Circulating adiponectin and cardiovascular mortality in patients with type 2 diabetes mellitus: Evidence of sexual dimorphism

Cardiovascular Diabetology

Volumn 13, Issue 1, 2014, Pages

  Menzaghi, Claudia ^a   Xu, Min ^b,c   Salvemini, Lucia ^a   De Bonis, Concetta ^a   Palladino, Giuseppe ^a   Huang, Tao ^b   Copetti, Massimiliano ^a   Zheng, Yan ^b   Li, Yanping ^b   Fini, Grazia ^a   Hu, Frank B ^b,d   Bacci, Simonetta ^a   Qi, Lu ^b,d   Trischitta, Vincenzo ^a,e  

^a CASA SOLLIEVO DELLA SOFFERENZA HOSPITAL   (Italy)

^b HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^c SHANGHAI SECOND MEDICAL UNIVERSITY   (China)

^d BRIGHAM AND WOMEN S HOSPITAL   (United States)

^e SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

Adipokines; Paradoxical effect; Prospective studies; Sex linked genes

Indexed keywords

ADIPONECTIN;

ADULT; AGED; ARTICLE; BLOOD SAMPLING; CARDIOVASCULAR MORTALITY; COHORT ANALYSIS; CONTROLLED STUDY; DIABETIC PATIENT; DISEASE ASSOCIATION; FEMALE; HUMAN; MAJOR CLINICAL STUDY; MALE; NON INSULIN DEPENDENT DIABETES MELLITUS; PREDICTIVE VALUE; PROSPECTIVE STUDY; PROTEIN BLOOD LEVEL; SEX DIFFERENCE; BLOOD; CARDIOVASCULAR DISEASE; COMPLICATION; FOLLOW UP; INCIDENCE; MIDDLE AGED; MORTALITY; RISK FACTOR; SEXUAL DEVELOPMENT; VERY ELDERLY;

ADIPONECTIN; ADULT; AGED; AGED, 80 AND OVER; CARDIOVASCULAR DISEASES; DIABETES MELLITUS, TYPE 2; FEMALE; FOLLOW-UP STUDIES; HUMANS; INCIDENCE; MALE; MIDDLE AGED; PROSPECTIVE STUDIES; RISK FACTORS; SEX CHARACTERISTICS;

EID: 84908102501     PISSN: None     EISSN: 14752840     Source Type: Journal    
DOI: 10.1186/s12933-014-0130-y     Document Type: Article

References (51)

1. Seshasai SR, Kaptoge S, Thompson A, Di Angelantonio E, Gao P, Sarwar N, Whincup PH, Mukamal KJ, Gillum RF, Holme I, Njølstad I, Fletcher A, Nilsson P, Lewington S, Collins R, Gudnason V, Thompson SG, Sattar N, Selvin E, Hu FB, Danesh J. Diabetes mellitus, fasting glucose, and risk of cause-specific death. N Engl J Med 2011, 364(9):829-841. 10.1056/NEJMoa1008862, 21366474.
2. Kadowaki T, Yamauchi T. Adiponectin and adiponectin receptors. Endocr Rev 2005, 26(3):439-451. 10.1210/er.2005-0005, 15897298.
3. Turer AT, Scherer PE. Adiponectin: mechanistic insights and clinical implications. Diabetologia 2012, 55(9):2319-2326. 10.1007/s00125-012-2598-x, 22688349.
4. Pischon 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. 10.1001/jama.291.14.1730, 15082700.
5. Persson J, Lindberg K, Gustafsson TP, Eriksson P, Paulsson-Berne G, Lundman P. Low plasma adiponectin concentration is associated with myocardial infarction in young individuals. J Intern Med 2010, 268(2):194-205. 10.1111/j.1365-2796.2010.02247.x, 20528971.
6. Sattar N, Wannamethee G, Sarwar N, Tchernova J, Cherry L, Wallace AM, Danesh J, Whincup PH. Adiponectin and coronary heart disease: a prospective study and meta-analysis. Circulation 2006, 114(7):623-629. 10.1161/CIRCULATIONAHA.106.618918, 16894037.
7. Pischon T, Hu FB, Girman CJ, Rifai N, Manson JE, Rexrode KM, Rimm EB. Plasma total and high molecular weight adiponectin levels and risk of coronary heart disease in women. Atherosclerosis 2011, 219(1):322-329. 10.1016/j.atherosclerosis.2011.07.011, 21813129.
8. Kim JY, Choi EY, Mun HS, Min PK, Yoon YW, Lee BK, Hong BK, Rim SJ, Kwon HM. Usefulness of metabolic syndrome score in the prediction of angiographic coronary artery disease severity according to the presence of diabetes mellitus: relation with inflammatory markers and adipokines. Cardiovasc Diabetol 2013, 12:140. 10.1186/1475-2840-12-140, 24088407.
9. Karas MG, Benkeser D, Arnold AM, Bartz TM, Djousse L, Mukamal KJ, Ix JH, Zieman SJ, Siscovick DS, Tracy RP, Mantzoros CS, Gottdiener JS, De Filippi CR, Kizer JR. Relations of plasma total and high-molecular-weight adiponectin to new-onset heart failure in adults ≥65 years of age (from the Cardiovascular Health study). Am J Cardiol 2014, 113(2):328-334. 10.1016/j.amjcard.2013.09.027, 24169012.
10. Baldasseroni S, Antenore A, Di Serio C, Orso F, Lonetto G, Bartoli N, Foschini A, Marella A, Pratesi A, Scarantino S, Fumagalli S, Monami M, Mannucci E, Marchionni N, Tarantini F. Adiponectin, diabetes and ischemic heart failure: a challenging relationship. Cardiovasc Diabetol 2012, 11:151. 10.1186/1475-2840-11-151, 23249664.
11. Dekker JM, Funahashi T, Nijpels G, Pilz S, Stehouwer CD, Snijder MB, Bouter LM, Matsuzawa Y, Shimomura I, Heine RJ. Prognostic value of adiponectin for cardiovascular disease and mortality. J Clin Endocrinol Metab 2008, 93(4):1489-1496. 10.1210/jc.2007-1436, 18211973.
12. Cavusoglu E, Ruwende C, Chopra V, Yanamadala S, Eng C, Clark LT, Pinsky DJ, Marmur JD. 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(19):2300-2309. 10.1093/eurheartj/ehl153, 16864609.
13. Pilz S, Mangge H, Wellnitz B, Seelhorst U, Winkelmann BR, Tiran B, Boehm BO, März W. Adiponectin and mortality in patients undergoing coronary angiography. J Clin Endocrinol Metab 2006, 91(11):4277-4286. 10.1210/jc.2006-0836, 16912132.
14. Poehls J, Wassel CL, Harris TB, Havel PJ, Swarbrick MM, Cummings SR, Newman AB, Satterfield S, Kanaya AM, Study HA. Association of adiponectin with mortality in older adults: the health, aging, and body composition study. Diabetologia 2009, 52(4):591-595. 10.1007/s00125-009-1261-7, 19159917.
15. Wannamethee SG, Whincup PH, Lennon L, Sattar N. Circulating adiponectin levels and mortality in elderly men with and without cardiovascular disease and heart failure. Arch Intern Med 2007, 167(14):1510-1517. 10.1001/archinte.167.14.1510, 17646605.
16. Lindberg S, Pedersen SH, Møgelvang R, Bjerre M, Frystyk J, Flyvbjerg A, Galatius S, Jensen JS. Usefulness of adiponectin as a predictor of all cause mortality in patients with ST-segment elevation myocardial infarction treated with primary percutaneous coronary intervention. Am J Cardiol 2012, 109(4):492-496. 10.1016/j.amjcard.2011.09.041, 22105783.
17. Kizer JR, Benkeser D, Arnold AM, Mukamal KJ, Ix JH, Zieman SJ, Siscovick DS, Tracy RP, Mantzoros CS, Defilippi CR, Newman AB, Djousse L. Associations of total and high-molecular-weight adiponectin with all-cause and cardiovascular mortality in older persons: the cardiovascular health study. Circulation 2012, 126(25):2951-2961. 10.1161/CIRCULATIONAHA.112.135202, 23159554.
18. Wannamethee SG, Welsh P, Whincup PH, Sawar N, Thomas MC, Gudnarsson V, Sattar N. High adiponectin and increased risk of cardiovascular disease and mortality in asymptomatic older men: does NT-proBNP help to explain this association?. Eur J Cardiovasc Prev Rehabil 2011, 18(1):65-71. 20505514.
19. Persson J, Folkersen L, Ekstrand J, Helleberg J, Gabrielsen A, Lundman P, Hedin U, Paulsson-Berne G. High plasma adiponectin concentration is associated with all-cause mortality in patients with carotid atherosclerosis. Atherosclerosis 2012, 225(2):491-496. 10.1016/j.atherosclerosis.2012.09.036, 23092825.
20. Sook Lee E, Park SS, Kim E, Sook Yoon Y, Ahn HY, Park CY, Ho Yun Y, Woo Oh S. Association between adiponectin levels and coronary heart disease and mortality: a systematic review and meta-analysis. Int J Epidemiol 2013, 42(4):1029-1039. 10.1093/ije/dyt087, 23739486.
21. Wu ZJ, Cheng YJ, Gu WJ, Aung LH. Adiponectin is associated with increased mortality in patients with already established cardiovascular disease: a systematic review and meta-analysis. Metabolism 2014, 63(9):1157-1166. 10.1016/j.metabol.2014.05.001, 24933398.
22. Forsblom C, Thomas MC, Moran J, Saraheimo M, Thorn L, Wadén J, Gordin D, Frystyk J, Flyvbjerg A, Groop PH. Serum adiponectin concentration is a positive predictor of all-cause and cardiovascular mortality in type 1 diabetes. J Intern Med 2011, 270(4):346-355. 10.1111/j.1365-2796.2011.02406.x, 21615808.
23. Alam A, Molnar MZ, Czira ME, Rudas A, Ujszaszi A, Kalantar-Zadeh K, Rosivall L, Mucsi I. Serum adiponectin levels and mortality after kidney transplantation. Clin J Am Soc Nephrol 2013, 8(3):460-467. 10.2215/CJN.04370512, 23220424.
24. Tabák AG, Carstensen M, Witte DR, Brunner EJ, Shipley MJ, Jokela M, Roden M, Kivimäki M, Herder C. Adiponectin trajectories before type 2 diabetes diagnosis: Whitehall II study. Diabetes Care 2012, 35(12):2540-2547. 10.2337/dc11-2263, 22933430.
25. Kollerits B, Fliser D, Heid IM, Ritz E, Kronenberg F, Group MS. Gender-specific association of adiponectin as a predictor of progression of chronic kidney disease: the mild to moderate kidney disease study. Kidney Int 2007, 71(12):1279-1286. 10.1038/sj.ki.5002191, 17457380.
26. Durand JL, Nawrocki AR, Scherer PE, Jelicks LA. Gender differences in adiponectin modulation of cardiac remodeling in mice deficient in endothelial nitric oxide synthase. J Cell Biochem 2012, 113(10):3276-3287. 10.1002/jcb.24206, 22644792.
27. Côté M, Cartier A, Reuwer AQ, Arsenault BJ, Lemieux I, Després JP, Wareham NJ, Kastelein JJ, Boekholdt SM, Khaw KT. Adiponectin and risk of coronary heart disease in apparently healthy men and women (from the EPIC-Norfolk prospective population study). Am J Cardiol 2011, 108(3):367-373. 10.1016/j.amjcard.2011.03.053, 21550577.
28. Krzyzanowska K, Aso Y, Mittermayer F, Inukai T, Brix J, Schernthaner G. High-molecular-weight adiponectin does not predict cardiovascular events in patients with type 2 diabetes. Transl Res 2009, 153(4):199-203. 10.1016/j.trsl.2009.01.009, 19304279.
29. Bacci S, Rizza S, Prudente S, Spoto B, Powers C, Facciorusso A, Pacilli A, Lauro D, Testa A, Zhang YY, Di Stolfo G, Mallamaci F, Tripepi G, Xu R, Mangiacotti D, Aucella F, Lauro R, Gervino EV, Hauser TH, Copetti M, De Cosmo S, Pellegrini F, Zoccali C, Federici M, Doria A, Trischitta V. The ENPP1 Q121 variant predicts major cardiovascular events in high-risk individuals: evidence for interaction with obesity in diabetic patients. Diabetes 2011, 60(3):1000-1007. 10.2337/db10-1300, 21282363.
30. Menzaghi C, Bacci S, Salvemini L, Mendonca C, Palladino G, Fontana A, De Bonis C, Marucci A, Goheen E, Prudente S, Morini E, Rizza S, Kanagaki A, Fini G, Mangiacotti D, Federici M, De Cosmo S, Pellegrini F, Doria A, Trischitta V. Serum resistin, cardiovascular disease and all-cause mortality in patients with type 2 diabetes. PLoS One 2013, 8(6):e64729. 10.1371/journal.pone.0064729, 23755138.
31. Rimm EB, Giovannucci EL, Willett WC, Colditz GA, Ascherio A, Rosner B, Stampfer MJ. Prospective study of alcohol consumption and risk of coronary disease in men. Lancet 1991, 338(8765):464-468. 10.1016/0140-6736(91)90542-W, 1678444.
32. Colditz GA, Manson JE, Hankinson SE. The nurses' health study: 20-year contribution to the understanding of health among women. J Womens Health 1997, 6(1):49-62. 10.1089/jwh.1997.6.49, 9065374.
33. Lin J, Hu FB, Qi L, Curhan GC. Genetic polymorphisms of angiotensin-2 type 1 receptor and angiotensinogen and risk of renal dysfunction and coronary heart disease in type 2 diabetes mellitus. BMC Nephrol 2009, 10:9. 10.1186/1471-2369-10-9, 19327134.
34. Classification and diagnosis of diabetes mellitus and other categories of glucose intolerance. Diabetes 1979, 28(12):1039-1057. 10.2337/diab.28.12.1039.
35. Manson JE, Colditz GA, Stampfer MJ, Willett WC, Krolewski AS, Rosner B, Arky RA, Speizer FE, Hennekens CH. A prospective study of maturity-onset diabetes mellitus and risk of coronary heart disease and stroke in women. Arch Intern Med 1991, 151(6):1141-1147. 10.1001/archinte.1991.00400060077013, 2043016.
36. Report of the expert committee on the diagnosis and classification of diabetes mellitus. Diabetes Care 1997, 20(7):1183-1197.
37. Zhang WL, Lopez-Garcia E, Li TY, Hu FB, Van Dam RM. Coffee consumption and risk of cardiovascular events and all-cause mortality among women with type 2 diabetes. Diabetologia 2009, 52(5):810-817. 10.1007/s00125-009-1311-1, 19266179.
38. Qi L, Li T, Rimm E, Zhang C, Rifai N, Hunter D, Doria A, Hu FB. The +276 polymorphism of the APM1 gene, plasma adiponectin concentration, and cardiovascular risk in diabetic men. Diabetes 2005, 54(5):1607-1610. 10.2337/diabetes.54.5.1607, 15855354.
39. Qi L, Doria A, Manson JE, Meigs JB, Hunter D, Mantzoros CS, Hu FB. Adiponectin genetic variability, plasma adiponectin, and cardiovascular risk in patients with type 2 diabetes. Diabetes 2006, 55(5):1512-1516. 10.2337/db05-1520, 16644713.
40. Qi Q, Workalemahu T, Zhang C, Hu FB, Qi L. Genetic variants, plasma lipoprotein (a) levels, and risk of cardiovascular morbidity and mortality among two prospective cohorts of type 2 diabetes. Eur Heart J 2012, 33(3):325-334. 10.1093/eurheartj/ehr350, 21900290.
41. Menzaghi C, Salvemini L, Paroni G, De Bonis C, Mangiacotti D, Fini G, Doria A, Di Paola R, Trischitta V. Circulating high molecular weight adiponectin isoform is heritable and shares a common genetic background with insulin resistance in nondiabetic White Caucasians from Italy: evidence from a family-based study. J Intern Med 2009, 267(3):287-294. 10.1111/j.1365-2796.2009.02141.x, 19761474.
42. Pischon T, Hotamisligil GS, Rimm EB. Adiponectin: stability in plasma over 36 hours and within-person variation over 1 year. Clin Chem 2003, 49(4):650-652. 10.1373/49.4.650, 12651819.
43. Fine JP, Gray RJ. A proportional hazard model for the subdistribution of a competing risk. J Am Stat Assoc 1999, 94:496-509. 10.1080/01621459.1999.10474144.
44. Singer JR, Palmas W, Teresi J, Weinstock R, Shea S, Luchsinger JA. Adiponectin and all-cause mortality in elderly people with type 2 diabetes. Diabetes Care 2012, 35(9):1858-1863. 10.2337/dc11-2215, 22773703.
45. Sattar N, Nelson SM. Adiponectin, diabetes, and coronary heart disease in older persons: unraveling the paradox. J Clin Endocrinol Metab 2008, 93(9):3299-3301. 10.1210/jc.2008-1435, 18772460.
46. Khan RS, Kato TS, Chokshi A, Chew M, Yu S, Wu C, Singh P, Cheema FH, Takayama H, Harris C, Reyes-Soffer G, Knöll R, Milting H, Naka Y, Mancini D, Schulze PC. Adipose tissue inflammation and adiponectin resistance in patients with advanced heart failure: correction after ventricular assist device implantation. Circ Heart Fail 2012, 5(3):340-348. 10.1161/CIRCHEARTFAILURE.111.964031, 22379072.
47. Van Berendoncks AM, Garnier A, Beckers P, Hoymans VY, Possemiers N, Fortin D, Martinet W, Van Hoof V, Vrints CJ, Ventura-Clapier R, Conraads VM. Functional adiponectin resistance at the level of the skeletal muscle in mild to moderate chronic heart failure. Circ Heart Fail 2010, 3(2):185-194. 10.1161/CIRCHEARTFAILURE.109.885525, 20103776.
48. Pai JK, Pischon T, Ma J, Manson JE, Hankinson SE, Joshipura K, Curhan GC, Rifai N, Cannuscio CC, Stampfer MJ, Rimm EB. Inflammatory markers and the risk of coronary heart disease in men and women. N Engl J Med 2004, 351(25):2599-2610. 10.1056/NEJMoa040967, 15602020.
49. Suzuki S, Sagara K, Otsuka T, Matsuno S, Funada R, Uejima T, Oikawa Y, Koike A, Nagashima K, Kirigaya H, Yajima J, Sawada H, Aizawa T, Yamashita T. Gender-specific relationship between serum uric acid level and atrial fibrillation prevalence. Circ J 2012, 76(3):607-611. 10.1253/circj.CJ-11-1111, 22156312.
50. Haring R, Völzke H, Vasan RS, Felix SB, Nauck M, Dörr M, Wallaschofski H. Sex-specific associations of serum prolactin concentrations with cardiac remodeling: longitudinal results from the Study of Health Pomerania (SHIP). Atherosclerosis 2012, 221(2):570-576. 10.1016/j.atherosclerosis.2012.01.017, 22293228.
51. Kanaya AM, Grady D, Barrett-Connor E. Explaining the sex difference in coronary heart disease mortality among patients with type 2 diabetes mellitus: a meta-analysis. Arch Intern Med 2002, 162(15):1737-1745. 10.1001/archinte.162.15.1737, 12153377.