Abstract
Purpose
The purpose of this study was to investigate the relationship between dietary flavonoids intake and metabolic syndrome (MetS) in Korean women with polycystic ovary syndrome (PCOS). Methods: A total of 223 subjects (mean age; 27.3 ± 4.2 yrs, range; 17–38 yrs) were divided into the MetS group (n = 27) and non-MetS group (n = 196). Dietary intake data were assessed by 24-hour recall method for two non-consecutive days and the average of the two days was used to estimate the usual dietary intake. Dietary habits were assessed using the Mini Dietary Assessment (MDA) score. We analyzed the intakes of six flavonoid classes (anthocyanidins, flavan-3-ols, flavanones, flavones, flavonols, and isoflavones) using a flavonoids database. Results: After adjustment for age, total energy intake, alcohol consumption, smoking, regular exercise, and oral contraceptive use, dietary flavonols intake was significantly lower in the MetS group (5.1 ± 2.4 mg/d) than in the non-MetS group (8.9 ± 2.8 mg/d) (p = 0.0472). Intakes of other flavonoids except for flavonols did not differ between the two groups. In MDA scores, significant differences were observed only for that related to daily consumption of fruit or fruit juice (p = 0.0180). A significant inverse relationship was observed between flavonols intake and the risk of MetS (4th vs. 1st quartile, OR = 0.11, 95% CI = 0.02–0.62, p for trend = 0.0131). Conclusion: These results suggest that higher intake of flavonols may be beneficial for MetS in PCOS women.
References
1. Azziz R, Woods KS, Reyna R, Key TJ, Knochenhauer ES, Yildiz BO. The prevalence and features of the polycystic ovary syndrome in an unselected population. J Clin Endocrinol Metab. 2004; 89(6):2745–2749.
2. Goodarzi MO, Dumesic DA, Chazenbalk G, Azziz R. Polycystic ovary syndrome: etiology, pathogenesis and diagnosis. Nat Rev Endocrinol. 2011; 7(4):219–231.
3. Boudreaux MY, Talbott EO, Kip KE, Brooks MM, Witchel SF. Risk of T2DM and impaired fasting glucose among PCOS subjects: results of an 8-year follow-up. Curr Diab Rep. 2006; 6(1):77–83.
4. Wild RA, Carmina E, Diamanti-Kandarakis E, Dokras A, Escobar-Morreale HF, Futterweit W, Lobo R, Norman RJ, Talbott E, Dumesic DA. Assessment of cardiovascular risk and prevention of cardiovascular disease in women with the polycystic ovary syndrome: a consensus statement by the Androgen Excess and Polycystic Ovary Syndrome (AE-PCOS) Society. J Clin Endocrinol Metab. 2010; 95(5):2038–2049.
5. Hahn S, Tan S, Sack S, Kimmig R, Quadbeck B, Mann K, Janssen OE. Prevalence of the metabolic syndrome in German women with polycystic ovary syndrome. Exp Clin Endocrinol Diabetes. 2007; 115(2):130–135.
6. Cussons AJ, Watts GF, Burke V, Shaw JE, Zimmet PZ, Stuckey BG. Cardiometabolic risk in polycystic ovary syndrome: a comparison of different approaches to defining the metabolic syndrome. Hum Reprod. 2008; 23(10):2352–2358.
7. Gambineri A, Repaci A, Patton L, Grassi I, Pocognoli P, Cognig-ni GE, Pasqui F, Pagotto U, Pasquali R. Prominent role of low HDL-cholesterol in explaining the high prevalence of the metabolic syndrome in polycystic ovary syndrome. Nutr Metab Cardiovasc Dis. 2009; 19(11):797–804.
8. Lee H, Oh JY, Hong Y, Sung YA, Chung H. Prevalence of metabolic syndrome in young Korean women with polycystic ovary syndrome. J Korean Diabetes Assoc. 2006; 30(4):285–291.
9. Kouki R, Schwab U, Hassinen M, Komulainen P, Heikkilä H, Lakka TA, Rauramaa R. Food consumption, nutrient intake and the risk of having metabolic syndrome: the DR's EXTRA Study. Eur J Clin Nutr. 2011; 65(3):368–377.
10. Martínez-González MÁ. Martín-Calvo N. The major European dietary patterns and metabolic syndrome. Rev Endocr Metab Disord. 2013; 14(3):265–271.
11. Almoosawi S, Tsang C, Ostertag LM, Fyfe L, Al-Dujaili EA. Differential effect of polyphenol-rich dark chocolate on biomarkers of glucose metabolism and cardiovascular risk factors in healthy, overweight and obese subjects: a randomized clinical trial. Food Funct. 2012; 3(10):1035–1043.
12. Barona J, Aristizabal JC, Blesso CN, Volek JS, Fernandez ML. Grape polyphenols reduce blood pressure and increase flow-mediated vasodilation in men with metabolic syndrome. J Nutr. 2012; 142(9):1626–1632.
13. Sohrab G, Hosseinpour-Niazi S, Hejazi J, Yuzbashian E, Mirmiran P, Azizi F. Dietary polyphenols and metabolic syndrome among Iranian adults. Int J Food Sci Nutr. 2013; 64(6):661–667.
14. Steffen Y, Gruber C, Schewe T, Sies H. Mono-O-methylated fla-vanols and other flavonoids as inhibitors of endothelial NADPH oxidase. Arch Biochem Biophys. 2008; 469(2):209–219.
15. Xiao ZP, Peng ZY, Peng MJ, Yan WB, Ouyang YZ, Zhu HL. Flavonoids health benefits and their molecular mechanism. Mini Rev Med Chem. 2011; 11(2):169–177.
16. Fauser BC, Tarlatzis BC, Rebar RW, Legro RS, Balen AH, Lobo R, Carmina E, Chang J, Yildiz BO, Laven JS, Boivin J, Petraglia F, Wijeyeratne CN, Norman RJ, Dunaif A, Franks S, Wild RA, Dumesic D, Barnhart K. Consensus on women's health aspects of polycystic ovary syndrome (PCOS): the Amsterdam ESHRE/AS-RM-Sponsored 3rd PCOS Consensus Workshop Group. Fertil Steril. 2012; 97(1):28–38.e25.
17. Korean Diabetes Association. Treatment guideline for diabetes. the. 4th edition.Seoul: Korean Diabetes Association;2011.
18. The Korean Nutrition Society. Nutritional assessment program ‘CAN-Pro 4.0' [CD-ROM]. Seoul: The Korean Nutrition Society;2011.
19. Yang YK, Kim JY, Kwon O. Development of flavonoid database for commonly consumed foods by Koreans. Korean J Nutr. 2012; 45(3):283–292.
20. Kim WY, Cho MS, Lee HS. Development and validation of mini dietary assessment index for Koreans. Korean J Nutr. 2003; 36(1):83–92.
21. Edwards RL, Lyon T, Litwin SE, Rabovsky A, Symons JD, Jalili T. Quercetin reduces blood pressure in hypertensive subjects. J Nutr. 2007; 137(11):2405–2411.
22. Jacques PF, Cassidy A, Rogers G, Peterson JJ, Meigs JB, Dwyer JT. Higher dietary flavonol intake is associated with lower incidence of type 2 diabetes. J Nutr. 2013; 143(9):1474–1480.
23. Holden JM, Bhagwat SA, Haytowitz DB, Gebhardt SE, Dwyer JT, Peterson J, Beecher GR, Eldridge AL, Balentine D. Development of a database of critically evaluated flavonoids data: application of USDA's data quality evaluation system. J Food Compost Anal. 2005; 18(8):829–844.
24. Erdman JW Jr, Balentine D, Arab L, Beecher G, Dwyer JT, Folts J, Harnly J, Hollman P, Keen CL, Mazza G, Messina M, Scalbert A, Vita J, Williamson G, Burrowes J. Flavonoids and heart health: proceedings of the ILSI North America Flavonoids Workshop, May 31-June 1, 2005, Washington, DC. J Nutr. 2007; 137(3 Suppl 1):718S–737S.
25. Kim JY, Kwon O. Culinary plants and their potential impact on metabolic overload. Ann N Y Acad Sci. 2011; 1229:133–139.
26. Galleano M, Calabro V, Prince PD, Litterio MC, Piotrkowski B, Vazquez-Prieto MA, Miatello RM, Oteiza PI, Fraga CG. Flavonoids and metabolic syndrome. Ann N Y Acad Sci. 2012; 1259:87–94.
27. van Dam RM, Naidoo N, Landberg R. Dietary flavonoids and the development of type 2 diabetes and cardiovascular diseases: review of recent findings. Curr Opin Lipidol. 2013; 24(1):25–33.
28. Siasos G, Tousoulis D, Tsigkou V, Kokkou E, Oikonomou E, Va-vuranakis M, Basdra EK, Papavassiliou AG, Stefanadis C. Flavonoids in atherosclerosis: an overview of their mechanisms of action. Curr Med Chem. 2013; 20(21):2641–2660.
29. Landberg R, Sun Q, Rimm EB, Cassidy A, Scalbert A, Mantzoros CS, Hu FB, van Dam RM. Selected dietary flavonoids are associated with markers of inflammation and endothelial dysfunction in U.S. women. J Nutr. 2011; 141(4):618–625.
30. Coskun O, Kanter M, Korkmaz A, Oter S. Quercetin, a flavonoid antioxidant, prevents and protects streptozotocin-induced oxidative stress and beta-cell damage in rat pancreas. Pharmacol Res. 2005; 51(2):117–123.
31. Mahesh T, Menon VP. Quercetin allievates oxidative stress in streptozotocin-induced diabetic rats. Phytother Res. 2004; 18(2):123–127.
32. Kobori M, Masumoto S, Akimoto Y, Takahashi Y. Dietary quercetin alleviates diabetic symptoms and reduces streptozotocin-induced disturbance of hepatic gene expression in mice. Mol Nutr Food Res. 2009; 53(7):859–868.
33. Vessal M, Hemmati M, Vasei M. Antidiabetic effects of quercetin in streptozocin-induced diabetic rats. Comp Biochem Physiol C Toxicol Pharmacol. 2003; 135C(3):357–364.
34. Yang YK. Construction of flavonoid database for the estimation of flavonoid intake in Korean [Dissertation]. Seoul: Ewha Womans University;2011.
35. Yoo S, Nicklas T, Baranowski T, Zakeri IF, Yang SJ, Srinivasan SR, Berenson GS. Comparison of dietary intakes associated with metabolic syndrome risk factors in young adults: the Bogalusa Heart Study. Am J Clin Nutr. 2004; 80(4):841–848.
36. Yang YJ, Kim YJ, Yang YK, Kim JY, Kwon O. Dietary flavan-3-ols intake and metabolic syndrome risk in Korean adults. Nutr Res Pract. 2012; 6(1):68–77.
37. U.S. Department of Health and Human Services; U.S. Department of Agriculture. Dietary guidelines for Americans 2005. 6th edition.Washington, D.C.: U.S. Government Printing Office;2005.
38. Estaquio C, Castetbon K, Kesse-Guyot E, Bertrais S, Deschamps V, Dauchet L, Péneau S, Galan P, Hercberg S. The French National Nutrition and Health Program score is associated with nutritional status and risk of major chronic diseases. J Nutr. 2008; 138(5):946–953.
39. World Cancer Research Fund; American Institute for Cancer Research. Food, nutrition, physical activity, and the prevention of cancer: a global perspective. Washington D.C.: American Institute for Cancer Research;2007.
40. Lee HS, Cho YH, Park J, Shin HR, Sung MK. Dietary intake of phytonutrients in relation to fruit and vegetable consumption in Korea. J Acad Nutr Diet. 2013; 113(9):1194–1199.
41. The Korean Nutrition Society. Dietary reference intakes for Koreans, 1st revision. Seoul: The Korean Nutrition Society;2010.
42. Vural B, Caliskan E, Turkoz E, Kilic T, Demirci A. Evaluation of metabolic syndrome frequency and premature carotid atherosclerosis in young women with polycystic ovary syndrome. Hum Reprod. 2005; 20(9):2409–2413.
43. Fox CS, Massaro JM, Hoffmann U, Pou KM, Maurovich-Hor-vat P, Liu CY, Vasan RS, Murabito JM, Meigs JB, Cupples LA, D'Agostino RB Sr, O'Donnell CJ. Abdominal visceral and subcutaneous adipose tissue compartments: association with metabolic risk factors in the Framingham Heart Study. Circulation. 2007; 116(1):39–48.
Table 1.
All (n = 223) | Non-MetS2) (n = 196) | MetS3) (n = 27) | p value4) | |
---|---|---|---|---|
Age (yr) | 27.3 ± 4.20 | 27.0 ± 3.90 | 29.4 ± 5.50 | < 0.0401 |
Height (cm) | 161.5 ± 5.500 | 161.1 ± 5.300 | 164.4 ± 5.600 | < 0.0034 |
Weight (kg) | 59.0 ± 12.8 | 56.2 ± 10.0 | 79.4 ± 12.8 | < 0.0001 |
BMI (kg/m 2) | 22.5 ± 4.40 | 21.6 ± 3.50 | 29.3 ± 4.10 | < 0.0001 |
Waist (cm) | 76.5 ± 10.8 | 74.0 ± 8.40 | 94.7 ± 9.10 | < 0.0001 |
Hip (cm) | 91.4 ± 8.10 | 89.9 ± 6.90 | 102.5 ± 7.600 | < 0.0001 |
Waist-to hip ratio (WHR) | 0.83 ± 0.06 | 0.82 ± 0.06 | 0.92 ± 0.04 | < 0.0001 |
Occupation | < 0.07715) | |||
Students | 58 (26.0) | 54 (27.6) | 4 (14.8) | |
Employed | 127 (57.0) | 113 (57.6) | 14 (51.9) | |
Househwives | 10 (04.5) | 8 (04.1) | 2 (07.4) | |
Others | 28 (12.5) | 21 (10.7) | 7 (25.9) | |
Nutritional supplement use | 40 (17.9) | 37 (18.8) | 3 (11.1) | < 0.42845) |
Oral contraceptive use | 105 (47.1) | 92 (46.9) | 13 (48.2) | < 0.7099 |
Smoking | < 0.00325) | |||
Current smoker | 26 (11.7) | 17 (08.7) | 9 (33.3) | |
Ex smoker | 11 (04.9) | 9 (04.6) | 2 (07.4) | |
Non smoker | 184 (82.5) | 168 (85.7) | 16 (59.3) | |
Current alcohol drinking | 157 (70.4) | 139 (70.9) | 18 (66.7) | < 0.8969 |
Regular exercise | 106 (47.5) | 94 (48.0) | 32 (44.4) | < 0.8058 |
Table 2.
All (n = 223) N | Non-MetS2) (n = 196) | MetS3) (n = 27) | p value5) | ||
---|---|---|---|---|---|
Unadjusted | Adjusted6) | ||||
Systolic blood pressure (mmHg) | 113.8 ± 15.64) | 111.3 ± 14.2 | 131.5 ± 14.7 | < 0.0001 | < 0.0001 |
Diastolic blood pressure (mmHg) | 068.5 ± 11.4 | 066.7 ± 10.3 | 081.4 ± 10.8 | < 0.0001 | < 0.0001 |
Total cholesterol (mg/dl) | 178.8 ± 1.20 | 176.7 ± 1.20 | 194.9 ± 1.20 | < 0.0053 | < 0.0044 |
Triglyceride (mg/dl) | 079.6 ± 1.6 | 71.6 ± 1.5 | 172.9 ± 1.40 | < 0.0001 | < 0.0001 |
HDL cholesterol (mg/dl) | 057.4 ± 1.3 | 60.3 ± 1.2 | 40.0 ± 1.2 | < 0.0001 | < 0.0001 |
LDL cholesterol (mg/dl) | 100.2 ± 1.30 | 97.1 ± 1.3 | 124.7 ± 1.30 | < 0.0001 | < 0.0001 |
Glucose0 (mg/dl)7) | 087.6 ± 1.1 | 86.5 ± 1.1 | 96.1 ± 1.1 | < 0.0001 | < 0.0001 |
Glucose120 (mg/dl)8) | 100.3 ± 1.20 | 97.3 ± 1.2 | 125.1 ± 1.20 | < 0.0001 | < 0.0001 |
Table 3.
All (n = 223) N | Non-MetS2) (n = 196) | MetS3) (n = 27) | p value4) | ||
---|---|---|---|---|---|
Unadjusted | adjusted6) | ||||
Plants foods (g/d) | 742.1 ± 1.4 | 748.9 ± 1.5 | 694.4 ± 1.4 | 0.3152 | 0.3180 |
Cereals/potatoes products | 228.2 ± 1.5 | 226.8 ± 1.5 | 238.2 ± 1.5 | 0.5584 | 0.0132 |
Sugars | 6.9 ± 2.9 | 7.2 ± 2.8 | 9.8 ± 8.0 | 0.1255 | 0.2949 |
Beans/nuts | 17.7 ± 5.7 | 19.2 ± 5.3 | 5.1 ± 3.5 | 0.0770 | 0.1538 |
Fruits/vegetables/mushrooms/seaweeds | 251.8 ± 1.9 | 253.5 ± 1.9 | 240.0 ± 1.6 | 0.5748 | 0.8543 |
Oils | 6.3 ± 2.3 | 6.3 ± 2.3 | 6.5 ± 1.8 | 0.7970 | 0.2018 |
Beverages | 111.9 ± 4.6 | 108.3 ± 4.8 | 146.4 ± 3.0 | 0.4083 | 0.7534 |
Nutrients | |||||
Energy (kcal/d) | 1,414.4 ± 1.3 | 1,429.2 ± 1.3 | 1,311.5 ± 1.4 | 0.1369 | 0.2567 |
Carbohydrate (g/d) | 202.3 ± 1.4 | 202.8 ± 1.4 | 199.0 ± 1.4 | 0.7609 | 0.0037 |
Protein (g/d) | 52.9 ± 1.4 | 53.5 ± 1.4 | 48.5 ± 1.5 | 0.1551 | 0.3599 |
Fat (g) | 41.3 ± 1.5 | 42.4 ± 1.5 | 34.0 ± 1.6 | 0.0073 | 0.0045 |
Cholesterol (mg/d) | 216.3 ± 1.9 | 226.0 ± 1.8 | 157.5 ± 2.2 | 0.0323 | 0.0112 |
Fiber (g/d) | 13.7 ± 1.5 | 13.8 ± 1.5 | 13.0 ± 1.5 | 0.4373 | 0.7123 |
Calcium (mg/d) | 398.8 ± 1.6 | 403.8 ± 1.6 | 364.2 ± 1.5 | 0.2655 | 0.8027 |
Iron (mg/d) | 9.9 ± 1.5 | 10.1 ± 1.5 | 8.9 ± 1.5 | 0.1332 | 0.4926 |
Zinc (mg/d) | 7.3 ± 1.4 | 7.5 ± 1.4 | 6.5 ± 1.4 | 0.0438 | 0.1314 |
Flavonoids (mg/d) | |||||
Anthocyanidins | 5.6 ± 5.2 | 5.7 ± 5.6 | 4.7 ± 2.7 | 0.4772 | 0.9798 |
Flavan-3-ols | 2.0 ± 24.35) | 2.0 ± 23.2 | 1.7 ± 41.1 | 0.8435 | 0.5523 |
Flavanones | 5.2 ± 12.75) | 5.2 ± 12.8 | 5.1 ± 13.9 | 0.9893 | 0.7857 |
Flavones | 0.3 ± 3.3 | 0.3 ± 3.2 | 0.3 ± 3.9 | 0.7950 | 0.8802 |
Flavonols | 8.3 ± 2.7 | 8.9 ± 2.8 | 5.1 ± 2.4 | 0.0090 | 0.0472 |
Isoflavones | 1.4 ± 21.65) | 1.5 ± 21.4 | 1.1 ± 24.2 | 0.5937 | 0.9145 |
Total | 39.8 ± 3.1 | 41.5 ± 2.8 | 29.2 ± 4.9 | 0.2676 | 0.1827 |
Table 4.
Component of MDA | All (n = 223) |
Non-MetS (n = 196)3) |
MetS4) (n = 27) |
p value5) | |
---|---|---|---|---|---|
I drink 1 or more bottles of milk or its products (yogurt, yoplait, etc.) daily. | Always | 58 (26.01) | 51 (26.02) | 7 (25.93) | 0.7411 |
Generally | 71 (31.84) | 64 (32.65) | 7 (25.93) | ||
Seldom | 94 (42.15) | 81 (41.33) | 13 (48.15) | ||
For each meal, I consume foods made up of a combination of meat, fish, eggs, beans, tobu, etc. | Always | 48 (21.52) | 39 (19.90) | 9 (33.33) | 0.2537 |
Generally | 97 (43.50) | 88 (44.90) | 9 (33.33) | ||
Seldom | 78 (34.98) | 69 (35.20) | 9 (33.33) | ||
For each meal, I consume vegetables other than Kimchi. | Always | 57 (25.56) | 51 (26.02) | 6 (22.22) | 0.2208 |
Generally | 99 (44.39) | 83 (42.35) | 16 (59.26) | ||
Seldom | 67 (30.04) | 62 (31.63) | 5 (18.52) | ||
I consume at least 1 fruit or fruit juice (1 glass) daily. | Always | 53 (23.77) | 47 (23.98) | 6 (22.22) | 0.0180 |
Generally | 81 (36.32) | 77 (39.29) | 4 (14.81) | ||
Seldom | 89 (39.91) | 72 (36.73) | 17 (62.96) | ||
I consume fried or stir-fried foods at least 2 times per week. | Always | 31 (13.90) | 26 (13.27) | 9 (33.33) | 0.4676 |
Generally | 94 (42.15) | 81 (41.33) | 13 (48.15) | ||
Seldom | 98 (43.95) | 89 (45.41) | 5 (18.52) | ||
I consume high fat content eats (bacon, ribs, eel, etc.) at least 2 times per week. | Always | 19 (08.52) | 17 (08.67) | 2 (07.41) | 0.9144 |
Generally | 67 (30.04) | 58 (29.59) | 9 (33.33) | ||
Seldom | 137 (61.43) | 121 (61.73) | 16 (59.26) | ||
I tent to add extra salt or soy sauce while taking my meal. | Always | 9 (04.05) | 8 (04.10) | 1 (03.70) | 0.5682 |
Generally | 34 (15.32) | 28 (14.36) | 6 (22.22) | ||
Seldom | 179 (80.63) | 159 (81.54) | 20 (74.07) | ||
I have three regular meals a day. | Always | 48 (21.52) | 44 (22.45) | 4 (14.81) | 0.3579 |
Generally | 66 (29.60) | 55 (28.06) | 11 (40.74) | ||
Seldom | 109 (48.88) | 97 (22.45) | 12 (44.44) | ||
I consume ice cream, cake, biscuit varieties, carbonated beverages, etc. as snack at least 2 times per week. | Always | 23 (10.31) | 17 (08.67) | 6 (22.22) | 0.0786 |
Generally | 60 (26.91) | 55 (28.06) | 5 (18.52) | ||
Seldom | 140 (62.78) | 124 (63.27) | 16 (59.26) | ||
I tend to consume a wide range of foods evenly (I have a balanced diet.). | Always | 67 (30.04) | 60 (30.61) | 7 (25.93) | 0.8089 |
Generally | 100 (44.84) | 88 (44.90) | 12 (44.44) | ||
Seldom | 56 (25.11) | 48 (24.49) | 8 (29.63) | ||
Total score of MDA6) | 32.7 ± 6.4 | 32.9 ± 6.4 | 31.6 ± 6.5 | 0.33437) |