European Journal of Internal Medicine
Volume 20, Issue 3 , Pages 253-260 , May 2009

The role of inflammation on atherosclerosis, intermediate and clinical cardiovascular endpoints in type 2 diabetes mellitus

Received 26 September 2007 ,Revised 23 June 2008 ,Accepted 7 July 2008.

References 

  1. Barrett-Connor EL, Cohn BA, Wingard DL, Edelstein SL. Why is diabetes mellitus a stronger risk factor for fatal ischemic heart disease in women than in men? The Rancho Bernardo Study. JAMA. 1991;265:627–631
  2. Haffner SM, Lehto S, Ronnemaa T, Pyorala K, Laakso M. 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;339:229–234
  3. Kannel WB, McGee DL. Diabetes and cardiovascular disease. The Framingham study. JAMA. 1979;241:2035–2038
  4. Stamler J, Vaccaro O, Neaton JD, Wentworth D. Diabetes, other risk factors, and 12-yr cardiovascular mortality for men screened in the Multiple Risk Factor Intervention Trial. Diabetes Care. 1993;16:434–444
  5. Vaccaro O, Eberly LE, Neaton JD, Yang L, Riccardi G, Stamler J. Impact of diabetes and previous myocardial infarction on long-term survival: 25-year mortality follow-up of primary screenees of the Multiple Risk Factor Intervention Trial. Arch Intern Med. 2004;164:1438–1443
  6. Libby P, Ridker PM, Maseri A. Inflammation and atherosclerosis. Circulation. 2002;105:1135–1143
  7. Ridker PM, Buring JE, Shih J, Matias M, Hennekens CH. Prospective study of C-reactive protein and the risk of future cardiovascular events among apparently healthy women. Circulation. 1998;98:731–733
  8. Ridker PM. Clinical application of C-reactive protein for cardiovascular disease detection and prevention. Circulation. 2003;107:363–369
  9. Duncan BB, Schmidt MI, Pankow JS, Ballantyne CM, Couper D, Vigo A, et al. Low-grade systemic inflammation and the development of type 2 diabetes: the atherosclerosis risk in communities study. Diabetes. 2003;52:1799–1805
  10. Mehta JL, Rasouli N, Sinha AK, Molavi B. Oxidative stress in diabetes: a mechanistic overview of its effects on atherogenesis and myocardial dysfunction. Int J Biochem Cell Biol. 2006;38:794–803
  11. Moreno PR, Murcia AM, Palacios IF, Leon MN, Bernardi VH, Fuster V, et al. Coronary composition and macrophage infiltration in atherectomy specimens from patients with diabetes mellitus. Circulation. 2000;102:2180–2184
  12. Burke AP, Kolodgie FD, Zieske A, Fowler DR, Weber DK, Varghese PJ, et al. Morphologic findings of coronary atherosclerotic plaques in diabetics: a postmortem study. Arterioscler Thromb Vasc Biol. 2004;24:1266–1271
  13. Marfella R, D'Amico M, Esposito K, Baldi A, Di FC, Siniscalchi M. The ubiquitin–proteasome system and inflammatory activity in diabetic atherosclerotic plaques: effects of rosiglitazone treatment. Diabetes. 2006;55:622–632
  14. Lassila M, Allen TJ, Cao Z, Thallas V, Jandeleit-Dahm KA, Candido R, et al. Imatinib attenuates diabetes-associated atherosclerosis. Arterioscler Thromb Vasc Biol. 2004;24:935–942
  15. Wendt T, Harja E, Bucciarelli L, Qu W, Lu Y, Rong LL, et al. RAGE modulates vascular inflammation and atherosclerosis in a murine model of type 2 diabetes. Atherosclerosis. 2006;185:70–77
  16. Bucciarelli LG, Wendt T, Qu W, Lu Y, Lalla E, Rong LL, et al. RAGE blockade stabilizes established atherosclerosis in diabetic apolipoprotein E-null mice. Circulation. 2002;106:2827–2835
  17. Sommeijer DW, Beganovic A, Schalkwijk CG, Ploegmakers H, van der Loos CM, van Aken BE, et al. More fibrosis and thrombotic complications but similar expression patterns of markers for coagulation and inflammation in symptomatic plaques from DM2 patients. J Histochem Cytochem. 2004;52:1141–1149
  18. Schleicher ED, Wagner E, Nerlich AG. Increased accumulation of the glycoxidation product N(epsilon)-(carboxymethyl)lysine in human tissues in diabetes and aging. J Clin Invest. 1997;99:457–468
  19. Tan KC, Chow WS, Tam S, Bucala R, Betteridge J. Association between acute-phase reactants and advanced glycation end products in type 2 diabetes. Diabetes Care. 2004;27:223–228
  20. Kilhovd BK, Berg TJ, Birkeland KI, Thorsby P, Hanssen KF. Serum levels of advanced glycation end products are increased in patients with type 2 diabetes and coronary heart disease. Diabetes Care. 1999;22:1543–1548
  21. Sharp PS, Rainbow S, Mukherjee S. Serum levels of low molecular weight advanced glycation end products in diabetic subjects. Diabet Med. 2003;20:575–579
  22. Cai W, He JC, Zhu L, Lu C, Vlassara H. Advanced glycation end product (AGE) receptor 1 suppresses cell oxidant stress and activation signaling via EGF receptor. Proc Natl Acad Sci USA. 2006;103:13801–13806
  23. Lu C, He JC, Cai W, Liu H, Zhu L, Vlassara H. Advanced glycation endproduct (AGE) receptor 1 is a negative regulator of the inflammatory response to AGE in mesangial cells. Proc Natl Acad Sci USA. 2004;101:11767–11772
  24. Basta G, Lazzerini G, Massaro M, Simoncini T, Tanganelli P, Fu C, et al. Advanced glycation end products activate endothelium through signal-transduction receptor RAGE: a mechanism for amplification of inflammatory responses. Circulation. 2002;105:816–822
  25. Brett J, Schmidt AM, Yan SD, Zou YS, Weidman E, Pinsky D, et al. Survey of the distribution of a newly characterized receptor for advanced glycation end products in tissues. Am J Pathol. 1993;143:1699–1712
  26. Brownlee M. Advanced protein glycosylation in diabetes and aging. Annu Rev Med. 1995;46:223–234
  27. Baynes JW. Role of oxidative stress in development of complications in diabetes. Diabetes. 1991;40:405–412
  28. Nakamura K, Yamagishi S, Adachi H, Kurita-Nakamura Y, Matsui T, Yoshida T, et al. Serum levels of sRAGE, the soluble form of receptor for advanced glycation end products, are associated with inflammatory markers in patients with type 2 diabetes. Mol Med. 2007;13:185–189
  29. Ehlermann P, Eggers K, Bierhaus A, Most P, Weichenhan D, Greten J, et al. Increased proinflammatory endothelial response to S100A8/A9 after preactivation through advanced glycation end products. Cardiovasc Diabetol. 2006;5:6
  30. Cipollone F, Iezzi A, Fazia M, Zucchelli M, Pini B, Cuccurullo C, et al. The receptor RAGE as a progression factor amplifying arachidonate-dependent inflammatory and proteolytic response in human atherosclerotic plaques: role of glycemic control. Circulation. 2003;108:1070–1077
  31. Kislinger T, Fu C, Huber B, Qu W, Taguchi A, DU YS, et al. N(epsilon)-(carboxymethyl)lysine adducts of proteins are ligands for receptor for advanced glycation end products that activate cell signaling pathways and modulate gene expression. J Biol Chem. 1999;274:31740–31749
  32. Cipollone F, Iezzi A, Fazia M, Zucchelli M, Pini B, Cuccurullo C, et al. The receptor RAGE as a progression factor amplifying arachidonate-dependent inflammatory and proteolytic response in human atherosclerotic plaques: role of glycemic control. Circulation. 2003;108:1070–1077
  33. Figarola JL, Shanmugam N, Natarajan R, Rahbar S. Anti-inflammatory effects of the advanced glycation end product inhibitor LR-90 in human monocytes. Diabetes. 2007;56:647–655
  34. Bucciarelli LG, Wendt T, Qu W, Lu Y, Lalla E, Rong LL, et al. RAGE blockade stabilizes established atherosclerosis in diabetic apolipoprotein E-null mice. Circulation. 2002;106:2827–2835
  35. Herrmann J, Ciechanover A, Lerman LO, Lerman A. The ubiquitin–proteasome system in cardiovascular diseases—a hypothesis extended. Cardiovasc Res. 2004;61:11–21
  36. Palombella VJ, Rando OJ, Goldberg AL, Maniatis T. The ubiquitin–proteasome pathway is required for processing the NF-kappa B1 precursor protein and the activation of NF-kappa B. Cell. 1994;78:773–785
  37. Parikh A, Daneman D. Is carotid ultrasound a useful tool in assessing cardiovascular disease in individuals with diabetes?. Diabetes Technol Ther. 2004;6:65–69
  38. Lehmann ED, Riley WA, Clarkson P, Gosling RG. Non-invasive assessment of cardiovascular disease in diabetes mellitus. Lancet. 1997;350(Suppl 1):SI14–SI19
  39. Metcalf PA, Folsom AR, Davis CE, Wu KK, Heiss G. Haemostasis and carotid artery wall thickness in non-insulin dependent diabetes mellitus. Diabetes Res Clin Pract. 2000;47:25–35
  40. Mita T, Watada H, Uchino H, Shimizu T, Hirose T, Tanaka Y, et al. Association of C-reactive protein with early-stage carotid atherosclerosis in Japanese patients with early-state type 2 diabetes mellitus. Endocr J. 2006;53:693–698
  41. Sander D, Schulze-Horn C, Bickel H, Gnahn H, Bartels E, Conrad B. Combined effects of hemoglobin A1c and C-reactive protein on the progression of subclinical carotid atherosclerosis: the INVADE study. Stroke. 2006;37:351–357
  42. Corrado E, Rizzo M, Muratori I, Coppola G, Novo S. Association of elevated fibrinogen and C-reactive protein levels with carotid lesions in patients with newly diagnosed hypertension or type II diabetes. Arch Med Res. 2006;37:1004–1009
  43. Nystrom T, Nygren A, Sjoholm A. Persistent endothelial dysfunction is related to elevated C-reactive protein (CRP) levels in type II diabetic patients after acute myocardial infarction. Clin Sci (Lond). 2005;108:121–128
  44. Wakabayashi I, Masuda H. Lipoprotein (a) as a determinant of arterial stiffness in elderly patients with type 2 diabetes mellitus. Clin Chim Acta. 2006;373:127–131
  45. Wakabayashi I, Masuda H. Association of acute-phase reactants with arterial stiffness in patients with type 2 diabetes mellitus. Clin Chim Acta. 2006;365:230–235
  46. Nakamura A, Shikata K, Hiramatsu M, Nakatou T, Kitamura T, Wada J, et al. Serum interleukin-18 levels are associated with nephropathy and atherosclerosis in Japanese patients with type 2 diabetes. Diabetes Care. 2005;28:2890–2895
  47. Takebayashi K, Suetsugu M, Matsutomo R, Wakabayashi S, Aso Y, Inukai T. Correlation of high-sensitivity C-reactive protein and plasma fibrinogen with individual complications in patients with type 2 diabetes. South Med J. 2006;99:23–27
  48. Leinonen ES, Hiukka A, Hurt-Camejo E, Wiklund O, Sarna SS, Mattson HL, et al. Low-grade inflammation, endothelial activation and carotid intima-media thickness in type 2 diabetes. J Intern Med. 2004;256:119–127
  49. Sigurdardottir V, Fagerberg B, Hulthe J. Preclinical atherosclerosis and inflammation in 61-year-old men with newly diagnosed diabetes and established diabetes. Diabetes Care. 2004;27:880–884
  50. Dullaart RP, de VR, van TA, Sluiter WJ. Lower plasma adiponectin is a marker of increased intima-media thickness associated with type 2 diabetes mellitus and with male gender. Eur J Endocrinol. 2007;156:387–394
  51. Stocker DJ, Taylor AJ, Langley RW, Jezior MR, Vigersky RA. A randomized trial of the effects of rosiglitazone and metformin on inflammation and subclinical atherosclerosis in patients with type 2 diabetes. Am Heart J. 2007;153:445–446
  52. Hedblad B, Zambanini A, Nilsson P, Janzon L, Berglund G. Rosiglitazone and carotid IMT progression rate in a mixed cohort of patients with type 2 diabetes and the insulin resistance syndrome: main results from the Rosiglitazone Atherosclerosis Study. J Intern Med. 2007;261:293–305
  53. Tan KC, Chow WS, Tam SC, Ai VH, Lam CH, Lam KS. Atorvastatin lowers C-reactive protein and improves endothelium-dependent vasodilation in type 2 diabetes mellitus. J Clin Endocrinol Metab. 2002;87:563–568
  54. Martens FM, Visseren FL, de Koning EJ, Rabelink TJ. Short-term pioglitazone treatment improves vascular function irrespective of metabolic changes in patients with type 2 diabetes. J Cardiovasc Pharmacol. 2005;46:773–778
  55. Ballantyne CM, Hoogeveen RC, Bang H, Coresh J, Folsom AR, Chambless LE, et al. Lipoprotein-associated phospholipase A2, high-sensitivity C-reactive protein and risk for incident ischemic stroke in middle-aged men and women in the Atherosclerosis Risk in, Communities (ARIC) study. Arch Intern Med. 2005;165:2479–2484
  56. Bos MJ, Schipper CM, Koudstaal PJ, Witteman JC, Hofman A, Breteler MM. High serum C-reactive protein level is not an independent predictor for stroke: the Rotterdam Study. Circulation. 2006;114:1591–1598
  57. Cushman M, Arnold AM, Psaty BM, Manolio TA, Kuller LH, Burke GL, et al. C-reactive protein and the 10-year incidence of coronary heart disease in older men and women: the cardiovascular health study. Circulation. 2005;112:25–31
  58. Folsom AR, Aleksic N, Catellier D, Juneja HS, Wu KK. C-reactive protein and incident coronary heart disease in the Atherosclerosis Risk In Communities (ARIC) study. Am Heart J. 2002;144:233–238
  59. Heinrich J, Balleisen L, Schulte H, Assmann G, van de LJ. Fibrinogen and factor VII in the prediction of coronary risk. Results from the PROCAM study in healthy men. Arterioscler Thromb. 1994;14:54–59
  60. Koenig W, Lowel H, Baumert J, Meisinger C. C-reactive protein modulates risk prediction based on the Framingham Score: implications for future risk assessment: results from a large cohort study in southern Germany. Circulation. 2004;109:1349–1353
  61. Rost NS, Wolf PA, Kase CS, Kelly-Hayes M, Silbershatz H, Massaro JM, et al. Plasma concentration of C-reactive protein and risk of ischemic stroke and transient ischemic attack: the Framingham study. Stroke. 2001;32:2575–2579
  62. Streja D, Cressey P, Rabkin SW. Associations between inflammatory markers, traditional risk factors, and complications in patients with type 2 diabetes mellitus. J Diabetes its Complicat. 2003;17:120–127
  63. de Jager J, Dekker JM, Kooy A, Kostense PJ, Nijpels G, Heine RJ, et al. Endothelial dysfunction and low-grade inflammation explain much of the excess cardiovascular mortality in individuals with type 2 diabetes: the Hoorn Study. Arterioscler Thromb Vasc Biol. 2006;26:1086–1093
  64. Matsumoto K, Sera Y, Abe Y, Ueki Y, Tominaga T, Miyake S. Inflammation and insulin resistance are independently related to all-cause of death and cardiovascular events in Japanese patients with type 2 diabetes mellitus. Atherosclerosis. 2003;169:317–321
  65. Schulze MB, Rimm EB, Li T, Rifai N, Stampfer MJ, Hu FB. C-reactive protein and incident cardiovascular events among men with diabetes. Diabetes Care. 2004;27:889–894
  66. Wattanakit K, Folsom AR, Chambless LE, Nieto FJ. Risk factors for cardiovascular event recurrence in the Atherosclerosis Risk in Communities (ARIC) study. Am Heart J. 2005;149:606–612
  67. Schillinger M, Exner M, Amighi J, Mlekusch W, Sabeti S, Rumpold H, et al. Joint effects of C-reactive protein and glycated hemoglobin in predicting future cardiovascular events of patients with advanced atherosclerosis. Circulation. 2003;108:2323–2328
  68. Jager A, van H, Kostense PJ, Emeis JJ, Yudkin JS, Nijpels G, et al. von Willebrand factor, C-reactive protein, and 5-year mortality in diabetic and nondiabetic subjects: the Hoorn Study. Arterioscler Thromb Vasc Biol. 1999;19:3071–3078
  69. Sander D, Schulze-Horn C, Bickel H, Gnahn H, Bartels E, Conrad B. Combined effects of hemoglobin A1c and C-reactive protein on the progression of subclinical carotid atherosclerosis: the INVADE study. Stroke. 2006;37:351–357
  70. Corrado E, Rizzo M, Muratori I, Coppola G, Novo S. Association of elevated fibrinogen and C-reactive protein levels with carotid lesions in patients with newly diagnosed hypertension or type II diabetes. Arch Med Res. 2006;37:1004–1009

PII: S0953-6205(08)00208-2

doi: 10.1016/j.ejim.2008.07.008

European Journal of Internal Medicine
Volume 20, Issue 3 , Pages 253-260 , May 2009