Diabetes Research and Clinical Practice
Volume 78, Issue 3, Supplement , Pages S3-S13 , 20 December 2007

Effects of thiazolidinediones on the triad of type 2 diabetes mellitus, insulin resistance and cardiovascular disease

References 

  1. Peel S, D’Alonza CA. Factors associated with long-term survival of diabetes. J. Am. Med. Assoc. 1970;214:1833–1840
  2. Panzram G. Mortality and survival in type 2 diabetes (non-insulin-dependent) diabetes Mellitus. Diabetologia. 1987;30:23–131
  3. CDC Diabetes, National Diabetes Fact Sheet, United States, 2005. http://www.cdc.gov/diabetes/pubs/factsheet05.htm (accessed February 12, 2007).
  4. Hurst RT, Lee RW. Increased incidence of coronary atherosclerosis in type 2 diabetes mellitus: mechanisms and management. Ann. Intern. Med. 2003;139:824–834
  5. Haffner SM, Lehto S, Ronnemaa T, Pyorala K, Laakso M. Mortality from coronary heart disease in subject with type 2 diabetes and in non-diabetic subjects with and without prior myocardial infarction. N. Eng. J. Med. 1998;339:229–234
  6. Evans JM, Wang J, Morris AD. Comparison of cardiovascular risk between patients with type 2 diabetes and those who had a myocardial infarction. BMJ. 2002;324:939–942
  7. Juutilainen A, Lehto S, Ronnemaa T, Pyorala K, Laakso M. Type 2 diabetes as a coronary heart disease equivalent: an 18-year prospective population-based study in Finnish subjects. Diabetes Care. 2005;28:2901–2907
  8. Miettinen H, Lehto S, Saloman V, Mahonan M, Niemala M, Haffner SM, et al. Impact of diabetes on mortality after the first myocardial infarction. The FINMONICA Myocardial Infarction Registry Study Group. Diabetes Care. 1998;21:69–75
  9. Mukamal KJ, Nesto RW, Cohen MC, Muller JE, Maclure M, Sherwood JB, et al. Impact of diabetes Mellitus on long-term survival after acute myocardial infarction: compatibility of risk with prior MI. Diabetes Care. 2001;24:1422–1427
  10. Idris I, Thomson GA, Sharma JC. Diabetes and stroke. Int. J. Clin. Pract. 2006;60:48–56
  11. DeFronzo R. Pathogenesis of type 2 diabetes. Med. Clin. North Am. 2004;88:787–835
  12. Beckman JA, Creager MA, Libby P. Diabetes and atherosclerosis: epidemiology, pathophysiology and management. JAMA. 2002;287:2570–2581
  13. Grundy SM, Hansen B, Smith S, Cleeman JI, Kahn RA. Clinical management of metabolic syndrome: report of the American Heart Association/National Heart, Lung, and Blood Institute/American Diabetes Association conference on scientific issues related to management. Circulation. 2004;109:551–556
  14. Lorenzo C, Williams K, Hunt KJ, Haffner SM. The National Cholesterol Education Program-Adult Treatment Panel III. International Diabetes Federation, and the World Health Organization definitions of the metabolic syndrome as predictors of incident cardiovascular disease and diabetes. Diabetes Care. 2007;30:8–13
  15. Ninomiya JK, L’Italien G, Criqui MH, Whyte JL, Gamst A, Chen RS. Association of the metabolic syndrome with history of myocardial infarction and stroke in the Third National Health and Nutrition Examination Survey. Circulation. 2004;109:42–46
  16. Lakka HM, Laaksonen DE, Lakka TA, Niskanen LK, Kumpusalo E, Tuomilheto J, et al. The metabolic syndrome and total cardiovascular disease mortality in middle age men. JAMA. 2002;288:2709–2716
  17. Lehto S, Rönnemaa T, Pyörälä K, Laakso M. Cardiovascular risk factors clustering with endogenous hyperinsulinaemia predict death from coronary heart disease in patients with Type II diabetes. Diabetologia. 2000;43:148–155
  18. Alexander CM, Landsman PB, Teutsch SM, Haffner SM. NCEP-defined Metabolic syndrome, diabetes, and prevalence of coronary heart disease among NHANES III. Participants age 50 years and older. Diabetes. 2003;52:1210–1214
  19. Bonora E, Kiechl S, Willeit J, Oberhollenzer F, Egger G, Targher G, et al. Prevalence of insulin resistance in metabolic disorders: the Bruneck Study. Diabetes. 1998;47:1643–1649
  20. Bonora E, Formentini G, Calcaterra F, Lombardi S, Marini F, Zenari L, et al. HOMA-estimated insulin resistance is an independent predictor of cardiovascular disease in type 2 diabetes subjects: prospective data from the Verona Diabetes Complications Study. Diabetes Care. 2002;25:1135–1141
  21. Hanley AJ, Williams K, Stern MO, Haffner SM. Homeostasis model assessment of insulin resistance in relation to the incidence of cardiovascular disease: the San Antonio Heart Study. Diabetes Care. 2002;25:1177–1184
  22. Sowers JR. Treatment of hypertension in patients with diabetes. Arch. Intern. Med. 2004;164:1850–1857
  23. Blood Pressure Lowering Treatment Trialists . Effects of different blood pressure-lowering regimens on major cardiovascular events in individuals with and without diabetes mellitus: results of prospectively designed overviews of randomized trials. Arch. Intern. Med. 2005;165:1410–1419
  24. Costa J, Borges M, David C, Carneiro AV. Efficacy of lipid lowering drug treatment for diabetic and non-diabetic patients: meta-analysis of randomized controlled trials. BMJ. 2006;332:1115–1124
  25. Saito I, Folsom AR, Brancati FL, Duncan BB, Chambless LE, McGovern PG. Nontraditional risk factors for coronary heart disease incidence among persons with diabetes: the Atherosclerosis Risk in Communities (ARIC) Study. Ann. Intern. Med. 2000;133:81–89
  26. Ridker PM, Hennekens CH, Burning JE, Rifai N. C-reactive protein and other markers of inflammation in the prediction of cardiovascular disease in women. N. Eng. J. Med. 2000;342:836–843
  27. Festa A, D’Agostino R, Howard G, Mykakanen L, Tracy RP, Haffner SM. Chronic subclinical inflammation as part of the insulin resistance syndrome: the Insulin Resistance Atherosclerosis Study (IRIS). Circulation. 2000;102:42–47
  28. Fonseca V, DeSouza C, Asnani S, Jialal I. Nontraditional risk factors for cardiovascular disease in diabetes. Endoc. Rev. 2004;25:153–175
  29. Hotta K, Funahashi T, Arita Y, Takahashi M, Matsuda M, Okamoto Y, et al. Plasma concentration of a novel, adipose-specific protein, adiponectin, in type 2 diabetes patients. Arterioscler. Thrombo. Vasc. Biol. 2000;20:1595–1599
  30. Lehmann JM, Moore LB, Smith-Oliver TA, Wilkison WO, Willson TM, Kliewer SA. An antidiabetic thiazolidinedione is a high affinity ligand for peroxisome proliferator-activated receptor gamma (PPAR gamma). J. Biol. Chem. 1995;270:12953–12956
  31. Wilson TM, Lambert MH, Kliewer SA. Peroxisome proliferator-activated receptor gamma and metabolic disease. Annu. Rev. Biochem. 2001;70:341–367
  32. Yki-Jarvinen H. Thiazolidinediones. N. Engl. J. Med. 2004;351:1106–1118
  33. Lee C, Olson P, Evans RM. Minireview: lipid metabolism, metabolic disease, and peroxisome proliferator-activetes receptors. Endocrinology. 2003;144:2201–2207
  34. Van Wijk JPH, deKoning EJP, Martens EP, Rabelink TJ. Thiazolidinediones and blood lipids in type 2 diabetes. Arterioscler. Thromb. Vasc. Biol. 2003;23:1744–1749
  35. Chiquette E, Ramirez G, DeFronzo R. A meta-analysis comparing the effect of thiazolidinediones on cardiovascular risk factors. Arch. Intern. Med. 2004;164:2097–2104
  36. Goldberg RB, Kendall DM, Deeg MA, Buse JB, Zagar AJ, Pinaire JA, et al. A comparison of lipid and glycemic effects of pioglitazone and rosiglitazone in patients with type 2 diabetes and dyslipidemia. Diabetes Care. 2005;28:1547–1554
  37. Chobanian AV, Bakris GL, Black HR, Cushman WC, Green LA, Izzo JL, et al. The seventh report of the Joint National Committee on Prevention, detection, evaluation, and treatment of high blood pressure: the jnc 7 REPORT. JAMA. 2003;289:2560–2572[erratum appears in JAMA 290 (2003) 197]
  38. UK Prospective Diabetes Study Group . Tight blood pressure control and risk of macrovascular and microvascular complications in type 2 diabetes: UKPDS 38. BMJ. 1998;317:703–713
  39. Hansson L, Zanchetti A, Carruthers SG, Dahlof B, Elmfeldt D, Julius S, et al. Effects of intensive blood-pressure lowering and low-dose aspirin in patients with hypertension: principal results of the Hypertension Optimal Treatment (HOT) randomized trial: HOT Study Group. Lancet. 1998;351:1755–1762
  40. Hirose H, Kawai T, Yamamoto Y, Taniyama M, Tomita M, Matsubara K, et al. Effects of pioglitazone on metabolic parameters, body fat distribution, and serum adiponectin levels in Japanese male patients with type 2 diabetes. Metabolism. 2002;51:314–317
  41. Martens FM, Visseren FLJ, Lemay J, de Koning EJ, Rabelink TJ. Metabolic and additional vascular effects on thiazolidinediones. Drugs. 2002;62:1463–1480
  42. Natali A, Baleweg S, Toschi E, Capaldo B, Barbaro D, Gastaldelli A, et al. Vascular effects of improving metabolic control with metformin or rosiglitazone in type 2 diabetes. Diabetes Care. 2004;27:1349–1357
  43. Bennett SMA, Agrawal A, Elasha H, Heise M, Jones NP, Walker M, et al. Rosiglitazone improves insulin sensitivity, glucose tolerance and ambulatory blood pressure in subjects with impaired glucose tolerance. Diabet. Med. 2004;21:415–422
  44. Raji A, Selly EW, Bekins SA, Williams GH, Simonson DC, Wilding JPH. Rosiglitazone improves insulin sensitivity and lower blood pressure in hypertensive patients. Diabetes Care. 2003;26:172–178
  45. Shargorodsky M, Wainstein J, Gavish D, Leibovitz E, Matas Z, Zimlichman R. Treatment with rosiglitazone reduces hyperinsulinemia and improves arterial elasticity in patients with type 2 diabetes mellitus. Am. J. Hypertens. 2003;16:617–622[erratum appears in Am. J. Hypertens. 16 (2003) 894]
  46. St. John Sutton M, Rendell M, Dandona P, Dole J, Murphy K, Patwardhan R, et al. A comparison of effects of rosiglitazone and glyburide on cardiovascular function and glycemic control in patients with type 2 diabetes. Diabetes Care. 2002;25:2058–2064
  47. Dormandy JA, Charbonnel B, Eckland DJ, Erdmann E, Massi-Benedetti M, Moules IK, et al. Proactive Investigators. Secondary prevention of macrovascular events in patients with type 2 diabetes in the PROactive Study (PROspective pioglitAzone Clinical Trial In macroVascular Events): a randomised controlled trial. Lancet. 2005;366:1279–1289
  48. Gerstein HC, Mann JFE, Yi Q, Zinman B, Dinneen SF, Hoogwerf B, et al. Albuminuria and risk of cardiovascular events, death, and heart failure in diabetic and nondiabetic individuals. JAMA. 2001;286:421–426
  49. El-Atat FA, Stas SN, McFarlane SI, Sowers JR. The relationship between hyperinsulinemia, hypertension, and progressive renal disease. J. Am. Soc. Nephrol. 2004;15:2816–2827
  50. Nakamura T, Ushiyama C, Shimada N, Hayashi K, Ebinahara I, Koide H. Comparative effects of pioglitazone, glibenclamide, and voglibose on urinary endothelian-1 and albumin excretion in diabetes patients. J. Diabet. Complications. 2000;14:250–254
  51. Aljabri K, Kozak SE, Thompson DM. Addition of pioglitazone or bedtime insulin to maximal doses of sulfonylurea and metformin in type 2 diabetes patients with poor glucose control: a prospective, randomized trial. Am. J. Med. 2004;116:230–235
  52. Yanagawa T, Araki A, Sasamoto K, Shirabe S, Yamanouchi T. Effect of antidiabetic medications on microalbuminuria in patients with type 2 diabetes. Metabolism. 2004;53:353–357
  53. Bakris G, Viberti G, Weston WM, Heise M, Porter LE, Freed MI. Rosiglitazone reduces urinary albumin excretion in type II diabetes. J. Hum. Hypertens. 2003;17:7–12
  54. Lebovitz HE, Dole JF, Patwardhan R, Rappaport EB, Freed MI. Rosiglitazone monotherapy is effective in patients with type 2 diabetes. J. Clin. Endocrinol. Metab. 2001;86:280–288
  55. Ridker PM. Evaluating novel cardiovascular risk factors: can we better predict heart attacks?. Ann. Intern. Med. 1999;130:933–937
  56. Danish J, Wheeler JG, Hirschfield GM, Shinichi E, Eiriksdottir G, Rumley A, et al. C-reactive protein and other circulating markers of inflammation in the prediction of coronary heart disease. N. Engl. J. Med. 2004;350:1387–1397
  57. Pradhan AD, Manson JE, Rifai N, Buring JE, Ridker PM. C-reactive protein, interleukin 6, and risk of developing type 2 diabetes mellitus. JAMA. 2001;286:327–334
  58. Haffner SM, Greenberg AS, Weston WM, Chen H, Williams K, Freed MI. Effect of rosiglitazone treatment on nontraditional markers of cardiovascular disease in patients with type 2 diabetes. Circulation. 2002;106:679–684
  59. Satoh N, Ogawa O, Usui T, Tagami T, Kono S, Uesugi H, et al. Antiatherogenic effect of pioglitazone in type 2 diabetic patients irrespective of the responsiveness to its antidiabetic effect. Diabetes Care. 2003;26:2493–2499
  60. Pfutzner A, Marx N, Lubben G, Langenfeld M, Walcher D, Konrad T, et al. Improvement of cardiovascular risk markers by pioglitazone is independent from glycemic control. J. Am. Coll. Cardiol. 2005;45:1925–1931
  61. Haffner SM, D’Agostino R, Mykkanen L, Tracy T, Howard B, Rewers M, et al. Insulin sensitivity in subjects with type 2 diabetes. Relationship to cardiovascular risk factors: the Insulin Resistance Atherosclerosis Study. Diabetes Care. 1999;22:562–568
  62. Freed M, Fuell D, Menci L, Heise M, Goldstein B. Effect of combination therapy with rosiglitazone and glibenclamide on PAI-1 antigen, PAI-1 activity, and tPA in patients with type 2 diabetes. Diabetologia. 2000;43(Suppl.):A267
  63. Dollery CM, McEwan JR, Henney AM. Matrix metalloproteinases and cardiovascular disease. Circ. Res. 1995;77:863–868
  64. Loftus IM, Naylor AR, Bell PRF, Thompson MM. Plasma MMP-9: a marker of carotid plaque instability. Eur. J. Vasc. Endovasc. Surg. 2001;21:17–21
  65. Brown DL, Hibbs MS, Kearney M, Loushin C, Isner JM. Identification of 92-kD gelatinases in human coronary atherosclerotic lesions. Circulation. 1995;91:2125–2131
  66. Tayebjee MH, Lim HS, MacFadyen RJ, Lip GYH. Matrix metalloproteinase-9 and tissue inhibitor of metalloproteinase-1 and -2 in type 2 diabetes. Diabetes Care. 2004;27:2049–2051
  67. Marx N, Froehlich J, Siam L, Ittner J, Wierse G, Schmidt A, et al. Antidiabetic PPAR-activator rosiglitazone reduces MMP-9 serum levels in type 2 diabetic patients with coronary artery disease. Arterioscler. Thromb. Vasc. Biol. 2003;23:283–288
  68. Ludmer PL, Selwyn AP, Shook TL, Wayne RR, Mudge GH, Alexander RW, et al. Paradoxical vasoconstriction induced by acetylcholine in atherosclerotic coronary arteries. N. Eng. J. Med. 1986;315:1046–1051
  69. Calles-Escandon J, Cipolla M. Diabetes and endothelial dysfunction: a clinical perspective. Endoc. Rev. 2001;22:36–52
  70. Pistrosch F, Passauer J, Fischer S, Fuecker K, Hanefeld M, Gross P. In type 2 diabetes, rosiglitazone therapy for insulin resistance ameliorates endothelial dysfunction independent of glucose control. Diabetes Care. 2004;27:484–490
  71. Sidhu JS, Cowan D, Kaski JC. Effects of rosiglitazone on endothelial function in men with coronary artery disease without diabetes. Am. J. Cardiol. 2004;94:151–156
  72. Hetzel J, Balletshofer B, Ritting K, Walcher D, Kratzer W, Hombach V, et al. Rapid effects of rosiglitazone treatment on endothelial function and inflammatory biomarkers. Arterioscler. Thromb. Vasc. Biol. 2005;25:1804–1809
  73. Sourij H, Zweiker R, Wascher TC. Effects of pioglitazone on endothelial function, insulin sensitivity, and glucose control in subjects with coronary artery disease and new-onset type 2 diabetes. Diabetes Care. 2006;29:1039–1045
  74. Crouse JR. Imaging atherosclerosis: state of the art. J. Lipid Res. 2006;47:1677–1699
  75. Hodis HN, Mack WJ, LaBree L, Seizer RH, Liu C-R, Liu C-H, et al. The role of carotid arterial intima-media thickness in predicting clinical coronary events. Ann. Intern. Med. 1998;128:262–269
  76. Satoh N, Ogawa Y, Usui T, Tagami T, Kono S, Uesugi H, et al. Antiatherogenic effect of pioglitazone in type 2 diabetic patients irrespective of the responsiveness to its antidiabetic effect. Diabetes Care. 2003;26:2493–2499
  77. Koshiyama H, Shimono D, Kuwamura N, Minanikawa J, Nakamura Y. Inhibitory effect of pioglitazone on carotid arterial wall thickness in type 2 diabetes. J. Clin. Endocrinol. Metab. 2001;86:3452–3456
  78. Langenfeld MR, Forst T, Hohberg C, Kahn P, Lubben G, Konrad T, et al. Pioglitazone decreases carotid intima-media thickness independently of glycemic control in patients with type 2 diabetes mellitus. Circulation. 2005;111:2525–2531
  79. Minamikawa J, Tanaka S, Yamauchi M, Inoue D, Koshiyama H. Potent inhibitory effect of troglitazone on carotid arterial wall thickness in type 2 diabetes. J. Clin. Endocrinol. Metab. 1998;83:1818–1820
  80. Mazzone T, Meyer PM, Feinstein SB, Davidson MH, Kondos GT, D’Agostino RB, et al. Effect of pioglitazone compared with glimepiride on carotid intima-media thickness in type 2 diabetes: a randomized trial. JAMA. 2006;296:2572–2581
  81. Choi D, Kim SK, Choi S-H, Ho Y-G, Ahn C-W, Jang Y, et al. Preventative effects of rosiglitazone on restenosis after coronary stent implantation in patients with type 2 diabetes. Diabetes Care. 2004;27:2654–2660
  82. Nishio K, Sakurai M, Kusuyama T, Shigemitsu M, Fukui T, Kawamura K, et al. A randomized comparison of pioglitazone to inhibit restenosis after coronary stenting in patients with type 2 diabetes. Diabetes Care. 2006;29:101–106
  83. UK Prospective Diabetes Study (UKPDS) Group . Intensive blood-glucose control with sulfonylurea or insulin compared with conventional treatment and risk of complications in patients with type 2 diabetes (UKPDS 33). Lancet. 1998;352:837–853
  84. UK Prospective Diabetes Study (UKPDS) Group . Effect of intensive blood-glucose control with metformin on complications in overweight patients with type 2 diabetes (UKPDS 34). Lancet. 1998;352:854–865
  85. Ryden L, Thrainsdottir I, Swedberg K. Adjudication of serious heart failure in patients from PROactive. Lancet. 2007;369:189–190
  86. E. Erdmann, The effect of pioglitazone on recurrent myocardial infarction in 2445 patients with type 2 diabetes and previous myocardial infarction: results from the PROactive study presented at AHA Association Meeting, November 2005.
  87. Wilcox R, Bousser MG, Betteridge DJ, Schernthaner G, Pirags V, Kupfner S, et al. Effects of pioglitazone in patients with type 2 diabetes with or without previous stroke. Results from PROACTIVE (PROspective pioglitAzone Clinical Trial In MacroVascular Events 04). Stroke. 2007;38:865–873
  88. Pioglitazone Effect on Regression of Intravascular Sonographic Coronary Obstruction Prospective Evaluation (PERISCOPE). http://www.clinicaltrials.gov/ct/gui/show/NCT00225277 (accessed February 13, 2007).
  89. The VICTORY Trial: Vein-Coronary Atherosclerosis and Rosiglitazone after Bypass Surgery. http://www.clinicaltrials.gov/ct/show/NCT00169832?order=1 (accessed February13, 2007).
  90. Rosiglitazone vs. a Sulfonylurea on Progression of Atherosclerosis in Patients with CVD and T2D (APPROACH). http://www.clinicaltrials.gov/ct/show/NCT00116831?order=40 (accessed February 13, 2007).
  91. Pioglitazone Protects DM Patients Against Re-Infarction (PPAR Study). http://www.clinicaltrials.gov/ct/show/NCT00212004?order=9 (accessed February 13, 2007).
  92. ACCORD. http://www.nih.gov/news/pr/feb2003/nhlbi-20.htm (accessed February14, 2007).
  93. Home PD, Pocock SJ, Beck-Nielsen H, Gomis R, Hanefled M, Dargie H, et al. Rosiglitazone evaluated for cardiac outcomes and regulation of glycemia in diabetes (RECORD): study design and protocol. Diabetologia. 2005;48:1726–1735
  94. Sobel BE, Frye R, Detre KM. Bypass Angioplasty Revascularization Investigation 2 Diabetes Trial. Burgeoning dilemmas in the management of diabetes and cardiovascular disease: rationale for the Bypass Angioplasty Revascularization Investigation 2 Diabetes (BARI 2D) Trial. Circulation. 2003;107:636–642
  95. Barnett AH. Introduction: beyond glycemic control in type 2 diabetes. Cur. Med. Res. Opin. 2006;22(Suppl. 2):S1–S4
  96. American Diabetes Association . Standards of medical care in diabetes. Diabetes Care. 2006;29(Suppl. 1):S4–S42
  97. Gaede P, Vedel P, Larsen N, Jensen GVH, Parving H-H, Pedersen O. Multifactorial intervention and cardiovascular disease in patients with Type 2 Diabetes. N. Engl. J. Med. 2003;348:382–393

PII: S0168-8227(07)00494-9

doi: 10.1016/j.diabres.2007.09.010

Diabetes Research and Clinical Practice
Volume 78, Issue 3, Supplement , Pages S3-S13 , 20 December 2007