Diabetes Metab J.  2016 Dec;40(6):482-493. 10.4093/dmj.2016.40.6.482.

Clinical Course and Risk Factors of Diabetic Retinopathy in Patients with Type 2 Diabetes Mellitus in Korea

Affiliations
  • 1Division of Endocrinology and Metabolism, Department of Internal Medicine, St. Vincent's Hospital, College of Medicine, The Catholic University of Korea, Suwon, Korea. kosh@catholic.ac.kr
  • 2Division of Endocrinology and Metabolism, Department of Internal Medicine, Yeouido St. Mary's Hospital, College of Medicine, The Catholic University of Korea, Seoul, Korea.
  • 3Department of Ophthalmology, St. Vincent's Hospital, College of Medicine, The Catholic University of Korea, Suwon, Korea.
  • 4Epidemiology Branch, National Institute of Environmental Health Sciences, National Institutes of Health, U.S. Department of Health and Human Services, Research Triangle Park, NC, USA.

Abstract

BACKGROUND
We investigated clinical course and risk factors for diabetic retinopathy (DR) in patients with type 2 diabetes mellitus (T2DM).
METHODS
A total of 759 patients with T2DM without DR were included from January 2001 to December 2004. Retinopathy evaluation was performed at least annually by ophthalmologists. The severity of the DR was classified into five categories according to the International Clinical Diabetic Retinopathy Severity Scales.
RESULTS
Of the 759 patients, 523 patients (68.9%) completed the follow-up evaluation. During the follow-up period, 235 patients (44.9%) developed DR, and 32 patients (13.6%) progressed to severe nonproliferative DR (NPDR) or proliferative DR (PDR). The mean duration of diabetes at the first diagnosis of mild NPDR, moderate NPDR, and severe NPDR or PDR were 14.8, 16.7, and 17.3 years, respectively. After adjusting multiple confounding factors, the significant risk factors for the incidence of DR risk in patients with T2DM were old age, longer duration of diabetes, higher mean glycosylated hemoglobin (HbA1c), and albuminuria. Even in the patients who had been diagnosed with diabetes for longer than 10 years at baseline, a decrease in HbA1c led to a significant reduction in the risk of developing DR (hazard ratio, 0.73 per 1% HbA1c decrement; 95% confidence interval, 0.58 to 0.91; P=0.005).
CONCLUSION
This prospective cohort study demonstrates that glycemic control, diabetes duration, age, and albuminuria are important risk factors for the development of DR. More aggressive retinal screening for T2DM patients diagnosed with DR should be required in order to not miss rapid progression of DR.

Keyword

Diabetes mellitus, type 2; Diabetic retinopathy; Risk factors

MeSH Terms

Albuminuria
Cohort Studies
Diabetes Mellitus, Type 2*
Diabetic Retinopathy*
Diagnosis
Follow-Up Studies
Hemoglobin A, Glycosylated
Humans
Incidence
Korea*
Mass Screening
Prospective Studies
Retinaldehyde
Risk Factors*
Weights and Measures
Retinaldehyde

Figure

  • Fig. 1 Clinical course of diabetic retinopathy in this cohort. PRP, panretinal photocoagulation; DR, diabetic retinopathy; NPDR, nonproliferative diabetic retinopathy; IR, incidence rate; PDR, proliferative.

  • Fig. 2 Cumulative incidence for diabetic retinopathy according to the (A) mean glycosylated hemoglobin (HbA1c), (B) mean low density lipoprotein cholesterol (LDL-C) level, and (C) duration of diabetes.


Cited by  3 articles

Relationship between Clinical Features of Diabetic Retinopathy and Systemic Factors in Patients with Newly Diagnosed Type II Diabetes Mellitus
Hyeseong Hwang, Jin Young Kim, Tae Keun Oh, Ju Byung Chae, Dong Yoon Kim
J Korean Med Sci. 2020;35(23):e179.    doi: 10.3346/jkms.2020.35.e179.

Past and Current Status of Adult Type 2 Diabetes Mellitus Management in Korea: A National Health Insurance Service Database Analysis
Seung-Hyun Ko, Kyungdo Han, Yong-ho Lee, Junghyun Noh, Cheol-Young Park, Dae-Jung Kim, Chang Hee Jung, Ki-Up Lee, Kyung-Soo Ko,
Diabetes Metab J. 2018;42(2):93-100.    doi: 10.4093/dmj.2018.42.2.93.

Glycemic Control and Retinal Microvascular Changes in Type 2 Diabetes Mellitus Patients without Clinical Retinopathy
Kangmin Lee, Ga Hye Lee, Seung Eun Lee, Jee Myung Yang, Kunho Bae
Diabetes Metab J. 2024;48(5):983-992.    doi: 10.4093/dmj.2023.0149.


Reference

1. Cheung N, Mitchell P, Wong TY. Diabetic retinopathy. Lancet. 2010; 376:124–136.
2. Yau JW, Rogers SL, Kawasaki R, Lamoureux EL, Kowalski JW, Bek T, Chen SJ, Dekker JM, Fletcher A, Grauslund J, Haffner S, Hamman RF, Ikram MK, Kayama T, Klein BE, Klein R, Krishnaiah S, Mayurasakorn K, O'Hare JP, Orchard TJ, Porta M, Rema M, Roy MS, Sharma T, Shaw J, Taylor H, Tielsch JM, Varma R, Wang JJ, Wang N, West S, Xu L, Yasuda M, Zhang X, Mitchell P, Wong TY. Meta-Analysis for Eye Disease (META-EYE) Study Group. Global prevalence and major risk factors of diabetic retinopathy. Diabetes Care. 2012; 35:556–564.
3. Park YM, Ko SH, Lee JM, Kim DJ, Kim DJ, Han K, Bower JK, Ahn YB. Committee of Clinical Practice Guideline, Korean Diabetes Association. Glycaemic and haemoglobin A1c thresholds for detecting diabetic retinopathy: the fifth Korea National Health and Nutrition Examination Survey (2011). Diabetes Res Clin Pract. 2014; 104:435–442.
4. Lee R, Wong TY, Sabanayagam C. Epidemiology of diabetic retinopathy, diabetic macular edema and related vision loss. Eye Vis (Lond). 2015; 2:17.
5. Cheung N, Wong TY. Diabetic retinopathy and systemic vascular complications. Prog Retin Eye Res. 2008; 27:161–176.
6. American Diabetes Association. Standards of medical care in diabetes: 2016. Diabetes Care. 2016; 39:Suppl 1. S1–S106.
7. Korean Diabetes Association. Treatment guideline for diabetes. 5th ed. Seoul: Gold' Planning and Development;2015.
8. Younis N, Broadbent DM, Vora JP, Harding SP. Liverpool Diabetic Eye Study. Incidence of sight-threatening retinopathy in patients with type 2 diabetes in the Liverpool Diabetic Eye Study: a cohort study. Lancet. 2003; 361:195–200.
9. Klein R, Klein BE, Moss SE, Davis MD, DeMets DL. The Wisconsin epidemiologic study of diabetic retinopathy. III. Prevalence and risk of diabetic retinopathy when age at diagnosis is 30 or more years. Arch Ophthalmol. 1984; 102:527–532.
10. The Diabetes Control and Complications Trial Research Group. The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. N Engl J Med. 1993; 329:977–986.
11. Stratton IM, Kohner EM, Aldington SJ, Turner RC, Holman RR, Manley SE, Matthews DR. UKPDS 50: risk factors for incidence and progression of retinopathy in type II diabetes over 6 years from diagnosis. Diabetologia. 2001; 44:156–163.
12. ACCORD Study Group. ACCORD Eye Study Group. Chew EY, Ambrosius WT, Davis MD, Danis RP, Gangaputra S, Greven CM, Hubbard L, Esser BA, Lovato JF, Perdue LH, Goff DC Jr, Cushman WC, Ginsberg HN, Elam MB, Genuth S, Gerstein HC, Schubart U, Fine LJ. Effects of medical therapies on retinopathy progression in type 2 diabetes. N Engl J Med. 2010; 363:233–244.
13. UK Prospective Diabetes Study Group. Tight blood pressure control and risk of macrovascular and microvascular complications in type 2 diabetes: UKPDS 38. BMJ. 1998; 317:703–713.
14. Keech AC, Mitchell P, Summanen PA, O'Day J, Davis TM, Moffitt MS, Taskinen MR, Simes RJ, Tse D, Williamson E, Merrifield A, Laatikainen LT, d'Emden MC, Crimet DC, O'Connell RL, Colman PG. FIELD study investigators. Effect of fenofibrate on the need for laser treatment for diabetic retinopathy (FIELD study): a randomised controlled trial. Lancet. 2007; 370:1687–1697.
15. Ismail-Beigi F, Craven T, Banerji MA, Basile J, Calles J, Cohen RM, Cuddihy R, Cushman WC, Genuth S, Grimm RH Jr, Hamilton BP, Hoogwerf B, Karl D, Katz L, Krikorian A, O'Connor P, Pop-Busui R, Schubart U, Simmons D, Taylor H, Thomas A, Weiss D, Hramiak I. ACCORD trial group. Effect of intensive treatment of hyperglycaemia on microvascular outcomes in type 2 diabetes: an analysis of the ACCORD randomised trial. Lancet. 2010; 376:419–430.
16. Klein BE, Klein R, Moss SE. Is serum cholesterol associated with progression of diabetic retinopathy or macular edema in persons with younger-onset diabetes of long duration? Am J Ophthalmol. 1999; 128:652–654.
17. Lloyd CE, Klein R, Maser RE, Kuller LH, Becker DJ, Orchard TJ. The progression of retinopathy over 2 years: the Pittsburgh Epidemiology of Diabetes Complications (EDC) Study. J Diabetes Complications. 1995; 9:140–148.
18. Funatsu H, Shimizu E, Noma H, Mimura T, Hori S. Association between serum lipoprotein (a) level and progression of non-proliferative diabetic retinopathy in type 2 diabetes. Acta Ophthalmol. 2009; 87:501–505.
19. Wong TY, Cheung N, Tay WT, Wang JJ, Aung T, Saw SM, Lim SC, Tai ES, Mitchell P. Prevalence and risk factors for diabetic retinopathy: the Singapore Malay Eye Study. Ophthalmology. 2008; 115:1869–1875.
20. Ko SH, Kwon HS, Kim DJ, Kim JH, Kim NH, Kim CS, Song KH, Won JC, Lim S, Choi SH, Han K, Park YM, Cha BY. Taskforce Team of Diabetes Fact Sheet of the Korean Diabetes Association. Higher prevalence and awareness, but lower control rate of hypertension in patients with diabetes than general population: the fifth Korean National Health and Nutrition Examination Survey in 2011. Diabetes Metab J. 2014; 38:51–57.
21. Levey AS, Bosch JP, Lewis JB, Greene T, Rogers N, Roth D. A more accurate method to estimate glomerular filtration rate from serum creatinine: a new prediction equation. Modification of Diet in Renal Disease Study Group. Ann Intern Med. 1999; 130:461–470.
22. Yun JS, Kim JH, Song KH, Ahn YB, Yoon KH, Yoo KD, Park YM, Ko SH. Cardiovascular autonomic dysfunction predicts severe hypoglycemia in patients with type 2 diabetes: a 10-year follow-up study. Diabetes Care. 2014; 37:235–241.
23. Yun JS, Ko SH, Ko SH, Song KH, Yoo KD, Yoon KH, Park YM, Ahn YB. Cardiovascular disease predicts severe hypoglycemia in patients with type 2 diabetes. Diabetes Metab J. 2015; 39:498–506.
24. Early Treatment Diabetic Retinopathy Study Research Group. Effects of aspirin treatment on diabetic retinopathy. ETDRS report number 8. Ophthalmology. 1991; 98:5 Suppl. 757–765.
25. Wilkinson CP, Ferris FL 3rd, Klein RE, Lee PP, Agardh CD, Davis M, Dills D, Kampik A, Pararajasegaram R, Verdaguer JT. Global Diabetic Retinopathy Project Group. Proposed international clinical diabetic retinopathy and diabetic macular edema disease severity scales. Ophthalmology. 2003; 110:1677–1682.
26. Grambsch PM, Therneau TM. Proportional hazards tests and diagnostics based on weighted residuals. Biometrika. 1994; 81:515–526.
27. ADVANCE Collaborative Group. Patel A, MacMahon S, Chalmers J, Neal B, Billot L, Woodward M, Marre M, Cooper M, Glasziou P, Grobbee D, Hamet P, Harrap S, Heller S, Liu L, Mancia G, Mogensen CE, Pan C, Poulter N, Rodgers A, Williams B, Bompoint S, de Galan BE, Joshi R, Travert F. Intensive blood glucose control and vascular outcomes in patients with type 2 diabetes. N Engl J Med. 2008; 358:2560–2572.
28. Azad N, Agrawal L, Emanuele NV, Klein R, Bahn GD, Reaven P. VADT Study Group. Association of blood glucose control and pancreatic reserve with diabetic retinopathy in the Veterans Affairs Diabetes Trial (VADT). Diabetologia. 2014; 57:1124–1131.
29. Kawasaki R, Tanaka S, Tanaka S, Abe S, Sone H, Yokote K, Ishibashi S, Katayama S, Ohashi Y, Akanuma Y, Yamada N, Yamashita H. Japan Diabetes Complications Study Group. Risk of cardiovascular diseases is increased even with mild diabetic retinopathy: the Japan Diabetes Complications Study. Ophthalmology. 2013; 120:574–582.
30. Luk AO, Ma RC, Lau ES, Yang X, Lau WW, Yu LW, Chow FC, Chan JC, So WY. Risk association of HbA1c variability with chronic kidney disease and cardiovascular disease in type 2 diabetes: prospective analysis of the Hong Kong Diabetes Registry. Diabetes Metab Res Rev. 2013; 29:384–390.
31. Penno G, Solini A, Bonora E, Fondelli C, Orsi E, Zerbini G, Morano S, Cavalot F, Lamacchia O, Laviola L, Nicolucci A, Pugliese G. Renal Insufficiency And Cardiovascular Events Study Group. HbA1c variability as an independent correlate of nephropathy, but not retinopathy, in patients with type 2 diabetes: the Renal Insufficiency And Cardiovascular Events (RIACE) Italian multicenter study. Diabetes Care. 2013; 36:2301–2310.
32. Hirakawa Y, Arima H, Zoungas S, Ninomiya T, Cooper M, Hamet P, Mancia G, Poulter N, Harrap S, Woodward M, Chalmers J. Impact of visit-to-visit glycemic variability on the risks of macrovascular and microvascular events and all-cause mortality in type 2 diabetes: the ADVANCE trial. Diabetes Care. 2014; 37:2359–2365.
33. Gorst C, Kwok CS, Aslam S, Buchan I, Kontopantelis E, Myint PK, Heatlie G, Loke Y, Rutter MK, Mamas MA. Long-term glycemic variability and risk of adverse outcomes: a systematic review and meta-analysis. Diabetes Care. 2015; 38:2354–2369.
34. Rema M, Srivastava BK, Anitha B, Deepa R, Mohan V. Association of serum lipids with diabetic retinopathy in urban South Indians: the Chennai Urban Rural Epidemiology Study (CURES) Eye Study 2. Diabet Med. 2006; 23:1029–1036.
35. Klein R, Sharrett AR, Klein BE, Moss SE, Folsom AR, Wong TY, Brancati FL, Hubbard LD, Couper D. ARIC Group. The association of atherosclerosis, vascular risk factors, and retinopathy in adults with diabetes: the atherosclerosis risk in communities study. Ophthalmology. 2002; 109:1225–1234.
36. Tapp RJ, Shaw JE, Harper CA, de Courten MP, Balkau B, McCarty DJ, Taylor HR, Welborn TA, Zimmet PZ. AusDiab Study Group. The prevalence of and factors associated with diabetic retinopathy in the Australian population. Diabetes Care. 2003; 26:1731–1737.
37. Klein BE, Moss SE, Klein R, Surawicz TS. The Wisconsin Epidemiologic Study of Diabetic Retinopathy. XIII. Relationship of serum cholesterol to retinopathy and hard exudate. Ophthalmology. 1991; 98:1261–1265.
38. Yun JS, Ko SH, Kim JH, Moon KW, Park YM, Yoo KD, Ahn YB. Diabetic retinopathy and endothelial dysfunction in patients with type 2 diabetes mellitus. Diabetes Metab J. 2013; 37:262–269.
39. Wong TY, Klein R, Islam FM, Cotch MF, Folsom AR, Klein BE, Sharrett AR, Shea S. Diabetic retinopathy in a multi-ethnic cohort in the United States. Am J Ophthalmol. 2006; 141:446–455.
40. Gaede P, Vedel P, Parving HH, Pedersen O. Intensified multifactorial intervention in patients with type 2 diabetes mellitus and microalbuminuria: the Steno type 2 randomised study. Lancet. 1999; 353:617–622.
41. Colhoun HM, Betteridge DJ, Durrington PN, Hitman GA, Neil HA, Livingstone SJ, Thomason MJ, Mackness MI, Charlton-Menys V, Fuller JH. CARDS investigators. Primary prevention of cardiovascular disease with atorvastatin in type 2 diabetes in the Collaborative Atorvastatin Diabetes Study (CARDS): multicentre randomised placebo-controlled trial. Lancet. 2004; 364:685–696.
42. Salinero-Fort MA, San Andres-Rebollo FJ, de Burgos-Lunar C, Arrieta-Blanco FJ, Gomez-Campelo P. MADIABETES Group. Four-year incidence of diabetic retinopathy in a Spanish cohort: the MADIABETES study. PLoS One. 2013; 8:e76417.
43. Bergerhoff K, Clar C, Richter B. Aspirin in diabetic retinopathy: a systematic review. Endocrinol Metab Clin North Am. 2002; 31:779–793.
44. Tung TH, Chen SJ, Shih HC, Chou P, Li AF, Shyong MP, Lee FL, Liu JH. Assessing the natural course of diabetic retinopathy: a population-based study in Kinmen, Taiwan. Ophthalmic Epidemiol. 2006; 13:327–333.
45. Gong Q, Gregg EW, Wang J, An Y, Zhang P, Yang W, Li H, Li H, Jiang Y, Shuai Y, Zhang B, Zhang J, Gerzoff RB, Roglic G, Hu Y, Li G, Bennett PH. Long-term effects of a randomised trial of a 6-year lifestyle intervention in impaired glucose tolerance on diabetes-related microvascular complications: the China Da Qing Diabetes Prevention Outcome Study. Diabetologia. 2011; 54:300–307.
Full Text Links
  • DMJ
Actions
Cited
CITED
export Copy
Close
Share
  • Twitter
  • Facebook
Similar articles
Copyright © 2024 by Korean Association of Medical Journal Editors. All rights reserved.     E-mail: koreamed@kamje.or.kr