Journal List > J Korean Ophthalmol Soc > v.57(2) > 1010507

Lee, Jee, and Epidemiology Survey Committee of the Korean Ophthalmology Society: Association between Grapes Intake and Diabetic Retinopathy: Inhibitory Effect of Resveratol on Diabetic Retinopathy

Abstract

Purpose

To evaluate the association between grape intake and diabetic retinopathy.

Methods

A population-based cross-sectional study using a nation-wide, stratified, multistage, clustered sampling method included 1,555 subjects aged ≥30 years who participated in the Korean National Health and Nutritional Examination Survey 2008-2011. All participants performed standardized interviews, food frequency questionnaires (FFQ), and comprehensive ophthalmic examinations. Grape intake was evaluated by an FFQ using 10 intervals of average frequency of grape intake during the past year. Diabetic retinopathy (DR) was evaluated by 7 standard retinal fundus photographs after pharmacological pupil dilatation. DR was classified as any DR, proliferative DR, or vision-threatening DR by the modified Air House classification system.

Results

The prevalence of diabetes was 16.9 ± 1.2%. As the grape intake frequency increases in FFQ, the odds ratio (OR) for any DR, proliferative DR, and vision-threatening DR were 0.86 (95% confidence interval [CI], 0.75-0.98), 0.65 (95% CI, 0.48-0.88), and 0.77 (95% CI, 0.60-0.99) respectively. Compared to the group with a grape intake of less than once per month, the OR for any DR, proliferative DR, and vision-threatening DR in the group with a grape intake of more than 2-3 times per month were 0.54 (95% CI 0.33-0.89), 0.25 (95% CI 0.07-0.81), 0.36 (95% CI 0.13-0.95), respectively.

Conclusions

The intake of grapes was inversely associated with the prevalence of DR.

REFERENCES

1). Klein BE. Overview of epidemiologic studies of diabetic retinopathy. Ophthalmic epidemiol. 2007; 14:179–83.
2). Aiello LP, Gardner TW, King GL, et al. Diabetic retinopathy. Diabetes Care. 1998; 21:143–56.
crossref
3). Brown MM, Brown GC, Sharma S, Shah G. Utility values and diabetic retinopathy. Am J Ophthalmol. 1999; 128:324–30.
crossref
4). Wong TY, Klein R, Islam FM, et al. Diabetic retinopathy in a multi-ethnic cohort in the United States. Am J Ophthalmol. 2006; 141:446–55.
crossref
5). Williams R, Airey M, Baxter H, et al. Epidemiology of diabetic retinopathy and macular oedema: a systematic review. Eye (Lond). 2004; 18:963–83.
crossref
6). Kempen JH, O'Colmain B, Leske MC, et al. The prevalence of diabetic retinopathy among adults in the United States. Arch Ophthalmol. 2004; 122:552–63.
crossref
7). Yau JW, Rogers SL, Kawasaki R, et al. Global prevalence and major risk factors of diabetic retinopathy. Diabetes Care. 2012; 35:556–64.
crossref
8). 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.
crossref
9). Jee D, Kim EC. Inverse association between high blood 25-hydroxyvitamin D levels and diabetic retinopathy in a representative Korean population. PLoS One. 2014; 9:e115199.
crossref
10). Ghadiri Soufi F, Arbabi-Aval E, Rezaei Kanavi M, Ahmadieh H. Anti-inflammatory properties of resveratrol in the retinas of type 2 diabetic rats. Clin Exp Pharmacol Physiol. 2015; 42:63–8.
crossref
11). Losso JN, Truax RE, Richard G. Trans-resveratrol inhibits hyperglycemia-induced inflammation and connexin downregulation in retinal pigment epithelial cells. J Agric Food Chem. 2010; 58:8246–52.
crossref
12). Kim YH, Kim YS, Roh GS, et al. Resveratrol blocks diabetes-induced early vascular lesions and vascular endothelial growth factor induction in mouse retinas. Acta Ophthalmol. 2012; 90:e31–7.
crossref
13). Yar AS, Menevse S, Dogan I, et al. Investigation of ocular neo-vascularization-related genes and oxidative stress in diabetic rat eye tissues after resveratrol treatment. J Med Food. 2012; 15:391–8.
crossref
14). Soufi FG, Mohammad-Nejad D, Ahmadieh H. Resveratrol improves diabetic retinopathy possibly through oxidative stress - nuclear factor kB - apoptosis pathway. Pharmacol Rep. 2012; 64:1505–14.
15). Rokicki D, Zdanowski R, Lewicki S, et al. Inhibition of proliferation, migration and invasiveness of endothelial murine cells culture induced by resveratrol. Cent Eur J Immunol. 2014; 39:449–54.
16). Liu XQ, Wu BJ, Pan WH, et al. Resveratrol mitigates rat retinal ischemic injury: the roles of matrix metalloproteinase-9, inducible nitric oxide, and heme oxygenase-1. J Ocul Pharmacol Ther. 2013; 29:33–40.
crossref
17). Bola C, Bartlett H, Eperjesi F. Resveratrol and the eye: activity and molecular mechanisms. Graefes Arch Clin Exp Ophthalmol. 2014; 252:699–713.
crossref
18). Semba RD, Ferrucci L, Bartali B, et al. Resveratrol levels and all-cause mortality in older community-dwelling adults. JAMA Intern Med. 2014; 174:1077–84.
crossref
19). Park HA. The Korea national health and nutrition examination survey as a primary data source. Korean J Fam Med. 2013; 34:79.
crossref
20). Kim Y, Park S, Kim NS, Lee BK. Inappropriate survey design analysis of the Korean National Health and Nutrition Examination Survey may produce biased results. J Prev Med Public Health. 2013; 46:96–104.
crossref
21). Rim HT, Park SY, Yoon JS. Hormone replacement therapy and eye diseases: KNHANES IV. J Korean Ophthalmol Soc. 2012; 53:1445–50.
crossref
22). Lim HT, Choi KS. Factors associated with screening for diabetic retinopathy in diabetic patients aged > or = 40 years using the KNHANES IV. J Korean Ophthalmol Soc. 2012; 53:516–21.
23). Diabetic retinopathy study. Report Number 6. Design, methods, and baseline results. Report Number 7. A modification of the Airlie House classification of diabetic retinopathy. Prepared by the Diabetic Retinopathy. Invest Ophthalmol Vis Sci. 1981; 21((1 Pt 2)):1–226.
24). Willett WC, Sampson L, Stampfer MJ, et al. Reproducibility and validity of a semiquantitative food frequency questionnaire. Am J Epidemiol. 1985; 122:51–65.
crossref
25). Kim SJ, Choi MK. Factors Associated with Fruit and Vegetable Consumption of Subjects Having a History of Stroke: Using 5th Korea National Health and Nutrition Examination Survey (2010, 2011). J Comm Nutr. 2014; 19:468–78.
crossref
26). Scanlon PH, Aldington SJ, Stratton IM. Epidemiological issues in diabetic retinopathy. Middle East Afr J Ophthalmol. 2013; 20:293–300.
crossref
27). Marmot MG, Rose G, Shipley MJ, Thomas BJ. Alcohol and mortality: a U-shaped curve. Lancet. 1981; 1((8220 Pt 1)):580–3.
crossref
28). Shaper AG, Wannamethee G, Walker M. Alcohol and mortality in British men: explaining the U-shaped curve. Lancet. 1988; 2:1267–73.
crossref
29). Biagi M, Bertelli AA. Wine, alcohol and pills: What future for the French paradox? Life Sci. 2015; 131:19–22.
crossref
30). Wollin SD, Jones PJ. Alcohol, red wine and cardiovascular disease. J Nutr. 2001; 131:1401–4.
crossref
31). Guerrero RF, Garcia-Parrilla MC, Puertas B, Cantos-Villar E. Wine, resveratrol and health: a review. Nat Prod Commun. 2009; 4:635–58.
crossref
32). Pendurthi UR, Williams JT, Rao LV. Resveratrol, a polyphenolic compound found in wine, inhibits tissue factor expression in vascular cells: a possible mechanism for the cardiovascular benefits associated with moderate consumption of wine. Arterioscler Thromb Vasc Biol. 1999; 19:419–26.
33). Stervbo U, Vang O, Bonnesen C. A review of the content of the putative chemopreventive phytoalexin resveratrol in red wine. Food Chemistry. 2007; 101:449–57.
crossref
34). Romero-Pérez AI, Lamuela-Raventós RM, Andrés-Lacueva C, de la Torre-Boronat MC. Method for the quantitative extraction of resveratrol and piceid isomers in grape berry skins. Effect of powdery mildew on the stilbene content. J Agric Food Chem. 2001; 49:210–5.
crossref
35). Press SJ, Wilson S. Choosing between logistic regression and discriminant analysis. J Amer Statist Assoc. 1978; 73:699–705.
crossref

Figure 1.
Flow diagram presenting the selection of study participants. KNHANES = Korea National Health and Nutritional Examination Survey.
jkos-57-276f1.tif
Table 1.
Demographic and clinical characteristics, according to DR status, as reported in the Korean National Health and Nutrition Examination Survey 2008-2011
Characteristic Without DR (n = 1,286) With DR (n = 269) Total (n = 1,555) p-value
Sex (male, %) 55.7 (1.5) 52.1 (3.6) 55.1 (1.4) 0.361
Age (years) 57.1 (0.4) 59.5 (0.9) 58.3 (0.5) 0.015*
BMI (kg/m2) 25.2 (0.1) 24.2 (0.1) 24.7 (0.1) <0.001*
Hypertension (%) 57.9 (1.7) 54.4 (3.3) 57.3 (1.5) 0.648
Fasting glucose (mg/dL) 140.6 (1.4) 160.8 (3.6) 150.7 (1.9) <0.001*
HbA1c (%) 7.2 (0.1) 8.1 (0.1) 7.6 (0.1) <0.001*
Diabetes duration (years) 6.9 (0.2) 11.0 (0.5) 9.0 (0.3) <0.001*

Data are expressed as weighted means or weighted frequency (%) with standard errors.

DR = diabetic retinopathy; BMI = body mass index.

* Data were compared by Student's t-test, p < 0.05.

Table 2.
Prevalence of DR according to the frequency of grape intake in a representative Korean population
Grape intake DR
Prevalence 95% confidence interval N (unweighted)
0: never 23.5 (3.2) 17.8-30.4 67/314
1: 1-11 times/year 18.9 (3.0) 13.6-25.6 55/285
2: 1 time/month 17.6 (2.6) 13.0-23.4 60/345
3: 2-3 times/month 2.5 (1.8) 9.3-16.5 54/405
4: 1-2 times/week 14.3 (3.6) 8.5-22.9 20/112
5: 3-4 times/week 11.3 (4.1) 5.4-22.0 10/86
6: 5-6 times/week 32.0 (20.6) 6.8-75.1 3/6
7: 1 time/day 0 (0) 0 0/2
8: 2 times/day 0 0 0
9: 3 times/day 0 0 0

Data are expressed as weighted frequency (%) with standard errors.

DR = diabetic retinopathy.

Table 3.
Multiple logistic regression analysis between intake of grapes (continuous variable) and any DR, PDR, and VTDR in a representative Korean population
Characteristics Grapes intake levels by FFQ as continuous variable
Odds ratio 95% confidence interval p-value
Any DR
  Model 1 0.83 0.74-0.93 0.002*
  Model 2 0.84 0.74-0.95 0.005*
  Model 3 0.86 0.75-0.98 0.024*
PDR
  Model 1 0.61 0.45-0.82 0.001*
  Model 2 0.69 0.52-0.92 0.013*
  Model 3 0.65 0.48-0.88 0.006*
VTDR
  Model 1 0.69 0.56-0.85 0.001*
  Model 2 0.77 0.63-0.95 0.018*
  Model 3 0.77 0.60-0.99 0.041*

Odds ratio were expressed with 95% confidence intervals. Model 1: Crude, Model 2: adjusted for sex and age, Model 3: adjusted for sex, age, hypertension, fasting glucose level, Hemoglobin A1c, body mass index and diabetes duration.

DR = diabetic retinopathy; PDR = proliferative diabetic retinopathy; VTDR = vision threatening diabetic retinopathy; FFQ = food frequency questionnaires.

* p < 0.05.

Table 4.
Multiple logistic regression analysis between the quartile intake of grapes and any DR, PDR, and VTDR in a representative Korean population
Characteristics Quartile grapes intake levels
Quartile 1 (<1/month) Quartile 2 (1/month) Quartile 3 (2-3 times/month) Quartile 4 (≥ 1/week) P for trend
Any DR
  Prevalence 21.0 (2.2) 17.3 (2.6) 12.6 (1.8) 13.2 (2.7) 0.017*
  Model 1 Reference 0.78 (0.50-1.21) 0.54 (0.35-0.82)* 0.57 (0.33-0.96)* 0.020*
  Model 2 Reference 0.79 (0.51-1.23) 0.55 (0.36-0.86)* 0.58 (0.34-0.99)* 0.042*
  Model 3 Reference 0.82 (0.50-1.35) 0.54 (0.33-0.89)* 0.65 (0.39-1.10) 0.065
PDR
  Prevalence 0.7 (0.2) 0.3 (0.1) 0.1 (0.1) 0.2 (0.1) 0.001*
  Model 1 Reference 0.33 (0.13-0.84) 0.18 (0.07-0.46)* 0.30 (0.10-0.87)* 0.001*
  Model 2 Reference 0.42 (0.16-1.06) 0.24 (0.09-0.62)* 0.42 (0.14-1.29)* 0.017*
  Model 3 Reference 0.64 (0.23-1.78) 0.25 (0.07-0.81)* 0.22 (0.05-0.87)* 0.042*
VTDR
  Prevalence 1.1 (1.7) 0.4 (0.1) 0.4 (0.1) 0.4 (0.2) 0.001*
  Model 1 Reference 0.37 (0.17-0.80) 0.32 (0.16-0.62)* 0.35 (0.15-0.83)* 0.003*
  Model 2 Reference 0.46 (0.21-0.99) 0.41 (0.21-0.81)* 0.50 (0.21-1.22) 0.049*
  Model 3 Reference 0.62 (0.26-1.45) 0.36 (0.13-0.95)* 0.50 (0.16-1.54) 0.093

Prevalence was expressed with standard error, and odds ratio were expressed with 95% confidence intervals. Model 1: Crude, Model 2: adjusted for sex and age, Model 3: adjusted for sex, age, hypertension, fasting glucose level, Hemoglobin A1c, body mass index, and diabetes duration. DR = diabetic retinopathy; PDR = proliferative diabetic retinopathy; VTDR = vision threatening diabetic retinopathy.

* p < 0.05.

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