Skip to main content

Advertisement

Log in

Adiponectin circulating levels and 10-year (2002–2012) cardiovascular disease incidence: the ATTICA Study

  • Original Article
  • Published:
Endocrine Aims and scope Submit manuscript

Abstract

Purpose

Adiponectin is an adipokine with anti-inflammatory and cardiovascular-protective properties. Existing epidemiological evidence is conflicting on the exact relationship between adiponectin and long-term cardiovascular disease (CVD) risk. Our aim was to prospectively assess whether circulating adiponectin is associated with long-term incident CVD.

Methods

A population-based, prospective study in adults (>18 years) without previous CVD history (ATTICA study). Circulating total adiponectin levels were measured at baseline (2001–2002) in a sub-sample (n = 531; women/men: 222/309; age: 40 ± 11 years) of the ATTICA cohort and complete 10-year follow-up data were available in 366 of these participants (women/men: 154/212; age: 40 ± 12 years).

Results

After adjusting for multiple factors, including age, sex, body mass index, waist circumference, smoking, physical activity, Mediterranean diet adherence, hypertension, diabetes, and hypercholesterolemia, our logistic regression analysis indicates that an increase in circulating total adiponectin levels by 1 unit was associated with 36% lower CVD risk (relative risk [RR]: 0.64, 95% confidence interval [CI] 0.42–0.96; p = 0.03). Further adjusting for interleukin-6 plasma levels had no significant impact (RR: 0.60, 95% CI 0.38–0.94; p = 0.03), while additional adjustment for circulating C-reactive protein (CRP) modestly attenuated this association (RR: 0.63, 95% CI 0.40–0.99; p = 0.046).

Conclusions

In our study, elevated circulating total adiponectin levels were associated with lower 10-year CVD risk in adults without previous CVD, independently of other established CVD risk factors. This association appeared to be modestly attenuated by CRP, yet was not mediated by interleukin-6 which is the main endocrine/circulating pro-inflammatory cytokine.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. S. Galic, J.S. Oakhill, G.R. Steinberg, Adipose tissue as an endocrine organ. Mol. Cell. Endocrinol. 316(2), 129–139 (2010)

    Article  CAS  PubMed  Google Scholar 

  2. C.M. Rondinone, Adipocyte-derived hormones, cytokines, and mediators. Endocrine 29(1), 81–90 (2006)

    Article  CAS  PubMed  Google Scholar 

  3. M. Fasshauer, M. Blüher, Adipokines in health and disease. Trends Pharmacol. Sci. 36(7), 461–470 (2015)

    Article  CAS  PubMed  Google Scholar 

  4. I. Kyrou, H.S. Mattu, K. Chatha, H.S. Randeva, Chapter 7—fat hormones, adipokines. in Endocrinology of the Heart in Health and Disease, ed. by J.C. Schisler, C.H. Lang, M.S. Willis (Academic Press, London, UK, San Diego, CA, 2017), pp. 167–205

  5. K. Brochu-Gaudreau, C. Rehfeldt, R. Blouin, V. Bordignon, B.D. Murphy, M.F. Palin, Adiponectin action from head to toe. Endocrine 37(1), 11–32 (2010)

    Article  CAS  PubMed  Google Scholar 

  6. R.S. Ahima, Metabolic actions of adipocyte hormones: focus on adiponectin. Obesity 14(Suppl 1), 9S–15S (2006)

    Article  CAS  PubMed  Google Scholar 

  7. A.T. Turer, P.E. Scherer, Adiponectin: mechanistic insights and clinical implications. Diabetologia 55(9), 2319–2326 (2012)

    Article  CAS  PubMed  Google Scholar 

  8. O. Yousuf, B.D. Mohanty, S.S. Martin, P.H. Joshi, M.J. Blaha, K. Nasir, R.S. Blumenthal, M.J. Budoff, High-sensitivity C-reactive protein and cardiovascular disease: a resolute belief or an elusive link? J. Am. Coll. Cardiol. 62(5), 397–408 (2013)

    Article  CAS  PubMed  Google Scholar 

  9. J.S. Yudkin, M. Kumari, S.E. Humphries, V. Mohamed-Ali, Inflammation, obesity, stress and coronary heart disease: is interleukin-6 the link? Atherosclerosis 148(2), 209–214 (2000)

    Article  CAS  PubMed  Google Scholar 

  10. J.R. Kizer, Adiponectin, cardiovascular disease, and mortality: parsing the dual prognostic implications of a complex adipokine. Metabolism 63(9), 1079–1083 (2014)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. T. Pischon, C.J. Girman, G.S. Hotamisligil, N. Rifai, F.B. Hu, E.B. Rimm, Plasma adiponectin levels and risk of myocardial infarction in men. JAMA 291(14), 1730–1737 (2004)

    Article  CAS  PubMed  Google Scholar 

  12. N. Sattar, G. Wannamethee, N. Sarwar, J. Tchernova, L. Cherry, A.M. Wallace, J. Danesh, P.H. Whincup, Adiponectin and coronary heart disease: a prospective study and meta-analysis. Circulation 114(7), 623–629 (2006)

    Article  CAS  PubMed  Google Scholar 

  13. J. Poehls, C.L. Wassel, T.B. Harris, P.J. Havel, M.M. Swarbrick, S.R. Cummings, A.B. Newman, S. Satterfield, A.M. Kanaya, Health ABC study. Association of adiponectin with mortality in older adults: the health, aging, and body composition study. Diabetologia 52(4), 591–595 (2009)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. E. Cavusoglu, C. Ruwende, V. Chopra, S. Yanamadala, C. Eng, L.T. Clark, D.J. Pinsky, J.D. Marmur, Adiponectin is an independent predictor of all-cause mortality, cardiac mortality, and myocardial infarction in patients presenting with chest pain. Eur. Heart J. 27(19), 2300–2309 (2006)

    Article  CAS  PubMed  Google Scholar 

  15. C. Kistorp, J. Faber, S. Galatius, F. Gustafsson, J. Frystyk, A. Flyvbjerg, P. Hildebrandt, Plasma adiponectin, body mass index, and mortality in patients with chronic heart failure. Circulation. 112(12), 1756–1762 (2005)

    Article  CAS  PubMed  Google Scholar 

  16. C. Pitsavos, D.B. Panagiotakos, C. Chrysohoou, C. Stefanadis, Epidemiology of cardiovascular risk factors in Greece: aims, design and baseline characteristics of the ATTICA study. BMC Public Health 20(3), 32 (2003)

    Article  Google Scholar 

  17. K. Katsouyanni, E.B. Rimm, C. Gnardellis, D. Trichopoulos, E. Polychronopoulos, A. Trichopoulou, Reproducibility and relative validity of an extensive semi-quantitative food frequency questionnaire using dietary records and biochemical markers among Greek schoolteachers. Int. J. Epidemiol. 26(Suppl 1), S118–S127 (1997)

    Article  PubMed  Google Scholar 

  18. D.B. Panagiotakos, C. Pitsavos, C. Stefanadis, Dietary patterns: a Mediterranean diet score and its relation to clinical and biological markers of cardiovascular disease risk. Nutr. Metab. Cardiovasc. Dis. 16(8), 559–568 (2006)

    Article  PubMed  Google Scholar 

  19. G. Papathanasiou, G. Georgoudis, M. Papandreou, P. Spyropoulos, D. Georgakopoulos, V. Kalfakakou, A. Evangelou, Reliability measures of the short International Physical Activity Questionnaire (IPAQ) in Greek young adults. Hell. J. Cardiol. 50(4), 283–294 (2009)

    Google Scholar 

  20. K.G. Alberti, P. Zimmet, J. Shaw IDF Epidemiology Task Force Consensus Group The metabolic syndrome—a new worldwide definition. Lancet 366(9491), 1059–1062 (2005)

    Article  PubMed  Google Scholar 

  21. D.B. Panagiotakos, E.N. Georgousopoulou, C. Pitsavos, C. Chrysohoou, V. Metaxa, G.A. Georgiopoulos, K. Kalogeropoulou, D. Tousoulis, C. Stefanadis ATTICA Study Group Ten-year (2002–2012) cardiovascular disease incidence and all-cause mortality, in urban Greek population: the ATTICA Study. Int. J. Cardiol. 180, 178–184 (2015)

    Article  PubMed  Google Scholar 

  22. D. Rothenbacher, H. Brenner, W. März, W. Koenig Adiponectin, risk of coronary heart disease and correlations with cardiovascular risk markers. Eur. Heart J. 26(16), 1640–1646 (2005)

    Article  CAS  PubMed  Google Scholar 

  23. T. Pischon, F.B. Hu, C.J. Girman, N. Rifai, J.E. Manson, K.M. Rexrode, E.B. Rimm, Plasma total and high molecular weight adiponectin levels and risk of coronary heart disease in women. Atherosclerosis 219(1), 322–329 (2011)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. J. Frystyk, C. Berne, L. Berglund, K. Jensevik, A. Flyvbjerg, B. Zethelius, Serum adiponectin is a predictor of coronary heart disease: a population-based 10-year follow-up study in elderly men. J. Clin. Endocrinol. Metab. 92(2), 571–576 (2007)

    Article  CAS  PubMed  Google Scholar 

  25. D.Y. Ho, N.R. Cook, K.A. Britton, E. Kim, M.A. Creager, P.M. Ridker, A.D. Pradhan, High-molecular-weight and total adiponectin levels and incident symptomatic peripheral artery disease in women: a prospective investigation. Circulation 124(21), 2303–2311 (2011)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. I. Saito, K. Yamagishi, C.L. Chei, R. Cui, T. Ohira, A. Kitamura, M. Kiyama, H. Imano, T. Okada, T. Kato, S. Hitsumoto, Y. Ishikawa, T. Tanigawa, H. Iso, Total and high molecular weight adiponectin levels and risk of cardiovascular disease in individuals with high blood glucose levels. Atherosclerosis 229(1), 222–227 (2013)

    Article  CAS  PubMed  Google Scholar 

  27. M.B. Schulze, I. Shai, E.B. Rimm, T. Li, N. Rifai, F.B. Hu, Adiponectin and future coronary heart disease events among men with type 2 diabetes. Diabetes 54(2), 534–539 (2005)

    Article  CAS  PubMed  Google Scholar 

  28. M. Kumada, S. Kihara, S. Sumitsuji, T. Kawamoto, S. Matsumoto, N. Ouchi, Y. Arita, Y. Okamoto, I. Shimomura, H. Hiraoka, T. Nakamura, T. Funahashi, Y. Matsuzawa; Osaka CAD Study Group, Coronary artery disease. Association of hypoadiponectinemia with coronary artery disease in men. Arterioscler. Thromb. Vasc. Biol. 23(1), 85–9 (2003)

    Article  CAS  PubMed  Google Scholar 

  29. M. Ai, S. Otokozawa, B.F. Asztalos, C.C. White, L.A. Cupples, K. Nakajima, S. Lamon-Fava, P.W. Wilson, Y. Matsuzawa, E.J. Schaefer, Adiponectin: an independent risk factor for coronary heart disease in men in the Framingham offspring Study. Atherosclerosis 217(2), 543–548 (2011)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. H. Zhang, X. Mo, Y. Hao, J. Huang, X. Lu, J. Cao, D. Gu, Adiponectin levels and risk of coronary heart disease: a meta-analysis of prospective studies. Am. J. Med. Sci. 345(6), 455–461 (2013)

    Article  PubMed  Google Scholar 

  31. B.C. Zhang, W.J. Liu, W.L. Che, Y.W. Xu, Serum total adiponectin level and risk of cardiovascular disease in Han Chinese populations: a meta-analysis of 17 case–control studies. Clin. Endocrinol. 77(3), 370–378 (2012)

    Article  CAS  Google Scholar 

  32. J.L. Parker-Duffen, K. Walsh, Cardiometabolic effects of adiponectin. Best Pract. Res. Clin. Endocrinol. Metab. 28(1), 81–91 (2014)

    Article  CAS  PubMed  Google Scholar 

  33. C. Caselli, A. D’Amico, M. Cabiati, T. Prescimone, S. Del Ry, D. Giannessi, Back to the heart: the protective role of adiponectin. Pharmacol. Res. 82, 9–20 (2014)

    Article  CAS  PubMed  Google Scholar 

  34. T.A. Hopkins, N. Ouchi, R. Shibata, K. Walsh, Adiponectin actions in the cardiovascular system. Cardiovasc. Res. 74(1), 11–18 (2007)

    Article  CAS  PubMed  Google Scholar 

  35. N. Ouchi, S. Kihara, Y. Arita, Y. Okamoto, K. Maeda, H. Kuriyama, K. Hotta, M. Nishida, M. Takahashi, M. Muraguchi, Y. Ohmoto, T. Nakamura, S. Yamashita, T. Funahashi, Y. Matsuzawa, Adiponectin, an adipocyte-derived plasma protein, inhibits endothelial NF-kappaB signaling through a cAMP-dependent pathway. Circulation 102(11), 1296–1301 (2000)

    Article  CAS  PubMed  Google Scholar 

  36. Y. Hattori, Y. Nakano, S. Hattori, A. Tomizawa, K. Inukai, K. Kasai, High molecular weight adiponectin activates AMPK and suppresses cytokine-induced NF-kappaB activation in vascular endothelial cells. FEBS Lett. 582(12), 1719–1724 (2008)

    Article  CAS  PubMed  Google Scholar 

  37. R. Ouedraogo, X. Wu, S.Q. Xu, L. Fuchsel, H. Motoshima, K. Mahadev, K. Hough, R. Scalia, B.J. Goldstein, Adiponectin suppression of high-glucose-induced reactive oxygen species in vascular endothelial cells: evidence for involvement of a cAMP signaling pathway. Diabetes 55(6), 1840–1846 (2006)

    Article  CAS  PubMed  Google Scholar 

  38. H. Chen, M. Montagnani, T. Funahashi, I. Shimomura, M.J. Quon, Adiponectin stimulates production of nitric oxide in vascular endothelial cells. J. Biol. Chem. 278(45), 45021–45026 (2003)

    Article  CAS  PubMed  Google Scholar 

  39. R. Ouedraogo, Y. Gong, B. Berzins, X. Wu, K. Mahadev, K. Hough, L. Chan, B.J. Goldstein, R. Scalia, Adiponectin deficiency increases leukocyte-endothelium interactions via upregulation of endothelial cell adhesion molecules in vivo. J. Clin. Invest. 117(6), 1718–1726 (2007)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. N. Ouchi, S. Kihara, Y. Arita, M. Nishida, A. Matsuyama, Y. Okamoto, M. Ishigami, H. Kuriyama, K. Kishida, H. Nishizawa, K. Hotta, M. Muraguchi, Y. Ohmoto, S. Yamashita, T. Funahashi, Y. Matsuzawa, Adipocyte-derived plasma protein, adiponectin, suppresses lipid accumulation and class A scavenger receptor expression in human monocyte-derived macrophages. Circulation 103(8), 1057–63 (2001)

    Article  CAS  PubMed  Google Scholar 

  41. M. Karmazyn, D.M. Purdham, V. Rajapurohitam, A. Zeidan, Signaling mechanisms underlying the metabolic and other effects of adipokines on the heart. Cardiovasc. Res. 79(2), 279–286 (2008)

    Article  CAS  PubMed  Google Scholar 

  42. N. Ouchi, R. Shibata, K. Walsh, Cardioprotection by adiponectin. Trends Cardiovasc. Med. 16(5), 141–146 (2006)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. R. Shibata, K. Sato, D.R. Pimentel, Y. Takemura, S. Kihara, K. Ohashi, T. Funahashi, N. Ouchi, K. Walsh, Adiponectin protects against myocardial ischemia-reperfusion injury through AMPK- and COX-2-dependent mechanisms. Nat. Med. 11(10), 1096–1103 (2005)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. R. Shibata, Y. Izumiya, K. Sato, K. Papanicolaou, S. Kihara, W.S. Colucci, F. Sam, N. Ouchi, K. Walsh, Adiponectin protects against the development of systolic dysfunction following myocardial infarction. J. Mol. Cell. Cardiol. 42(6), 1065–1074 (2007)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. R.S. Lindsay, H.E. Resnick, J. Zhu, M.L. Tun, B.V. Howard, Y. Zhang, J. Yeh, L.G. Best, Adiponectin and coronary heart disease: the Strong Heart Study. Arterioscler. Thromb. Vasc. Biol. 25(3), e15–e16 (2005)

    Article  CAS  PubMed  Google Scholar 

  46. G.A. Laughlin, E. Barrett-Connor, S. May, C. Langenberg, Association of adiponectin with coronary heart disease and mortality: the Rancho Bernardo study. Am. J. Epidemiol. 165(2), 164–174 (2007)

    Article  PubMed  Google Scholar 

  47. M. Côté, A. Cartier, A.Q. Reuwer, B.J. Arsenault, I. Lemieux, J.P. Després, N.J. Wareham, J.J. Kastelein, S.M. Boekholdt, K.T. Khaw, Adiponectin and risk of coronary heart disease in apparently healthy men and women (from the EPIC-norfolk prospective population study). Am. J. Cardiol. 108(3), 367–373 (2011)

    Article  PubMed  Google Scholar 

  48. W. Koenig, N. Khuseyinova, J. Baumert, C. Meisinger, H. Löwel, Serum concentrations of adiponectin and risk of type 2 diabetes mellitus and coronary heart disease in apparently healthy middle-aged men: results from the 18-year follow-up of a large cohort from southern Germany. J. Am. Coll. Cardiol. 48(7), 1369–1377 (2006)

    Article  CAS  PubMed  Google Scholar 

  49. D.A. Lawlor, G. Davey Smith, S. Ebrahim, C. Thompson, N. Sattar, Plasma adiponectin levels are associated with insulin resistance, but do not predict future risk of coronary heart disease in women. J. Clin. Endocrinol. Metab. 90(10), 5677–5683 (2005)

    Article  CAS  PubMed  Google Scholar 

  50. L.H. Kuller, G. Grandits, J.D. Cohen, J.D. Neaton, R. Prineas; Multiple Risk Factor Intervention Trial Research Group, Lipoprotein particles, insulin, adiponectin, C-reactive protein and risk of coronary heart disease among men with metabolic syndrome. Atherosclerosis 195(1), 122–128 (2007)

    Article  CAS  PubMed  Google Scholar 

  51. M. Matsumoto, S. Ishikawa, E. Kajii, Association of adiponectin with cerebrovascular disease: a nested case–control study. Stroke 39(2), 323–328 (2008)

    Article  CAS  PubMed  Google Scholar 

  52. N. Sattar, P. Watt, L. Cherry, S. Ebrahim, G. Davey Smith, D.A. Lawlor, High molecular weight adiponectin is not associated with incident coronary heart disease in older women: a nested prospective case–control study. J. Clin. Endocrinol. Metab. 93(5), 1846–1849 (2008)

    Article  CAS  PubMed  Google Scholar 

  53. Y. Hatano, M. Matsumoto, S. Ishikawa, E. Kajii, Plasma adiponectin level and myocardial infarction: the JMS cohort study. J. Epidemiol. 19(2), 49–55 (2009)

    Article  PubMed  PubMed Central  Google Scholar 

  54. A.D. Ogorodnikova, S. Wassertheil-Smoller, P. Mancuso, M.R. Sowers, S.N. Rajpathak, M.A. Allison, A.E. Baird, B. Rodriguez, R.P. Wildman, High-molecular-weight adiponectin and incident ischemic stroke in postmenopausal women: a Women’s Health Initiative Study. Stroke 41(7), 1376–1381 (2010)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. M. Arregui, B. Buijsse, A. Fritsche, R. di Giuseppe, M.B. Schulze, S. Westphal, B. Isermann, H. Boeing, C. Weikert, Adiponectin and risk of stroke: prospective study and meta-analysis. Stroke 45(1), 10–7 (2014)

    Article  CAS  PubMed  Google Scholar 

  56. E. Sook Lee, S.S. Park, E. Kim, Y. Sook Yoon, H.Y. Ahn, C.Y. Park, Y. Ho Yun, S. Woo Oh, Association between adiponectin levels and coronary heart disease and mortality: a systematic review and meta-analysis. Int. J. Epidemiol. 42(4), 1029–1039 (2013)

    Article  PubMed  Google Scholar 

  57. D.A. Kanhai, M.E. Kranendonk, C.S. Uiterwaal, Y. van der Graaf, L.J. Kappelle, F.L. Visseren, Adiponectin and incident coronary heart disease and stroke. A systematic review and meta-analysis of prospective studies. Obes. Rev. 14(7), 555–567 (2013)

    Article  CAS  PubMed  Google Scholar 

  58. H. Cena, M.L. Fonte, G. Turconi, Relationship between smoking and metabolic syndrome. Nutr Rev. 69(12), 745–753 (2011)

    Article  PubMed  Google Scholar 

  59. J.S. Tsai, F.R. Guo, S.C. Chen, B.H. Lue, T.Y. Chiu, C.Y. Chen, S.H. Hung, L.M. Chuang, C.Y. Chen, Smokers show reduced circulating adiponectin levels and adiponectin mRNA expression in peripheral blood mononuclear cells. Atherosclerosis 218(1), 168–173 (2011)

    Article  CAS  PubMed  Google Scholar 

  60. K. Kotani, A. Hazama, A. Hagimoto, K. Saika, M. Shigeta, K. Katanoda, M. Nakamura, Adiponectin and smoking status: a systematic review. J. Atheroscler. Thromb. 19(9), 787–794 (2012)

    Article  CAS  PubMed  Google Scholar 

  61. M. Kryfti, K. Dimakou, M. Toumbis, Z. Daniil, C. Hatzoglou, K.I. Gourgoulianis, Effects of smoking cessation on serum leptin and adiponectin levels. Tob. Induc. Dis. 13, 30 (2015)

    Article  PubMed  PubMed Central  Google Scholar 

  62. F. Simpson, J.P. Whitehead, Adiponectin—it’s all about the modifications. Int. J. Biochem. Cell Biol. 42(6), 785–788 (2010)

    Article  CAS  PubMed  Google Scholar 

  63. Y. Wang, K.S. Lam, M.H. Yau, A. Xu, Post-translational modifications of adiponectin: mechanisms and functional implications. Biochem. J. 409(3), 623–633 (2008)

    Article  CAS  PubMed  Google Scholar 

  64. T. Yamauchi, M. Iwabu, M. Okada-Iwabu, T. Kadowaki, Adiponectin receptors: a review of their structure, function and how they work. Best Pract. Res. Clin. Endocrinol. Metab. 28(1), 15–23 (2014)

    Article  CAS  PubMed  Google Scholar 

  65. C. Hug, J. Wang, N.S. Ahmad, J.S. Bogan, T.S. Tsao, H.F. Lodish, T-cadherin is a receptor for hexameric and high-molecular-weight forms of Acrp30/adiponectin. Proc. Natl Acad. Sci. USA 101(28), 10308–10313 (2004)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. M.S. Denzel, M.C. Scimia, P.M. Zumstein, K. Walsh, P. Ruiz-Lozano, B. Ranscht, T-cadherin is critical for adiponectin-mediated cardioprotection in mice. J. Clin. Invest. 120(12), 4342–4352 (2010)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. C. Menzaghi, M. Xu, L. Salvemini, C. De Bonis, G. Palladino, T. Huang, M. Copetti, Y. Zheng, Y. Li, G. Fini, F.B. Hu, S. Bacci, L. Qi, V. Trischitta, Circulating adiponectin and cardiovascular mortality in patients with type 2 diabetes mellitus: evidence of sexual dimorphism. Cardiovasc. Diabetol. 13, 130 (2014)

    Article  PubMed  PubMed Central  Google Scholar 

  68. H. Nishizawa, I. Shimomura, K. Kishida, N. Maeda, H. Kuriyama, H. Nagaretani, M. Matsuda, H. Kondo, N. Furuyama, S. Kihara, T. Nakamura, Y. Tochino, T. Funahashi, Y. Matsuzawa, Androgens decrease plasma adiponectin, an insulin-sensitizing adipocyte-derived protein. Diabetes 51(9), 2734–41 (2002)

    Article  CAS  PubMed  Google Scholar 

  69. J. Lew, M. Sanghavi, C.R. Ayers, D.K. McGuire, T. Omland, D. Atzler, M.O. Gore, I. Neeland, J.D. Berry, A. Khera, A. Rohatgi, J.A. de Lemos, Sex-based differences in cardiometabolic biomarkers. Circulation 135(6), 544–555 (2017)

    Article  CAS  PubMed  Google Scholar 

  70. A.W. Schoenenberger, D. Pfaff, B. Dasen, A. Frismantiene, P. Erne, T.J. Resink, M. Philippova, Gender-specific associations between circulating T-cadherin and high molecular weight-adiponectin in patients with stable coronary artery disease. PLoS One 10(6), e0131140 (2015)

    Article  PubMed  PubMed Central  Google Scholar 

  71. U. Alehagen, E. Vorkapic, L. Ljungberg, T. Länne, D. Wågsäter, Gender difference in adiponectin associated with cardiovascular mortality. BMC Med. Genet. 16, 37 (2015)

    Article  PubMed  PubMed Central  Google Scholar 

  72. A. Muñoz-Garach, I. Cornejo-Pareja, F.J. Tinahones, Does metabolically healthy obesity exist? Nutrients. 8(6), E320; 1–10 (2016)

  73. S. Ahl, M. Guenther, S. Zhao, R. James, J. Marks, A. Szabo, S. Kidambi, Adiponectin levels differentiate metabolically healthy vs unhealthy among obese and nonobese white individuals. J. Clin. Endocrinol. Metab. 100(11), 4172–4180 (2015)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. A.P. Doumatey, A.R. Bentley, J. Zhou, H. Huang, A. Adeyemo, C.N. Rotimi, Paradoxical hyperadiponectinemia is associated with the metabolically healthy obese (MHO) phenotype in African Americans. J Endocrinol Metab. 2(2), 51–65 (2012)

    CAS  PubMed  PubMed Central  Google Scholar 

  75. J.A. Morrison, C.J. Glueck, S. Daniels, P. Wang, D. Stroop, Paradoxically high adiponectin in obese 16-year-old girls protects against appearance of the metabolic syndrome and its components seven years later. J. Pediatr. 158(2), 208–214.e1 (2011)

    Article  CAS  PubMed  Google Scholar 

  76. J.A. Morrison, C.J. Glueck, S. Daniels, P. Wang, P. Horn, D. Stroop, Paradoxically high adiponectin and the healthy obese phenotype in obese black and white 16-year-old girls. Transl. Res. 156(5), 302–308 (2010)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. C.A. Aguilar-Salinas, E.G. García, L. Robles, D. Riaño, D.G. Ruiz-Gomez, A.C. García-Ulloa, M.A. Melgarejo, M. Zamora, L.E. Guillen-Pineda, R. Mehta, S. Canizales-Quinteros, M.T. Tusie Luna, F.J. Gómez-Pérez, High adiponectin concentrations are associated with the metabolically healthy obese phenotype. J. Clin. Endocrinol. Metab. 93(10), 4075–4079 (2008)

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors would like to thank the ATTICA study group of investigators: Yannis Skoumas, Natasa Katinioti, Labros Papadimitriou, Constantina Masoura, Spiros Vellas, Yannis Lentzas, Manolis Kambaxis, Konstanitna Paliou, Vassiliki Metaxa, Agathi Ntzouvani, Dimitris Mpougatas, Nikolaos Skourlis, Christina Papanikolaou, Aikaterini Kalogeropoulou, Evangelia Pitaraki, Alexandros Laskaris, Mihail Hatzigeorgiou, Athanasios Grekas, and Eleni Kokkou for assistance in the initial physical examination and/or the follow-up evaluation; Efi Tsetsekou for her assistance in psychological evaluation and follow-up evaluation, as well as the laboratory team: Carmen Vassiliadou and George Dedousis (genetic analysis), Marina Toutouza-Giotsa, Constantina Tselika and Sia Poulopoulou (biochemical analysis), and Maria Toutouza for the database management.

Funding

The ATTICA study is supported by research grants from the Hellenic Cardiology Society (HCS2002) and the Hellenic Atherosclerosis Society (HAS2003). Demosthenes Panagiotakos and Ekavi Georgousopoulou have received grants by the Coca-Cola Company.

Author information

Authors and Affiliations

Authors

Consortia

Corresponding author

Correspondence to Demosthenes B. Panagiotakos.

Ethics declarations

Conflict of interest

The authors declare that they have no competing interests.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kyrou, I., Tsantarlioti, O., Panagiotakos, D.B. et al. Adiponectin circulating levels and 10-year (2002–2012) cardiovascular disease incidence: the ATTICA Study. Endocrine 58, 542–552 (2017). https://doi.org/10.1007/s12020-017-1434-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12020-017-1434-y

Keywords

Navigation