European Journal of Internal Medicine
Volume 19, Issue 2 , Pages 115-121 , March 2008

The impact of metabolic syndrome and CRP on vascular phenotype in type 2 diabetes mellitus

  • Reza Alizadeh Dehnavi

      Affiliations

    • Vascular Medicine, Department of General Internal Medicine & Endocrinology, Leiden University Medical Centre, Leiden, The Netherlands
    • Corresponding Author InformationCorresponding author. Vascular Medicine C4-R, Department General Internal Medicine & Endocrinology, Leiden University Medical Centre, P.O. Box 9600, 2300 RC Leiden, The Netherlands. Tel.: +31 71 5264684; fax: +31 71 5248140.
  • ,
  • Edith D. Beishuizen

      Affiliations

    • Vascular Medicine, Department of General Internal Medicine & Endocrinology, Leiden University Medical Centre, Leiden, The Netherlands
  • ,
  • Marcel A. van de Ree

      Affiliations

    • Department of Internal Medicine, Diakonessenhuis, Utrecht, The Netherlands
  • ,
  • Saskia Le Cessie

      Affiliations

    • Department of Medical Statistics and Bio-Informatics, Leiden University Medical Centre, Leiden, The Netherlands
  • ,
  • Menno V. Huisman

      Affiliations

    • Vascular Medicine, Department of General Internal Medicine & Endocrinology, Leiden University Medical Centre, Leiden, The Netherlands
  • ,
  • Cornelis Kluft

      Affiliations

    • Gaubius Laboratory TNO-QoL, Leiden, The Netherlands
  • ,
  • Hans M.G. Princen

      Affiliations

    • Gaubius Laboratory TNO-QoL, Leiden, The Netherlands
  • ,
  • Jouke T. Tamsma

      Affiliations

    • Vascular Medicine, Department of General Internal Medicine & Endocrinology, Leiden University Medical Centre, Leiden, The Netherlands

Received 27 August 2006 ,Revised 20 April 2007 ,Accepted 12 June 2007.

References 

  1. Kannel WB, McGee DL. Diabetes and cardiovascular disease. The Framingham study. JAMA. 1979;241(19):2035–2038
  2. Role of cardiovascular risk factors in prevention and treatment of macrovascular disease in diabetes. American Diabetes Association Diabetes Care. 1989;12(8):573–579
  3. 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(2):434–444
  4. 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(5):1210–1214
  5. 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(4):229–234
  6. Ridker PM, Wilson PW, Grundy SM. Should C-reactive protein be added to metabolic syndrome and to assessment of global cardiovascular risk?. Circulation. 2004;109(23):2818–2825
  7. Ridker PM, Buring JE, Cook NR, Rifai N. C-reactive protein, the metabolic syndrome, and risk of incident cardiovascular events: an 8-year follow-up of 14719 initially healthy American women. Circulation. 2003;107(3):391–397
  8. Järvisalo MJ, Harmoinen A, Hakanen M, Paakkunainen U, Viikari J, Hartiala J, et al. Elevated serum C-reactive protein levels and early arterial changes in healthy children. Arterioscler Thromb Vasc Biol. 2002;22(8):1323–1328
  9. Blackburn R, Giral P, Bruckert E, André JM, Gonbert S, Bernard M, et al. Elevated C-reactive protein constitutes an independent predictor of advanced carotid plaques in dyslipidemic subjects. Arterioscler Thromb Vasc Biol. 2001;21(12):1962–1968
  10. Heinrich J, Schulte H, Schonfeld R, Kohler E, Assmann G. Association of variables of coagulation, fibrinolysis and acute-phase with atherosclerosis in coronary and peripheral arteries and those arteries supplying the brain. Thromb Haemost. 1995;73(3):374–379
  11. Hak AE, Stehouwer CD, Bots ML, Polderman KH, Schalkwijk CG, Westendorp IC, et al. Associations of C-reactive protein with measures of obesity, insulin resistance, and subclinical atherosclerosis in healthy, middle-aged women. Arterioscler Thromb Vasc Biol. 1999;19(8):1986–1991
  12. Willeit J, Kiechl S, Oberhollenzer F, Rungger G, Egger G, Bonora E, et al. Distinct risk profiles of early and advanced atherosclerosis: prospective results from the Bruneck Study. Arterioscler Thromb Vasc Biol. 2000;20(2):529–537
  13. Timpson NJ, Lawlor DA, Harbord RM, Gaunt TR, Day IN, Palmer LJ, et al. C-reactive protein and its role in metabolic syndrome: Mendelian randomisation study. Lancet. 2005;366(9501):1954–1959
  14. Arad Y, Newstein D, Cadet F, Roth M, Guerci AD. Association of multiple risk factors and insulin resistance with increased prevalence of asymptomatic coronary artery disease by an electron-beam computed tomographic study. Arterioscler Thromb Vasc Biol. 2001;21(12):2051–2058
  15. The effect of aggressive versus standard lipid lowering by atorvastatin on diabetic dyslipidemia: the DALI study: a double-blind, randomized, placebo-controlled trial in patients with type 2 diabetes and diabetic dyslipidemia. Diabetes Care. 2001;24(8):1335–1341
  16. World Health Organization . Definition, diagnosis and classification of diabetes mellitus and its complications: report of a WHO Consultation. In: Part 1: diagnosis and classification of diabetes mellitus. Geneva, Switzerland: World Health Organization; 1999;Available at: http://whqlibdoc.who.int/hq/1999/WHO_NCD_NCS_99.2.pdf. Accessed December 12, 2003
  17. de Maat MP, de Bart AC, Hennis BC, Meijer P, Havelaar AC, Mulder PG, et al. Interindividual and intraindividual variability in plasma fibrinogen, TPA antigen, PAI activity, and CRP in healthy, young volunteers and patients with angina pectoris. Arterioscler Thromb Vasc Biol. 1996;16(9):1156–1162
  18. Clauss A. Rapid physiological coagulation method in determination of fibrinogen. Acta Haematol. 1957;17(4):237–246
  19. Meijer P, Pollet DE, Wauters J, Kluft C. Specificity of antigen assays of plasminogen activator inhibitor in plasma: Innotest PAI-1 immunoassay evaluated. Clin Chem. 1994;40(1):110–115
  20. Ingerslev J. A sensitive ELISA for von Willebrand factor (vWf:Ag). Scand J Clin Lab Invest. 1987;47(2):143–149
  21. van Venrooij FV, van de Ree MA, Bots ML, Stolk RP, Huisman MV, Banga JD, et al. Aggressive lipid lowering does not improve endothelial function in type 2 diabetes: the Diabetes Atorvastatin Lipid Intervention (DALI) Study: a randomized, double-blind, placebo-controlled trial. Diabetes Care. 2002;25(7):1211–1216
  22. Naumnik B, Borawski J, Pawlak K, Mysliwiec M. Renal function, proteinuria and ACE-inhibitor therapy as determinants of plasma levels of endothelial markers. Nephrol Dial Transplant. 2002;17(3):526–528
  23. Rustom R, Leggat H, Tomura HR, Hay CR, Bone JM. Plasma thrombomodulin in renal disease: effects of renal function and proteinuria. Clin Nephrol. 1998;50(6):337–341
  24. Aso Y, Inukai T, Takemura Y. Mechanisms of elevation of serum and urinary concentrations of soluble thrombomodulin in diabetic patients: possible application as a marker for vascular endothelial injury. Metabolism. 1998;47(3):362–365
  25. van Dam MJ, de Groot E, Clee SM, Hovingh K, Roelants R, Brooks-Wilson A, et al. Association between increased arterial-wall thickness and impairment in ABCA1-driven cholesterol efflux: an observational study. Lancet. 2002;359(9300):37–42
  26. Lempiainen P, Mykkanen L, Pyorala K, Laakso M, Kuusisto J. Insulin resistance syndrome predicts coronary heart disease events in elderly nondiabetic men. Circulation. 1999;100(2):123–128
  27. Anand SS, Yi Q, Gerstein H, Lonn E, Jacobs R, Vuksan V, et al. Relationship of metabolic syndrome and fibrinolytic dysfunction to cardiovascular disease. Circulation. 2003;108(4):420–425
  28. Sakkinen PA, Wahl P, Cushman M, Lewis MR, Tracy RP. Clustering of procoagulation, inflammation, and fibrinolysis variables with metabolic factors in insulin resistance syndrome. Am J Epidemiol. 2000;152(10):897–907
  29. Bonora E, Kiechl S, Willeit J, Oberhollenzer F, Egger G, Bonadonna RC, et al. Carotid atherosclerosis and coronary heart disease in the metabolic syndrome: prospective data from the Bruneck study. Diabetes Care. 2003;26(4):1251–1257
  30. Hulthe J, Bokemark L, Wikstrand J, Fagerberg B. The metabolic syndrome, LDL particle size, and atherosclerosis: the Atherosclerosis and Insulin Resistance (AIR) study. Arterioscler Thromb Vasc Biol. 2000;20(9):2140–2147
  31. Olijhoek JK, van Der Graaf Y, Banga JD, Algra A, Rabelink TJ, Visseren FL, et al. The metabolic syndrome is associated with advanced vascular damage in patients with coronary heart disease, stroke, peripheral arterial disease or abdominal aortic aneurysm. Eur Heart J. 2004;25(4):342–348
  32. Hsia J, Bittner V, Tripputi M, Howard BV. Metabolic syndrome and coronary angiographic disease progression: the women's angiographic vitamin & estrogen trial. Am Heart J. 2003;146(3):439–445
  33. Meigs JB, Mittleman MA, Nathan DM, Tofler GH, Singer DE, Murphy-Sheehy PM, et al. Hyperinsulinemia, hyperglycemia, and impaired hemostasis: the Framingham offspring study. JAMA. 2000;283(2):221–228
  34. Juhan-Vague I, Alessi MC, Mavri A, Morange PE. Plasminogen activator inhibitor-1, inflammation, obesity, insulin resistance and vascular risk. J Thromb Haemost. 2003;1(7):1575–1579
  35. Sobel BE, Woodcock-Mitchell J, Schneider DJ, Holt RE, Marutsuka K, Gold H, et al. Increased plasminogen activator inhibitor type 1 in coronary artery atherectomy specimens from type 2 diabetic compared with nondiabetic patients: a potential factor predisposing to thrombosis and its persistence. Circulation. 1998;97(22):2213–2221
  36. Beishuizen ED, van de Ree MA, Jukema JW, Tamsma JT, van der Vijver JC, Meinders AE, et al. Two-year statin therapy does not alter the progression of intima-media thickness in patients with type 2 diabetes without manifest cardiovascular disease. Diabetes Care. 2004;27(12):2887–2892
  37. Evans M, Anderson RA, Graham J, Ellis GR, Morris K, Davies S, et al. Ciprofibrate therapy improves endothelial function and reduces postprandial lipemia and oxidative stress in type 2 diabetes mellitus. Circulation. 2000;101(15):1773–1779
  38. Beishuizen ED, Tamsma JT, Jukema JW, van de Ree MA, van der Vijver JC, Meinders AE, et al. The effect of statin therapy on endothelial function in type 2 diabetes without manifest cardiovascular disease. Diabetes Care. 2005;28(7):1668–1674
  39. Tan KC, Chow WS, Tam SC, Ai VH, Lam CH, Lam KS, et al. Atorvastatin lowers C-reactive protein and improves endothelium-dependent vasodilation in type 2 diabetes mellitus. J Clin Endocrinol Metab. 2002;87(2):563–568

 Grant support: The study was supported in part by an unconditional research grant from Pfizer BV, The Netherlands.

PII: S0953-6205(07)00255-5

doi: 10.1016/j.ejim.2007.06.011

European Journal of Internal Medicine
Volume 19, Issue 2 , Pages 115-121 , March 2008