Skip to main content
SpringerLink
Log in

Cardiovascular Disease Morbidity and Mortality in Patients with Type 1 Diabetes Mellitus

Management Strategies

  • Leading Article
  • Published:
Treatments in Endocrinology

Abstract

There is an increased risk of cardiovascular disease (CVD) mortality and morbidity in patients with type 1 diabetes mellitus compared with the general population as shown by epidemiologic studies measuring cardiovascular endpoints, as well as by autopsy, angiographic, and coronary calcification studies. Most of the excess CVD risk associated with type 1 diabetes is concentrated in the subset of approximately 35% of patients who develop diabetic nephropathy (after 20 years of diabetes duration), who also typically have dyslipidemias, elevated blood pressure, and hyperglycemia, factors contributing to CVD. For reasons that remain speculative, the relative risks from CVD are higher in women than in men with type 1 diabetes compared with the general population, which effectively eliminates the gender differences in CVD. As in the general population and in patients with type 2 diabetes, education and lifestyle changes, interventions to reduce hyperglycemia, blood pressure, microalbuminuria, lipid control, and the use of aspirin are important management areas in order to reduce the increased risk of CVD. Whether management with aspirin and statins should be started in type 1 diabetic patients at a younger age or at a lower risk score than in the general population is still under investigation. There is a need for a better understanding of the pathophysiology of vascular complications in type 1 diabetes, more specific risk engines in type 1 diabetes, and accurate estimations of the absolute and relative risk for CVD in order to improve management of CVD in these high-risk patients.

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

Table I

Similar content being viewed by others

References

  1. Matsushima M, LaPorte RE, Maruyama M, et al. Geographic variation in mortality among individuals with youth-onset diabetes mellitus across the world: DERI Mortality Study Group. Diabetes Epidemiology Research International. Diabetologia 1997; 40: 212–6

    Article  PubMed  CAS  Google Scholar 

  2. Fuller JH, Stevens LK, Wang SL. International variations in cardiovascular mortality associated with diabetes mellitus: the WHO Multinational Study of Vascular Disease in Diabetes. Ann Med 1996; 28: 319–22

    Article  PubMed  CAS  Google Scholar 

  3. Dorman JS, LaPorte RE, Kuller LH, et al. The Pittsburgh insulin-dependent diabetes mellitus (IDDM) morbidity and mortality study: mortality results. Diabetes 1984; 33: 271–6

    Article  PubMed  CAS  Google Scholar 

  4. Moss SE, Klein R, Klein BE. Cause-specific mortality in a population-based study of diabetes. Am J Public Health 1991; 81: 1158–62

    Article  PubMed  CAS  Google Scholar 

  5. Sartor G, Nystrom L, Dahlquist G. The Swedish Childhood Diabetes Study: a seven-fold decrease in short-term mortality? Diabet Med 1991; 8: 18–21

    Article  PubMed  CAS  Google Scholar 

  6. Joner G, Patrick S. The mortality of children with type 1 (insulin-dependent) diabetes mellitus in Norway, 1973–1988. Diabetologia 1991; 34: 29–32

    Article  PubMed  CAS  Google Scholar 

  7. Walters DP, Gatling W, Houston AC, et al. Mortality in diabetic subjects: an eleven-year follow-up of a community-based population. Diabet Med 1994; 11: 968–73

    Article  PubMed  CAS  Google Scholar 

  8. Swerdlow AJ, Jones ME. Mortality during 25 years of follow-up of a cohort with diabetes. Int J Epidemiol 1996; 25: 1250–61

    Article  PubMed  CAS  Google Scholar 

  9. Warner DP, McKinney PA, Law GR, et al. Mortality and diabetes from a population based register in Yorkshire 1978-93. Arch Dis Child 1998; 78: 435–8

    Article  PubMed  CAS  Google Scholar 

  10. Laing SP, Swerdlow AJ, Slater SD, et al. The British Diabetic Association Cohort Study: II. Cause-specific mortality in patients with insulin-treated diabetes mellitus. Diabet Med 1999; 16: 466–71

    Article  PubMed  CAS  Google Scholar 

  11. Nishimura R, LaPorte RE, Dorman JS, et al. Mortality trends in type 1 diabetes: the Allegheny County (Pennsylvania) Registry 1965–1999. Diabetes Care 2001; 24: 823–7

    Article  PubMed  CAS  Google Scholar 

  12. Morrish NJ, Wang SL, Stevens LK, et al. Mortality and causes of death in the WHO Multinational Study of Vascular Disease in Diabetes. Diabetologia 2001; 44Suppl. 2: S14–21

    Article  PubMed  Google Scholar 

  13. Wibell L, Nystrom L, Ostman J, et al. Increased mortality in diabetes during the first 10 years of the disease: a population-based study (DISS) in Swedish adults 15–34 years old at diagnosis. J Intern Med 2001; 249: 263–70

    Article  PubMed  CAS  Google Scholar 

  14. Roper NA, Bilous RW, Kelly WF, et al. Cause-specific mortality in a population with diabetes: South Tees Diabetes Mortality Study. Diabetes Care 2002; 25: 43–8

    Article  PubMed  Google Scholar 

  15. Florkowski CM, Scott RS, Graham PJ, et al. Cause-specific and total mortality in the Canterbury (New Zealand) insulin-treated diabetic registry population: a 15-year follow-up study. Diabet Med 2003; 20: 191–7

    Article  PubMed  CAS  Google Scholar 

  16. Laing SP, Swerdlow AJ, Slater SD, et al. The British Diabetic Association Cohort Study: I. All-cause mortality in patients with insulin-treated diabetes mellitus. Diabet Med 1999; 16: 459–65

    Article  PubMed  CAS  Google Scholar 

  17. Laing SP, Swerdlow AJ, Slater SD, et al. Mortality from heart disease in a cohort of 23,000 patients with insulin-treated diabetes. Diabetologia 2003; 46: 760–5

    Article  PubMed  CAS  Google Scholar 

  18. Laing SP, Swerdlow AJ, Carpenter LM, et al. Mortality from cerebrovascular disease in a cohort of 23 000 patients with insulin-treated diabetes. Stroke 2003; 34: 418–21

    Article  PubMed  Google Scholar 

  19. Krolewski AS, Kosinski EJ, Warram JH, et al. Magnitude and determinants of coronary artery disease in juvenile-onset, insulin-dependent diabetes mellitus. Am J Cardiol 1987; 59: 750–5

    Article  PubMed  CAS  Google Scholar 

  20. Portuese EI, Kuller L, Becker D, et al. High mortality from unidentified CVD in IDDM: time to start screening? Diabetes Res Clin Pract 1995; 30: 223–31

    Article  PubMed  CAS  Google Scholar 

  21. Moreno PR, Murcia AM, Palacios IF, et al. Coronary composition and macrophage infiltration in atherectomy specimens from patients with diabetes mellitus. Circulation 2000; 102: 2180–4

    Article  PubMed  CAS  Google Scholar 

  22. Burchfiel CM, Reed DM, Marcus EB, et al. Association of diabetes mellitus with coronary atherosclerosis and myocardial lesions: an autopsy study from the Honolulu Heart Program. Am J Epidemiol 1993; 137: 1328–40

    PubMed  CAS  Google Scholar 

  23. Valsania P, Zarich SW, Kowalchuk GJ, et al. Severity of coronary artery disease in young patients with insulin-dependent diabetes mellitus. Am Heart J 1991; 122: 695–700

    Article  PubMed  CAS  Google Scholar 

  24. Pajunen P, Taskinen MR, Nieminen MS, et al. Angiographic severity and extent of coronary artery disease in patients with type 1 diabetes mellitus. Am J Cardiol 2000; 86: 1080–5

    Article  PubMed  CAS  Google Scholar 

  25. Colhoun HM, Rubens MB, Underwood SR, et al. The effect of type 1 diabetes mellitus on the gender difference in coronary artery calcification. J Am Coll Cardiol 2000; 36: 2160–7

    Article  PubMed  CAS  Google Scholar 

  26. Rossing P, Hougaard P, Borch-Johnsen K, et al. Predictors of mortality in insulin dependent diabetes: 10 year observational follow-up study. BMJ 1996; 313: 779–84

    Article  PubMed  CAS  Google Scholar 

  27. Lloyd CE, Kuller LH, Ellis D, et al. Coronary artery disease in IDDM: gender differences in risk factors but not risk. Arterioscler Thromb Vasc Biol 1996; 16: 720–6

    Article  PubMed  CAS  Google Scholar 

  28. Soedamah-Muthu SS, Chaturvedi N, Toeller M, et al. Risk factors for coronary heart disease in type 1 diabetic patients in Europe: the EURODIAB Prospective Complications Study (PCS). Diabetes Care 2003; 27: 530–7

    Article  Google Scholar 

  29. Borch-Johnsen K, Kreiner S. Proteinuria: value as predictor of cardiovascular mortality in insulin-dependent diabetes mellitus. BMJ Clin Res Ed 1987; 294: 1651–4

    Article  CAS  Google Scholar 

  30. Barrett-Connor EL, Cohn BA, Wingard DL, et al. Why is diabetes mellitus a stronger risk factor for fatal ischemic heart disease in women than in men? The Rancho Bernardo Study. JAMA 1991; 265: 627–31

    Article  PubMed  CAS  Google Scholar 

  31. Lee WL, Cheung AM, Cape D, et al. Impact of diabetes on coronary artery disease in women and men: a meta-analysis of prospective studies. Diabetes Care 2000; 23: 962–8

    Article  PubMed  CAS  Google Scholar 

  32. Barrett-Connor E, Giardina EGV, Anselm KG, et al. Women and heart disease. Arch Intern Med 2004; 164: 934–42

    Article  PubMed  Google Scholar 

  33. Chowienczyk PJ, Watts GF, Cockcroft JR, et al. Sex differences in endothelial function in normal and hypercholesterolaemic subjects. Lancet 1994; 344: 305–6

    Article  PubMed  CAS  Google Scholar 

  34. Weiner CP, Lizasoain I, Baylis SA, et al. Induction of calcium-dependent nitric oxide synthases by sex hormones. Proc Natl Acad Sci U S A 1994; 91: 5212–6

    Article  PubMed  CAS  Google Scholar 

  35. Kawano H, Motoyama T, Kugiyama K, et al. Menstrual cyclic variation of endothelium-dependent vasodilation of the brachial artery: possible role of estrogen and nitric oxide. Proc Assoc Am Physicians 1996; 108: 473–80

    PubMed  CAS  Google Scholar 

  36. Bolego C, Cignarella A, Zancan V, et al. Diabetes abolishes the vascular protective effects of estrogen in female rats. Life Sci 1999; 64: 741–9

    Article  PubMed  CAS  Google Scholar 

  37. Chan P, Pan WH. Coagulation activation in type 2 diabetes mellitus: the higher coronary risk of female diabetic patients. Diabet Med 1995; 12: 504–7

    Article  PubMed  CAS  Google Scholar 

  38. Carr MD. Diabetes mellitus: a hypercoagulable state. J Diabetes Complications 2001; 15: 44–54

    Article  PubMed  CAS  Google Scholar 

  39. Borch-Johnsen K, Andersen PK, Deckert T. The effect of proteinuria on relative mortality in type 1 (insulin-dependent) diabetes mellitus. Diabetologia 1985; 28: 590–6

    Article  PubMed  CAS  Google Scholar 

  40. Jensen T, Borch JK, Kofoed EA, et al. Coronary heart disease in young type 1 (insulin-dependent) diabetic patients with and without diabetic nephropathy: incidence and risk factors. Diabetologia 1987; 30: 144–8

    Article  PubMed  CAS  Google Scholar 

  41. Hovind P, Tarnow L, Rossing P, et al. Predictors for the development of microalbuminuria and macroalbuminuria in patients with type 1 diabetes: inception cohort study. BMJ 2004; 328: 1105–8

    Article  PubMed  Google Scholar 

  42. Orchard TJ, Olson JC, Erbey JR, et al. Insulin resistance-related factors, but not glycemia, predict coronary artery disease in type 1 diabetes: 10-year follow-up data from the Pittsburgh Epidemiology of Diabetes Complications study. Diabetes Care 2003; 26: 1374–9

    Article  PubMed  Google Scholar 

  43. Stehouwer CD, Lambert J, Donker AJ, et al. Endothelial dysfunction and patho-genesis of diabetic angiopathy. Cardiovasc Res 1997; 34: 55–68

    Article  PubMed  CAS  Google Scholar 

  44. Deckert T, Feldt RB, Borch JK, et al. Albuminuria reflects widespread vascular damage: the Steno hypothesis. Diabetologia 1989; 32: 219–26

    Article  PubMed  CAS  Google Scholar 

  45. Lotufo PA, Gaziano JM, Chae CU, et al. Diabetes and all-cause and coronary heart disease mortality among US male physicians. Arch Intern Med 2001 Jan 22; 161: 242–7

    Article  PubMed  CAS  Google Scholar 

  46. Cho E, Rimm EB, Stampfer MJ, et al. The impact of diabetes mellitus and prior myocardial infarction on mortality from all causes and from coronary heart disease in men. J Am Coll Cardiol 2002; 40: 954–60

    Article  PubMed  Google Scholar 

  47. Hu FB, Stampfer MJ, Solomon CG, et al. The impact of diabetes mellitus on mortality from all causes and coronary heart disease in women: 20 years of follow-up. Arch Intern Med 2001 Jul 23; 161: 1717–23

    Article  PubMed  CAS  Google Scholar 

  48. Weis U, Turner B, Gibney J, et al. Long-term predictors of coronary artery disease and mortality in type 1 diabetes. QJM 2001; 94: 623–30

    Article  PubMed  CAS  Google Scholar 

  49. Deckert T, Yokoyama H, Mathiesen E, et al. Cohort study of predictive value of urinary albumin excretion for atherosclerotic vascular disease in patients with insulin-dependent diabetes. BMJ 1996; 312: 871–4

    Article  PubMed  CAS  Google Scholar 

  50. Lehto S, Ronnemaa T, Pyorala K, et al. Poor glycemic control predicts coronary heart disease events in patients with type 1 diabetes without nephropathy. Arterioscler Thromb Vasc Biol 1999; 19: 1014–9

    Article  PubMed  CAS  Google Scholar 

  51. Klein R. Hyperglycemia and microvascular and macrovascular disease in diabetes. Diabetes Care 1995; 18: 258–68

    Article  PubMed  CAS  Google Scholar 

  52. Moss SE, Klein R, Klein BE, et al. The association of glycemia and cause-specific mortality in a diabetic population. Arch Intern Med 1994; 154: 2473–9

    Article  PubMed  CAS  Google Scholar 

  53. Selvin E, Marinopoulos S, Berkenblit G, et al. Meta-analysis: glycosylated hemoglobin and cardiovascular disease in diabetes mellitus. Ann Intern Med 2004; 141: 421–31

    PubMed  CAS  Google Scholar 

  54. Forrest KY, Becker DY, Kuller LH, et al. Are predictors of coronary heart disease and lower-extremity arterial disease in type 1 diabetes the same? A prospective study. Atherosclerosis 2000; 148: 159–69

    Article  PubMed  CAS  Google Scholar 

  55. Olson JC, Erbey JR, Forrest KY, et al. Glycemia (or, in women, estimated glucose disposal rate) predict lower extremity arterial disease events in type 1 diabetes. Metabolism 2002; 51: 248–54

    Article  PubMed  CAS  Google Scholar 

  56. Vlassara H. Advanced glycation end-products and atheroscelerosis. Annals of Medicine 1996; 28: 419–26

    Article  PubMed  CAS  Google Scholar 

  57. Chaturvedi N, Bandinelli S, Mangili R, et al. Microalbuminuria in type 1 diabetes: rates, risk factors and glycemic threshold. Kidney Int 2001; 60: 219–27

    Article  PubMed  CAS  Google Scholar 

  58. Coonrod BA, Ellis D, Becker DJ, et al. Predictors of microalbuminuria in individuals with IDDM: Pittsburgh Epidemiology of Diabetes Complications Study. Diabetes Care 1993; 16: 1376–83

    Article  PubMed  CAS  Google Scholar 

  59. Krolewski AS, Laffel LM, Krolewski M, et al. Glycosylated hemoglobin and the risk of microalbuminuria in patients with insulin-dependent diabetes mellitus. N Engl J Med 1995; 332: 1251–5

    Article  PubMed  CAS  Google Scholar 

  60. Colhoun HM, Lee ET, Bennett PH, et al. Risk factors for renal failure: the WHO Multinational Study of Vascular Disease in Diabetes. Diabetologia 2001; 44Suppl. 2: S46–53

    Article  PubMed  CAS  Google Scholar 

  61. The DCCT Research Group. The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus: the Diabetes Control and Complications Trial Research Group. N Engl J Med 1993; 329: 977–86

    Article  Google Scholar 

  62. The DCCT/EDIC Research Group. Effect of intensive therapy on the microvascu-lar complications of type 1 diabetes mellitus. JAMA 2002; 287: 2563–9

    Article  Google Scholar 

  63. The DCCT/EDIC Research Group. Sustained effect of intensive treatment of type 1 diabetes mellitus on development and progression of diabetic nephropathy: the Epidemiology of Diabetes Interventions and Complications (EDIC) Study. JAMA 2003; 290: 2159–67

    Article  Google Scholar 

  64. The DCCT/EDIC Research Group. Intensive diabetes therapy and carotid intimamedia thickness in type 1 diabetes mellitus. N Engl J Med 2003; 348: 2294–303

    Article  Google Scholar 

  65. Stratton IM, Adler AI, Neil HA, et al. Association of glycaemia with macrovascular and microvascular complications of type 2 diabetes (UKPDS 35): prospective observational study. BMJ 2000; 321: 405–12

    Article  PubMed  CAS  Google Scholar 

  66. UKPDS Study Group. Intensive blood-glucose control with sulphonylureas or insulin compared with conventional treatment and risk of complications in patients with type 2 diabetes (UKPDS 33): UK Prospective Diabetes Study (UKPDS) Group. Lancet 1998; 352: 837–53

    Article  Google Scholar 

  67. Advance Management Committee. Study rationale and design of ADVANCE: Action in Diabetes and Vascular disease: preterax and diamicron MR controlled evaluation. Diabetologia 2001; 44 1118-20

    Google Scholar 

  68. The DCCT Research Group. Hypoglycemia in the Diabetes Control and Complications Trial: the Diabetes Control and Complications Trial Research Group. Diabetes 1997; 46: 271–86

    Article  Google Scholar 

  69. The DCCT Research Group. Adverse events and their association with treatment regimens in the Diabetes Control and Complications Trial. Diabetes Care 1995; 18: 1415–27

    Article  Google Scholar 

  70. The DCCT Research Group. Weight gain associated with intensive therapy in the Diabetes Control and Complications Trial: the DCCT Research Group. Diabetes Care 1988; 11: 567–73

    Article  Google Scholar 

  71. Klein R, Klein BE, Moss SE, et al. Association of ocular disease and mortality in a diabetic population. Arch Ophthalmol 1999; 117: 1487–95

    Article  PubMed  CAS  Google Scholar 

  72. Fuller JH, Stevens LK, Wang SL. Risk factors for cardiovascular mortality and morbidity: the WHO Mutinational Study of Vascular Disease in Diabetes. Diabetologia 2001; 44Suppl. 2: S54–64

    Article  PubMed  CAS  Google Scholar 

  73. Viberti GC, Hill RD, Jarrett RJ, et al. Microalbuminuria as a predictor of clinical nephropathy in insulin-dependent diabetes mellitus. Lancet 1982; I: 1430–2

    Article  Google Scholar 

  74. Mogensen CE, Christensen CK. Predicting diabetic nephropathy in insulin-dependent patients. N Engl J Med 1984; 311: 89–93

    Article  PubMed  CAS  Google Scholar 

  75. Mathiesen ER, Oxenboll B, Johansen K, et al. Incipient nephropathy in type 1 (insulin-dependent) diabetes. Diabetologia 1984; 26: 406–10

    Article  PubMed  CAS  Google Scholar 

  76. Klein R, Klein BE, Moss SE, et al. The 10-year incidence of renal insufficiency in people with type 1 diabetes. Diabetes Care 1999; 22: 743–51

    Article  PubMed  CAS  Google Scholar 

  77. Fuller JH, Head J. Blood pressure, proteinuria and their relationship with circulatory mortality: the WHO Multinational Study of Vascular Disease in Diabetics. Diabete Metab 1989; 15: 273–7

    PubMed  CAS  Google Scholar 

  78. Christiansen JS. Glomerular hyperfiltration in diabetes mellitus. Diabet Med 1985; 2: 235–9

    Article  PubMed  CAS  Google Scholar 

  79. Mogensen CE, Hansen KW, Osterby R, et al. Blood pressure elevation versus abnormal albuminuria in the genesis and prediction of renal disease in diabetes. Diabetes Care 1992; 15: 1192–204

    Article  PubMed  CAS  Google Scholar 

  80. Mathiesen ER, Ronn B, Jensen T, et al. Relationship between blood pressure and urinary albumin excretion in development of microalbuminuria. Diabetes 1990; 39: 245–9

    Article  PubMed  CAS  Google Scholar 

  81. Microalbuminuria Collaborative Study Group. Predictors of the development of microalbuminuria in patients with type 1 diabetes mellitus: a seven-year prospective study. The Microalbuminuria Collaborative Study Group. Diabet Med 1999; 16: 918–25

    Article  Google Scholar 

  82. Chaturvedi N, Sjolie AK, Stephenson JM, et al. Effect of lisinopril on progression of retinopathy in normotensive people with type 1 diabetes: the EUCLID Study Group. EURODIAB Controlled Trial of Lisinopril in Insulin-Dependent Diabetes Mellitus. Lancet 1998; 351: 28–31

    Article  PubMed  CAS  Google Scholar 

  83. The EUCLID Study Group. Randomised placebo-controlled trial of lisinopril in normotensive patients with insulin-dependent diabetes and normoalbuminuria or microalbuminuria: the EUCLID Study Group. Lancet 1997; 349: 1787–92

    Article  Google Scholar 

  84. ACE Inhibitors in Diabetic Nephropathy Trialist Group. Should all patients with type 1 diabetes mellitus and microalbuminuria receive angiotensin-converting enzyme inhibitors? A meta-analysis of individual patient data. Ann Intern Med 2001; 134: 370–9

    Google Scholar 

  85. Agarwal R. Treatment of hypertension in patients with diabetes: lessons from recent trials. Cardiol Rev 2001; 9: 36–44

    Article  PubMed  CAS  Google Scholar 

  86. Kaplan NM. Management of hypertension in patients with Ttpe 2 diabetes mellitus: guidelines based on current evidence. Ann Intern Med 2001; 135: 1079–83

    PubMed  CAS  Google Scholar 

  87. Hansson L, Zanchetti A, Carruthers SG, et al. Effects of intensive blood-pressure lowering and low-dose aspirin in patients with hypertension: principal results of the Hypertension Optimal Treatment (HOT) randomised trial. HOT Study Group. Lancet 1998; 351: 1755–62

    Article  PubMed  CAS  Google Scholar 

  88. Turner R, Cull C, Holman R, et al. Tight blood pressure control and risk of macrovascular and microvascular complications in type 2 diabetes: UKPDS 38. UK Prospective Diabetes Study Group. BMJ 1998; 317: 703–13

    Article  Google Scholar 

  89. Estacio RO, Jeffers BW, Hiatt WR, et al. The effect of nisoldipine as compared with enalapril on cardiovascular outcomes in patients with non-insulin-dependent diabetes and hypertension. N Engl J Med 1998; 338: 645–52

    Article  PubMed  CAS  Google Scholar 

  90. Brenner BM, Cooper ME, de Zeeuw D, et al. Effects of losartan on renal and cardiovascular outcomes in patients with type 2 diabetes and nephropathy. N Engl J Med 2001; 345: 861–9

    Article  PubMed  CAS  Google Scholar 

  91. Parving HH, Lehnert H, Brochner-Mortensen J, et al. The effect of irbesartan on the development of diabetic nephropathy in patients with type 2 diabetes. N Engl J Med 2001; 345: 870–8

    Article  PubMed  CAS  Google Scholar 

  92. Dahlof B, Devereux RB, Kjeldsen SE, et al. Cardiovascular morbidity and mortality in the Losartan Intervention For Endpoint reduction in hypertension study (LIFE): a randomised trial against atenolol. Lancet 2002; 359: 995–1003

    Article  PubMed  CAS  Google Scholar 

  93. Lewis EJ, Hunsicker LG, Bain RP, et al. The effect of angiotensin-converting-enzyme inhibition on diabetic nephropathy: the Collaborative Study Group. N Engl J Med 1993; 329: 1456–62

    Article  PubMed  CAS  Google Scholar 

  94. Kasiske BL, Kalil RS, Ma JZ, et al. Effect of antihypertensive therapy on the kidney in patients with diabetes: a meta-regression analysis. Ann Intern Med 1993; 118: 129–38

    PubMed  CAS  Google Scholar 

  95. Gansevoort RT, Sluiter WJ, Hemmelder MH, et al. Antiproteinuric effect of blood-pressure-lowering agents: a meta-analysis of comparative trials. Nephrol Dial Transplant 1995; 10: 1963–74

    PubMed  CAS  Google Scholar 

  96. Weidmann P, Schneider M, Bohlen L. Therapeutic efficacy of different anti-hypertensive drugs in human diabetic nephropathy: an updated meta-analysis. Nephrol Dial Transplant 1995; 10Suppl. 9: 39–45

    PubMed  Google Scholar 

  97. De Backer G, Ambrosioni E, Borch-Johnsen K, et al. European guidelines on cardiovascular disease prevention in clinical practice: Third Joint Task Force of European and Other Societies on Cardiovascular Disease Prevention in Clinical Practice. Eur Heart J 2003; 24: 1601–10

    Article  PubMed  Google Scholar 

  98. American Diabetes Association. Treatment of hypertension in adults with diabetes. Diabetes Care 2002; 25: 199–201

    Article  Google Scholar 

  99. Joint National Committee. The sixth report of the Joint National Committee on prevention, detection, evaluation, and treatment of high blood pressure. Arch Intern Med 1997; 157: 2413–46

    Article  Google Scholar 

  100. Tuomilehto J, Rastenyte D, Birkenhager WH, et al. Effects of calcium-channel blockade in older patients with diabetes and systolic hypertension: Systolic Hypertension in Europe Trial Investigators. N Engl J Med 1999; 340: 677–84

    Article  PubMed  CAS  Google Scholar 

  101. Dullaart RP. Plasma lipoprotein abnormalities in type 1 (insulin-dependent) diabetes mellitus. Neth J Med 1995; 46: 44–54

    Article  PubMed  CAS  Google Scholar 

  102. Betteridge DJ. Lipid disorders in diabetes mellitus. In: Pickup J, Williams G, editors. Textbook of diabetes. 2nd ed. Oxford: Blackwell Science, 1997: 1–31

    Google Scholar 

  103. Jensen T, Stender S, Deckert T. Abnormalities in plasma concentrations of lipoproteins and fibrinogen in type 1 (insulin-dependent) diabetic patients with increased urinary albumin excretion. Diabetologia 1988; 31: 142–5

    Article  PubMed  CAS  Google Scholar 

  104. Sibley SD, Hokanson JE, Steffes MW, et al. Increased small dense LDL and intermediate-density lipoprotein with albuminuria in type 1 diabetes. Diabetes Care 1999; 22: 1165–70

    Article  PubMed  CAS  Google Scholar 

  105. Mattock MB, Cronin N, Cavallo-Perin P, et al. Plasma lipids and urinary albumin excretion rate in type 1 diabetes mellitus: the EURODIAB IDDM Complications Study. Diabet Med 2001; 18: 59–67

    Article  PubMed  CAS  Google Scholar 

  106. Jones SL, Close CF, Mattock MB, et al. Plasma lipid and coagulation factor concentrations in insulin dependent diabetics with microalbuminuria. BMJ 1989; 298: 487–90

    Article  PubMed  CAS  Google Scholar 

  107. Jay RH, Jones SL, Hill CE, et al. Blood rheology and cardiovascular risk factors in type 1 diabetes: relationship with microalbuminuria. Diabet Med 1991; 8: 662–7

    Article  PubMed  CAS  Google Scholar 

  108. Groop PH. Lipidaemia and diabetic renal disease. In: Mogensen CE, editor. The kidney hypertension in diabetes mellitus. 4th ed. Boston (MA) & London: Kluwer Academic Publishers, 1998: 357–69

    Google Scholar 

  109. Soedamah-Muthu SS, Chang YF, Otvos J, et al. Lipoprotein subclass measurements by nuclear magnetic resonance spectroscopy improve the prediction of coronary artery disease in type 1 diabetes: a prospective report from the Pittsburgh Epidemiology of Diabetes Complications Study. Diabetologia 2003; 46: 674–82

    Article  PubMed  CAS  Google Scholar 

  110. Hokanson JE, Austin MA. Plasma triglyceride level is a risk factor for cardiovascular disease independent of high-density lipoprotein cholesterol level: a meta-analysis of population-based prospective studies. J Cardiovasc Risk 1996; 3: 213–9

    Article  PubMed  CAS  Google Scholar 

  111. Brewer HB. Hypertriglyceridemia: changes in the plasma lipoproteins associated with an increased risk of cardiovascular disease. Am J Cardiol 1999; 83: 3F–12F

    Article  PubMed  CAS  Google Scholar 

  112. Collins R, Armitage J, Parish S, et al. MRC/BHF Heart Protection Study of cholesterol-lowering with simvastatin in 5963 people with diabetes: a randomised placebo-controlled trial. Lancet 2003; 361: 2005–16

    Article  PubMed  Google Scholar 

  113. Colhoun HM, Betteridge DJ, Durrington PN, et al. Primary prevention of cardiovascular disease with atorvastatin in type 2 diabetes in the collaborative atorvastatin diabetes study (CARDS): a multicentre randomised placebo-controlled trial. Lancet 2004; 364: 685–96

    Article  PubMed  CAS  Google Scholar 

  114. The ALLHAT Officers and Coordinators for the ALLHAT Collaborative Research Group. Major outcomes in moderately hypercholesterolemic, hypertensive patients randomized to pravastatin vs usual care. JAMA 2002; 288: 2998–3007

    Article  Google Scholar 

  115. Sever PS, Dahlof B, Poulter NR, et al. Prevention of coronary and stroke events with atorvastatin in hypertensive patients who have average or lower-than-average cholesterol concentrations, in the Anglo-Scandinavian Cardiac Outcomes Trial-Lipid Lowering Arm (ASCOT-LLA): a multicentre randomised controlled trial. Lancet 2003; 361: 1149–58

    Article  PubMed  CAS  Google Scholar 

  116. Heart Protection Study Collaborative Group. MRC/BHF Heart Protection Study of cholesterol lowering with simvastatin in 20536 high-risk individuals: a randomised placebo-controlled trial. Lancet 2002; 360: 7–22

    Article  Google Scholar 

  117. Bellosta S, Paoletti R, Corsini A. Safety of statins: focus on clinical pharmacokinetics and drug interactions. Circulation 2004; 109: III–50–7

    Article  CAS  Google Scholar 

  118. Edison RJ, Muenke M. Mechanistic and epidemiologic considerations in the evaluation of adverse birth outcomes following gestational exposure to statins. Am J Med Genetics 2004; 131A: 287–98

    Article  Google Scholar 

  119. Rubins HB, Robins SJ, Collins D, et al. Diabetes, plasma insulin and cardiovascular disease. Arch Intern Med 2002; 162: 2597–604

    Article  PubMed  CAS  Google Scholar 

  120. Steiner G, DAIS Investigators. Effect of fenofibrate on progression of coronary-artery disease in type 2 diabetes: the Diabetes Atherosclerosis Intervention Study, a randomised study. Lancet 2001; 357: 905–10

    Article  CAS  Google Scholar 

  121. Koskinen P, Manttari M, Manninen V, et al. Coronary heart disease incidence in NIDDM patients in the Helsinki Heart Study. Diabetes Care 1992; 15: 820–5

    Article  PubMed  CAS  Google Scholar 

  122. Elkeles RS, Diamond JR, Poulter C, et al. Cardiovascular outcomes in type 2 diabetes. Diabetes Care 1998; 54: 641–8

    Article  Google Scholar 

  123. The Field Study Investigators. The need for a large-scale trial of fibrate therapy in diabetes: the rationale and design of the Fenofibrate Intervention and Event Lowering in Diabetes (FIELD) study. Cardiovascular Diabetology 2004; 3: 1–11

    Article  Google Scholar 

  124. European Diabetes Policy Group. A desktop guide to type 1 (insulin-dependent) diabetes mellitus: European Diabetes Policy Group 1998. Diabet Med 1999; 16: 253–66

    Article  Google Scholar 

  125. American Diabetes Association. Management of dyslipidemia in children and adolescents with diabetes. Diabetes Care 2003; 26: 2194–7

    Article  Google Scholar 

  126. National Cholesterol Education Program (NCEP). Highlights of the report of the Expert Panel on Blood Cholesterol Levels in Children and Adolescents. Pediatrics 1992; 89: 495–501

    Google Scholar 

  127. Williams CL, Hayman LL, Daniels SR, et al. Cardiovascular health in childhood: a statement for health professionals from the Committee on Atherosclerosis, Hypertension, and Obesity in the Young (AHOY) of the Council on Cardiovascular Disease in the Young, American Heart Association. Circulation 2002; 106: 143–60

    Article  PubMed  Google Scholar 

  128. Colwell JA. Aspirin therapy in diabetes. Diabetes Care 2003; 26Suppl. 1: S87–8

    PubMed  Google Scholar 

  129. Antiplatelet Trialist’s Collaboration. Collaborative overview of randomised trials of antiplatelet therapy: I. Prevention of death, myocardial infarction, and stroke by prolonged antiplatelet therapy in various categories of patients. Antiplatelet Trialists’ Collaboration. BMJ 1994; 308: 81–106

    Article  Google Scholar 

  130. 130. Antithrombotic Trialists’ Collaboration. Collaborative meta-analysis of randomised trials of antiplatelet therapy for prevention of death, myocardial infarction, and stroke in high risk patients. BMJ 2002; 324: 71–86

    Article  Google Scholar 

  131. Sanmuganathan PS, Ghahramani P, Jackson PR, et al. Aspirin for primary prevention of coronary heart disease: safety and absolute benefit related to coronary risk derived from meta-analysis of randomised trials. Heart 2001; 85: 265–71

    Article  PubMed  CAS  Google Scholar 

  132. Hebert PR, Hennekens CH. An overview of the 4 randomized trials of aspirin therapy in the primary prevention of vascular disease. Arch Intern Med 2000; 160: 3123–7

    Article  PubMed  CAS  Google Scholar 

  133. Sacco M, Pellegrini F, Roncaglioini MC, et al. Primary prevention of cardiovascu-lar events with low-dose aspirin and vitamin E in type 2 diabetic patients: results of the primary prevention project (PPP) trial. Diabetes Care 2003; 26: 3264–72

    Article  PubMed  CAS  Google Scholar 

  134. ETDRS Investigators. Aspirin effects on mortality and morbidity in patients with diabetes mellitus: Early Treatment Diabetic Retinopathy Study report 14. ETDRS Investigators. JAMA 1992; 268: 1292–300

    Article  Google Scholar 

  135. Ramsay LE, Williams B, Johnston GD, et al. British Hypertension Society guidelines for hypertension management 1999: summary. BMJ 1999; 319: 630–5

    Article  PubMed  CAS  Google Scholar 

  136. British Cardiac Society, British Hyperlipidaemia Association, British Hypertension Society, endorsed by the British Diabetic Association. Joint British recommendations on prevention of coronary heart disease in clinical practice: British Cardiac Society, British Hyperlipidaemia Association, British Hypertension Society, endorsed by the British Diabetic Association. Heart 1998; 80Suppl. 2: S1–29

    Google Scholar 

  137. Steering Committee of the Physicians’ Health Study Research Group. Final report on the aspirin component of the ongoing Physicians’ Health Study: Steering Committee of the Physicians’ Health Study Research Group. N Engl J Med 1989; 321: 129–135

    Article  Google Scholar 

  138. Redberg RF, Greenland P, Fuster V, et al. Prevention Conference VI: diabetes and cardiovascular disease: writing group III: risk assessment in persons with diabetes. Circulation 2002; 105: el44–52

    Article  Google Scholar 

  139. Haffner SM, Lehto S, Ronnemaa T, et al. Mortality from coronary heart disease in subjects with type 2 diabetes and in nondiabetic subjects with and without prior myocardial infarction. N Engl J Med 1998; 339: 229–34

    Article  PubMed  CAS  Google Scholar 

  140. Malmberg K, Yusuf S, Gerstein HC, et al. 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 2000; 102: 1014–9

    Article  PubMed  CAS  Google Scholar 

  141. Simons LA, McCallum J, Friedlander Y, et al. Diabetes, mortality and coronary heart disease in the prospective Dubbo study of Australian elderly. Aust N Z J Med 1996; 26: 66–74

    Article  PubMed  CAS  Google Scholar 

  142. Kuller LH, Velentgas P, Barzilay J, et al. Diabetes mellitus: subclinical cardiovascular disease and risk of incident cardiovascular disease and all-cause mortality. Arterioscler Thromb Vasc Biol 2000; 20: 823–9

    Article  PubMed  CAS  Google Scholar 

  143. Evans JM, Wang J, Morris AD. Comparison of cardiovascular risk between patients with type 2 diabetes and those who had had a myocardial infarction: cross sectional and cohort studies. BMJ 2002; 324: 939–42

    Article  PubMed  Google Scholar 

  144. Becker A, Bos G, de Vegt F, 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. Eur Heart J 2003; 24: 1406–13

    Article  PubMed  Google Scholar 

  145. Chaturvedi N. Differing aspects of insulin resistance in diabetes complications: the shape of things to come. RD Lawrence Lecture 2000. Diabet Med 2002; 19: 973–7

    Article  PubMed  CAS  Google Scholar 

  146. Barzilay J, Freedland E. Inflammation and its association with glucose disorders and cardiovascular disease. Treat Endocrinol 2003; 2: 85–94

    Article  PubMed  Google Scholar 

  147. Stout RW. Hyperinsulinaemia: a possible risk factor for cardiovascular disease in diabetes mellitus. Horm Metab Res Suppl 1985; 15: 37–41

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. University Medical Center Utrecht, Julius Center for Health Sciences and Primary Care, Utrecht, The Netherlands

    Sabita S. Soedamah-Muthu

  2. Department of Internal Medicine, University Hospital Maastricht, PO Box 5800, Maastricht, 6202, AZ, The Netherlands

    Coen D.A. Stehouwer

Authors
  1. Sabita S. Soedamah-Muthu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Coen D.A. Stehouwer
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Coen D.A. Stehouwer.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Soedamah-Muthu, S.S., Stehouwer, C.D. Cardiovascular Disease Morbidity and Mortality in Patients with Type 1 Diabetes Mellitus. Mol Diag Ther 4, 75–86 (2005). https://doi.org/10.2165/00024677-200504020-00002

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.2165/00024677-200504020-00002

Keywords

Search

Navigation