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The association of smoking and risk of diabetic retinopathy in patients with type 1 and type 2 diabetes: a meta-analysis

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Abstract

Purpose

To clarify the relevance between smoking and diabetic retinopathy in patients with type 1 and type 2 diabetes mellitus.

Methods

Published evidence were searched in MEDLINE and EMBASE from the databases began until Feb. 2017. Studies evaluating the association between smoking and diabetic retinopathy or evaluating the risk factors of diabetic retinopathy including smoking were included.

Results

Totally 73 studies were identified, among which 19 studies included type 1 diabetes patients and 56 studies included type 2 diabetes patients. In type 1 diabetes, compare with non-smokers, the risk of diabetic retinopathy significantly increased in smokers (risk ratio (RR) = 1.23, 95% CI 1.14, 1.33, P < 0.001), and the risk of proliferative diabetic retinopathy also significantly increased in smokers (RR = 1.48, 95% CI 1.20, 1.81, P < 0.001). In type 2 diabetes, compare with non-smokers, the risk of diabetic retinopathy significantly decreased in smokers (RR = 0.92, 95% CI 0.86, 0.98, P = 0.02) and the risk of proliferative diabetic retinopathy also significantly decreased in smokers (RR = 0.68, 95% CI 0.61, 0.74, P < 0.001).

Conclusions

Compare with non-smokers, the risk of diabetic retinopathy significantly increased in smokers with type 1 diabetes while significantly decreased in smokers with type 2 diabetes. However, this result did not change the importance of smoking cessation for public health.

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References

  1. American Diabetes, A., Microvascular complications and foot care: standards of medical care in diabetes-2018. Diabetes Care 41(Suppl 1), S105–S118 (2018).

  2. R. Klein, Hyperglycemia and microvascular and macrovascular disease in diabetes. Diabetes Care 18(2), 258–268 (1995)

    Article  CAS  Google Scholar 

  3. R.O. Estacio, E. McFarling, S. Biggerstaff, B.W. Jeffers, D. Johnson, R.W. Schrier, Overt albuminuria predicts diabetic retinopathy in Hispanics with NIDDM. Am. J. Kidney Dis. 31(6), 947–953 (1998)

    Article  CAS  Google Scholar 

  4. M.C. Leske, S.Y. Wu, A. Hennis, Hyman. B, Nemesure. L, Yang. A.P, Schachat; Barbados Eye Study, G., Hyperglycemia, blood pressure, and the 9-year incidence of diabetic retinopathy: the Barbados Eye Studies. Ophthalmology 112(5), 799–805 (2005).

    Article  Google Scholar 

  5. E.Y. Chew, M.D. Davis, R.P. Danis, J.F. Lovato, L.H. Perdue, C. Greven, S. Genuth, D.C. Goff, L.A. Leiter, F. Ismail-Beigi, W.T. Ambrosius, Action to Control Cardiovascular Risk in Diabetes Eye Study Research, G., The effects of medical management on the progression of diabetic retinopathy in persons with type 2 diabetes: the Action to Control Cardiovascular Risk in Diabetes (ACCORD) Eye Study. Ophthalmology 121(12), 2443–2451 (2014).

    Article  Google Scholar 

  6. I.M. Stratton, E.M. Kohner, S.J. Aldington, R.C. Turner, R.R. Holman, S.E. Manley, D.R. Matthews, UKPDS 50:risk factors for incidence and progression of retinopathy in Type II diabetes over 6 years from diagnosis. Diabetologia 44(2), 156–163 (2001).

    Article  CAS  Google Scholar 

  7. W. Zhu, Y.F. Meng, Y. Wu, M. Xu, J. Lu, Association of alcohol intake with risk of diabetic retinopathy: a metaanalysis of observational studies. Sci. Rep 7(1), 4 (2017).

    Article  Google Scholar 

  8. F. Costa, R. Soares, Nicotine: a pro-angiogenic factor. Life Sci 84(23-24), 785–790 (2009).

    Article  CAS  Google Scholar 

  9. P.B. Morgado, H.C. Chen, V. Patel, L. Herbert, E.M. Kohner, The acute effect of smoking on retinal blood flow in subjects with and without diabetes. Ophthalmology 101(7), 1220–1226 (1994)

    Article  CAS  Google Scholar 

  10. I.D. Nicholl, R. Bucala, Advanced glycation endproducts and cigarette smoking. Cell Mol. Biol. 44(7), 1025–1033 (1998)

    CAS  PubMed  Google Scholar 

  11. M.E. Paetkau, T.A. Boyd, B. Winship, M. Grace, Cigarette smoking and diabetic retinopathy. Diabetes 26(1), 46–49 (1977)

    Article  CAS  Google Scholar 

  12. I. Muhlhauser, P. Sawicki, M. Berger, Cigarette-smoking as a risk factor for macroproteinuria and proliferative retinopathy in type 1 (insulin-dependent) diabetes. Diabetologia 29(8), 500–502 (1986)

    Article  CAS  Google Scholar 

  13. L.A. Kingsley, J.S. Dorman, B.H. Doft, T.J. Orchard, R.E. LaPorte, L.H. Kuller, A.L. Drash, An epidemiologic approach to the study of retinopathy: the Pittsburgh diabetic morbidity and retinopathy studies. Diabetes Res. Clin. Pract. 4(2), 99–109 (1988)

    Article  CAS  Google Scholar 

  14. M.C. Schumacher, K.R. Smith, Diabetes in Utah among adults: interaction between diabetes and other risk factors for microvascular and macrovascular complications. Am. J. Public Health 78(9), 1195–1201 (1988)

    Article  CAS  Google Scholar 

  15. K.M. West, L.S. Erdreich, J.A. Stober, Absence of a relationship between smoking and diabetic microangiopathy. Diabetes Care 3(2), 250–252 (1980)

    Article  CAS  Google Scholar 

  16. A.H. Barnett, J.R. Britton, B.A. Leatherdale, Study of possible risk factors for severe retinopathy in non-insulin dependent diabetes. Br. Med. J. 287(6391), 529 (1983)

    Article  CAS  Google Scholar 

  17. L. Yanko, U. Goldbourt, I.C. Michaelson, A. Shapiro, S. Yaari, Prevalence and 15-year incidence of retinopathy and associated characteristics in middle-aged and elderly diabetic men. Br. J. Ophthalmol. 67(11), 759–765 (1983)

    Article  CAS  Google Scholar 

  18. S. Telmer, J.S. Christiansen, A.R. Andersen, J. Nerup, T. Deckert, Smoking habits and prevalence of clinical diabetic microangiopathy in insulin-dependent diabetics. Acta Med. Scand. 215(1), 63–68 (1984)

    Article  CAS  Google Scholar 

  19. L.I. Rand, A.S. Krolewski, L.M. Aiello, J.H. Warram, R.S. Baker, T. Maki, Multiple factors in the prediction ofrisk of proliferative diabetic retinopathy. N. Engl. J. Med 313(23), 1433–1438 (1985).

    Article  CAS  Google Scholar 

  20. D.J. Ballard, L.J. Melton 3rd, M.S. Dwyer, J.C. Trautmann, C.P. Chu, W.M. O’Fallon, P.J. Palumbo, Risk factors for diabetic retinopathy: a population-based study in Rochester, Minnesota. Diabetes Care 9(4), 334–342 (1986)

    Article  CAS  Google Scholar 

  21. S.E. Moss, R. Klein, B.E. Klein, Association of cigarette smoking with diabetic retinopathy. Diabetes Care 14(2), 119–126 (1991)

    Article  CAS  Google Scholar 

  22. G. Marshall, S.K. Garg, W.E. Jackson, D.L. Holmes, H.P. Chase, Factors influencing the onset and progression of diabetic retinopathy in subjects with insulin-dependent diabetes mellitus. Ophthalmology 100(8), 1133–1139 (1993)

    Article  CAS  Google Scholar 

  23. J.M. Sparrow, B.K. McLeod, T.D. Smith, M.K. Birch, A.R. Rosenthal, The prevalence of diabetic retinopathy and maculopathy and their risk factors in the non-insulin-treated diabetic patients of an English town. Eye 7(Pt 1), 158–163 (1993).

    Article  Google Scholar 

  24. M.S. Chen, C.S. Kao, C.J. Chang, T.J. Wu, C.C. Fu, C.J. Chen, T.Y. Tai, Prevalence and risk factors of diabetic retinopathy among noninsulin-dependent diabetic subjects. Am. J. Ophthalmol. 114(6), 723–730 (1992)

    Article  CAS  Google Scholar 

  25. S.E. Moss, R. Klein, B.E. Klein, Cigarette smoking and ten-year progression of diabetic retinopathy. Ophthalmology 103(9), 1438–1442 (1996)

    Article  CAS  Google Scholar 

  26. Callaghan, B. C., Little, A. A., Feldman, E. L., Hughes, R. A., Enhanced glucose control for preventing and treating diabetic neuropathy. Cochrane Database Syst. Rev. 6, CD007543 (2012).

  27. X. Zeng, Y. Zhang, J.S. Kwong, C. Zhang, S. Li, F. Sun, Y. Niu, L. Du, The methodological quality assessmenttools for preclinical and clinical studies, systematic review and meta-analysis, and clinical practice guideline: asystematic review. J. Evid. Based Med 8(1), 2–10 (2015).

    Article  Google Scholar 

  28. G. Wells, The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp (2011).

  29. J.P.Higgins, D.G. Altman, P.C. Gotzsche, P. Juni, D. Moher, A.D. Oxman, J. Savovic, K.F. Schulz, L. Weeks, J.A. Sterne, G. Cochrane Bias Methods; Cochrane Statistical Methods, G., The Cochrane Collaboration’s tool for assessing risk of bias in randomised trials. BMJ 343, d5928 (2011).

    Article  Google Scholar 

  30. D.F. Stroup, J.A. Berlin, S.C. Morton, I. Olkin, G.D. Williamson, D. Rennie, D. Moher, B.J. Becker, T.A. Sipe, S.B. Thacker, Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis of observational studies in Epidemiology (MOOSE) group. JAMA 283(15), 2008–2012 (2000)

    Article  CAS  Google Scholar 

  31. I. Muhlhauser, R. Bender, U. Bott, V. Jorgens, M. Grusser, W. Wagener, H. Overmann, M. Berger, Cigarette smoking and progression of retinopathy and nephropathy in type 1 diabetes. Diabet. Med 13(6), 536–543 (1996).

    Article  CAS  Google Scholar 

  32. B. Karamanos, M. Porta, M. Songini, Z. Metelko, Z. Kerenyi, G. Tamas, R. Rottiers, L.K. Stevens, J.H. Fuller, Different risk factors of microangiopathy in patients with type I diabetes mellitus of short versus long duration. The EURODIAB IDDM Complications Study. Diabetologia 43(3), 348–355 (2000)

    Article  CAS  Google Scholar 

  33. N. Chaturvedi, J.M. Stephenson, J.H. Fuller, The relationship between smoking and microvascular complications in the EURODIAB IDDM Complications Study. Diabetes Care 18(6), 785–792 (1995)

    Article  CAS  Google Scholar 

  34. Diabetes, C., Complications Trial /Epidemiology of Diabetes, I., Complications Research, G., J.M. Lachin, N.H.White, D.P. Hainsworth, W. Sun, P.A. Cleary, D.M. Nathan, Effect of intensive diabetes therapy on the progressionof diabetic retinopathy in patients with type 1 diabetes: 18 years of follow-up in the DCCT/EDIC. Diabetes 64(2),631–642 (2015).

  35. H.P. Hammes, W. Kerner, S. Hofer, O. Kordonouri, K. Raile, R.W. Holl, D.P.-W.S. Group, Diabetic retinopathyin type 1 diabetes-a contemporary analysis of 8784 patients. Diabetologia 54(8), 1977–1984 (2011).

    Article  CAS  Google Scholar 

  36. V.H. Tam, E.P. Lam, B.C. Chu, K.K. Tse, L.M. Fung, Incidence and progression of diabetic retinopathy in Hong Kong Chinese with type 2 diabetes mellitus. J. Diabetes Complicat 23(3), 185–193 (2009).

    Article  Google Scholar 

  37. S.T. Tseng, S.T. Chou, B.H. Low, F.L. Su, Risk factors associated with diabetic retinopathy onset and progression in diabetes patients: a Taiwanese cohort study. Int. J. Clin. Exp. Med. 8(11), 21507–21515 (2015)

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Z.L. Zhong, S. Chen, Plasma plasminogen activator inhibitor-1 is associated with end-stage proliferative diabetic retinopathy in the Northern Chinese Han population. Exp. Diabetes Res 2012, 350852 (2012).

    PubMed  PubMed Central  Google Scholar 

  39. A. Leone, Biochemical markers of cardiovascular damage from tobacco smoke. Curr. Pharm. Des. 11(17), 2199–2208 (2005)

    Article  CAS  Google Scholar 

  40. M. Brownlee, H. Vlassara, A. Cerami, Nonenzymatic glycosylation and the pathogenesis of diabetic complications. Ann. Intern. Med. 101(4), 527–537 (1984)

    Article  CAS  Google Scholar 

  41. J.L. Wautier, P.J. Guillausseau, Advanced glycation end products, their receptors and diabetic angiopathy. Diabetes Metab. 27(5 Pt 1), 535–542 (2001)

    CAS  PubMed  Google Scholar 

  42. Y. Solberg, M. Rosner, M. Belkin, The association between cigarette smoking and ocular diseases. Surv. Ophthalmol. 42(6), 535–547 (1998)

    Article  CAS  Google Scholar 

  43. Hypertension in Diabetes Study (HDS): II Increased risk of cardiovascular complications in hypertensive type 2 diabetic patients. J. Hypertens. 11(3), 319–325 (1993).

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Author contributions

L.J. conceived and designed the systematic review protocol; Y.C., W.Y., X.G. performed the study selection and data extraction; X.C. and Y.C. performed the statistical analyses; and X.C., Y.C., X.H., and L.J. prepared the manuscript outlines and drafts. All authors contributed to the critical revision of manuscript drafts, as well as giving final approval for submitted manuscript content.

Funding

This study was supported by the National Key R and D Program of China (2016YFC1304901). The funding agency had no role in the study design, data collection or analysis, decision to publish or preparation of the manuscript.

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    Authors and Affiliations

    1. Department of Endocrinology and Metabolism, Peking University People’s Hospital, Beijing, China

      Xiaoling Cai, Wenjia Yang, Xueying Gao, Xueyao Han & Linong Ji

    2. Key laboratory of Carcinogenesis and Translational Research (Ministry of Education/Beijing), Department of Breast Oncology, Peking University Cancer Hospital & Institute, Beijing, China

      Yifei Chen

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    Conflict of interest

    L.J. has received fees for lecture presentations from AstraZeneca, Merck, Novartis, Lilly, Roche, Sanofi-Aventis and Takeda. L.J. has received consulting fees from companies including AstraZeneca, Merck, Novartis, Lilly, Roche, Sanofi-Aventis and Takeda. L.J. has received grants/research support from AstraZeneca, Bristol-Myers Squibb, Merck, Novartis, and Sanofi-Aventis. The remaining authors declare that they have no conflict of interest.

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    This article does not contain any studies with human participants or animals performed by any of the authors. We admit that this meta-analysis is complied with Ethical standards. Since this is a meta-analysis based on the published articles, therefore the ethical approval is not applicable.

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    These authors contributed equally: Xiaoling Cai, Yifei Chen.

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    Cai, X., Chen, Y., Yang, W. et al. The association of smoking and risk of diabetic retinopathy in patients with type 1 and type 2 diabetes: a meta-analysis. Endocrine 62, 299–306 (2018). https://doi.org/10.1007/s12020-018-1697-y

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