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Adipocytokines and the risk of coronary heart disease in healthy middle aged men: the PRIME Study

International Journal of Obesity volume 34, pages 118–126 (2010)Cite this article

Abstract

Background:

Adipokines play an important role in glucose, lipid and lipoprotein metabolisms, as well as in coagulation and inflammatory processes. So far, studies have evaluated the association of individual adipokines with future coronary heart disease (CHD) event and provided mixed results.

Objectives:

We sought to investigate the association of a set of adipocytokines, including total adiponectin, adipsin, resistin, leptin and plasminogen activator inihibitor-1 (PAI-1), with future CHD events in apparently healthy men.

Methods:

We built a nested case–control study within the PRIME Study, a multicenter prospective cohort of 9779 healthy European middle-aged men. Total adiponectin, adipsin, resistin, leptin and PAI-1 were measured in the baseline plasma sample of 617 men who developed a first CHD event (coronary death, myocardial infarction, stable or unstable angina) during 10 years of follow-up and in 1215 study-matched controls, by multiplex assays using commercial kits. HRs for CHD were estimated by conditional logistic regression analysis.

Results:

Median concentrations of total adiponectin, adipsin and resistin were similar in cases and in controls, whereas those of leptin and PAI-1 were higher in cases than in controls, 6.30 vs 5.40 ng ml−1, and 10.09 vs 8.48 IU ml−1, respectively. The risk of future CHD event increased with increasing quintiles of baseline leptin and PAI-1 concentrations only in unadjusted analysis (P-value for trend <0.003 and <0.0001, respectively). However, these associations were no longer significant after adjustment for usual CHD risk factors including hypertension, diabetes, smoking, total cholesterol, triglycerides and HDL cholesterol. Conversely, baseline CRP and IL-6 levels remained associated with CHD risk in multivariate analysis.

Conclusions:

In apparently healthy men, circulating total adiponectin, adipsin, resistin, leptin and PAI-1 were not independent predictors of future CHD event.

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References

  1. Bray GA, Gray DS . Obesity. Part I—Pathogenesis. West J Med 1988; 149: 429–441.

    CAS  PubMed  PubMed Central  Google Scholar 

  2. Berg AH, Scherer PE . Adipose tissue, inflammation, and cardiovascular disease. Circ Res 2005; 96: 939–949.

    Article  CAS  Google Scholar 

  3. Piegas LS, Avezum A, Pereira JC, Neto JM, Hoepfner C, Farran JA et al. Risk factors for myocardial infarction in Brazil. Am Heart J 2003; 146: 331–338.

    Article  Google Scholar 

  4. Walker SP, Rimm EB, Ascherio A, Kawachi I, Stampfer MJ, Willett WC . Body size and fat distribution as predictors of stroke among US men. Am J Epidemiol 1996; 144: 1143–1150.

    Article  CAS  Google Scholar 

  5. Zhang C, Rexrode KM, van Dam RM, Li TY, Hu FB . Abdominal obesity and the risk of all-cause, cardiovascular, and cancer mortality: sixteen years of follow-up in US women. Circulation 2008; 117: 1658–1667.

    Article  Google Scholar 

  6. Kershaw EE, Flier JS . Adipose tissue as an endocrine organ. J Clin Endocrinol Metab 2004; 89: 2548–2556.

    Article  CAS  Google Scholar 

  7. Trayhurn P, Wood IS . Adipokines: inflammation and the pleiotropic role of white adipose tissue. Br J Nutr 2004; 92: 347–355.

    Article  CAS  Google Scholar 

  8. Wajchenberg BL . Subcutaneous and visceral adipose tissue: their relation to the metabolic syndrome. Endocr Rev 2000; 21: 697–738.

    Article  CAS  Google Scholar 

  9. Bastelica D, Morange P, Berthet B, Borghi H, Lacroix O, Grino M et al. Stromal cells are the main plasminogen activator inhibitor-1-producing cells in human fat: evidence of differences between visceral and subcutaneous deposits. Arterioscler Thromb Vasc Biol 2002; 22: 173–178.

    Article  CAS  Google Scholar 

  10. de Jager W, te VH, Prakken BJ, Kuis W, Rijkers GT . Simultaneous detection of 15 human cytokines in a single sample of stimulated peripheral blood mononuclear cells. Clin Diagn Lab Immunol 2003; 10: 133–139.

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Ray CA, Bowsher RR, Smith WC, Devanarayan V, Willey MB, Brandt JT et al. Development, validation, and implementation of a multiplex immunoassay for the simultaneous determination of five cytokines in human serum. J Pharm Biomed Anal 2005; 36: 1037–1044.

    Article  CAS  Google Scholar 

  12. Yarnell JW . The PRIME study: classical risk factors do not explain the severalfold differences in risk of coronary heart disease between France and Northern Ireland Prospective Epidemiological Study of Myocardial Infarction. QJM 1998; 91: 667–676.

    Article  CAS  Google Scholar 

  13. Tunstall-Pedoe H, Kuulasma K, Amouyel P, Arveiler D, Rajakangas AM, Pajak A . Myocardial infarction and coronary deaths in the World Health Organization MONICA Project. Circulation 1994; 90: 583–612.

    Article  CAS  Google Scholar 

  14. Ducimetiere P, Ruidavets JB, Montaye M, Haas B, Yarnell J . Five-year incidence of angina pectoris and other forms of coronary heart disease in healthy men aged 50–59 in France and Northern Ireland: the Prospective Epidemiological Study of Myocardial Infarction (PRIME) Study. Int J Epidemiol 2001; 30: 1057–1062.

    Article  CAS  Google Scholar 

  15. Sattar N, Wannamethee G, Sarwar N, Tchernova J, Cherry L, Wallace AM et al. Adiponectin and coronary heart disease: a prospective study and meta-analysis. Circulation 2006; 114: 623–629.

    Article  CAS  Google Scholar 

  16. Lindsay RS, Resnick HE, Zhu J, Tun ML, Howard BV, Zhang Y et al. Adiponectin and coronary heart disease: the Strong Heart Study. Arterioscler Thromb Vasc Biol 2005; 25: e15–e16.

    Article  CAS  Google Scholar 

  17. Cavusoglu E, Ruwende C, Chopra V, Yanamadala S, Eng C, Clark LT et al. Adiponectin is an independent predictor of all-cause mortality, cardiac mortality, and myocardial infarction in patients presenting with chest pain. Eur Heart J 2006; 27: 2300–2309.

    Article  CAS  Google Scholar 

  18. Lawlor DA, Davey SG, Ebrahim S, Thompson C, Sattar N . Plasma adiponectin levels are associated with insulin resistance, but do not predict future risk of coronary heart disease in women. J Clin Endocrinol Metab 2005; 90: 5677–5683.

    Article  CAS  Google Scholar 

  19. Zoccali C, Mallamaci F, Tripepi G, Benedetto FA, Cutrupi S, Parlongo S et al. Adiponectin, metabolic risk factors, and cardiovascular events among patients with end-stage renal disease. J Am Soc Nephrol 2002; 13: 134–141.

    Article  CAS  Google Scholar 

  20. Costacou T, Zgibor JC, Evans RW, Otvos J, Lopes-Virella MF, Tracy RP et al. The prospective association between adiponectin and coronary artery disease among individuals with type 1 diabetes. The Pittsburgh Epidemiology of Diabetes Complications Study. Diabetologia 2005; 48: 41–48.

    Article  CAS  Google Scholar 

  21. Wolk R, Berger P, Lennon RJ, Brilakis ES, Johnson BD, Somers VK . Plasma leptin and prognosis in patients with established coronary atherosclerosis. J Am Coll Cardiol 2004; 44: 1819–1824.

    Article  CAS  Google Scholar 

  22. Kizer JR, Barzilay JI, Kuller LH, Gottdiener JS . Adiponectin and risk of coronary heart disease in older men and women. J Clin Endocrinol Metab 2008; 93: 3357–3364.

    Article  CAS  Google Scholar 

  23. Schnabel R, Messow CM, Lubos E, Espinola-Klein C, Rupprecht HJ, Bickel C et al. Association of adiponectin with adverse outcome in coronary artery disease patients: results from the AtheroGene study. Eur Heart J 2008; 29: 649–657.

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  25. von Eynatten M, Hamann A, Twardella D, Nawroth PP, Brenner H, Rothenbacher D et al. Atherogenic dyslipidaemia but not total- and high-molecular weight adiponectin are associated with the prognostic outcome in patients with coronary heart disease. Eur Heart J 2008; 29: 1307–1315.

    Article  CAS  Google Scholar 

  26. Laughlin GA, Barrett-Connor E, May S, Langenberg C . Association of adiponectin with coronary heart disease and mortality: the Rancho Bernardo study. Am J Epidemiol 2007; 165: 164–174.

    Article  Google Scholar 

  27. Koenig W, Khuseyinova N, Baumert J, Meisinger C, Löwel H . 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 2006; 48: 1369–1377.

    Article  CAS  Google Scholar 

  28. Kanaya AM, Wassel FC, Vittinghoff E, Havel PJ, Cesari M, Nicklas B et al. Serum adiponectin and coronary heart disease risk in older Black and White Americans. J Clin Endocrinol Metab 2006; 91: 5044–5050.

    Article  CAS  Google Scholar 

  29. Pajvani UB, Hawkins M, Combs TP, Rajala MW, Doebber T, Berger JP et al. Complex distribution, not absolute amount of adiponectin, correlates with thiazolidinedione-mediated improvement in insulin sensitivity. J Biol Chem 2004; 279: 12152–12162.

    Article  CAS  Google Scholar 

  30. Kobayashi H, Ouchi N, Kihara S, Walsh K, Kumada M, Abe Y et al. Selective suppression of endothelial cell apoptosis by the high molecular weight form of adiponectin. Circ Res 2004; 94: e27–e31.

    Article  CAS  Google Scholar 

  31. Sattar N, Watt P, Cherry L, Ebrahim S, Davey Smith G, Lawlor DA . 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 2008; 93: 1846–1849.

    Article  CAS  Google Scholar 

  32. Inoue T, Kotooka N, Morooka T, Komoda H, Uchida T, Aso Y et al. High molecular weight adiponectin as a predictor of long-term clinical outcome in patients with coronary artery disease. Am J Cardiol 2007; 100: 569–574.

    Article  CAS  Google Scholar 

  33. Folsom AR, Aleksic N, Park E, Salomaa V, Juneja H, Wu KK . Prospective study of fibrinolytic factors and incident coronary heart disease: the Atherosclerosis Risk in Communities (ARIC) Study. Arterioscler Thromb Vasc Biol 2001; 21: 611–617.

    Article  CAS  Google Scholar 

  34. Thogersen AM, Jansson JH, Boman K, Nilsson TK, Weinehall L, Huhtasaari F et al. High plasminogen activator inhibitor and tissue plasminogen activator levels in plasma precede a first acute myocardial infarction in both men and women: evidence for the fibrinolytic system as an independent primary risk factor. Circulation 1998; 98: 2241–2247.

    Article  CAS  Google Scholar 

  35. Lowe GD, Yarnell JW, Sweetnam PM, Rumley A, Thomas HF, Elwood PC . Fibrin D-dimer, tissue plasminogen activator, plasminogen activator inhibitor, and the risk of major ischaemic heart disease in the Caerphilly Study. Thromb Haemost 1998; 79: 129–133.

    Article  CAS  Google Scholar 

  36. Cushman M, Lemaitre RN, Kuller LH, Psaty BM, Macy EM, Sharrett AR et al. Fibrinolytic activation markers predict myocardial infarction in the elderly. The Cardiovascular Health Study. Arterioscler Thromb Vasc Biol 1999; 19: 493–498.

    Article  CAS  Google Scholar 

  37. Lara-Castro C, Luo N, Wallace P, Klein RL, Garvey WT . Adiponectin multimeric complexes and the metabolic syndrome trait cluster. Diabetes 2006; 55: 249–259.

    Article  CAS  Google Scholar 

  38. Tian L, Luo N, Klein RL, Chung BH, Garvey WT, Fu Y et al. Adiponectin reduces lipid accumulation in macrophage foam cells. Atherosclerosis 2009; 202: 152–161.

    Article  CAS  Google Scholar 

  39. Spranger J, Kroke A, Mohlig M, Bergmann MM, Ristow M, Boeing H et al. Adiponectin and protection against type 2 diabetes mellitus. Lancet 2003; 361: 226–228.

    Article  CAS  Google Scholar 

  40. Fain JN, Buehrer B, Bahouth SW, Tichansky DS, Madan AK . Comparison of messenger RNA distribution for 60 proteins in fat cells vs the nonfat cells of human omental adipose tissue. Metabolism 2008; 57: 1005–1015.

    Article  CAS  Google Scholar 

  41. Cianflone K, Zhang XJ, Genest Jr J, Sniderman A . Plasma acylation-stimulating protein in coronary artery disease. Arterioscler Thromb Vasc Biol 1997; 17: 1239–1244.

    CAS  PubMed  Google Scholar 

  42. Napolitano A, Lowell BB, Damm D, Leibel RL, Ravussin E, Jimerson DC et al. Concentrations of adipsin in blood and rates of adipsin secretion by adipose tissue in humans with normal, elevated and diminished adipose tissue mass. Int J Obes Relat Metab Disord 1994; 18: 213–218.

    CAS  PubMed  Google Scholar 

  43. Pischon T, Bamberger CM, Kratzsch J, Zyriax BC, Algenstaedt P, Boeing H et al. Association of plasma resistin levels with coronary heart disease in women. Obes Res 2005; 13: 1764–1771.

    Article  CAS  Google Scholar 

  44. Ohmori R, Momiyama Y, Kato R, Taniguchi H, Ogura M, Ayaori M et al. Associations between serum resistin levels and insulin resistance, inflammation, and coronary artery disease. J Am Coll Cardiol 2005; 46: 379–380.

    Article  Google Scholar 

  45. Reilly MP, Lehrke M, Wolfe ML, Rohatgi A, Lazar MA, Rader DJ . Resistin is an inflammatory marker of atherosclerosis in humans. Circulation 2005; 111: 932–939.

    Article  CAS  Google Scholar 

  46. Weikert C, Westphal S, Berger K, Dierkes J, Möhlig M, Spranger J et al. Plasma resistin levels and risk of myocardial infarction and ischemic stroke. J Clin Endocrinol Metab 2008; 93: 2647–2653.

    Article  CAS  Google Scholar 

  47. Kusminski CM, McTernan PG, Kumar S . Role of resistin in obesity, insulin resistance and Type II diabetes. Clin Sci (Lond) 2005; 109: 243–256.

    Article  CAS  Google Scholar 

  48. Patel L, Buckels AC, Kinghorn IJ, Murdock PR, Holbrook JD, Plumpton C et al. Resistin is expressed in human macrophages and directly regulated by PPAR gamma activators. Biochem Biophys Res Commun 2003; 300: 472–476.

    Article  CAS  Google Scholar 

  49. McTernan PG, McTernan CL, Chetty R, Jenner K, Fisher FM, Lauer MN et al. Increased resistin gene and protein expression in human abdominal adipose tissue. J Clin Endocrinol Metab 2002; 87: 2407.

    Article  CAS  Google Scholar 

  50. Bo S, Gambino R, Pagani A, Guidi S, Gentile L, Cassader M et al. Relationships between human serum resistin, inflammatory markers and insulin resistance. Int J Obes (Lond) 2005; 29: 1315–1320.

    Article  CAS  Google Scholar 

  51. Couillard C, Lamarche B, Mauriege P, Cantin B, Dagenais GR, Moorjani S et al. Leptinemia is not a risk factor for ischemic heart disease in men. Prospective results from the Quebec Cardiovascular Study. Diabetes Care 1998; 21: 782–786.

    Article  CAS  Google Scholar 

  52. Piestrzeniewicz K, Luczak K, Goch JH . Value of blood adipose tissue hormones concentration—adiponectin, resistin and leptin in the prediction of major adverse cardiac events (MACE) in 1-year follow-up after primary percutaneous coronary intervention in ST-segment el. Neuro Endocrinol Lett. 2008; 29: 581–588.

    CAS  PubMed  Google Scholar 

  53. Lawlor DA, Smith GD, Kelly A, Sattar N, Ebrahim S . Leptin and coronary heart disease risk: prospective case control study of British women. Obesity (Silver Spring) 2007; 15: 1694–1701.

    Article  CAS  Google Scholar 

  54. Wallace AM, McMahon AD, Packard CJ, Kelly A, Shepherd J, Gaw A et al. Plasma leptin and the risk of cardiovascular disease in the west of Scotland coronary prevention study (WOSCOPS). Circulation 2001; 104: 3052–3056.

    Article  CAS  Google Scholar 

  55. Piemonti L, Calori G, Mercalli A, Lattuada G, Monti P, Garancini MP et al. Fasting plasma leptin, tumor necrosis factor-alpha receptor 2, and monocyte chemoattracting protein 1 concentration in a population of glucose-tolerant and glucose-intolerant women: impact on cardiovascular mortality. Diabetes Care 2003; 26: 2883–2889.

    Article  CAS  Google Scholar 

  56. Mohamed-Ali V, Pinkney JH, Panahloo A, Goodrick S, Coppack SW, Yudkin JS et al. Relationships between plasma leptin and insulin concentrations, but not insulin resistance, in non-insulin-dependent (type 2) diabetes mellitus. Diabet Med 1997; 14: 376–380.

    Article  CAS  Google Scholar 

  57. Smith A, Patterson C, Yarnell J, Rumley A, Ben-Shlomo Y, Lowe G . Which hemostatic markers add to the predictive value of conventional risk factors for coronary heart disease and ischemic stroke? The Caerphilly Study. Circulation 2005; 112: 3080–3087.

    Article  Google Scholar 

  58. Juhan-Vague I, Pyke SD, Alessi MC, Jespersen J, Haverkate F, Thompson SG . Fibrinolytic factors and the risk of myocardial infarction or sudden death in patients with angina pectoris. ECAT Study Group. European Concerted Action on Thrombosis and Disabilities. Circulation 1996; 94: 2057–2063.

    Article  CAS  Google Scholar 

  59. Danesh J, Wheeler JG, Hirschfield GM, Eda S, Eiriksdottir G, Rumley A et al. C-reactive protein and other circulating markers of inflammation in the prediction of coronary heart disease. N Engl J Med 2004; 350: 1387–1397.

    Article  CAS  Google Scholar 

  60. Danesh J, Kaptoge S, Mann AG, Sarwar N, Wood A, Angleman SB et al. Long-term interleukin-6 levels and subsequent risk of coronary heart disease: two new prospective studies and a systematic review. PLoS Med 2008; 5: e78.

    Article  Google Scholar 

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Acknowledgements

We thank the following organizations which allowed the recruitment of the PRIME subjects: the Health screening centers organized by the Social Security of Lille (Institut Pasteur), Strasbourg, Toulouse and Tourcoing; Occupational Medicine Services of Haute-Garonne, of the Urban Community of Strasbourg; the Association Inter-entreprises des Services Médicaux du Travail de Lille et environs; the Comité pour le Développement de la Médecine du Travail; the Mutuelle Générale des PTT du Bas-Rhin; the Laboratoire d'Analyses de l'Institut de Chimie Biologique de la Faculté de Médecine de Strasbourg; the Department of Health (NI) and the Northern Ireland Chest Heart and Stroke Association.

We also thank the members of the event validation Committees: Professor L Guize†, Dr C Morrison, Dr M-T Guillanneuf and Professor M Giroud, and the Alliance Partnership Programme for its financial support.

The PRIME Study was supported by grants from INSERM, Merck, Sharpe and Dohme-Chibret Laboratory, the French Research Agency and the Foundation Heart and Arteries.

Author information

Authors and Affiliations

  1. Université de Lille Nord de France, Lille, France

    G Luc & E Machez

  2. INSERM U545, Faculté de Médecine, Pôle Recherche, University of Lille 2, Lille, France

    G Luc & E Machez

  3. UDSL, Lille, France

    G Luc & E Machez

  4. Institut Pasteur de Lille, Lille, France

    G Luc

  5. INSERM U970, Paris Cardiovascular Research Centre (PAARC); Paris V University,

    J-P Empana, A Bingham & P Ducimetiere

  6. Paris V University, Paris, France

    J-P Empana, A Bingham & P Ducimetiere

  7. INSERM U626, The Laboratory of Hematology, La Timone Hospital, Marseille, France

    P Morange & I Juhan-Vague

  8. Department of Epidemiology and Public Health, Faculté de Médecine, Strasbourg, France

    D Arveiler

  9. Department of Epidemiology, INSERM U558, Toulouse, France

    J Ferrieres

  10. INSERM U744, Institut Pasteur de Lille, Lille, France

    P Amouyel

  11. Department of Epidemiology and Public Health, Queen's University Belfast, Belfast, Northern Ireland

    A Evans & F Kee

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  1. G Luc
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  2. J-P Empana
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  10. A Bingham
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Corresponding author

Correspondence to G Luc.

Additional information

Members of the PRIME study group are listed in the Appendix

Appendix The PRIME Study Group

Appendix The PRIME Study Group

The PRIME Study is organized under an agreement between INSERM and the Merck, Sharpe and Dohme-Chibret Laboratory, with the following participating Laboratories:

The Strasbourg MONICA Project, Laboratoire d'Epidemiologie et de Sante Publique, EA1801, Strasbourg, F-67085, France, and Universite Louis Pasteur, Faculte de Medecine, Strasbourg, F-67085, France (D Arveiler, B Haas); The Toulouse MONICA Project, INSERM U558, and Département d'Epidemiologie, Universite Paul Sabatier—Toulouse Purpan, Toulouse, France (J Ferrières, JB. Ruidavets); The Lille MONICA Project, INSERM, U744, Lille, France, and Institut Pasteur de Lille, Lille, France; Université de Lille 2, Lille, France (P. Amouyel, M. Montaye); The Department of Epidemiology and Public Health, Queen's University, Belfast, Northern Ireland (A Evans, J Yarnell, F Kee), The Department of Atherosclerosis, INSERM, U545, Lille, Institut Pasteur de Lille, Lille, Université de Lille 2, Lille, France (G Luc, JM Bard); The Laboratory of Haematology, INSERM, U626, Marseille, Hôpital La Timone, Marseille, France (I Juhan-Vague, P Morange), The Laboratory of Endocrinology, INSERM U563, Toulouse, France (B Perret); The Vitamin Research Unit, The University of Bern, Bern, Switzerland (F Gey); The Nutrition and Metabolism Group, Centre for Clinical and Population Sciences, Queen's University Belfast, Northern Ireland (Woodside, I Young); The DNA Bank, INSERM U525, Paris, France (F Cambien); The Coordinating Center, INSERM, Unit 909, Villejuif, F-94807, France, and Université Paris V, Paris Cardiovascular Research Centre (PAARC), Paris, F-75015, France (P Ducimetiere, A Bingham)

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Luc, G., Empana, JP., Morange, P. et al. Adipocytokines and the risk of coronary heart disease in healthy middle aged men: the PRIME Study. Int J Obes 34, 118–126 (2010). https://doi.org/10.1038/ijo.2009.204

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