Serum adiponectin as a useful marker for metabolic syndrome in type 2 diabetic patients
Ji Eun Yun
Institute for Health Promotion, Graduate School of Public Health, Yonsei University, Seoul, Republic of Korea
Department of Epidemiology and Health Promotion, Graduate School of Public Health, Yonsei University, Seoul, Republic of Korea
Search for more papers by this authorJae Woong Sull
Institute for Health Promotion, Graduate School of Public Health, Yonsei University, Seoul, Republic of Korea
Department of Epidemiology and Health Promotion, Graduate School of Public Health, Yonsei University, Seoul, Republic of Korea
Search for more papers by this authorHee Yeon Lee
Institute for Health Promotion, Graduate School of Public Health, Yonsei University, Seoul, Republic of Korea
Department of Epidemiology and Health Promotion, Graduate School of Public Health, Yonsei University, Seoul, Republic of Korea
Search for more papers by this authorEunjung Park
Institute for Health Promotion, Graduate School of Public Health, Yonsei University, Seoul, Republic of Korea
Search for more papers by this authorSoriwool Kim
Institute for Health Promotion, Graduate School of Public Health, Yonsei University, Seoul, Republic of Korea
Search for more papers by this authorJaeseong Jo
Metabolic Syndrome Research Initiatives, Seoul, Republic of Korea
Search for more papers by this authorSun Ju Lee
Metabolic Syndrome Research Initiatives, Seoul, Republic of Korea
Search for more papers by this authorSang Yeon Kim
Metabolic Syndrome Research Initiatives, Seoul, Republic of Korea
Search for more papers by this authorYoung Ju Choi
Huh's Diabetes Center and the 21st Century Diabetes and Vascular Research Institute, Seoul, Republic of Korea
Search for more papers by this authorCorresponding Author
Sun Ha Jee
Institute for Health Promotion, Graduate School of Public Health, Yonsei University, Seoul, Republic of Korea
Department of Epidemiology and Health Promotion, Graduate School of Public Health, Yonsei University, Seoul, Republic of Korea
Department of Epidemiology and Health Promotion, Graduate School of Public Health, Yonsei University, Seoul, Republic of Korea.Search for more papers by this authorKap Bum Huh
Huh's Diabetes Center and the 21st Century Diabetes and Vascular Research Institute, Seoul, Republic of Korea
Search for more papers by this authorJi Eun Yun
Institute for Health Promotion, Graduate School of Public Health, Yonsei University, Seoul, Republic of Korea
Department of Epidemiology and Health Promotion, Graduate School of Public Health, Yonsei University, Seoul, Republic of Korea
Search for more papers by this authorJae Woong Sull
Institute for Health Promotion, Graduate School of Public Health, Yonsei University, Seoul, Republic of Korea
Department of Epidemiology and Health Promotion, Graduate School of Public Health, Yonsei University, Seoul, Republic of Korea
Search for more papers by this authorHee Yeon Lee
Institute for Health Promotion, Graduate School of Public Health, Yonsei University, Seoul, Republic of Korea
Department of Epidemiology and Health Promotion, Graduate School of Public Health, Yonsei University, Seoul, Republic of Korea
Search for more papers by this authorEunjung Park
Institute for Health Promotion, Graduate School of Public Health, Yonsei University, Seoul, Republic of Korea
Search for more papers by this authorSoriwool Kim
Institute for Health Promotion, Graduate School of Public Health, Yonsei University, Seoul, Republic of Korea
Search for more papers by this authorJaeseong Jo
Metabolic Syndrome Research Initiatives, Seoul, Republic of Korea
Search for more papers by this authorSun Ju Lee
Metabolic Syndrome Research Initiatives, Seoul, Republic of Korea
Search for more papers by this authorSang Yeon Kim
Metabolic Syndrome Research Initiatives, Seoul, Republic of Korea
Search for more papers by this authorYoung Ju Choi
Huh's Diabetes Center and the 21st Century Diabetes and Vascular Research Institute, Seoul, Republic of Korea
Search for more papers by this authorCorresponding Author
Sun Ha Jee
Institute for Health Promotion, Graduate School of Public Health, Yonsei University, Seoul, Republic of Korea
Department of Epidemiology and Health Promotion, Graduate School of Public Health, Yonsei University, Seoul, Republic of Korea
Department of Epidemiology and Health Promotion, Graduate School of Public Health, Yonsei University, Seoul, Republic of Korea.Search for more papers by this authorKap Bum Huh
Huh's Diabetes Center and the 21st Century Diabetes and Vascular Research Institute, Seoul, Republic of Korea
Search for more papers by this authorAbstract
Background
Although adiponectin is generally known as a predictor of metabolic syndrome, potential of adiponectin as a predictor for metabolic syndrome in type 2 diabetes is debated. The purpose of this study is to determine the association between adiponectin and metabolic syndrome in patients with type 2 diabetes.
Methods
Adiponectin and the risk of metabolic syndrome were examined among 1013 type 2 diabetes patients who visited Huh's Diabetes Center from January 2003 to June 2006. Adiponectin levels were classified into quartile groups, and metabolic syndrome was defined according to the standard of National Cholesterol Education Program (NCEP) Adult Treatment Panel (ATP) III. Insulin sensitivity was directly assessed using the short insulin tolerance test (SITT) (Kitt: %/ min).
Results
Adiponectin was significantly correlated with metabolic syndrome components. The age-adjusted correlations between adiponectin and clinical parameters including metabolic components were significant; adiponectin was negatively correlated with waist circumference, diastolic blood pressure and triglyceride, and positively correlated with high-density lipoprotein (HDL) cholesterol. Subjects with metabolic syndrome showed lower adiponectin levels than those without metabolic syndrome. After multivariate adjustment, participants with lower adiponectin levels also had a higher risk for metabolic syndrome (OR for lowest quartiles 2.21; 95% CI, 1.51–3.24). Metabolic syndrome risk was stronger among those with low adiponectin and severe insulin resistance simultaneously. This study has shown additive effects of adiponectin and insulin resistance on metabolic syndrome.
Conclusions
In type 2 diabetic patients, the adiponectin was a useful predictor of metabolic syndrome independent of potential confounding variables. Copyright © 2009 John Wiley & Sons, Ltd.
References
- 1Park HS, Park CY, Oh SW, Yoo HJ. Prevalence of obesity and metabolic syndrome in Korean adults. Obes Rev 2008; 9(2): 104–107.
- 2Funahashi T, Nakamura T, Shimomura I, et al. Role of adipocytokines on the pathogenesis of atherosclerosis in visceral obesity. Intern Med 1999; 38(2): 202–206.
- 3Kadowaki T, Yamauchi T, Kubota N, Hara K, Ueki K, Tobe K. Adiponectin and adiponectin receptors in insulin resistance, diabetes, and the metabolic syndrome. J Clin Invest 2006; 116(7): 1784–1792.
- 4Ouchi N, Kihara S, Arita Y, et al. Novel modulator for endothelial adhesion molecules: adipocyte-derived plasma protein adiponectin. Circulation 1999; 100(25): 2473–2476.
- 5Hotta K, Funahashi T, Arita Y, et al. Plasma concentrations of a novel, adipose-specific protein, adiponectin, in type 2 diabetic patients. Arterioscler Thromb Vasc Biol 2000; 20(6): 1595–1599.
- 6Ouchi N, Kihara S, Arita Y, et al. Adipocyte-derived plasma protein, adiponectin, suppresses lipid accumulation and class A scavenger receptor expression in human monocyte-derived macrophages. Circulation 2001; 103(8): 1057–1063.
- 7Snehalatha C, Mukesh B, Simon M, Viswanathan V, Haffner SM, Ramachandran A. Plasma adiponectin is an independent predictor of type 2 diabetes in Asian indians. Diabetes Care 2003; 26(12): 3226–3229.
- 8Duncan BB, Schmidt MI, Pankow JS, et al. Adiponectin and the development of type 2 diabetes: the atherosclerosis risk in communities study. Diabetes 2004; 53(9): 2473–2478.
- 9Higashiura K, Ura N, Ohata J, et al. Correlations of adiponectin level with insulin resistance and atherosclerosis in Japanese male populations. Clin Endocrinol (Oxf) 2004; 61(6): 753–759.
- 10Pischon T, Girman CJ, Hotamisligil GS, Rifai N, Hu FB, Rimm EB. Plasma adiponectin levels and risk of myocardial infarction in men. JAMA 2004; 291(14): 1730–1737.
- 11Nakamura Y, Shimada K, Fukuda D, et al. Implications of plasma concentrations of adiponectin in patients with coronary artery disease. Heart 2004; 90(5): 528–533.
- 12Dzielinska Z, Januszewicz A, Wiecek A, et al. Decreased plasma concentration of a novel anti-inflammatory protein–adiponectin–in hypertensive men with coronary artery disease. Thromb Res 2003; 110(5–6): 365–369.
- 13Choi KM, Lee J, Lee KW, et al. Serum adiponectin concentrations predict the developments of type 2 diabetes and the metabolic syndrome in elderly Koreans. Clin Endocrinol 2004; 61(1): 75–80.
- 14Mohan V, Deepa R, Pradeepa R, et al. Association of low adiponectin levels with the metabolic syndrome-the Chennai Urban Rural Epidemiology Study(CURES-4). Metabolism 2005; 54(4): 476–481.
- 15Santaniemi M, Kesaniemi YA, Ukkola O. Low plasma adiponectin concentration is an indicator of the metabolic syndrome. Eur J Endocrinol 2006; 155(5): 745–750.
- 16Gilardini L, McTernan PG, Girola A, et al. Adiponectin is a candidate marker of metabolic syndrome in obese children and adolescents. Atherosclerosis 2006; 189(2): 401–407.
- 17Hickman IJ, Whitehead JP, Prins JB, Macdonald GA. Raised alanine transaminase and decreased adiponectin are features of the metabolic syndrome in patients with type 2 diabetes. Diabetes Obes Metab 2007; 9(3): 438–440.
- 18Salas-Salvado J, Granada M, Bullo M, Corominas A, Casas P, Foz M. Plasma adiponectin distribution in a Mediterranean population and its association with cardiovascular risk factors and metabolic syndrome. Metabolism 2007; 56(11): 1486–1492.
- 19Wang J, Li H, Franco OH, Yu Z, Liu Y, Lin X. Adiponectin and metabolic syndrome in middle-aged and elderly Chinese. Obesity 2008; 16(1): 172–178.
- 20Mojiminiyi OA, Abdella NA, Al Arouj M, Ben Nakhi A. Adiponectin, insulin resistance and clinical expression of the metabolic syndrome in patients with Type 2 diabetes. Int J Obes 2007; 31(2): 213–220.
- 21Fukui M, Ose H, Kitagawa Y, et al. Metabolic syndrome is not associated with markers of subclinical atherosclerosis, serum adiponectin and endogenous androgen concentrations in Japanese men with type 2 diabetes. Diabet Med 2007; 24(8): 864–871.
- 22Jee SH, Lee S, Min S, et al. Development of ELISA-kit of quantitative analysis for adiponectin and their correlation with cardiovascular risk factors. Korean J Epidemiol 2007; 29(2): 165–175.
- 23Yoon SJ, Lee HS, Lee SW, et al. The association between adiponectin and diabetes in the Korean population. Metabolism 2008; 57(6): 853–857.
- 24Bonora E, Moghetti P, Zancanaro C, et al. Estimates of in vivo insulin action in man: comparison of insulin tolerance tests with euglycemic and hyperglycemic glucose clamp studies. J Clin Endocrinol Metab 1989; 68: 374–378.
- 25Alberti KGGM, Daly ME, Robibson A, Marshall SM, Maathers JC. The short insulin tolerance test is safe and reproducible. Diabet Med 1999; 16: 352–353.
- 26Park SW, Yun YS, Ahn CW, et al. Short insulin tolerance test for the determination of in vivo insulin sensitivity: a comparison with euglycemic clamp test. J Korean Diabetes Assoc 1998; 22: 199–208.
- 27Executive summary of the Third Report of the National Cholesterol Education Program (NCEP) expert panel on detection, evaluation, and treatment of high blood cholesterol in adults (Adult Treatment Panel III). JAMA 2001; 285: 2486–2497.
- 28Tan CE, Ma S, Wai D, Chew SK, Tai ES. Can we apply the national cholesterol education program adult treatment panel definition of the metabolic syndrome to Asians. Diabetes Care 2004; 27: 1182–1186.
- 29Matsubara M, Maruoka S, Katayose S. Decreased plasma adiponectin concentrations in women with dyslipidemia. J Clin Endocrinol Metab 2002; 87: 2764–2769.
- 30Tschritter O, Fritsche A, Thamer C, et al. Plasma adiponectin concentrations predict insulin sensitivity of both glucose and lipid metabolism. Diabetes 2003; 52: 239–243.
- 31Ryo M, Nakamura T, Kihara S, et al. Adiponectin as a biomarker of the metabolic syndrome. Circ J 2004; 68(11): 975–981.
- 32Valsamakis G, Chetty R, McTernan PG, et al. Fasting serum adiponectin concentration is reduced in Indo-Asian subjects and is related to HDL cholesterol. Diabetes Obes Metab 2003; 5: 131–135.
- 33Kim SM, Cho KH, Park HS. Relationship between plasma adiponectin levels and the metabolic syndrome among Korean people. Endocr J 2006; 53(2): 247–254.
- 34Xydakis AM, Case CC, Jones PH, et al. Adiponectin, inflammation, and the expression of the metabolic syndrome in obese individuals: the impact of rapid weight loss through caloric restriction. J Clin Endocrinol Metab 2004; 89: 2697–2703.
- 35Guzder RN, Gatling W, Mullee MA, Byrne CD. Impact of metabolic syndrome criteria on cardiovascular disease risk in people with newly diagnosed type 2 diabetes. Diabetologia 2006; 49(1): 49–55.
- 36Bonora E, Targher G, Formentini G, et al. The metabolic syndrome is an independent predictor of cardiovascular disease in Type 2 diabetic subjects. Prospective data from the Verona Diabetes Complications Study. Diabet Med 2004; 21(1): 52–58.
- 37Kershaw EE, Flier JS. Adipose tissue as an endocrine organ. J Clin Endocrinol Metab 2004; 89: 2548–2556.
- 38Matsuzawa Y, Funahashi T, Kihara S, Shimomura I. Adiponectin and metabolic syndrome. Arterioscler Thromb Vasc Biol 2004; 24: 29–33.
- 39Yu JG, Javorschi S, Hevener AL, et al. The effect of thiazolidinediones on plasma adiponectin levels in normal, obese, and type 2 diabetic subjects. Diabetes 2002; 51: 2968–2974.
- 40Möhlig M, Wegewitz U, Osterhoff M, et al. Insulin decreases human adiponectin plasma levels. Horm Metab Res 2002; 34: 655–658.
- 41Kang ES, Yun YS, Park SW, et al. Limitation of the validity of the homeostasis model assessment as an index of insulin resistance in Korea. Metabolism 2005; 54: 206–211.
- 42Young RP, Critchley JA, Anderson PJ, Lau MS, Lee KK, Chan JC. The short insulin tolerance test: feasibility study using venous sampling. Diabet Med 1996; 13: 429–433.
10.1002/(SICI)1096-9136(199605)13:5<429::AID-DIA98>3.0.CO;2-K CAS PubMed Web of Science® Google Scholar
- 43Pischon T, Hotamisligli GS, Rimm EB. Adiponectin: stability in plasma over 36 hours and within-person variation over 1 year. Clin Chem 2003; 49: 650–652.