Skip to main content

Advertisement

SpringerLink
Log in

Diabetic Cardiovascular Disease: Getting to the Heart of the Matter

  • Published:
Journal of Cardiovascular Translational Research Aims and scope Submit manuscript

Abstract

Diabetes is a major risk factor for heart disease, and heart disease is responsible for substantial morbidity and mortality among people living with diabetes. The diabetic metabolic milieu predisposes to aggressive obstructive coronary artery disease that causes heart attacks, heart failure, and death. Furthermore, diabetes can be associated with heart failure, independent of underlying coronary artery disease, hypertension, or valve abnormalities. The pathogenesis of the vascular and myocardial complications of diabetes is, as yet, incompletely understood. Although a number of medical and surgical approaches can improve outcomes in diabetic patients with cardiovascular disease, much remains to be learned in order to optimize approaches to these critical complications.

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

Access this article

Log in via an institution

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. Centers for Disease Control (2011). National Diabetes Fact Sheet. Available from: http://www.cdc.gov/diabetes/pubs/factsheet11.htm.

  2. Kannel, W. B., & McGee, D. L. (1979). Diabetes and cardiovascular disease. The Framingham study. JAMA: The Journal of the American Medical Association, 241(19), 2035–2038.

    Article  CAS  Google Scholar 

  3. Executive 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). (2001). JAMA, 285(19), 2486–2497.

  4. Abbott, R. D., Donahue, R. P., Kannel, W. B., & Wilson, P. W. (1988). The impact of diabetes on survival following myocardial infarction in men vs women. The Framingham study. JAMA: The Journal of the American Medical Association, 260(23), 3456–3460.

    Article  CAS  Google Scholar 

  5. Miettinen, H., Lehto, S., Salomaa, V., Mahonen, M., Niemela, M., Haffner, S. M., Pyorala, K., & Tuomilehto, J. (1998). Impact of diabetes on mortality after the first myocardial infarction. The Finmonica Myocardial Infarction Register Study Group. Diabetes Care, 21(1), 69–75.

    Article  PubMed  CAS  Google Scholar 

  6. Grundy, S. M., Pasternak, R., Greenland, P., Smith, S., Jr., & Fuster, V. (1999). Assessment of cardiovascular risk by use of multiple-risk-factor assessment equations: a statement for healthcare professionals from the american heart association and the american college of cardiology. Circulation, 100(13), 1481–1492.

    Article  PubMed  CAS  Google Scholar 

  7. Malmberg, K., Yusuf, S., Gerstein, H. C., Brown, J., Zhao, F., Hunt, D., Piegas, L., Calvin, J., Keltai, M., & Budaj, A. (2000). Impact of diabetes on long-term prognosis in patients with unstable angina and non-q-wave myocardial infarction: results of the oasis (organization to assess strategies for ischemic syndromes) registry. Circulation, 102(9), 1014–1019.

    Article  PubMed  CAS  Google Scholar 

  8. Smith, J. W., Marcus, F. I., & Serokman, R. (1984). Prognosis of patients with diabetes mellitus after acute myocardial infarction. The American Journal of Cardiology, 54(7), 718–721.

    Article  PubMed  CAS  Google Scholar 

  9. Stone, P. H., Muller, J. E., Hartwell, T., York, B. J., Rutherford, J. D., Parker, C. B., Turi, Z. G., Strauss, H. W., Willerson, J. T., Robertson, T., et al. (1989). The effect of diabetes mellitus on prognosis and serial left ventricular function after acute myocardial infarction: contribution of both coronary disease and diastolic left ventricular dysfunction to the adverse prognosis. The Milis Study Group. Journal of the American College of Cardiology, 14(1), 49–57.

    Article  PubMed  CAS  Google Scholar 

  10. Mak, K. H., Moliterno, D. J., Granger, C. B., Miller, D. P., White, H. D., Wilcox, R. G., Califf, R. M., & Topol, E. J. (1997). Influence of diabetes mellitus on clinical outcome in the thrombolytic era of acute myocardial infarction. GUSTO-I Investigators. Global utilization of streptokinase and tissue plasminogen activator for occluded coronary arteries. Journal of the American College of Cardiology, 30(1), 171–179.

    Article  PubMed  CAS  Google Scholar 

  11. The Bypass Angioplasty Revascularization Investigation (BARI) Investigators. (1996). Comparison of coronary bypass surgery with angioplasty in patients with multivessel disease. N Engl J Med, 335(4), 217-225.

    Google Scholar 

  12. Wingard, D. L., Barrett-Connor, E. L., Scheidt-Nave, C., & McPhillips, J. B. (1993). Prevalence of cardiovascular and renal complications in older adults with normal or impaired glucose tolerance or niddm. A population-based study. Diabetes Care, 16(7), 1022–1025.

    Article  PubMed  CAS  Google Scholar 

  13. Goldberg, I. J. (2001). Clinical review 124: Diabetic dyslipidemia: causes and consequences. Journal of Clinical Endocrinology and Metabolism, 86(3), 965–971.

    Article  PubMed  CAS  Google Scholar 

  14. Ginsberg, H. N. (1996). Diabetic dyslipidemia: basic mechanisms underlying the common hypertriglyceridemia and low hdl cholesterol levels. Diabetes, 45(Suppl 3), S27–S30.

    PubMed  CAS  Google Scholar 

  15. Haffner, S. M., Mykkanen, L., Festa, A., Burke, J. P., & Stern, M. P. (2000). Insulin-resistant prediabetic subjects have more atherogenic risk factors than insulin-sensitive prediabetic subjects: implications for preventing coronary heart disease during the prediabetic state. Circulation, 101(9), 975–980.

    Article  PubMed  CAS  Google Scholar 

  16. Gordon, D. J., & Rifkind, B. M. (1989). High-density lipoprotein—the clinical implications of recent studies. The New England Journal of Medicine, 321(19), 1311–1316.

    Article  PubMed  CAS  Google Scholar 

  17. Austin, M. A., Breslow, J. L., Hennekens, C. H., Buring, J. E., Willett, W. C., & Krauss, R. M. (1988). Low-density lipoprotein subclass patterns and risk of myocardial infarction. JAMA: The Journal of the American Medical Association, 260(13), 1917–1921.

    Article  CAS  Google Scholar 

  18. Watts, G. F., & Karpe, F. (2011). Triglycerides and atherogenic dyslipidaemia: extending treatment beyond statins in the high-risk cardiovascular patient. Heart, 97(5), 350–356.

    Article  PubMed  CAS  Google Scholar 

  19. Jaleel, A., Henderson, G. C., Madden, B. J., Klaus, K. A., Morse, D. M., Gopala, S., & Nair, K. S. (2010). Identification of de novo synthesized and relatively older proteins: accelerated oxidative damage to de novo synthesized apolipoprotein a-1 in type 1 diabetes. Diabetes, 59(10), 2366–2374.

    Article  PubMed  CAS  Google Scholar 

  20. Boemi, M., Leviev, I., Sirolla, C., Pieri, C., Marra, M., & James, R. W. (2001). Serum paraoxonase is reduced in type 1 diabetic patients compared to non-diabetic, first degree relatives; influence on the ability of hdl to protect ldl from oxidation. Atherosclerosis, 155(1), 229–235.

    Article  PubMed  CAS  Google Scholar 

  21. Mastorikou, M., Mackness, M., & Mackness, B. (2006). Defective metabolism of oxidized phospholipid by HDL from people with type 2 diabetes. Diabetes, 55(11), 3099–3103.

    Article  PubMed  CAS  Google Scholar 

  22. Ceriello, A., Taboga, C., Tonutti, L., Quagliaro, L., Piconi, L., Bais, B., Da Ros, R., & Motz, E. (2002). Evidence for an independent and cumulative effect of postprandial hypertriglyceridemia and hyperglycemia on endothelial dysfunction and oxidative stress generation: effects of short- and long-term simvastatin treatment. Circulation, 106(10), 1211–1218.

    Article  PubMed  Google Scholar 

  23. Morishita, R., Nakamura, S., Nakamura, Y., Aoki, M., Moriguchi, A., Kida, I., Yo, Y., Matsumoto, K., Nakamura, T., Higaki, J., & Ogihara, T. (1997). Potential role of an endothelium-specific growth factor, hepatocyte growth factor, on endothelial damage in diabetes. Diabetes, 46(1), 138–142.

    Article  PubMed  CAS  Google Scholar 

  24. Lehto, S., Niskanen, L., Suhonen, M., Ronnemaa, T., & Laakso, M. (1996). Medial artery calcification. A neglected harbinger of cardiovascular complications in non-insulin-dependent diabetes mellitus. Arteriosclerosis, Thrombosis, and Vascular Biology, 16(8), 978–983.

    Article  PubMed  CAS  Google Scholar 

  25. Mazurek, T., Zhang, L., Zalewski, A., Mannion, J. D., Diehl, J. T., Arafat, H., Sarov-Blat, L., O'Brien, S., Keiper, E. A., Johnson, A. G., Martin, J., Goldstein, B. J., & Shi, Y. (2003). Human epicardial adipose tissue is a source of inflammatory mediators. Circulation, 108(20), 2460–2466.

    Article  PubMed  Google Scholar 

  26. Wang, C. P., Hsu, H. L., Hung, W. C., Yu, T. H., Chen, Y. H., Chiu, C. A., Lu, L. F., Chung, F. M., Shin, S. J., & Lee, Y. J. (2009). Increased epicardial adipose tissue (EAT) volume in type 2 diabetes mellitus and association with metabolic syndrome and severity of coronary atherosclerosis. Clinical Endocrinology, 70(6), 876–882.

    Article  PubMed  Google Scholar 

  27. Baker, A. R., Silva, N. F., Quinn, D. W., Harte, A. L., Pagano, D., Bonser, R. S., Kumar, S., & McTernan, P. G. (2006). Human epicardial adipose tissue expresses a pathogenic profile of adipocytokines in patients with cardiovascular disease. Cardiovascular Diabetology, 5, 1.

    Article  PubMed  CAS  Google Scholar 

  28. Marchant, B., Umachandran, V., Stevenson, R., Kopelman, P. G., & Timmis, A. D. (1993). Silent myocardial ischemia: role of subclinical neuropathy in patients with and without diabetes. Journal of the American College of Cardiology, 22(5), 1433–1437.

    Article  PubMed  CAS  Google Scholar 

  29. Kronmal, R. A., Barzilay, J. I., Tracy, R. P., Savage, P. J., Orchard, T. J., & Burke, G. L. (2004). The relationship of fasting serum radioimmune insulin levels to incident coronary heart disease in an insulin-treated diabetic cohort. Journal of Clinical Endocrinology and Metabolism, 89(6), 2852–2858.

    Article  PubMed  CAS  Google Scholar 

  30. Gerstein, H. C., Miller, M. E., Byington, R. P., Goff, D. C., Jr., Bigger, J. T., Buse, J. B., Cushman, W. C., Genuth, S., Ismail-Beigi, F., Grimm, R. H., Jr., Probstfield, J. L., Simons-Morton, D. G., & Friedewald, W. T. (2008). Effects of intensive glucose lowering in type 2 diabetes. The New England Journal of Medicine, 358(24), 2545–2559.

    Article  PubMed  CAS  Google Scholar 

  31. Patel, A., MacMahon, S., Chalmers, J., Neal, B., Billot, L., Woodward, M., Marre, M., Cooper, M., Glasziou, P., Grobbee, D., Hamet, P., Harrap, S., Heller, S., Liu, L., Mancia, G., Mogensen, C. E., Pan, C., Poulter, N., Rodgers, A., Williams, B., Bompoint, S., de Galan, B. E., Joshi, R., & Travert, F. (2008). Intensive blood glucose control and vascular outcomes in patients with type 2 diabetes. The New England Journal of Medicine, 358(24), 2560–2572.

    Article  PubMed  CAS  Google Scholar 

  32. Skyler, J. S., Bergenstal, R., Bonow, R. O., Buse, J., Deedwania, P., Gale, E. A., Howard, B. V., Kirkman, M. S., Kosiborod, M., Reaven, P., & Sherwin, R. S. (2009). Intensive glycemic control and the prevention of cardiovascular events: implications of the accord, advance, and va diabetes trials: a position statement of the American Diabetes Association and a scientific statement of the American College of Cardiology Foundation and the American Heart Association. Circulation, 119(2), 351–357.

    Article  PubMed  Google Scholar 

  33. Gaede, P., Vedel, P., Larsen, N., Jensen, G. V., Parving, H. H., & Pedersen, O. (2003). Multifactorial intervention and cardiovascular disease in patients with type 2 diabetes. The New England Journal of Medicine, 348(5), 383–393.

    Article  PubMed  Google Scholar 

  34. Goldberg, R. B., Mellies, M. J., Sacks, F. M., Moye, L. A., Howard, B. V., Howard, W. J., Davis, B. R., Cole, T. G., Pfeffer, M. A., & Braunwald, E. (1998). Cardiovascular events and their reduction with pravastatin in diabetic and glucose-intolerant myocardial infarction survivors with average cholesterol levels: subgroup analyses in the Cholesterol and Recurrent Events (CARE) trial. The Care Investigators. Circulation, 98(23), 2513–2519.

    Article  PubMed  CAS  Google Scholar 

  35. The Scandinavian Simvastatin Survival Study (4s) (1994). Randomised trial of cholesterol lowering in 4444 patients with coronary heart disease. Lancet, 344(8934), 1383–1389.

    Google Scholar 

  36. Pyorala, K., Pedersen, T. R., Kjekshus, J., Faergeman, O., Olsson, A. G., & Thorgeirsson, G. (1997). Cholesterol lowering with simvastatin improves prognosis of diabetic patients with coronary heart disease. A subgroup analysis of the Scandinavian Simvastatin Survival Study (4s). Diabetes Care, 20(4), 614–620.

    Article  PubMed  CAS  Google Scholar 

  37. The Long-Term Intervention with Pravastatin in Ischaemic Disease (LIPID) Study Group. (1998). Prevention of cardiovascular events and death with pravastatin in patients with coronary heart disease and a broad range of initial cholesterol levels. N Engl J Med, 339(19), 1349–1357.

    Google Scholar 

  38. Heart Outcomes Prevention Evaluation Study Investigators. (2000). Effects of ramipril on cardiovascular and microvascular outcomes in people with diabetes mellitus: results of the HOPE Study and Micro-HOPE Substudy. Lancet 355(9200), 253–259.

    Google Scholar 

  39. Lindholm, L. H., Ibsen, H., Dahlof, B., Devereux, R. B., Beevers, G., de Faire, U., Fyhrquist, F., Julius, S., Kjeldsen, S. E., Kristiansson, K., Lederballe-Pedersen, O., Nieminen, M. S., Omvik, P., Oparil, S., Wedel, H., Aurup, P., Edelman, J., & Snapinn, S. (2002). Cardiovascular morbidity and mortality in patients with diabetes in the Losartan Intervention for Endpoint Reduction in Hypertension Study (LIFE): a randomised trial against atenolol. Lancet, 359(9311), 1004–1010.

    Article  PubMed  CAS  Google Scholar 

  40. Investigators, B. A. R. I. (2007). The final 10-year follow-up results from the BARI randomized trial. Journal of the American College of Cardiology, 49(15), 1600–1606.

    Article  Google Scholar 

  41. Banning, A. P., Westaby, S., Morice, M. C., Kappetein, A. P., Mohr, F. W., Berti, S., Glauber, M., Kellett, M. A., Kramer, R. S., Leadley, K., Dawkins, K. D., & Serruys, P. W. (2010). Diabetic and nondiabetic patients with left main and/or 3-vessel coronary artery disease: comparison of outcomes with cardiac surgery and paclitaxel-eluting stents. Journal of the American College of Cardiology, 55(11), 1067–1075.

    Article  PubMed  CAS  Google Scholar 

  42. Chaitman, B. R., Hardison, R. M., Adler, D., Gebhart, S., Grogan, M., Ocampo, S., Sopko, G., Ramires, J. A., Schneider, D., & Frye, R. L. (2009). The bypass angioplasty revascularization investigation 2 diabetes randomized trial of different treatment strategies in type 2 diabetes mellitus with stable ischemic heart disease: impact of treatment strategy on cardiac mortality and myocardial infarction. Circulation, 120(25), 2529–2540.

    Article  PubMed  CAS  Google Scholar 

  43. Levy, D., Larson, M. G., Vasan, R. S., Kannel, W. B., & Ho, K. K. (1996). The progression from hypertension to congestive heart failure. JAMA: The Journal of the American Medical Association, 275(20), 1557–1562.

    Article  CAS  Google Scholar 

  44. Owan, T. E., Hodge, D. O., Herges, R. M., Jacobsen, S. J., Roger, V. L., & Redfield, M. M. (2006). Trends in prevalence and outcome of heart failure with preserved ejection fraction. The New England Journal of Medicine, 355(3), 251–259.

    Article  PubMed  CAS  Google Scholar 

  45. Havranek, E. P., Masoudi, F. A., Westfall, K. A., Wolfe, P., Ordin, D. L., & Krumholz, H. M. (2002). Spectrum of heart failure in older patients: results from the national heart failure project. American Heart Journal, 143(3), 412–417.

    Article  PubMed  Google Scholar 

  46. Nichols, G. A., Hillier, T. A., Erbey, J. R., & Brown, J. B. (2001). Congestive heart failure in type 2 diabetes: prevalence, incidence, and risk factors. Diabetes Care, 24(9), 1614–1619.

    Article  PubMed  CAS  Google Scholar 

  47. Kannel, W. B., Hjortland, M., & Castelli, W. P. (1974). Role of diabetes in congestive heart failure: the Framingham Study. The American Journal of Cardiology, 34, 29–34.

    Article  PubMed  CAS  Google Scholar 

  48. Hamby, R. I., Zoneraich, S., & Sherman, S. (1974). Diabetic cardiomyopathy. JAMA: The Journal of the American Medical Association, 229, 1749–1754.

    Article  CAS  Google Scholar 

  49. Griffin, J. A., Osborn, B. W., & Smithline, H. A. (2005). The impact of diabetes on hospital admissions, length of stay and mortality in emergency department patients with acute decompensated heart failure without ischemia. Academic Emergency Medicine, 12, s97.

    Article  Google Scholar 

  50. Das, S. R., Drazner, M. H., Yancy, C. W., Stevenson, L. W., Gersh, B. J., & Dries, D. L. (2004). Effects of diabetes mellitus and ischemic heart disease on the progression from asymptomatic left ventricular dysfunction to symptomatic heart failure: a retrospective analysis from the Studies of Left Ventricular Dysfunction (SOLVD) Prevention trial. American Heart Journal, 148(5), 883–888.

    Article  PubMed  Google Scholar 

  51. Fein, F. S., & Sonnenblick, E. H. (1985). Diabetic cardiomyopathy. Progress in Cardiovascular Diseases, 27(4), 255–270.

    Article  PubMed  CAS  Google Scholar 

  52. Fein, F. S. (1990). Diabetic cardiomyopathy. Diabetes Care, 13(11), 1169–1179.

    Article  PubMed  CAS  Google Scholar 

  53. Fischer, M., Baessler, A., Hense, H. W., Hengstenberg, C., Muscholl, M., Holmer, S., Doring, A., Broeckel, U., Riegger, G., & Schunkert, H. (2003). Prevalence of left ventricular diastolic dysfunction in the community. Results from a doppler echocardiographic-based survey of a population sample. European Heart Journal, 24, 320–328.

    Article  PubMed  CAS  Google Scholar 

  54. Boyer, J. K., Thanigaraj, H., Schectman, K. B., & Perez, J. E. (2004). Prevalence of ventricular diastolic dysfunction in asymptomatic, normotensive patients with diabetes mellitus. The American Journal of Cardiology, 93, 870–875.

    Article  PubMed  Google Scholar 

  55. Di Bonito, P., Cuomo, S., Moio, N., Sibilio, G., Sabatini, D., Quattrin, S., & Capaldo, B. (1996). Diastolic dysfunction in patients with non-insulin-dependent diabetes mellitus of short duration. Diabetic Medicine, 13(4), 321–324.

    Article  PubMed  Google Scholar 

  56. Schannwell, C. M., Schneppenheim, M., Perings, S., Plehn, G., & Strauer, B. E. (2002). Left ventricular diastolic dysfunction as an early manifestation of diabetic cardiomyopathy. Cardiology, 98, 33–39.

    Article  PubMed  CAS  Google Scholar 

  57. Peterson, L. R., Waggoner, A. D., De las Fuentes, L., Schechtman, K. B., McGill, J. B., Gropler, R. J., & Davila-Roman, V. G. (2006). Alterations in left ventricular structure and function in type-1 diabetics: a focus on left atrial contribution to function. Journal of the American Society of Echocardiography, 19(6), 749–755.

    Article  PubMed  Google Scholar 

  58. Andersen, N. H., Poulsen, S. H., Eiskjaer, H., Poulsen, P. L., & Mogensen, C. E. (2003). Decreased left ventricular longitudinal contraction in normotensive and normoalbuminuric patients with type ii diabetes mellitus: a Doppler tissue tracking and strain rate echocardiography study. Clinical Science (London, England), 105(1), 59–66.

    Article  CAS  Google Scholar 

  59. Ernande, L., Rietzschel, E. R., Bergerot, C., De Buyzere, M. L., Schnell, F., Groisne, L., Ovize, M., Croisille, P., Moulin, P., Gillebert, T. C., & Derumeaux, G. (2010). Impaired myocardial radial function in asymptomatic patients with type 2 diabetes mellitus: a speckle-tracking imaging study. Journal of the American Society of Echocardiography, 23(12), 1266–1272.

    Article  PubMed  Google Scholar 

  60. Ng, A. C., Delgado, V., Bertini, M., van der Meer, R. W., Rijzewijk, L. J., Shanks, M., Nucifora, G., Smit, J. W., Diamant, M., Romijn, J. A., de Roos, A., Leung, D. Y., Lamb, H. J., & Bax, J. J. (2009). Findings from left ventricular strain and strain rate imaging in asymptomatic patients with type 2 diabetes mellitus. The American Journal of Cardiology, 104(10), 1398–1401.

    Article  PubMed  Google Scholar 

  61. Fang, Z. Y., Schull-Meade, R., Downey, M., Prins, J., & Marwick, T. H. (2005). Determinants of subclinical diabetic heart disease. Diabetologia, 48(2), 394–402.

    Article  PubMed  CAS  Google Scholar 

  62. Carugo, S., Giannattasio, C., Calchera, I., Paleari, F., Gorgoglione, M. G., Grappiolo, A., Gamba, P., Rovaris, G., Failla, M., & Mancia, G. (2001). Progression of functional and structural cardiac alterations in young normotensive uncomplicated patients with type 1 diabetes mellitus. Journal of Hypertension, 19(9), 1675–1680.

    Article  PubMed  CAS  Google Scholar 

  63. Galderisi, M., Anderson, K. M., Wilson, P. W., & Levy, D. (1991). Echocardiographic evidence for the existence of a distinct diabetic cardiomyopathy (the Framingham Heart Study). The American Journal of Cardiology, 68(1), 85–89.

    Article  PubMed  CAS  Google Scholar 

  64. Tenenbaum, A., Fisman, E. Z., Schwammenthal, E., Adler, Y., Benderly, M., Motro, M., & Shemesh, J. (2003). Increased prevalence of left ventricular hypertrophy in hypertensive women with type 2 diabetes mellitus. Cardiovascular Diabetology, 2, 4.

    Article  PubMed  Google Scholar 

  65. Lee, M., Gardin, J. M., Lynch, J. C., Smith, V. E., Tracy, R. P., Savage, P. J., Szklo, M., & Ward, B. J. (1997). Diabetes mellitus and echocardiographic left ventricular function in free-living elderly men and women: the Cardiovascular Health Study. American Heart Journal, 133, 36–43.

    Article  PubMed  CAS  Google Scholar 

  66. Devereux, R. B., Roman, M. J., Paranicas, M., O'Grady, M. J., Lee, E. T., Welty, T. K., Fabsitz, R. R., Robbins, D., Rhoades, E. R., & Howard, B. V. (2000). Impact of diabetes on cardiac structure and function: the Strong Heart Study. Circulation, 101(19), 2271–2276.

    Article  PubMed  CAS  Google Scholar 

  67. Zarich, S. W., Arbuckle, B. E., Cohen, L. R., Roberts, M., & Nesto, R. W. (1988). Diastolic abnormalities in young asymptomatic diabetic patients assessed by pulsed doppler echocardiography. Journal of the American College of Cardiology, 12, 114–120.

    Article  PubMed  CAS  Google Scholar 

  68. Zarich, S. W., & Nesto, R. W. (1989). Diabetic cardiomyopathy. American Heart Journal, 118, 1000–1012.

    Article  PubMed  CAS  Google Scholar 

  69. Celentano, A., Vaccaro, O., Tammaro, P., Galderisi, M., Crivaro, M., Oliviero, M., Imperatore, G., Palmieri, V., Iovino, B., & Riccardi, G. (1995). Early abnormalities of cardiac function in non-insulin-dependent diabetes mellitus and impaired glucose tolerance. The American Journal of Cardiology, 76, 1173–1176.

    Article  PubMed  CAS  Google Scholar 

  70. Mustonen, J. N., Uusitupa, M. I., Laakso, M., Vanninen, E., Lansimies, E., Kuikka, J. T., & Pyorala, K. (1994). Left ventricular systolic function in middle-aged patients with diabetes mellitus. The American Journal of Cardiology, 73, 1202–1208.

    Article  PubMed  CAS  Google Scholar 

  71. From, A. M., Scott, C. G., & Chen, H. H. (2010). The development of heart failure in patients with diabetes mellitus and pre-clinical diastolic dysfunction: a population-based study. Journal of the American College of Cardiology, 55(4), 300–305.

    Article  PubMed  Google Scholar 

  72. Takeda, Y., Sakata, Y., Mano, T., Ohtani, T., Kamimura, D., Tamaki, S., Omori, Y., Tsukamoto, Y., Aizawa, Y., Komuro, I., & Yamamoto, K. (2011). Competing risks of heart failure with preserved ejection fraction in diabetic patients. European Journal of Heart Failure, 13(6), 664–669.

    Article  PubMed  Google Scholar 

  73. Parissis, J. T., Rafouli-Stergiou, P., Mebazaa, A., Ikonomidis, I., Bistola, V., Nikolaou, M., Meas, T., Delgado, J., Vilas-Boas, F., Paraskevaidis, I., Anastasiou-Nana, M., & Follath, F. (2012). Acute heart failure in patients with diabetes mellitus: clinical characteristics and predictors of in-hospital mortality. Int J Cardiol, 157, 108–113.

    Google Scholar 

  74. Masoudi, F. A., & Inzucchi, S. E. (2007). Diabetes mellitus and heart failure: epidemiology, mechanisms, and pharmacotherapy. The American Journal of Cardiology, 99(4A), 113B–132B.

    Article  PubMed  CAS  Google Scholar 

  75. Komajda, M., Carson, P. E., Hetzel, S., McKelvie, R., McMurray, J., Ptaszynska, A., Zile, M. R., Demets, D., & Massie, B. M. (2011). Factors associated with outcome in heart failure with preserved ejection fraction: findings from the Irbesartan in Heart Failure with Preserved Ejection Fraction Study (I-Preserve). Circulation. Heart Failure, 4(1), 27–35.

    Article  PubMed  CAS  Google Scholar 

  76. Davis, B. R., Piller, L. B., Cutler, J. A., Furberg, C., Dunn, K., Franklin, S., Goff, D., Leenen, F., Mohiuddin, S., Papademetriou, V., Proschan, M., Ellsworth, A., Golden, J., Colon, P., & Crow, R. (2006). Role of diuretics in the prevention of heart failure: the Antihypertensive and Lipid-Lowering Treatment to Prevent Heart Attack Trial. Circulation, 113(18), 2201–2210.

    Article  PubMed  CAS  Google Scholar 

  77. Domanski, M., Krause-Steinrauf, H., Deedwania, P., Follmann, D., Ghali, J. K., Gilbert, E., Haffner, S., Katz, R., Lindenfeld, J., Lowes, B. D., Martin, W., McGrew, F., & Bristow, M. R. (2003). The effect of diabetes on outcomes of patients with advanced heart failure in the BEST trial. Journal of the American College of Cardiology, 42(5), 914–922.

    Article  PubMed  Google Scholar 

  78. Giacco, F., & Brownlee, M. (2010). Oxidative stress and diabetic complications. Circulation Research, 107(9), 1058–1070.

    Article  PubMed  CAS  Google Scholar 

  79. Perez, J. E., McGill, J. B., Santiago, J. V., Schechtman, K. B., Waggoner, A. D., Miller, J. G., & Sobel, B. E. (1992). Abnormal myocardial acoustic properties in diabetic patients and their correlation with the severity of disease. Journal of the American College of Cardiology, 19, 1154–1162.

    Article  PubMed  CAS  Google Scholar 

  80. Barzilay, J. I., Kronmal, R. A., Gottdiener, J. S., Smith, N. L., Burke, G. L., Tracy, R., Savage, P. J., & Carlson, M. (2004). The association of fasting glucose levels with congestive heart failure in diabetic adults > or =65 years: the Cardiovascular Health Study. Journal of the American College of Cardiology, 43(12), 2236–2241.

    Article  PubMed  CAS  Google Scholar 

  81. Iribarren, C., Karter, A. J., Go, A. S., Ferrara, A., Liu, J. Y., Sidney, S., & Selby, J. V. (2001). Glycemic control and heart failure among adult patients with diabetes. Circulation, 103(22), 2668–2673.

    Article  PubMed  CAS  Google Scholar 

  82. Frustaci, A., Kajstura, J., Chimenti, C., Jakoniuk, I., Leri, A., Maseri, A., Nadal-Ginard, B., & Anversa, P. (2000). Myocardial cell death in human diabetes. Circulation Research, 87, 1123–1132.

    Article  PubMed  CAS  Google Scholar 

  83. Anderson, E. J., Kypson, A. P., Rodriguez, E., Anderson, C. A., Lehr, E. J., & Neufer, P. D. (2009). Substrate-specific derangements in mitochondrial metabolism and redox balance in the atrium of the type 2 diabetic human heart. Journal of the American College of Cardiology, 54(20), 1891–1898.

    Article  PubMed  CAS  Google Scholar 

  84. Young, M., McNulty, P., & Taegtmeyer, H. (2002). Adaptation and maladaptation of the heart in diabetes: part II: potential mechanisms. Circulation, 105, 1861–1870.

    Article  PubMed  CAS  Google Scholar 

  85. Horowitz, J., & Klein, S. (2000). Whole body and abdominal lipolytic sensitivity to epinephrine is suppressed in upper body obese women. American Journal of Physiology, 278, E1144–E1152.

    PubMed  CAS  Google Scholar 

  86. Groop, L. C., Bonadonna, R. C., Del Prato, S., Ratheiser, K., Zyck, K., Ferrannini, E., & DeFronzo, R. A. (1989). Glucose and free fatty acid metabolism in non-insulin dependent diabetes mellitus: evidence for multiple sites of insulin resistance. The Journal of Clinical Investigation, 84, 205–213.

    Article  PubMed  CAS  Google Scholar 

  87. Miles, J. M., Wooldridge, D., Grellner, W. J., Windsor, S., Isley, W. L., Klein, S., & Harris, W. S. (2003). Nocturnal and postprandial free fatty acid kinetics in normal and type 2 diabetic subjects. Diabetes, 52, 675–681.

    Article  PubMed  CAS  Google Scholar 

  88. Peterson, L. R., Herrero, P., Schechtman, K. B., Racette, S. B., Waggoner, A. D., Kisrieva-Ware, Z., Dence, C., Klein, S., Marsala, J., Meyer, T., & Gropler, R. J. (2004). Effect of obesity and insulin resistance on myocardial substrate metabolism and efficiency in young women. Circulation, 109, 2191–2196.

    Article  PubMed  Google Scholar 

  89. Herrero, P., Peterson, L. R., McGill, J. B., Matthew, S., Lesniak, D., Dence, C., & Gropler, R. J. (2006). Increased myocardial fatty acid metabolism in patients with type 1 diabetes mellitus. Journal of the American College of Cardiology, 47(3), 598–604.

    Article  PubMed  CAS  Google Scholar 

  90. Diamant, M., Lamb, H., Groeneveld, Y., Endert, E., Smit, J., Bax, J., Romijn, J., de Roos, A., & Radder, J. (2003). Diastolic dysfunction is associated with altered myocardial metabolism in asymptomatic normotensive patients with well-controlled type 2 diabetes mellitus. Journal of the American College of Cardiology, 42, 328–335.

    Article  PubMed  CAS  Google Scholar 

  91. Scheuermann-Freestone, M., Madsen, P. L., Manners, D., Blamire, A. M., Buckingham, R. E., Styles, P., Radda, G. K., Neubauer, S., & Clarke, K. (2003). Abnormal cardiac and skeletal muscle energy metabolism in patients with type 2 diabetes. Circulation, 107, 3040–3046.

    Article  PubMed  CAS  Google Scholar 

  92. Szczepaniak, L. S., Dibbins, R. L., Metzger, G. J., Sartoni-D'Ambrosia, G., Arbique, D., Vongpatanasin, W., Unger, R., & Victor, R. G. (2003). Myocardial triglycerides and systolic function in humans: in vivo evaluation by localized proton spectroscopy and cardiac imaging. Magnetic Resonance in Medicine, 49, 417–423.

    Article  PubMed  CAS  Google Scholar 

  93. Alavaikko, M., Elfving, R., Hirvonen, E. J., & Jarvi, J. (1973). Triglycerides, cholesterol, and phospholipids in normal heart papillary muscle and inpatients suffering from diabetes, cholelithiasis, hypertension, and coronary atheroma. Journal of Clinical Pathology, 26, 285–293.

    Article  PubMed  CAS  Google Scholar 

  94. Sharma, S., Adrogue, J. V., Golfman, L., Uray, I., Lemm, J., Youker, K., Noon, G. P., Frazier, O. H., & Taegtmeyer, H. (2004). Intramyocardial lipid accumulation in the failing human heart resembles the lipotoxic rat heart. The FASEB Journal, 18, 1692–1700.

    Article  CAS  Google Scholar 

  95. Leinonen, J., Lehtimaki, T., Toyokuni, S., Okada, K., Tanaka, T., Hiai, H., Ochi, H., Laippala, P., Rantalaiho, V., Wirta, O., Pasternack, A., & Alho, H. (1997). New biomarker evidence of oxidative DNA damage in patients with non-insulin-dependent diabetes mellitus. FEBS Letters, 417(1), 150–152.

    Article  PubMed  CAS  Google Scholar 

  96. Murakami, K., Kondo, T., Ohtsuka, Y., Fujiwara, Y., Shimada, M., & Kawakami, Y. (1989). Impairment of glutathione metabolism in erythrocytes from patients with diabetes mellitus. Metabolism, 38(8), 753–758.

    Article  PubMed  CAS  Google Scholar 

  97. Nourooz-Zadeh, J., Tajaddini-Sarmadi, J., McCarthy, S., Betteridge, D. J., & Wolff, S. P. (1995). Elevated levels of authentic plasma hydroperoxides in NIDDM. Diabetes, 44(9), 1054–1058.

    Article  PubMed  CAS  Google Scholar 

  98. El-Mesallamy, H., Hamdy, N., Suwailem, S., & Mostafa, S. (2010). Oxidative stress and platelet activation: markers of myocardial infarction in type 2 diabetes mellitus. Angiology, 61(1), 14–18.

    Article  PubMed  CAS  Google Scholar 

  99. Iacobellis, G., Ribaudo, M. C., Zappaterreno, A., Vecci, E., Tiberti, C., Di Mario, U., & Leonetti, F. (2003). Relationship of insulin sensitivity and left ventricular mass in uncomplicated obesity. Obesity Research, 11(4), 518–524.

    Article  PubMed  Google Scholar 

  100. Rutter, M. K., Parise, H., Benjamin, E. J., Levy, D., Larson, M. G., Meigs, J. B., Nesto, R. W., Wilson, P. W., & Vasan, R. S. (2003). Impact of glucose intolerance and insulin resistance on cardiac structure and function: sex-related differences in the Framingham Heart Study. Circulation, 107(3), 448–454.

    Article  PubMed  CAS  Google Scholar 

  101. Abel, E. D. (2004). Insulin signaling in heart muscle: lessons from genetically engineered mouse models. Current Hypertension Reports, 6(6), 416–423.

    Article  PubMed  Google Scholar 

  102. Writing Team for the Diabetes Control and Complications Trial/Epidemiology of Diabetes Interventions and Complications Research Group, et al. (2002). Effect of intensive therapy on the microvascular complications of type 1 diabetes mellitus. JAMA: The Journal of the American Medical Association, 287(19), 2563–2569.

    Article  Google Scholar 

  103. UK Prospective Diabetes Study (UKPDS) Group, et al. (1998). Intensive blood-glucose control with sulphonylureas or insulin compared with conventional treatment and risk of complications in patients with type 2 diabetes (UKPDS 33). Lancet, 352(9131), 837–853.

    Article  Google Scholar 

  104. Holman, R. R., Paul, S. K., Bethel, M. A., Matthews, D. R., & Neil, H. A. (2008). 10-year follow-up of intensive glucose control in type 2 diabetes. The New England Journal of Medicine, 359(15), 1577–1589.

    Article  PubMed  CAS  Google Scholar 

  105. Stratton, I. M., Adler, A. I., Neil, H. A., Matthews, D. R., Manley, S. E., Cull, C. A., Hadden, D., Turner, R. C., & Holman, R. R. (2000). Association of glycaemia with macrovascular and microvascular complications of type 2 diabetes (UKPDS 35): prospective observational study. BMJ, 321(7258), 405–412.

    Article  PubMed  CAS  Google Scholar 

  106. Shekelle, P. G., Rich, M. W., Morton, S. C., Atkinson, C. S., Tu, W., Maglione, M., Rhodes, S., Barrett, M., Fonarow, G. C., Greenberg, B., Heidenreich, P. A., Knabel, T., Konstam, M. A., Steimle, A., & Warner Stevenson, L. (2003). Efficacy of angiotensin-converting enzyme inhibitors and beta-blockers in the management of left ventricular systolic dysfunction according to race, gender, and diabetic status: a meta-analysis of major clinical trials. Journal of the American College of Cardiology, 41(9), 1529–1538.

    Article  PubMed  CAS  Google Scholar 

  107. Hunt, S. A., Baker, D. W., Chin, M. H., Cinquegrani, M. P., Feldman, A. M., Francis, G. S., Ganiats, T. G., Goldstein, S., Gregoratos, G., Jessup, M. L., Noble, R. J., Packer, M., Silver, M. A., Stevenson, L. W., Gibbons, R. J., Antman, E. M., Alpert, J. S., Faxon, D. P., Fuster, V., Jacobs, A. K., Hiratzka, L. F., Russell, R. O., & Smith, S. C., Jr. (2001). Acc/aha guidelines for the evaluation and management of chronic heart failure in the adult: executive summary. A report of the American College of Cardiology/American Heart Association Task Force on practice guidelines (Committee to Revise the 1995 Guidelines for the Evaluation and Management of Heart Failure). Journal of the American College of Cardiology, 38(7), 2101–2113.

    Article  PubMed  CAS  Google Scholar 

  108. Hou, F. F., Zhang, X., Zhang, G. H., Xie, D., Chen, P. Y., Zhang, W. R., Jiang, J. P., Liang, M., Wang, G. B., Liu, Z. R., & Geng, R. W. (2006). Efficacy and safety of benazepril for advanced chronic renal insufficiency. The New England Journal of Medicine, 354(2), 131–140.

    Article  PubMed  CAS  Google Scholar 

  109. Masoudi, F. A., & Havranek, E. P. (2001). Race and responsiveness to drugs for heart failure. The New England Journal of Medicine, 345(10), 767. author reply 767-8.

    PubMed  CAS  Google Scholar 

  110. Lindholm, L. H., Ibsen, H., Borch-Johnsen, K., Olsen, M. H., Wachtell, K., Dahlof, B., Devereux, R. B., Beevers, G., de Faire, U., Fyhrquist, F., Julius, S., Kjeldsen, S. E., Kristianson, K., Lederballe-Pedersen, O., Nieminen, M. S., Omvik, P., Oparil, S., Wedel, H., Aurup, P., Edelman, J. M., & Snapinn, S. (2002). Risk of new-onset diabetes in the losartan intervention for endpoint reduction in hypertension study. Journal of Hypertension, 20(9), 1879–1886.

    Article  PubMed  CAS  Google Scholar 

  111. Pitt, B., Zannad, F., Remme, W. J., Cody, R., Castaigne, A., Perez, A., Palensky, J., & Wittes, J. (1999). The effect of spironolactone on morbidity and mortality in patients with severe heart failure. Randomized Aldactone Evaluation Study Investigators. The New England Journal of Medicine, 341(10), 709–717.

    Article  PubMed  CAS  Google Scholar 

  112. Pitt, B., Remme, W., Zannad, F., Neaton, J., Martinez, F., Roniker, B., Bittman, R., Hurley, S., Kleiman, J., & Gatlin, M. (2003). Eplerenone, a selective aldosterone blocker, in patients with left ventricular dysfunction after myocardial infarction. The New England Journal of Medicine, 348(14), 1309–1321.

    Article  PubMed  CAS  Google Scholar 

  113. Packer, M., Coats, A. J., Fowler, M. B., Katus, H. A., Krum, H., Mohacsi, P., Rouleau, J. L., Tendera, M., Castaigne, A., Roecker, E. B., Schultz, M. K., & DeMets, D. L. (2001). Effect of carvedilol on survival in severe chronic heart failure. The New England Journal of Medicine, 344(22), 1651–1658.

    Article  PubMed  CAS  Google Scholar 

  114. Kirpichnikov, D., McFarlane, S. I., & Sowers, J. R. (2003). Heart failure in diabetic patients: utility of beta-blockade. Journal of Cardiac Failure, 9(4), 333–344.

    Article  PubMed  CAS  Google Scholar 

  115. Rhenman, M. J., Rhenman, B., Icenogle, T., Christensen, R., & Copeland, J. (1988). Diabetes and heart transplantation. The Journal of Heart Transplantation, 7(5), 356–358.

    PubMed  CAS  Google Scholar 

  116. Marelli, D., Laks, H., Patel, B., Kermani, R., Marmureanu, A., Patel, J., & Kobashigawa, J. (2003). Heart transplantation in patients with diabetes mellitus in the current era. The Journal of Heart and Lung Transplantation, 22(10), 1091–1097.

    Article  PubMed  Google Scholar 

  117. Higgins, J., Pflugfelder, P. W., & Kostuk, W. J. (2009). Increased morbidity in diabetic cardiac transplant recipients. Canadian Journal of Cardiology, 25(4), e125–e129.

    Article  PubMed  Google Scholar 

  118. Hunt, S. A. (2005). ACC/AHA 2005 guideline update for the diagnosis and management of chronic heart failure in the adult: a report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines (Writing Committee to update the 2001 guidelines for the evaluation and management of heart failure). Journal of the American College of Cardiology, 46(6), e1–e82.

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

JES is supported by grants from the NIH (R01 DK064989, R01 HL096469) and the Burroughs Wellcome Foundation (1005935). LRP is supported by grants from the Washington University Institute of Clinical and Translational Sciences (NIH/NCRR UL1 RR024992) and the Washington University Diabetic Cardiovascular Disease Center.

Author information

Authors and Affiliations

  1. Diabetic Cardiovascular Disease Center, Department of Medicine, Washington University, St. Louis, MO, USA

    Linda R. Peterson & Jean E. Schaffer

  2. Mercy Clinic Heart and Vascular, St. Louis, MO, USA

    Clark R. McKenzie

Authors
  1. Linda R. Peterson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Clark R. McKenzie
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jean E. Schaffer
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jean E. Schaffer.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Peterson, L.R., McKenzie, C.R. & Schaffer, J.E. Diabetic Cardiovascular Disease: Getting to the Heart of the Matter. J. of Cardiovasc. Trans. Res. 5, 436–445 (2012). https://doi.org/10.1007/s12265-012-9374-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12265-012-9374-7

Keywords

Search

Navigation