Nutrition, Metabolism & Cardiovascular Diseases
Volume 21, Issue 4 , Pages 286-293 , April 2011

Microangiopathy is independently associated with presence, severity and composition of carotid atherosclerosis in type 2 diabetes

  • S. Vigili de Kreutzenberg

      Affiliations

    • Department of Clinical and Experimental Medicine, University of Padova, Via Giustiniani, 2, 35128 Padova, Italy
    • Corresponding Author InformationCorresponding author. Tel.: +39 49 8212183; fax: +39 49 8754179.
    • ,
  • A. Coracina

      Affiliations

    • Department of Clinical and Experimental Medicine, University of Padova, Via Giustiniani, 2, 35128 Padova, Italy
    • ,
  • A. Volpi

      Affiliations

    • Diabetologic Unit, Montebelluna Hospital, Treviso, Italy
    • ,
  • G.P. Fadini

      Affiliations

    • Department of Clinical and Experimental Medicine, University of Padova, Via Giustiniani, 2, 35128 Padova, Italy
    • ,
  • A.C. Frigo

      Affiliations

    • Department of Environmental Medicine and Public Health, University of Padova, Italy
    • ,
  • G. Guarneri

      Affiliations

    • Department of Clinical and Experimental Medicine, University of Padova, Via Giustiniani, 2, 35128 Padova, Italy
    • ,
  • A. Tiengo

      Affiliations

    • Department of Clinical and Experimental Medicine, University of Padova, Via Giustiniani, 2, 35128 Padova, Italy
    • ,
  • A. Avogaro

      Affiliations

    • Department of Clinical and Experimental Medicine, University of Padova, Via Giustiniani, 2, 35128 Padova, Italy

Received 14 July 2009 ,Revised 7 October 2009 ,Accepted 9 October 2009.

References 

  1. Brownlee M. The pathobiology of diabetic complications: a unifying mechanism. Diabetes. 2005;54:1615–1625
  2. Goldin A, Beckman JA, Schmidt AM, Creager MA. Advanced glycation end products: sparking the development of diabetic vascular injury. Circulation. 2006;114:597–605
  3. Doyle B, Caplice N. Plaque neovascularization and antiangiogenic therapy for atherosclerosis. J Am Coll Cardiol. 2007;49:2073–2080
  4. Prati P, Tosetto A, Vanuzzo D, et al. Carotid intima media thickness and plaques can predict the occurrence of ischemic cerebrovascular events. Stroke. 2008;39:2470–2476
  5. Lorenz MW, Markus HS, Bots ML, Rosvall M, Sitzer M. Prediction of clinical cardiovascular events with carotid intima–media thickness: a systematic review and meta-analysis. Circulation. 2007;115:459–467
  6. Bernard S, Serusclat A, Targe F, et al. Incremental predictive value of carotid ultrasonography in the assessment of coronary risk in a cohort of asymptomatic type 2 diabetic subjects. Diabetes Care. 2005;28:1158–1162
  7. Vigili de Kreutzenberg S, Tiengo A, Avogaro A. Cerebrovascular disease in diabetes mellitus: the role of carotid intima–media thickness. Nutr Metab Cardiovasc Dis. 2009;19:667–673
  8. Wofford JL, Kahl FR, Howard GR, et al. Relation of extent of extracranial carotid artery atherosclerosis as measured by B-mode ultrasound to the extent of coronary atherosclerosis. Arterioscler Thromb. 1991;11:1786–1794
  9. Taylor AJ. Atherosclerosis imaging to detect and monitor cardiovascular risk. Am J Cardiol. 2002;90:8L–11L
  10. 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
  11. Chambless LE, Heiss G, Folsom AR, et al. Association of coronary heart disease incidence with carotid arterial wall thickness and major risk factors: the Atherosclerosis Risk in Communities (ARIC) Study, 1987–1993. Am J Epidemiol. 1997;146:483–494
  12. Rohani M, Jogestrand T, Ekberg M, et al. Interrelation between the extent of atherosclerosis in the thoracic aorta, carotid intima–media thickness and the extent of coronary artery disease. Atherosclerosis. 2005;179:311–316
  13. Henry RM, Kostense PJ, Spijkerman AM, et al. Arterial stiffness increases with deteriorating glucose tolerance status: the Hoorn Study. Circulation. 2003;107:2089–2095
  14. Wei M, Gonzalez C, Haffner SM, O'Leary DH, Stern MP. Ultrasonographically assessed maximum carotid artery wall thickness in Mexico City residents and Mexican Americans living in San Antonio, Texas. Association with diabetes and cardiovascular risk factors. Arterioscler Thromb Vasc Biol. 1996;16:1388–1392
  15. Burke GL, Evans GW, Riley WA, et al. Arterial wall thickness is associated with prevalent cardiovascular disease in middle-aged adults. The Atherosclerosis Risk in Communities (ARIC) Study. Stroke. 1995;26:386–391
  16. Juutilainen A, Lehto S, Ronnemaa T, Pyorala K, Laakso M. Retinopathy predicts cardiovascular mortality in type 2 diabetic men and women. Diabetes Care. 2007;30:292–299
  17. Cheung N, Wang JJ, Klein R, et al. Diabetic retinopathy and the risk of coronary heart disease: the Atherosclerosis Risk in Communities Study. Diabetes Care. 2007;30:1742–1746
  18. Simons PC, Algra A, Bots ML, Grobbee DE, van der Graaf Y. Common carotid intima–media thickness and arterial stiffness: indicators of cardiovascular risk in high-risk patients. The SMART Study (Second Manifestations of ARTerial disease). Circulation. 1999;100:951–957
  19. Wong TY, Rosamond W, Chang PP, et al. Retinopathy and risk of congestive heart failure. JAMA. 2005;293:63–69
  20. Malecki MT, Osmenda G, Walus-Miarka M, et al. Retinopathy in type 2 diabetes mellitus is associated with increased intima–media thickness and endothelial dysfunction. Eur J Clin Invest. 2008;38:925–930
  21. Spijkerman AM, Gall MA, Tarnow L, et al. Endothelial dysfunction and low-grade inflammation and the progression of retinopathy in Type 2 diabetes. Diabet Med. 2007;24:969–976
  22. Krantz JS, Mack WJ, Hodis HN, et al. Early onset of subclinical atherosclerosis in young persons with type 1 diabetes. J Pediatr. 2004;145:452–457
  23. Grading diabetic retinopathy from stereoscopic color fundus photographs–an extension of the modified Airlie House classification. ETDRS report number 10. Early Treatment Diabetic Retinopathy Study Research Group. Ophthalmology. 1991;98:786–806
  24. Touboul PJ, Hennerici MG, Meairs S, et al. Mannheim carotid intima–media thickness consensus (2004–2006). An update on behalf of the Advisory Board of the 3rd and 4th Watching the Risk Symposium, 13th and 15th European Stroke Conferences, Mannheim, Germany, 2004, and Brussels, Belgium, 2006. Cerebrovasc Dis. 2007;23:75–80
  25. Carotid artery plaque composition—relationship to clinical presentation and ultrasound B-mode imaging. European Carotid Plaque Study Group. Eur J Vasc Endovasc Surg. 1995;10:23–30
  26. Mathiesen EB, Bonaa KH, Joakimsen O. Echolucent plaques are associated with high risk of ischemic cerebrovascular events in carotid stenosis: the tromso study. Circulation. 2001;103:2171–2175
  27. Howard G, Sharrett AR, Heiss G, et al. Carotid artery intimal–medial thickness distribution in general populations as evaluated by B-mode ultrasound. ARIC investigators. Stroke. 1993;24:1297–1304
  28. Ebrahim S, Papacosta O, Whincup P, et al. Carotid plaque, intima media thickness, cardiovascular risk factors, and prevalent cardiovascular disease in men and women: the British Regional Heart Study. Stroke. 1999;30:841–850
  29. Pujia A, Rubba P, Spencer MP. Prevalence of extracranial carotid artery disease detectable by echo-Doppler in an elderly population. Stroke. 1992;23:818–822
  30. Finn AV, Kolodgie FD, Virmani R. Correlation between carotid intimal/medial thickness and atherosclerosis. A point of view from pathology. Arterioscler Thromb Vasc Biol. 2009;[Epub ahead of printing]
  31. D'Armiento FP, Bianchi A, de Nigris F, et al. Age-related effects on atherogenesis and scavenger enzymes of intracranial and extracranial arteries in men without classic risk factors for atherosclerosis. Stroke. 2001;32:2472–2479
  32. van Oostrom O, Velema E, Schoneveld AH, et al. Age-related changes in plaque composition: a study in patients suffering from carotid artery stenosis. Cardiovasc Pathol. 2005;14:126–134
  33. Crouse JR, Tang R, Espeland MA, et al. Associations of extracranial carotid atherosclerosis progression with coronary status and risk factors in patients with and without coronary artery disease. Circulation. 2002;106:2061–2066
  34. Parrinello G, Barbagallo CM, Pinto A, et al. Carotid atherosclerosis in hypercholesterolemic patients: relationship with cardiovascular events. Nutr Metab Cardiovasc Dis. 2001;11:96–103
  35. Mannami T, Konishi M, Baba S, Nishi N, Terao A. Prevalence of asymptomatic carotid atherosclerotic lesions detected by high-resolution ultrasonography and its relation to cardiovascular risk factors in the general population of a Japanese city: the Suita study. Stroke. 1997;28:518–525
  36. Lee TH, Hsu WC, Chen CJ, Chen ST. Etiologic study of young ischemic stroke in Taiwan. Stroke. 2002;33:1950–1955
  37. Kablak-Ziembicka A, Tracz W, Przewlocki T, et al. Association of increased carotid intima–media thickness with the extent of coronary artery disease. Heart. 2004;90:1286–1290
  38. Zureik M, Temmar M, Adamopoulos C, et al. Carotid plaques, but not common carotid intima–media thickness, are independently associated with aortic stiffness. J Hypertens. 2002;20:85–93
  39. Chawluk JB, Kushner MJ, Bank WJ, et al. Atherosclerotic carotid artery disease in patients with retinal ischemic syndromes. Neurology. 1988;38:858–863
  40. Klein R, Sharrett AR, Klein BE, et al. Are retinal arteriolar abnormalities related to atherosclerosis?: the atherosclerosis risk in communities study. Arterioscler Thromb Vasc Biol. 2000;20:1644–1650
  41. Wong TY, Klein R, Nieto FJ, et al. Retinal microvascular abnormalities and 10-year cardiovascular mortality: a population-based case–control study. Ophthalmology. 2003;110:933–940
  42. Klein R, Sharrett AR, Klein BE, et al. The association of atherosclerosis, vascular risk factors, and retinopathy in adults with diabetes: the atherosclerosis risk in communities study. Ophthalmology. 2002;109:1225–1234
  43. Rema M, Mohan V, Deepa R, Ravikumar R. Association of carotid intima–media thickness and arterial stiffness with diabetic retinopathy: the Chennai Urban Rural Epidemiology Study (CURES-2). Diabetes Care. 2004;27:1962–1967
  44. Klein R, Marino EK, Kuller LH, et al. The relation of atherosclerotic cardiovascular disease to retinopathy in people with diabetes in the Cardiovascular Health Study. Br J Ophthalmol. 2002;86:84–90
  45. van Hecke MV, Dekker JM, Nijpels G, et al. Are retinal microvascular abnormalities associated with large artery endothelial dysfunction and intima–media thickness? The Hoorn Study. Clin Sci (Lond). 2006;110:597–604
  46. Mykkanen L, Zaccaro DJ, O'Leary DH, et al. Microalbuminuria and carotid artery intima–media thickness in nondiabetic and NIDDM subjects. The Insulin Resistance Atherosclerosis Study (IRAS). Stroke. 1997;28:1710–1716
  47. Kramer H, Jacobs DR, Bild D, et al. Urine albumin excretion and subclinical cardiovascular disease. The multi-ethnic study of atherosclerosis. Hypertension. 2005;46:38–43
  48. Agewall S, Wikstrand J, Ljungman S, Fagerberg B. Urinary albumin excretion is associated with the intima–media thickness of the carotid artery in hypertensive males with non-insulin-dependent diabetes mellitus. J Hypertens. 1995;13:463–469
  49. Yokoyama H, Aoki T, Imahori M, Kuramitsu M. Subclinical atherosclerosis is increased in type 2 diabetic patients with microalbuminuria evaluated by intima–media thickness and pulse wave velocity. Kidney Int. 2004;66:448–454
  50. Keech AC, Grieve SM, Patel A, et al. Urinary albumin levels in the normal range determine arterial wall thickness in adults with type 2 diabetes: a field substudy. Diabet Med. 2005;22:1558–1565
  51. Nomura M, Kasami R, Ohashi M, Yamada Y, Abe H. Significantly higher incidence of carotid atherosclerosis found in Japanese type 2 diabetic patients with early nephropathy. Diabetes Res Clin Pract. 2004;66(Suppl. 1):S161–S163
  52. Fadini GP, Sartore S, Baesso I, et al. Endothelial progenitor cells and the diabetic paradox. Diabetes Care. 2006;29:714–716
  53. Duh E, Aiello LP. Vascular endothelial growth factor and diabetes: the agonist versus antagonist paradox. Diabetes. 1999;48:1899–1906

PII: S0939-4753(09)00237-3

doi: 10.1016/j.numecd.2009.10.003

Nutrition, Metabolism & Cardiovascular Diseases
Volume 21, Issue 4 , Pages 286-293 , April 2011

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