPubMed Landers J, Liu E, Estevez J, Henderson T, Craig JE. Presence of diabetic retinopathy is associated with worse 10-year mortality among Indigenous Australians in Central Australia: The Central Australian ocular health study. Clin Exp Ophthalmol. 2019;47(2):226–32.CrossRefPubMed
26.
go back to reference Grauslund J. Long-term mortality and retinopathy in type 1 diabetes. Acta Ophthalmol. 2010; 88 Thesis1:1–14. Grauslund J. Long-term mortality and retinopathy in type 1 diabetes. Acta Ophthalmol. 2010; 88 Thesis1:1–14.
27.
go back to reference Shukla SY, Hariprasad AS, Hariprasad SM. Long-term mortality in diabetic patients with tractional retinal detachments. Ophthalmol Retina. 2017;1(1):8–11.CrossRefPubMed Shukla SY, Hariprasad AS, Hariprasad SM. Long-term mortality in diabetic patients with tractional retinal detachments. Ophthalmol Retina. 2017;1(1):8–11.CrossRefPubMed
28.
go back to reference Banerjee PJ, Moya R, Bunce C, Charteris DG, Yorston D, Wickham L. Long-term survival rates of patients undergoing vitrectomy for proliferative diabetic retinopathy. Ophthalmic Epidemiol. 2016;23(2):94–8.CrossRefPubMed Banerjee PJ, Moya R, Bunce C, Charteris DG, Yorston D, Wickham L. Long-term survival rates of patients undergoing vitrectomy for proliferative diabetic retinopathy. Ophthalmic Epidemiol. 2016;23(2):94–8.CrossRefPubMed
29.
go back to reference Liu E, Estevez J, Kaidonis G, Hassall M, Phillips R, Raymond G, et al. Long-term survival rates of patients undergoing vitrectomy for diabetic retinopathy in an Australian population: a population-based audit. Clin Exp Ophthalmol. 2019;47(5):598–604.CrossRefPubMed Liu E, Estevez J, Kaidonis G, Hassall M, Phillips R, Raymond G, et al. Long-term survival rates of patients undergoing vitrectomy for diabetic retinopathy in an Australian population: a population-based audit. Clin Exp Ophthalmol. 2019;47(5):598–604.CrossRefPubMed
30.
go back to reference Roy M, Rendas-Baum R, Skurnick J. Mortality in African-americans with type 1 diabetes: the New Jersey 725. Diabet Med. 2006;23(6):698–706.CrossRefPubMed Roy M, Rendas-Baum R, Skurnick J. Mortality in African-americans with type 1 diabetes: the New Jersey 725. Diabet Med. 2006;23(6):698–706.CrossRefPubMed
31.
go back to reference Torffvit O, Lövestam-Adrian M, Agardh E, Agardh CD. Nephropathy, but not retinopathy, is associated with the development of heart disease in Type 1 diabetes: a 12-year observation study of 462 patients. Diabet Med. 2005;22:723–9.CrossRefPubMed Torffvit O, Lövestam-Adrian M, Agardh E, Agardh CD. Nephropathy, but not retinopathy, is associated with the development of heart disease in Type 1 diabetes: a 12-year observation study of 462 patients. Diabet Med. 2005;22:723–9.CrossRefPubMed
32.
go back to reference Heller T, Kloos C, Lehmann T, Schiel R, Lorkowski S, Wolf G, et al. Mortality and its causes in a german cohort with diabetes mellitus Type 1 after 20 years of follow-up: the JEVIN trial. Exp Clin Endocrinol Diabetes. 2018;126(6):387–93.CrossRefPubMed Heller T, Kloos C, Lehmann T, Schiel R, Lorkowski S, Wolf G, et al. Mortality and its causes in a german cohort with diabetes mellitus Type 1 after 20 years of follow-up: the JEVIN trial. Exp Clin Endocrinol Diabetes. 2018;126(6):387–93.CrossRefPubMed
Metadata
Title
Diabetic retinopathy predicts cardiovascular mortality in diabetes: a meta-analysis
Authors
Xiao-Hong Xu
Bo Sun
Shan Zhong
Dong-Dong Wei
Ze Hong
Ai-Qiang Dong
Publication date
01-12-2020
Publisher
BioMed Central
Published in
BMC Cardiovascular Disorders / Issue 1/2020
Electronic ISSN: 1471-2261
DOI
https://doi.org/10.1186/s12872-020-01763-z

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