J Korean Ophthalmol Soc.  2016 May;57(5):779-785. 10.3341/jkos.2016.57.5.779.

The Association between Diabetic Retinopathy and Framingham Risk Score in Koreans with Type II Diabetes

• Kim DY
• Song SJ
• Bae JH
• Park CY
• Rhee EJ

• KMID: 2212721
• DOI: http://doi.org/10.3341/jkos.2016.57.5.779

Abstract

PURPOSE
In this study, we compared the risk of cardiovascular complications between diabetic retinopathy (DR) groups based on the Framingham Risk Score.
METHODS
Subjects 40 years of age or older were enrolled in the present study from September 2008 to September 2009. Five scales were used to evaluate the severity of DR for the most severely affected eye in each patient: no DR, mild nonproliferative DR (NPDR), moderate NPDR, severe NPDR and proliferative DR (PDR). The first group included no DR patients and the second group included mild NPDR patients. The third group included moderate NPDR, severe NPDR and PDR patients. The Framingham Risk Score was analyzed among the groups to determine whether a difference in score existed.
RESULTS
DR was found in 126 subjects. The first group included 403 subjects, the second group 22 subjects and the third group 104 subjects. The average Framingham Risk Score that appeared with increasing severity of DR was 10.89 ± 7.98 in the first group, 12.25 ± 10.84 in the second group and 13.25 ± 10.66 in the third group. The average difference between the first and third groups was statistically significant (p = 0.014).
CONCLUSIONS
In our study, the Framingham Risk Score increased significantly with more severe DR (p = 0.042). Our results are useful when considering the easily accessible identification of DR and that cardiovascular disease is one of the main causes of death worldwide. However, confirming the exact causal relationship based on our results is difficult because the study design was cross-sectional and additional studies are necessary.

Keyword

Cardiovascular complication; Diabetic retinopathy; Framingham Risk Score; Macrovascular complication; Microvascular complication

MeSH Terms

Cardiovascular Diseases
Cause of Death
Diabetic Retinopathy*
Humans
Weights and Measures

Reference

References

1. Williams R. Airey M. Baxter H, et al. Epidemiology of diabetic retinopathy and macular oedema: a systematic review. Eye (Lond). 2004; 18:963–83.

2. Danaei G. Finucane MM. Lu Y, et al. National, regional, and global trends in fasting plasma glucose and diabetes prevalence since 1980: systematic analysis of health examination surveys and epidemiological studies with 370 country-years and 2.7 million participants. Lancet. 2011; 378:31–40.

3. Cheung CY. Ikram MK. Sabanayagam C. Wong TY. Retinal microvasculature as a model to study the manifestations of hypertension. Hypertension. 2012; 60:1094–103.

4. Price SA. Gorelik A. Fourlanos S, et al. Obesity is associated with retinopathy and macrovascular disease in type 1 diabetes. Obes Res Clin Pract. 2014; 8:e178–82.

5. Mottl AK. Pajewski N. Fonseca V, et al. The degree of retinopathy is equally predictive for renal and macrovascular outcomes in the ACCORD Trial. J Diabetes Complications. 2014; 28:874–9.

6. Venkatesh P. Tibrewal S. Bhowmik D, et al. Prevalence of systemic co-morbidities in patients with various grades of diabetic retinopathy. Indian J Med Res. 2014; 140:77–83.

7. Henis O. Shahar Y. Steinvil A, et al. Erectile dysfunction is associated with severe retinopathy in diabetic men. Urology. 2011; 77:1133–6.

8. Juutilainen A. Lehto S. Rönnemaa T, et al. Retinopathy predicts cardiovascular mortality in type 2 diabetic men and women. Diabetes Care. 2007; 30:292–9.

9. Gimeno-Orna JA. Faure-Nogueras E. Castro-Alonso FJ. Boned-Juliani B. Ability of retinopathy to predict cardiovascular disease in patients with type 2 diabetes mellitus. Am J Cardiol. 2009; 103:1364–7.

10. Pálsson R. Patel UD. Cardiovascular complications of diabetic kidney disease. Adv Chronic Kidney Dis. 2014; 21:273–80.

11. De Cosmo S. Rossi MC. Pellegrini F, et al. Kidney dysfunction and related cardiovascular risk factors among patients with type 2 diabetes. Nephrol Dial Transplant. 2014; 29:657–62.

12. Wang Y. Katzmarzyk PT. Horswell R, et al. Kidney function and the risk of cardiovascular disease in patients with type 2 diabetes. Kidney Int. 2014; 85:1192–9.

13. Kim JJ. Hwang BH. Choi IJ, et al. A prospective two-center study on the associations between microalbuminuria, coronary atherosclerosis and long-term clinical outcome in asymptomatic patients with type 2 diabetes mellitus: evaluation by coronary CT angiography. Int J Cardiovasc Imaging. 2015; 31:193–203.

14. Kanjilal S. Rao VS. Mukherjee M, et al. Application of cardiovascular disease risk prediction models and the relevance of novel biomarkers to risk stratification in Asian Indians. Vasc Health Risk Manag. 2008; 4:199–211.

15. Setayeshgar S. Whiting SJ. Pahwa P. Vatanparast H. Predicted 10-year risk of cardiovascular disease among Canadian adults using modified Framingham Risk Score in association with dietary intake. Appl Physiol Nutr Metab. 2015; 40:1068–74.

16. Jones CA. Ross L. Surani N, et al. Framingham ten-year general cardiovascular disease risk: agreement between BMI-based and cholesterol-based estimates in a South Asian convenience sample. PLoS One. 2015; 10:e0119183.

17. Selvarajah S. Kaur G. Haniff J, et al. Comparison of the Framingham Risk Score, SCORE and WHO/ISH cardiovascular risk prediction models in an Asian population. Int J Cardiol. 2014; 176:211–8.

18. Artigao-Rodenas LM. Carbayo-Herencia JA. Divisón-Garrote JA, et al. Framingham risk score for prediction of cardiovascular diseases: a population-based study from southern Europe. PLoS One. 2013; 8:e73529.

19. Jee D. Lee WK. Kang S. Prevalence and risk factors for diabetic retinopathy: the Korea National Health and Nutrition Examination Survey 2008-2011. Invest Ophthalmol Vis Sci. 2013; 54:6827–33.

20. Keenan TD. Johnston RL. Donachie PH, et al. United Kingdom National Ophthalmology Database Study: Diabetic Retinopathy; Report 1: prevalence of centre-involving diabetic macular oedema and other grades of maculopathy and retinopathy in hospital eye services. Eye (Lond). 2013; 27:1397–404.

21. D’Agostino RB Sr. Vasan RS. Pencina MJ, et al. General cardiovascular risk profile for use in primary care: the Framingham Heart Study. Circulation. 2008; 117:743–53.

22. Valmadrid CT. Klein R. Moss SE. Klein BE. The risk of cardiovascular disease mortality associated with microalbuminuria and gross proteinuria in persons with older-onset diabetes mellitus. Arch Intern Med. 2000; 160:1093–100.

23. Srinath Reddy K. Shah B. Varghese C. Ramadoss A. Responding to the threat of chronic diseases in India. Lancet. 2005; 366:1744–9.

24. Yusuf S. Reddy S. Ounpuu S. Anand S. Global burden of cardiovascular diseases: part I: general considerations, the epidemiologic transition, risk factors, and impact of urbanization. Circulation. 2001; 104:2746–53.

25. Grundy SM. Benjamin IJ. Burke GL, et al. Diabetes and cardiovascular disease: a statement for healthcare professionals from the American Heart Association. Circulation. 1999; 100:1134–46.

26. Selvin E. Marinopoulos S. Berkenblit G, et al. Meta-analysis: glycosylated hemoglobin and cardiovascular disease in diabetes mellitus. Ann Intern Med. 2004; 141:421–31.

27. Xu T. Liu W. Cai X, et al. Risk of coronary heart disease in different criterion of impaired fasting glucose: a meta-analysis. Medicine (Baltimore). 2015; 94:e1740.

28. Bansal D. Nayakallu RS. Gudala K, et al. Agreement between Framingham risk score and United Kingdom Prospective Diabetes Study risk engine in identifying high coronary heart disease risk in North Indian population. Diabetes Metab J. 2015; 39:321–7.

29. de la Hera JM. García-Ruiz JM. Delgado E. Diabetes and screening for coronary heart disease: where should we focus our efforts? Rev Esp Cardiol (Engl Ed). 2015; 68:830–3.

30. Cheung N. Wang JJ. Klein R, et al. Diabetic retinopathy and the risk of coronary heart disease: the Atherosclerosis Risk in Communities Study. Diabetes Care. 2007; 30:1742–6.

31. Klein R. Klein BE. Moss SE. Cruickshanks KJ. Association of ocular disease and mortality in a diabetic population. Arch Ophthalmol. 1999; 117:1487–95.

32. Miettinen H. Haffner SM. Lehto S, et al. Retinopathy predicts coronary heart disease events in NIDDM patients. Diabetes Care. 1996; 19:1445–8.

33. Hiller R. Sperduto RD. Podgor MJ, et al. Diabetic retinopathy and cardiovascular disease in type II diabetics. The Framingham Heart Study and the Framingham Eye Study. Am J Epidemiol. 1988; 128:402–9.

34. Takeda Y. Sakata Y. Mano T, et al. Diabetic retinopathy is associated with impaired left ventricular relaxation. J Card Fail. 2011; 17:556–60.

35. Grunwald JE. Alexander J. Ying GS, et al. Retinopathy and chronic kidney disease in the Chronic Renal Insufficiency Cohort (CRIC) study. Arch Ophthalmol. 2012; 130:1136–44.

36. Reaven PD. Emanuele N. Moritz T, et al. Proliferative diabetic retinopathy in type 2 diabetes is related to coronary artery calcium in the Veterans Affairs Diabetes Trial (VADT). Diabetes Care. 2008; 31:952–7.

37. Parvanova A. Iliev I. Filipponi M, et al. Insulin resistance and proliferative retinopathy: a cross-sectional, case-control study in 115 patients with type 2 diabetes. J Clin Endocrinol Metab. 2004; 89:4371–6.

38. Moreno PR. Fuster V. New aspects in the pathogenesis of diabetic atherothrombosis. J Am Coll Cardiol. 2004; 44:2293–300.

39. Spranger J. Pfeiffer AF. New concepts in pathogenesis and treatment of diabetic retinopathy. Exp Clin Endocrinol Diabetes. 2001; 109:2. S438–50.

40. Feener EP. King GL. Vascular dysfunction in diabetes mellitus. Lancet. 1997; 350:1. SI9–13.

41. Liu Y. Teng X. Zhang W, et al. Association between diabetic retinopathy and subclinical atherosclerosis in China: results from a community-based study. Diab Vasc Dis Res. 2015; 12:366–72.

42. Becker A. van Hinsbergh VW. Jager A, et al. Why is soluble intercellular adhesion molecule-1 related to cardiovascular mortality? Eur J Clin Invest. 2002; 32:1–8.

43. Jager A. van Hinsbergh VW. Kostense PJ, et al. Increased levels of soluble vascular cell adhesion molecule 1 are associated with risk of cardiovascular mortality in type 2 diabetes: the Hoorn study. Diabetes. 2000; 49:485–91.

44. Matsumoto K. Sera Y. Ueki Y, et al. Comparison of serum concentrations of soluble adhesion molecules in diabetic microangiopathy and macroangiopathy. Diabet Med. 2002; 19:822–6.

45. McLeod DS. Lefer DJ. Merges C. Lutty GA. Enhanced expression of intracellular adhesion molecule-1 and P-selectin in the diabetic human retina and choroid. Am J Pathol. 1995; 147:642–53.