Atherothrombosis in patients with type 2 diabetes mellitus: An overview of pathophysiology;Aterotrombosi e diabete mellito di tipo 2: Analisi dei principali meccanismi fisiopatogenetici

Giornale Italiano di Cardiologia

Volumn 11, Issue 6, 2010, Pages 467-477

  Mafrici, Antonio ^a   Proietti, Riccardo ^b  

^a OSPEDALE NIGUARDA CA GRANDA   (Italy)

^b SANT'ANDREA HOSPITAL   (Italy)

Author keywords

Atherothrombosis; Diabetes mellitus; Endothelial dysfunction; Insulin resistance

Indexed keywords

ATHEROSCLEROSIS; BLOOD CLOTTING; DISEASE COURSE; FIBRINOLYSIS; HUMAN; HYPERGLYCEMIA; INSULIN RESISTANCE; MACROPHAGE; MONOCYTE; NON INSULIN DEPENDENT DIABETES MELLITUS; PATHOPHYSIOLOGY; PHENOTYPE; REVIEW; THROMBOCYTE ADHESION; THROMBOSIS; VASCULAR ENDOTHELIUM; CEREBROVASCULAR ACCIDENT; COMPARATIVE STUDY; DIABETIC ANGIOPATHY; HEART INFARCTION; HEMOSTASIS; INSULIN DEPENDENT DIABETES MELLITUS; METABOLISM; PERIPHERAL VASCULAR DISEASE; PHYSIOLOGY;

ATHEROSCLEROSIS; DIABETES MELLITUS, TYPE 1; DIABETES MELLITUS, TYPE 2; DIABETIC ANGIOPATHIES; ENDOTHELIUM, VASCULAR; HEMOSTASIS; HUMANS; INSULIN RESISTANCE; MYOCARDIAL INFARCTION; PERIPHERAL VASCULAR DISEASES; STROKE; THROMBOSIS;

EID: 77954505659     PISSN: 18276806     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (92)

1. King H, Aubert RE, Herman WH. Global burden of diabetes 1995-2025: prevalence, numerical estimates, and projections. Diabetes Care 1998; 21: 1414-31.
2. Grant PJ, Summers LH. Diabetes, impaired fibrinolysis, and thrombosis. In: Marso SP, Stern DM, eds. Diabetes and cardiovascular disease. Philadelphia, PA: Lippincott Williams and Wilkins, 2005: 268-91.
3. Kannel WB, McGee DL. Diabetes and cardiovascular risk factor: the Framingham study. Circulation 1979; 59: 8-13. (Pubitemid 9082394)
4. Haffner SM, Letho S, Rönnemaa T, Pyörälä K, Laakso M. Mortality from coronary heart disease in subjects with type 2 diabetes and nondiabetic subjects with and without prior myocardial infarction. N Engl J Med 1998; 339: 229-34.
5. McGuire DK, Newby LK, Bhapkar MV, et al, for the SYMPHONY and 2nd SYMPHONY Investigators. Association of diabetes mellitus and glycemic control strategies with clinical outcomes after acute coronary syndromes. Am Heart J 2004; 147: 246-52.
6. Bassand JP, Hamm CW, Ardissino D, et al. Guidelines for the diagnosis and treatment of non-ST-segment elevation acute coronary syndromes. Eur Heart J 2007; 28: 1598-660.
7. Abizaid A, Costa MA, Centemero M, et al. Clinical and economic impact of diabetes mellitus on percutaneous and surgical treatment of multivessel coronary disease patients: insights from the Arterial Revascularization Therapy Study (ARTS) trial. Circulation 2001; 104: 533-8.
8. Herlitz J, Wognsen GB, Emanuelsson H, et al. Mortality and morbidity in diabetic and nondiabetic patients during a 2-year period after coronary artery bypass grafting. Diabetes Care 1996; 19: 698-703. (Pubitemid 126752470)
9. Cannon P, Weintraub WS, Demopoulos LA, et al, for the TACTICS-TIMI 18 Investigators. Comparison of early invasive and conservative strategies in patients with unstable coronary syndromes treated with the glycoprotein IIb/IIIa inhibitor tirofiban. N Engl J Med 2001; 344: 1879-87.
10. Pell JP, Pell AC, Jeffrey RR, et al. Comparison of survival following coronary artery bypass grafting vs percutaneous coronary intervention in diabetic and non-diabetic patients: retrospective cohort study of 6320 procedures. Diabet Med 2004; 21: 790-92.
11. Jansson PA. Endothelial dysfunction in insulin resistance and type 2 diabetes. J Intern Med 2007; 262: 173-83.
12. Vaidyula VR, Borden G, Koneti Rao A. Platelet and monocyte activation by hyperglycemia and hyperinsulinemia in healthy subjects. Platelets 2006; 17: 577-85.
13. Grant PJ. Diabetes mellitus as a prothrombotic condition. J Intern Med 2007; 262: 157-72. Il lavoro costituisce una completa rassegna sui meccanismi trombotici che il diabete mellito rende più evidenti.
14. Dortimer AC, Shenoy PN, Shiroff RA, et al. Diffuse coronary artery disease in diabetic patients: fact or fiction? Circulation 1978; 57: 133-6.
15. Davies MJ. The pathological basis of angina pectoris. Cardiovasc Drugs Ther 1989; 3 (Suppl 1): 249-55.
16. 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.
17. Devaraj S, Vega-Lopez S, Jialal I. Antioxidants, oxidative stress, and inflammation in diabetes. In: Marso SP, Stern DM, eds. Diabetes and cardiovascular disease. Philadelphia, PA: Lippincott Williams and Wilkins, 2005: 19-35.
18. Rask-Madsen C, King GL. Mechanisms of disease: endothelial dysfunction in insulin resistance and diabetes. Nat Clin Pract Endocrinol Metab 2007; 3: 46-56.
19. Deedwania PC. Mechanisms of endothelial dysfunction in the metabolic syndrome. Curr Diab Rep 2003; 3: 289-92.
20. Beckman JA, Creager MA, Libby P. Diabetes and atherosclerosis: epidemiology, pathophysiology, and management. JAMA 2002; 287: 2570-81.
21. Brownlee M. The pathobiology of diabetic complications. A unifying mechanism. Diabetes 2005; 54: 1615-25. Lettura di Micheal Brownlee che con magistrale semplicità descrive in maniera precisa i meccanismi patologici del diabete meilito.
22. Bansilal S, Farkouh ME, Fuster V. Role of insulin resistance and hyperglycemia in the development of atherosclerosis. Am J Cardiol 2007; 99: 6B-14B.
23. Hartge MN, Unger T, Kintscher U. The endothelium and vascular inflammation in diabetes. Diabetes Vasc Dis Res 2007; 4: 84-8.
24. Duckworth WC. Hyperglycemia and cardiovascular disease. Curr Atheroscler Rep 2001; 3: 383-91.
25. Schalkwijk CG, Stehouwer CD. Vascular complications in diabetes mellitus: the role of endothelial dysfunction. Clin Sci 2005; 109: 143-59.
26. Cosentino F, Hishikawa K, Katusic ZS, Luscher TF. High glucose increases nitric oxide synthase expression and superoxide anion generation in human aortic endothelial cells. Circulation 1997; 96: 25-8. (Pubitemid 27298398)
27. Giugliano D, Ceriello A, Paolisso G. Oxidative stress and diabetic vascular complications. Diabetes Care 1996; 19: 257-67. (Pubitemid 26070354)
28. McVeigh GE. Impaired endothelium-dependent and independent vasodilation in patients with type 2 (non-insulin-dependent) diabetes mellitus. Diabetologia 1992; 35: 771-6.
29. Kario K, Matsuo T, Kobayashi H, Matso T, Miyata T. Activation of tissue factor-induced coagulation and endothelial cell dysfunction in non-insulin-dependent diabetic patients with microalbuminuria. Arterioscler Thromb Vasc Biol 1995; 15: 1114-20.
30. Uemura S, Matsuhita H, Li W, et al. Diabetes mellitus enhances vascular matrix metalloproteinase activity: role of oxidative stress. Circ Res 2001; 88: 1291-8.
31. Fadini GP, Agostini C, Avogaro A. Endothelial progenitor cells and vascular biology in diabetes mellitus: current knowledge and future perspectives. Curr Diabetes Rev 2005; 1: 41-58.
32. Muniyappa R, Montagnani M, Kon Koh K, Quon MJ. Cardiovascular actions of insulin. Endocr Rev 2007; 28: 463-91. Interessante e completa disamina dell'argomento, con numerose citazioni bibliografiche e riferimenti clinici.
33. Schulmann IH, Zhou MS. Vascular insulin resistance: a potential link between cardiovascular and metabolic diseases. Curr Hypertens Rep 2009; 11: 48-55.
34. Federici M, Lauro R. Diabetes and atherosclerosis - running on a common road. Aliment Pharmacol Ther 2005; 22 (Suppl 2): 11-5. (Pubitemid 41564374)
35. Sobel BE, Schneider DJ. Platelet function, coagulopathy, and impaired fibrinolysis in diabetes. Cardiol Clin 2004; 22: 511-26.
36. Kelly RV, Steinhubl S. Platelet dysfunction. In: Marso SP, Stern DM, eds. Diabetes and cardiovascular disease. Philadelphia, PA: Lippincott Williams and Wilkins, 2005: 251-67.
37. Schafer A, Bauersachs J. Endothelial dysfunction, impaired endogenous platelet inhibition and platelet activation in diabetes and atherosclerosis. Curr Vasc Pharmacol 2008; 6: 52-60. Il lavoro costituisce una recente analisi dei processi molecolarl attraverso cul agisce l'iperglicemia.
38. Ferriera IA, Mocking AI, Feijge AH et al. Platelet inhibition by insulin is absent in type 2 diabetes mellitus. Arterioscler Thromb Vasc Biol 2006; 26: 417-22.
39. Angiolillo DJ, Capranzano P, Goto S, et al. A randomized study assessing the impact of cilostazol on platelet function profiles in patients with diabetes mellitus and coronary artery disease on dual anti-platelet therapy: results of the OPTIMUS-2 study. Eur Heart J 2008; 29: 2202-11.
40. Stratmann B, Tschoepe D. Pathobiology and cell interactions of platelets in diabetes. Diab Vasc Dis Res 2005; 2: 16-23. Il lavoro è una dettagliata analisi dei mediatori motecolari rilasciati dalle piastrine. (Pubitemid 40333200)
41. Watanabe Y. Effect of insulin on murine megakaryocytopoiesis in a liquid culture system. Cell Struct Funct 1987; 12: 311-6. (Pubitemid 18080154)
42. Brown AS, Hong Y, de Belder A, et al. Megakaryocyte ploidy and platelet changes in human diabetes and atherosclerosis. Arterioscler Thromb Vasc Biol 1997; 17: 802-7.
43. Anfossi G, Trovati M. Pathophysiology of platelet resistance to anti-aggregating agents in insulin-resistance and type 2 diabetes: implications for anti-aggregating therapy. Cardiovasc Hematol Agents Med Chem 2006; 4: 111-28.
44. Winocour PD, Datala C, Perry DW, Kinlough-Rathbone. Decreased platelet membrane fluidity due to glycation or acetylation of membrane proteins. Thromb Haemost 1992; 68: 577-82.
45. Balleisen L, Assmann G, Bailey J, Epping PH, Shulte H, van de Loo J. Epidemiological study on factor VII, factor VIII and fibrinogen in an industrial population-II. Baseline data on the relation to blood pressure, blood glucose, uric acid, and lipid fractions. Thromb Haemost 1985; 54: 721-3.
46. Heywood DM, Mansfield MW, Grant PJ. Factor VII gene polymorphisms, factor VII:C levels and features of insulin resistance in non-insulin-dependent diabetes mellitus. Thromb Haemost 1996; 75: 401-6.
47. Carvalho de Sousa J, Bruckert E, Giral P et al. Coagulation factor VII and plasma triglycerides. Decreased catabolism as a possible mechanism of factor VII hyperactivity. Haemostasis 1989; 19: 125-30.
48. Conlan MG, Folsom AR, Finch A, et al. Associations of factor VIII and von Willebrand factor with age, race, sex and risk factors for atherosclerosis. The Atherosclerosis Risk in Communities study. Thromb Haemost 1993; 70: 380-5.
49. Haffner SM. Insulin resistance, inflammation and the prediabetic state. Am J Cardiol 2003; 92: 18j-26j.
50. Barazzoni R, Zanetti M, Davanzo G et al. Increased fibrinogen production in type 2 diabetic patients without detectable vascular complications: correlation with plasma glucagon concentrations. J Clin Endocrinol Metab 2000; 85: 3121-5.
51. Schmitz A, Ingerslev J. Haemostatic measures in type 2 diabetic patients with microalbuminuria. Diabet Med 1990; 7: 521-5. (Pubitemid 20199798)
52. Asakawa H, Tokunaga K, Kawakami F. Elevation of fibrinogen and thrombin-antithrombin III complex levels of type 2 diabetes mellitus patients with retinopathy and nephropathy. J Diabetes Complications 2000; 14: 121-6.
53. Missov RM, Stolk RP, van der Bom JG, et al. Plasma fibrinogen in NIDDM: the Rotterdam study. Diabetes Care 1996; 19: 157-9.
54. Reid HL, Vigilance J, Wright-Pascoe RA, Choo-Kang E. The influence of persistent hyperglycaemia on hyperfibrinogenaemia and hyperviscosity in diabetes mellitus. West Indian Med J 2000; 49: 281-4. (Pubitemid 33621518)
55. Emanuele N, Azad N, Abraira C, et al. Effect of intensive glycemic control on fibrinogen, lipids and lipoproteins: Veterans Affairs Cooperative Study in Type II Diabetes Mellitus. Arch Intern Med 1998; 158: 2485-90.
56. Tessari P, Kiwanuka E, Barazzoni R, Vettore M, Zanetti M. Diabetic nephropathy is associated with increased albumin and fibrinogen production in patients with type 2 diabetes. Diabetologie 2006; 49: 1955-61.
57. Tessari P, Kiwanuka E, Millioni R, et al. Albumin and fibrinogen synthesis and insulin effect in type 2 diabetic patients with normoalbuminuria. Diabetes Care 2006; 29: 323-8.
58. Barazzoni R, Kiwanuka E, Zanetti M, Cristini M, Vettore M, Tessari P. Insulin acutely increases fibrinogen production in individuals with type 2 diabetes but not in individuals without diabetes. Diabetes 2003; 52: 1851-6.
59. Sawdey MS, Loskutoff DJ. Regulation of murine type 1 plasminogen activator inhibitor gene expression in vivo. Tissue specificity and induction by lipopolysaccharide, tumor necrosis factor-alpha and transforming growth factor-beta. J Clin Investig 1991; 88: 1346-53.
60. Kooistra T, Bosma PJ, Töns HA, van den Berg AP, Meyer P, Princen HM. Plasminogen activator inhibitor 1: biosynthesis and mRNA level are increased by insulin in cultured human hepatocytes. Thromb Haemost 1989; 62: 723-8.
61. Mussoni L, Maderna P, Camera M, et al. Atherogenic lipoproteins and realease of plasminogen activator inhibitor-1 (PAI-1) by endothelial cells. Fibrinolysis 1990; 4: 79-81.
62. Nordt TK, Klassen KJ, Schneider DJ, Sobel BE. Augementation of synthesis of plasma plasminogen activator inhibitor type-1 in arterial cells by glucose and its implications for local fibrinolysis. Arterioscler Thromb 1993; 13: 1822-8.
63. Calles-Escandon J, Mirza SA, Sobel BE, Schneider DJ. Induction of hyperinsulinemia combined with hyperglycemia and hypertriglyceridemia increases plasminogen activator inhibitor 1 in blood in normal human subjects. Diabetes 1998; 47: 290-3. (Pubitemid 28079991)
64. Festa A, D'Agostino R, Mykkanen L, et al. Relative contribution of insulin and its precursors to fibrinogen and PAI-1 in a large population with different states of glucose tolerance. The Insulin Resistance Atherosclerosis Study (IRAS). Arterioscler Thromb Vasc Biol 1999; 19: 562-8.
65. Festa A, Williams K, Tracy R. Progression of plasminogen activator-1 and fibrinogen levels in relation to incident type 2 diabetes. Circulation 2006; 113: 1753-9.
66. Levitan EB, Song Y, Ford ES, Liu S. Is nondiabetic hyperglycemia a risk factor for cardiovascular disease? A meta-analysis of prospective studies. Arch Intern Med 2004; 164: 2147-55.
67. Ishihara M, Kojima S, Sakamot T, et al. Acute hyperglycemia is associated with adverse outcome after acute myocardial infarction in the coronary intervention era. Am Heart J 2005; 150: 814-20.
68. Undas A, Wiek I, Stepien E, Zmudka K, Tracz W. Hyperglycemia is associated with enhanced thrombin formation, platelet activation, and fibrin clot resistance to lysis in patients with acute coronary syndrome. Diabetes Care 2008; 31: 1590-5.
69. Deedwania P, Kosiborod M, Barrett E, et al. Hyperglycemia and acute coronary syndrome: a scientific statement from the American Heart Association Diabetes Committee of the Council on Nutrition, Physical Activity, and Metabolism. Circulation 2008; 117: 1610-9. Recente statement che puntualizza e approfondisce le problematiche relative all'iperglicemia nei pazienti con sindrome coronarica acuta.
70. Beckman JA. Endothelial dysfunction. In: Marso SP, Stern DM, eds. Diabetes and cardiovascular disease. Philadelphia, PA: Lippincott Williams and Wilkins, 2005: 239-50.
71. De Luca G, Gibson CM, Bellandi F, et al. Diabetes mellitus is associated with distal embolization, impaired myocardial perfusion, and higher mortality in patients with ST-segment elevation myocardial infarction treated with primary angioplasty and glycoprotein IIb/IIIa inhibitors. Atherosclerosis 2009; 207: 181-5.
72. Bartnik M, Rydén L, Ferrari R, et al. The prevalence of abnormal glucose regulation in patients with coronary artery disease across Europe. The Euro Heart Survey on diabetes and the heart. Eur Heart J 2004; 25: 1880-90.
73. Mozaffarian D, Marfisi R, Levantesi G, et al. Incidence of newonset diabetes and impaired fasting glucose in patients with recent myocardial infarction and the effect of clinical lifestyle risk factors. Lancet 2007; 370: 667-75.
74. Show SM, Filds JE, Yonan N, Williams SG. Pleiotropic effects and cholesterol-lowering therapy. Cardiology 2009; 112: 4-12.
75. Bangalore S, Parkar S, Grossman E, Messerli FH. A meta-analysis of 94 492 patients with hypertension treated with beta blockers to determine the risk of new-onset diabetes mellitus. Am J Cardiol 2007; 100: 1254-62.
76. Elliott WJ, Meyer PM. Incident diabetes in clinical trials of antihypertensive drugs: a network meta-analysis. Lancet 2007; 369: 201-7.
77. Wallhaus TR, Taylor M, DeGrado TR, e al. Myocardial free fatty acid and glucose use after carvedilol treatment in patients with congestive heart failure. Circulation 2001; 103: 244-6.
78. Natarajan A, Zaman AG, Marshall SM. Platelet hyperactivity in type 2 diabetes: role of antiplatelet agents. Diab Vasc Dis Res 2008; 5: 138-44. Aggiornata revisione della letteratura. (Pubitemid 351839287)
79. Buse JB, Ginsberg HN, Bakris GL, et al. Primary prevention of cardiovascular diseases in people with diabetes mellitus: a scientific statement from the American Heart Association and the American Diabetes Association. Diabetes Care 2007; 30: 162-72.
80. Antithrombotic Trialists' Collaboration. Collaborative metaanalysis of randomised trials of antiplatelet therapy for prevention of death, myocardial infarction, and stroke in high risk patients. BMJ 2002; 324: 71-86.
81. Sacco M, Pellegrini F, Roncaglioni MC, Avanzini F, Tognoni G, Nicolucci A, for the PPP Collaborative Group. Primary prevention of cardiovascular 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.
82. Cubbon RM, Gale CP, Rajwani A, et al. Aspirin and mortality in patients with diabetes sustaining acute coronary syndrome. Diabetes Care 2008; 31: 363-5.
83. Hankey GJ, Eikelboom JW. Aspirin resistance. Lancet 2006; 367: 606-17.
84. A randomised, blinded, trial of clopidogrel versus aspirin in patients at risk of ischaemic events (CAPRIE). CAPRIE Steering Committee. Lancet 1996; 348: 1329-39.
85. Serebruany VL Malinin AI, Pokov A, Barsness G, Hanley DF. Effects of clopidogrel and aspirin in combination versus aspirin alone on platelet activation and major receptor expression in diabetic patients: the PLavix Use for Treatment Of Diabetes (PLUTO-Diabetes) trial. Am Heart J 2008; 155: 93.e1-7.
86. Yusuf S, Zhao F, Mehta SR, Chrolavicius S, Tognoni G, Fox KK. Effects of clopidogrel in addition to aspirin in patients with acute coronary syndromes without ST-segment elevation. N Engl J Med 2001; 345: 494-502.
87. Mehta SR, Yusuf S, Peters RJ, et al. Effects of pretreatment with clopidogrel and aspirin followed by long-term therapy in patients undergoing percutaneous coronary intervention: the PCI-CURE study. Lancet 2001; 358: 527-33.
88. Roffi M, Chew DP, Mukherjee D, et al. Platelet glycoprotein IIb/IIIa inhibitors reduce mortality in diabetic patients with non-ST-segment-elevation acute coronary syndromes. Circulation 2001; 104: 2767-71.
89. Bhatt DL, Marso SP, Lincoff AM, Wolski KE, Ellis SG, Topol EJ. Abciximab reduces mortality in diabetics following percutaneous coronary intervention. J Am Coll Cardiol 2000; 35: 922-8.
90. Angiolillo DJ, Bernardo E, Sabaté M, et al. Impact of platelet reactivity on cardiovascular outcomes in patients with type 2 diabetes mellitus and coronary artery disease. J Am Coll Cardiol 2007; 50: 1541-7.
91. Singh I, Shafiq N, Pandhi P, et al. Triple antiplatelet therapy vs dual antiplatelet therapy in patients undergoing percutaneous coranary intervention: an evidence-based approach to answering a clinical query. Br J Clin Pharmacol 2009; 68: 4.
92. Timmer JR, Ottervanger JP, de Boer MJ, et al. Hyperglycemia is an important predictor of impaired coronary flow before reperfusion therapy in ST-segment elevation myocardial infarction. J Am Coll Cardiol 2005; 45: 999-1002.