Association between fish and shellfish, and omega-3 PUFAs intake and CVD risk factors in middle-aged female patients with type 2 diabetes

  • Kim, Hyesook (Department of Nutritional Science and Food Management, Ewha Womans University) ;
  • Park, Seokyung (Department of Clinical Nutrition Science, The Graduate School of Clinical Health Sciences, Ewha Womans University) ;
  • Yang, Hyesu (Department of Nutritional Science and Food Management, Ewha Womans University) ;
  • Choi, Young Ju (Huh's Diabetes Clinic & the 21C Diabetes and Vascular Research Institute) ;
  • Huh, Kap Bum (Huh's Diabetes Clinic & the 21C Diabetes and Vascular Research Institute) ;
  • Chang, Namsoo (Department of Nutritional Science and Food Management, Ewha Womans University)
  • Received : 2015.02.03
  • Accepted : 2015.04.13
  • Published : 2015.10.01


BACKGROUND/OBJECTIVES: This study was performed to investigate the association between the dietary intake of fish and shellfish, and omega-3 polyunsaturated fatty acids (PUFAs) and cardiovascular disease (CVD) risk factors in the middle-aged Korean female patients with Type 2 diabetes (T2D). SUBJECTS/METHODS: A cross-sectional analysis was performed with 356 female patients (means age: 55.5 years), who were recruited from the Huh's Diabetes Clinic in Seoul, Korea between 2005 and 2011. The dietary intake was assessed by a validated semi-quantitative food frequency questionnaire and analyzed using the Computer Aided Nutritional Analysis program (CAN-Pro) version 4.0 software. RESULTS: In a multiple regression analysis after the adjustment for confounding factors such as age, BMI, duration of diagnosed T2D, alcohol consumption, fiber intake, sodium intake, and total energy intake, fish and shellfish intake of the subjects was negatively associated with triglyceride and pulse wave velocity (PWV). Omega-3 PUFAs intake was negatively associated with triglyceride, systolic blood pressures, diastolic blood pressures, and PWV. The multiple logistic regression analysis with the covariates showed a significant inverse relationship between the omega-3 PUFAs consumption and prevalence of hypertriglyceridemia [OR (95% CI) for greater than the median compared to less than the median: 0.395 (0.207-0.753)]. CONCLUSIONS: These results suggest that the consumption of fish and shellfish, good sources of omega-3 PUFAs, may reduce the risk factors for CVD in the middle-aged female patients with T2D.


Supported by : National Research Foundation of Korea (NRF)


  1. Ministry of Health and Welfare, Korea Centers for Disease Control and Prevention. Korea Health Statistics 2010: Korea National Health and Nutrition Examination Survey (KNHANES V-1). Cheongwon: Korea Centers for Disease Control and Prevention; 2011.
  2. Statistics Korea. Annual Report on the Cause of Death Statistics. Daejeon: Statistics Korea; 2012.
  3. Huxley R, Barzi F, Woodward M. Excess risk of fatal coronary heart disease associated with diabetes in men and women: meta-analysis of 37 prospective cohort studies. BMJ 2006;332:73-8.
  4. Kim HK, Kim CH, Kim EH, Bae SJ, Choe J, Park JY, Park SW, Yun YD, Baek SJ, Mok Y, Jee SH. Impaired fasting glucose and risk of cardiovascular disease in Korean men and women: the Korean Heart Study. Diabetes Care 2013;36:328-35.
  5. Zhang J, Wang C, Li L, Man Q, Meng L, Song P, Froyland L, Du ZY. Dietary inclusion of salmon, herring and pompano as oily fish reduces CVD risk markers in dyslipidaemic middle-aged and elderly Chinese women. Br J Nutr 2012;108:1455-65.
  6. Mozaffarian D, Rimm EB. Fish intake, contaminants, and human health: evaluating the risks and the benefits. JAMA 2006;296:1885-99.
  7. Saravanan P, Davidson NC, Schmidt EB, Calder PC. Cardiovascular effects of marine omega-3 fatty acids. Lancet 2010;376:540-50.
  8. Siscovick DS, Raghunathan T, King I, Weinmann S, Bovbjerg VE, Kushi L, Cobb LA, Copass MK, Psaty BM, Lemaitre R, Retzlaff B, Knopp RH. Dietary intake of long-chain n-3 polyunsaturated fatty acids and the risk of primary cardiac arrest. Am J Clin Nutr 2000;71:208S-212S.
  9. Mizushima S, Moriguchi EH, Ishikawa P, Hekman P, Nara Y, Mimura G, Moriguchi Y, Yamori Y. Fish intake and cardiovascular risk among middle-aged Japanese in Japan and Brazil. J Cardiovasc Risk 1997;4:191-9.
  10. Iso H, Kobayashi M, Ishihara J, Sasaki S, Okada K, Kita Y, Kokubo Y, Tsugane S; JPHC Study Group. Intake of fish and n3 fatty acids and risk of coronary heart disease among Japanese: the Japan Public Health Center-Based (JPHC) Study Cohort I. Circulation 2006;113:195-202.
  11. Hu FB, Cho E, Rexrode KM, Albert CM, Manson JE. Fish and long-chain omega-3 fatty acid intake and risk of coronary heart disease and total mortality in diabetic women. Circulation 2003;107:1852-7.
  12. Moore CS, Bryant SP, Mishra GD, Krebs JD, Browning LM, Miller GJ, Jebb SA. Oily fish reduces plasma triacylglycerols: a primary prevention study in overweight men and women. Nutrition 2006;22:1012-24.
  13. Kris-Etherton PM, Harris WS, Appel LJ; American Heart Association. Nutrition Committee. Fish consumption, fish oil, omega-3 fatty acids, and cardiovascular disease. Circulation 2002;106:2747-57.
  14. Harris WS, Miller M, Tighe AP, Davidson MH, Schaefer EJ. Omega-3 fatty acids and coronary heart disease risk: clinical and mechanistic perspectives. Atherosclerosis 2008;197:12-24.
  15. Harris WS, Ginsberg HN, Arunakul N, Shachter NS, Windsor SL, Adams M, Berglund L, Osmundsen K. Safety and efficacy of Omacor in severe hypertriglyceridemia. J Cardiovasc Risk 1997;4:385-91.
  16. Maas AH, Franke HR. Women's health in menopause with a focus on hypertension. Neth Heart J 2009;17:68-72.
  17. Friedewald WT, Levy RI, Fredrickson DS. Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem 1972;18:499-502.
  18. Lauer RM, Lee J, Clarke WR. Factors affecting the relationship between childhood and adult cholesterol levels: the Muscatine Study. Pediatrics 1988;82:309-18.
  19. Yamashina A, Tomiyama H, Takeda K, Tsuda H, Arai T, Hirose K, Koji Y, Hori S, Yamamoto Y. Validity, reproducibility, and clinical significance of noninvasive brachial-ankle pulse wave velocity measurement. Hypertens Res 2002;25:359-64.
  20. Oh SY, Kim EM, Shin MH, Lee SH, Kim JE, Lee HS, Jo JS, Kim WY. Development and validation of food frequency questionnaire for adults. Proceedings of the Korean Society of Health Promotion Annual Spring Conference; 2007 May 19; Seoul. Seoul: Korean Society of Health Promotion; 2007.
  21. The Korean Nutrition Society. Nutritional assessment program 'CAN-Pro 4.0' [CD-ROM]. Seoul: The Korean Nutrition Society; 2011.
  22. United State Department of Agriculture, Agricultural Research Service. USDA National Nutrient Database for Standard Reference, Release 26 [Internet]. Washington, D.C.: Agricultural Research Service; 2013. Available from:
  23. National Fisheries Research & Development Institute (KR). Fatty acid composition of fisheries products in Korea. Busan: National Fisheries Research & Development Institute; 2012.
  24. Dewailly E E, Blanchet C, Gingras S, Lemieux S, Sauve L, Bergeron J, Holub BJ. Relations between n-3 fatty acid status and cardiovascular disease risk factors among Quebecers. Am J Clin Nutr 2001;74:603-11.
  25. Okuda N, Ueshima H, Okayama A, Saitoh S, Nakagawa H, Rodriguez BL, Sakata K, Choudhury SR, Curb JD, Stamler J; INTERLIPID Research Group. Relation of long chain n-3 polyunsaturated fatty acid intake to serum high density lipoprotein cholesterol among Japanese men in Japan and Japanese-American men in Hawaii: the INTERLIPID study. Atherosclerosis 2005;178:371-9.
  26. Friday KE, Childs MT, Tsunehara CH, Fujimoto WY, Bierman EL, Ensinck JW. Elevated plasma glucose and lowered triglyceride levels from omega-3 fatty acid supplementation in type II diabetes. Diabetes Care 1989;12:276-81.
  27. Rivellese AA, Maffettone A, Iovine C, Di Marino L, Annuzzi G, Mancini M, Riccardi G. Long-term effects of fish oil on insulin resistance and plasma lipoproteins in NIDDM patients with hypertriglyceridemia. Diabetes Care 1996;19:1207-13.
  28. Woodman RJ, Mori TA, Burke V, Puddey IB, Watts GF, Beilin LJ. Effects of purified eicosapentaenoic and docosahexaenoic acids on glycemic control, blood pressure, and serum lipids in type 2 diabetic patients with treated hypertension. Am J Clin Nutr 2002;76:1007-15.
  29. Lankinen M, Kolehmainen M, Jaaskelainen T, Paananen J, Joukamo L, Kangas AJ, Soininen P, Poutanen K, Mykkanen H, Gylling H, Oresic M, Jauhiainen M, Ala-Korpela M, Uusitupa M, Schwab U. Effects of whole grain, fish and bilberries on serum metabolic profile and lipid transfer protein activities: a randomized trial (Sysdimet). PLoS One 2014;9:e90352.
  30. Nilsen DW, Albrektsen G, Landmark K, Moen S, Aarsland T, Woie L. Effects of a high-dose concentrate of n-3 fatty acids or corn oil introduced early after an acute myocardial infarction on serum triacylglycerol and HDL cholesterol. Am J Clin Nutr 2001;74:50-6.
  31. Harris WS. n-3 fatty acids and serum lipoproteins: human studies. Am J Clin Nutr 1997;65:1645S-1654S.
  32. Park Y, Harris WS. Omega-3 fatty acid supplementation accelerates chylomicron triglyceride clearance. J Lipid Res 2003;44:455-63.
  33. Rustan AC, Nossen JO, Christiansen EN, Drevon CA. Eicosapentaenoic acid reduces hepatic synthesis and secretion of triacylglycerol by decreasing the activity of acyl-coenzyme A:1,2-diacylglycerol acyltransferase. J Lipid Res 1988;29:1417-26.
  34. Morris MC, Sacks F, Rosner B. Does fish oil lower blood pressure? A meta-analysis of controlled trials. Circulation 1993;88:523-33.
  35. Kasim SE, Stern B, Khilnani S, McLin P, Baciorowski S, Jen KL. Effects of omega-3 fish oils on lipid metabolism, glycemic control, and blood pressure in type II diabetic patients. J Clin Endocrinol Metab 1988;67:1-5.
  36. Margolin G, Huster G, Glueck CJ, Speirs J, Vandegrift J, Illig E, Wu J, Streicher P, Tracy T. Blood pressure lowering in elderly subjects: a double-blind crossover study of omega-3 and omega-6 fatty acids. Am J Clin Nutr 1991;53:562-72.
  37. Bonaa KH, Bjerve KS, Straume B, Gram IT, Thelle D. Effect of eicosapentaenoic and docosahexaenoic acids on blood pressure in hypertension. A population-based intervention trial from the Tromso study. N Engl J Med 1990;322:795-801.
  38. Needleman P, Raz A, Minkes MS, Ferrendelli JA, Sprecher H. Triene prostaglandins: prostacyclin and thromboxane biosynthesis and unique biological properties. Proc Natl Acad Sci U S A 1979;76:944-8.
  39. Yin K, Chu ZM, Beilin LJ. Blood pressure and vascular reactivity changes in spontaneously hypertensive rats fed fish oil. Br J Pharmacol 1991;102:991-7.
  40. Hashimoto M, Hossain S, Yamasaki H, Yazawa K, Masumura S. Effects of eicosapentaenoic acid and docosahexaenoic acid on plasma membrane fluidity of aortic endothelial cells. Lipids 1999;34:1297-304.
  41. Lund EK, Harvey LJ, Ladha S, Clark DC, Johnson IT. Effects of dietary fish oil supplementation on the phospholipid composition and fluidity of cell membranes from human volunteers. Ann Nutr Metab 1999;43:290-300.
  42. Hamazaki T, Urakaze M, Sawazaki S, Yamazaki K, Taki H, Yano S. Comparison of pulse wave velocity of the aorta between inhabitants of fishing and farming villages in Japan. Atherosclerosis 1988;73:157-60.
  43. Sekikawa A, Shin C, Masaki KH, Barinas-Mitchell EJ, Hirooka N, Willcox BJ, Choo J, White J, Evans RW, Fujiyoshi A, Okamura T, Miura K, Muldoon MF, Ueshima H, Kuller LH, Sutton-Tyrrell K; ERA JUMP Study Group. Association of total marine fatty acids, eicosapentaenoic and docosahexaenoic acids, with aortic stiffness in Koreans, Whites, and Japanese Americans. Am J Hypertens 2013;26:1321-7.
  44. Fukuoka Y, Nuruki N, Amiya S, Tofuku K, Aosaki S, Tsubouchi H. Effects of a fish-based diet and administration of pure eicosapentaenoic acid on brachial-ankle pulse wave velocity in patients with cardiovascular risk factors. J Cardiol 2014;63:211-7.
  45. Payne RA, Wilkinson IB, Webb DJ. Arterial stiffness and hypertension: emerging concepts. Hypertension 2010;55:9-14.
  46. Jia Y, Turek JJ. Altered NF-kappaB gene expression and collagen formation induced by polyunsaturated fatty acids. J Nutr Biochem 2005;16:500-6.
  47. McEniery CM, McDonnell BJ, So A, Aitken S, Bolton CE, Munnery M, Hickson SS, Yasmin, Maki-Petaja KM, Cockcroft JR, Dixon AK, Wilkinson IB; Anglo-Cardiff Collaboration Trial Investigators. Aortic calcification is associated with aortic stiffness and isolated systolic hypertension in healthy individuals. Hypertension 2009;53:524-31.
  48. Abedin M, Lim J, Tang TB, Park D, Demer LL, Tintut Y. N-3 fatty acids inhibit vascular calcification via the p38-mitogen-activated protein kinase and peroxisome proliferator-activated receptorgamma pathways. Circ Res 2006;98:727-9.
  49. Health Insurance Review & Assessment Service; National Health Insurance Service. National Health Insurance Statistical Yearbook 2011. Seoul: National Health Insurance Service; 2012.

Cited by

  1. Effects of folic acid supplementation on serum homocysteine levels, lipid profiles, and vascular parameters in post-menopausal Korean women with type 2 diabetes mellitus vol.11, pp.4, 2017,
  2. Lean Fish Consumption Is Associated with Beneficial Changes in the Metabolic Syndrome Components: A 13-Year Follow-Up Study from the Norwegian Tromsø Study vol.9, pp.3, 2017,