Table of Contents Author Guidelines Submit a Manuscript
International Journal of Endocrinology
Volume 2015 (2015), Article ID 914057, 10 pages
http://dx.doi.org/10.1155/2015/914057
Research Article

Sex Differences in Cardiovascular Mortality in Diabetics and Nondiabetic Subjects: A Population-Based Study (Italy)

1Servizio Interaziendale di Epidemiologia, Azienda Unità Sanitaria Locale, Via Amendola 2, 42122 Reggio Emilia, Italy
2IRCCS Arcispedale Santa Maria Nuova, Viale Umberto I 50, 42123 Reggio Emilia, Italy
3Laboratorio Analisi Chimico Cliniche ed Endocrinologia, IRCCS Arcispedale Santa Maria Nuova, Viale Risorgimento 80, 42123 Reggio Emilia, Italy
4Dipartimento Cure Primarie, Azienda Unità Sanitaria Locale, Via Amendola 2, 42122 Reggio Emilia, Italy
5Dipartimento di Medicina Interna, Ospedale di Montecchio, Azienda Unità Sanitaria Locale, Via Barilla 16, 42027 Montecchio, Italy

Received 3 July 2014; Revised 3 October 2014; Accepted 5 October 2014

Academic Editor: Giuseppina T. Russo

Copyright © 2015 Paola Ballotari et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. International Diabetes Federation, IDF Diabetes Atlas, International Diabetes Federation, Brussels, Belgium, 6th edition, 2013.
  2. ISTAT, “Indagine Multiscopo ‘Aspetti della vita quotidiana’,” in Anno 2011, ISTAT, Rome, Italy, 2012. View at Google Scholar
  3. WHO, “World Health Organisation Study Group on Diabetes Mellitus,” Tech. Rep. 727, WHO, Geneva, Switzerland, 1985. View at Google Scholar
  4. R. J. Jarrett, “Diabetes, hyperglycaemia and arterial disease,” in Complications of Diabetes, H. Keen and R. J. Jarrett, Eds., pp. 179–203, Edward Arnold, London, UK, 2nd edition, 1982. View at Google Scholar
  5. G. L. Booth, M. K. Kapral, K. Fung, and J. V. Tu, “Relation between age and cardiovascular disease in men and women with diabetes compared with non-diabetic people: a population-based retrospective cohort study,” The Lancet, vol. 368, no. 9529, pp. 29–36, 2006. View at Publisher · View at Google Scholar · View at Scopus
  6. S. R. Preis, S.-J. Hwang, S. Coady et al., “Trends in all-cause and cardiovascular disease mortality among women and men with and without diabetes mellitus in the framingham heart study, 1950 to 2005,” Circulation, vol. 119, no. 13, pp. 1728–1735, 2009. View at Publisher · View at Google Scholar · View at Scopus
  7. T. Almdal, H. Scharling, J. S. Jensen, and H. Vestergaard, “The independent effect of type 2 diabetes mellitus on ischemic heart disease, stroke, and death: a population-based study of 13,000 men and women with 20 years of follow-up,” Archives of Internal Medicine, vol. 164, no. 13, pp. 1422–1426, 2004. View at Publisher · View at Google Scholar · View at Scopus
  8. K. N. Barnett, S. A. Ogston, M. E. T. McMurdo, A. D. Morris, and J. M. M. Evans, “A 12-year follow-up study of all-cause and cardiovascular mortality among 10 532 people newly diagnosed with Type 2 diabetes in Tayside, Scotland,” Diabetic Medicine, vol. 27, no. 10, pp. 1124–1129, 2010. View at Publisher · View at Google Scholar · View at Scopus
  9. N. Sarwar, P. Gao, S. R. Seshasai, R. Gobin, S. Kaptoge, and The Emerging Risk Factors Collaboration, “Diabetes mellitus, fasting blood glucose concentration, and risk of vascular disease: a collaborative meta-analysis of 102 prospective studies,” The Lancet, vol. 375, pp. 2215–2222, 2010. View at Google Scholar
  10. S. Vilbergsson, S. Vilbergsson, G. Sigurdsson, G. Sigurdsson, H. Sigvaldason, and N. Sigfusson, “Coronary heart disease mortality amongst non-insulin-dependent diabetic subjects in Iceland: the independent effect of diabetes. The Reykjavik Study 17-year follow up,” Journal of Internal Medicine, vol. 244, no. 4, pp. 309–316, 1998. View at Publisher · View at Google Scholar · View at Scopus
  11. W. J. Butler, L. D. Ostrander Jr., W. J. Carman, and D. E. Lamphiear, “Mortality from coronary heart disease in the tecumseh study. Long-term effect of diabetes mellitus, glucose tolerance and other risk factors,” The American Journal of Epidemiology, vol. 121, no. 4, pp. 541–547, 1985. View at Google Scholar · View at Scopus
  12. J. C. Kleinman, R. P. Donahue, M. I. Harris, F. F. Finucane, J. H. Madans, and D. B. Brock, “Mortality among diabetics in a national sample,” The American Journal of Epidemiology, vol. 128, no. 2, pp. 389–401, 1988. View at Google Scholar · View at Scopus
  13. G.-M. Lin, Y.-H. Li, C.-L. Lin, J.-H. Wang, and C.-L. Han, “Gender differences in the impact of diabetes on mortality in patients with established coronary artery disease: a report from the eastern Taiwan integrated health care delivery system of Coronary Heart Disease (ET-CHD) registry, 1997–2006,” Journal of Cardiology, vol. 61, no. 6, pp. 393–398, 2013. View at Publisher · View at Google Scholar · View at Scopus
  14. A. M. Kanaya, D. Grady, and E. Barrett-Connor, “Explaining the sex difference in coronary heart disease mortality among patients with type 2 diabetes mellitus: a meta-analysis,” Archives of Internal Medicine, vol. 162, no. 15, pp. 1737–1745, 2002. View at Publisher · View at Google Scholar · View at Scopus
  15. B. V. Howard, L. D. Cowan, O. Go, T. K. Welty, D. C. Robbins, and E. T. Lee, “Adverse effects of diabetes on multiple cardiovascular disease risk factors in women: the strong heart study,” Diabetes Care, vol. 21, no. 8, pp. 1258–1265, 1998. View at Publisher · View at Google Scholar · View at Scopus
  16. A. Becker, G. Bos, F. de Vegt et al., “Cardiovascular events in type 2 diabetes: comparison with nondiabetic individuals without and with prior cardiovascular disease: 10-Year follow-up of the Hoorn study,” European Heart Journal, vol. 24, no. 15, pp. 1406–1413, 2003. View at Publisher · View at Google Scholar · View at Scopus
  17. A. Juutilainen, S. Kortelainen, S. Lehto, T. Rönnemaa, K. Pyörälä, and M. Laakso, “Gender difference in the impact of type 2 diabetes on coronary heart disease risk,” Diabetes Care, vol. 27, no. 12, pp. 2898–2904, 2004. View at Publisher · View at Google Scholar · View at Scopus
  18. M. M. Roche and P. P. Wang, “Sex differences in all-cause and cardiovascular mortality, hospitalization for individuals with and without diabetes, and patients with diabetes diagnosed early and late,” Diabetes Care, vol. 36, no. 9, pp. 2582–2590, 2013. View at Publisher · View at Google Scholar · View at Scopus
  19. E. Barrett-Connor, E.-G. V. Giardina, A. K. Gitt, U. Gudat, H. O. Steinberg, and D. Tschoepe, “Women and heart disease: the role of diabetes and hyperglycemia,” Archives of Internal Medicine, vol. 164, no. 9, pp. 934–942, 2004. View at Publisher · View at Google Scholar · View at Scopus
  20. W. B. Kannel, “The Framingham Study: Historical insight on the impact of cardiovascular risk factors in men versus women,” Journal of Gender-Specific Medicine, vol. 5, no. 2, pp. 27–37, 2002. View at Google Scholar · View at Scopus
  21. E. L. Barrett-Connor, B. A. Cohn, D. L. Wingard, and S. L. Edelstein, “Why is diabetes mellitus a stronger risk factor for fatal ischemic heart disease in women than in men? The Rancho Bernardo Study,” Journal of the American Medical Association, vol. 265, no. 5, pp. 627–631, 1991. View at Publisher · View at Google Scholar · View at Scopus
  22. W. L. Lee, A. M. Cheung, D. Cape, and B. Zinman, “Impact of diabetes on coronary artery disease in women and men: a meta-analysis of prospective studies,” Diabetes Care, vol. 23, no. 7, pp. 962–968, 2000. View at Publisher · View at Google Scholar · View at Scopus
  23. R. Huxley, F. Barzi, and M. Woodward, “Adverse effects of diabetes on multiple cardiovascular disease risk factors in women: the strong heart study,” British Medical Journal, vol. 332, no. 7533, pp. 73–76, 2006. View at Publisher · View at Google Scholar · View at Scopus
  24. P. Ballotari, S. Chiatamone Ranieri, M. Vicentini et al., “Building a population-based diabetes register: an Italian experience,” Diabetes Research and Clinical Practice, vol. 103, no. 1, pp. 79–87, 2014. View at Publisher · View at Google Scholar · View at Scopus
  25. R. Gnavi, R. Picariello, L. la Karaghiosoff, G. Costa, and C. Giorda, “Determinants of quality in diabetes care process: the population-based Torino study,” Diabetes Care, vol. 32, no. 11, pp. 1986–1992, 2009. View at Publisher · View at Google Scholar · View at Scopus
  26. ISTAT, Resident population on December 31st, 2012, http://www.demo.istat.it/bil2012/index.html.
  27. N. Sarwar, P. Gao, and S. R. Seshasai, “Diabetes mellitus, fasting blood glucose concentration, and risk of vascular disease: a collaborative meta-analysis of 102 prospective studies,” The Lancet, vol. 375, no. 9733, pp. 2215–2222, 2010. View at Publisher · View at Google Scholar · View at Scopus
  28. T. K. Schramm, G. H. Gislason, L. Køber et al., “Diabetes patients requiring glucose-lowering therapy and nondiabetics with a prior myocardial infarction carry the same cardiovascular risk: a population study of 3.3 million people,” Circulation, vol. 117, no. 15, pp. 1945–1954, 2008. View at Publisher · View at Google Scholar · View at Scopus
  29. K. S. Taylor, C. J. Heneghan, A. J. Farmer et al., “All-cause and cardiovascular mortality in middle-aged people with type 2 diabetes compared with people without diabetes in a large U.K. primary care database,” Diabetes Care, vol. 36, no. 8, pp. 2366–2371, 2013. View at Publisher · View at Google Scholar · View at Scopus
  30. E. W. Gregg, Q. Gu, Y. J. Cheng, K. M. V. Narayan, and C. C. Cowie, “Mortality trends in men and women with diabetes, 1971 to 2000,” Annals of Internal Medicine, vol. 147, no. 3, pp. 149–155, 2007. View at Publisher · View at Google Scholar · View at Scopus
  31. H. H. Newnham and J. Silberberg, “Coronary heart disease. Women's hearts are hard to break,” The Lancet, vol. 349, pp. S13–S16, 1997. View at Google Scholar · View at Scopus
  32. C. E. Walden, R. H. Knopp, P. W. Wahl, K. W. Beach, and E. Strandness Jr., “Sex differences in the effect of diabetes mellitus on lipoprotein triglyceride and cholesterol concentrations,” The New England Journal of Medicine, vol. 311, no. 15, pp. 953–959, 1984. View at Publisher · View at Google Scholar · View at Scopus
  33. R. D. Siegel, A. Cupples, E. J. Schaefer, and P. W. F. Wilson, “Lipoproteins, apolipoproteins, and low-density lipoprotein size among diabetics in the Framingham offspring study,” Metabolism, vol. 45, no. 10, pp. 1267–1272, 1996. View at Publisher · View at Google Scholar · View at Scopus
  34. G. Penno, A. Solini, E. Bonora et al., “Gender differences in cardiovascular disease risk factors, treatments and complications in patients with type 2 diabetes: the RIACE Italian multicentre study,” Journal of Internal Medicine, vol. 274, no. 2, pp. 176–191, 2013. View at Publisher · View at Google Scholar · View at Scopus
  35. M. C. Rossi, M. R. Cristofaro, S. Gentile et al., “Sex disparities in the quality of diabetes care: biological and cultural factors may play a different role for different outcomes: a cross-sectional observational study from the amd annals initiative,” Diabetes Care, vol. 36, no. 10, pp. 3162–3168, 2013. View at Publisher · View at Google Scholar · View at Scopus
  36. M. J. Legato, A. Gelzer, R. Goland et al., “Gender-specific care of the patient with diabetes: review and recommendations,” Gender Medicine, vol. 3, no. 2, pp. 131–158, 2006. View at Publisher · View at Google Scholar · View at Scopus
  37. J. Dallongevillle, D. de Bacquer, J. Heidrich et al., “Gender differences in the implementation of cardiovascular prevention measures after an acute coronary event,” Heart, vol. 96, no. 21, pp. 1744–1749, 2010. View at Publisher · View at Google Scholar · View at Scopus
  38. V. G. Vimalananda, D. R. Miller, M. Palnati, C. L. Christiansen, and B. G. Fincke, “Gender disparities in lipid-lowering therapy among veterans with diabetes,” Womens Health Issues, vol. 21, no. 4 supplement, pp. S176–S181, 2011. View at Publisher · View at Google Scholar · View at Scopus
  39. C. Kim, E. A. Kerr, S. J. Bernstein, and S. L. Krein, “Gender disparities in lipid management: the presence of disparities depends on the quality measure,” American Journal of Managed Care, vol. 12, no. 3, pp. 133–136, 2006. View at Google Scholar · View at Scopus
  40. A. Festa, R. D'Agostino Jr., R. P. Tracy, and S. M. Haffner, “Elevated levels of acute-phase proteins and plasminogen activator inhibitor-1 predict the development of type 2 diabetes: the insulin resistance atherosclerosis study,” Diabetes, vol. 51, no. 4, pp. 1131–1137, 2002. View at Publisher · View at Google Scholar · View at Scopus
  41. L. H. Kuller, R. P. Tracy, J. Shaten, and E. N. Meilahn, “Relation of C-reactive protein and coronary heart disease in the MRFIT nested case-control study,” American Journal of Epidemiology, vol. 144, no. 6, pp. 537–547, 1996. View at Publisher · View at Google Scholar · View at Scopus
  42. J. B. Meigs, F. B. Hu, N. Rifai, and J. E. Manson, “Biomarkers of endothelial dysfunction and risk of type 2 diabetes mellitus,” Journal of the American Medical Association, vol. 291, no. 16, pp. 1978–1986, 2004. View at Publisher · View at Google Scholar · View at Scopus
  43. P. M. Ridker, M. Cushman, M. J. Stampfer, R. P. Tracy, and C. H. Hennekens, “Inflammation, aspirin, and the risk of cardiovascular disease in apparently healthy men,” The New England Journal of Medicine, vol. 336, no. 14, pp. 973–979, 1997. View at Publisher · View at Google Scholar · View at Scopus
  44. M. I. Schmidt, B. B. Duncan, A. R. Sharrett et al., “Markers of inflammation and prediction of diabetes mellitus in adults (Atherosclerosis Risk in Communities study): a cohort study,” The Lancet, vol. 353, no. 9165, pp. 1649–1652, 1999. View at Publisher · View at Google Scholar · View at Scopus
  45. H. O. Steinberg, G. Paradisi, J. Cronin et al., “Type II diabetes abrogates sex differences in endothelial function in premenopausal women,” Circulation, vol. 101, no. 17, pp. 2040–2046, 2000. View at Publisher · View at Google Scholar · View at Scopus
  46. F. Franconi, I. Campesi, S. Occhioni, and G. Tonolo, “Sex-gender differences in diabetes vascular complications and treatment,” Endocrine, Metabolic and Immune Disorders—Drug Targets, vol. 12, no. 2, pp. 179–196, 2012. View at Publisher · View at Google Scholar · View at Scopus
  47. R. P. Donahue, K. Rejman, L. B. Rafalson, J. Dmochowski, S. Stranges, and M. Trevisan, “Sex differences in endothelial function markers before conversion to pre-diabetes: does the clock start ticking earlier among women? The Western New York Study,” Diabetes Care, vol. 30, no. 2, pp. 354–359, 2007. View at Publisher · View at Google Scholar · View at Scopus
  48. M. E. Miller, D. E. Bonds, H. C. Gerstein et al., “The effects of baseline characteristics, glycaemia treatment approach, and glycated haemoglobin concentration on the risk of severe hypoglycaemia: post hoc epidemiological analysis of the ACCORD study,” BMJ, vol. 340, no. 7738, Article ID b5444, p. 138, 2010. View at Publisher · View at Google Scholar · View at Scopus
  49. R. R. Kalyani, M. Lazo, P. Ouyang et al., “Sex differences in diabetes and risk of incident coronary artery disease in healthy young and middle-aged adults,” Diabetes Care, vol. 37, no. 3, pp. 830–838, 2014. View at Publisher · View at Google Scholar · View at Scopus
  50. A. Ferrara, C. M. Mangione, C. Kim et al., “Sex disparities in control and treatment of modifiable cardiovascular disease risk factors among patients with diabetes,” Diabetes Care, vol. 31, no. 1, pp. 69–74, 2008. View at Publisher · View at Google Scholar · View at Scopus
  51. D. J. Wexler, R. W. Grant, J. B. Meigs, D. M. Nathan, and E. Cagliero, “Sex disparities in treatment of cardiac risk factors in patients with type 2 diabetes,” Diabetes Care, vol. 28, no. 3, pp. 514–520, 2005. View at Publisher · View at Google Scholar · View at Scopus
  52. R. Bugiardini, A. T. Yan, R. T. Yan et al., “Factors influencing underutilization of evidence-based therapies in women,” European Heart Journal, vol. 32, no. 11, pp. 1337–1344, 2011. View at Publisher · View at Google Scholar · View at Scopus
  53. S. Poon, S. G. Goodman, R. T. Yan et al., “Bridging the gender gap: insights from a contemporary analysis of sex-related differences in the treatment and outcomes of patients with acute coronary syndromes,” American Heart Journal, vol. 163, no. 1, pp. 66–73, 2012. View at Publisher · View at Google Scholar · View at Scopus
  54. S. H. Saydah, J. Fradkin, and C. C. Cowie, “Poor control of risk factors for vascular disease among adults with previously diagnosed diabetes,” The Journal of the American Medical Association, vol. 291, no. 3, pp. 335–342, 2004. View at Publisher · View at Google Scholar · View at Scopus
  55. J. L. Jarvie and J. M. Foody, “Recognizing and improving health care disparities in the prevention of cardiovascular disease in women,” Current Cardiology Reports, vol. 12, no. 6, pp. 488–496, 2010. View at Publisher · View at Google Scholar · View at Scopus
  56. C. Giorda, R. Picariello, E. Nada et al., “The impact of adherence to screening guidelines and of diabetes clinics referral on morbidity and mortality in diabetes,” PLoS ONE, vol. 7, no. 4, Article ID e33839, 2012. View at Publisher · View at Google Scholar · View at Scopus
  57. J. P. Garg and G. L. Bakris, “Microalbuminuria: marker of vascular dysfunction, risk factor for cardiovascular disease,” Vascular Medicine, vol. 7, no. 1, pp. 35–43, 2002. View at Publisher · View at Google Scholar · View at Scopus
  58. K. Klausen, K. Borch-Johnsen, B. Feldt-Rasmussen et al., “Very low levels of microalbuminuria are associated with increased risk of coronary heart disease and death independently of renal function, hypertension, and diabetes,” Circulation, vol. 110, no. 1, pp. 32–35, 2004. View at Publisher · View at Google Scholar · View at Scopus
  59. G. T. Russo, A. Giandalia, E. L. Romeo et al., “Lipid and non-lipid cardiovascular risk factors in postmenopausal type 2 diabetic women with and without coronary heart disease,” Journal of Endocrinological Investigation, vol. 37, no. 3, pp. 261–268, 2014. View at Publisher · View at Google Scholar · View at Scopus
  60. N. A. Roper, R. W. Bilous, W. F. Kelly, N. C. Unwin, and V. M. Connolly, “Cause-specific mortality in a population with diabetes: South tees diabetes mortality study,” Diabetes Care, vol. 25, no. 1, pp. 43–48, 2002. View at Publisher · View at Google Scholar · View at Scopus
  61. S. L. Seliger, C. Davis, and C. Stehman-Breen, “Gender and the progression of renal disease,” Current Opinion in Nephrology and Hypertension, vol. 10, no. 2, pp. 219–225, 2001. View at Publisher · View at Google Scholar · View at Scopus
  62. S. R. Silbiger and J. Neugarten, “The role of gender in the progression of renal disease,” Advances in Renal Replacement Therapy, vol. 10, no. 1, pp. 3–14, 2003. View at Publisher · View at Google Scholar · View at Scopus
  63. C. J. Schultz, T. Konopelska-Bahu, R. N. Dalton et al., “Microalbuminuria prevalence varies with age, sex, and puberty in children with type 1 diabetes followed from diagnosis in a longitudinal study,” Diabetes Care, vol. 22, no. 3, pp. 495–502, 1999. View at Publisher · View at Google Scholar · View at Scopus
  64. R. Garza, R. Medina, S. Basu, and J. A. Pugh, “Predictors of the rate of renal function decline in non-insulin-dependent diabetes mellitus,” American Journal of Nephrology, vol. 17, no. 1, pp. 59–67, 1997. View at Publisher · View at Google Scholar · View at Scopus
  65. P. Jacobsen, K. Rossing, L. Tarnow et al., “Progression of diabetic nephropathy in normotensive type 1 diabetic patients,” Kidney International, Supplement, vol. 56, no. 71, pp. S101–S105, 1999. View at Publisher · View at Google Scholar · View at Scopus
  66. M. I. Harris, K. M. Flegal, C. C. Cowie et al., “Prevalence of diabetes, impaired fasting glucose, and impaired glucose tolerance in U.S. adults: the Third National Health and Nutrition Examination Survey, 1988–1994,” Diabetes Care, vol. 21, no. 4, pp. 518–524, 1998. View at Publisher · View at Google Scholar · View at Scopus
  67. H. E. Resnick and B. V. Howard, “Diabetes and cardiovascular disease,” Annual Review of Medicine, vol. 53, pp. 245–267, 2002. View at Publisher · View at Google Scholar · View at Scopus
  68. C. Maric, “Sex, diabetes and the kidney,” American Journal of Physiology—Renal Physiology, vol. 296, no. 4, pp. F680–F688, 2009. View at Publisher · View at Google Scholar · View at Scopus
  69. A. Ceriello, S. de Cosmo, S. Gentile et al., Le Monografie Degli Annali AMD 2011 Focus Su: Pattern Assistenziali in Relazione al Livello di Funzionalità Renale, 2012.
  70. A. Solini, G. Penno, E. Bonora et al., “Diverging association of reduced glomerular filtration rate and albuminuria with coronary and noncoronary events in patients with type 2 diabetes: The renal insufficiency and cardiovascular events (RIACE) Italian multicenter study,” Diabetes Care, vol. 35, no. 1, pp. 143–149, 2012. View at Publisher · View at Google Scholar · View at Scopus
  71. M. L. Muiesan, E. Ambrosioni, F. V. Costa et al., “Sex differences in hypertension-related renal and cardiovascular diseases in Italy: the I-DEMAND study,” Journal of Hypertension, vol. 30, no. 12, pp. 2378–2386, 2012. View at Publisher · View at Google Scholar · View at Scopus