The incidence of type 2 diabetes is rapidly increasing throughout the world. As an independent risk factor for cardiovascular disease both at the microvascular and macrovascular level, diabetes is a condition that deserves the most aggressive medical management. The effectiveness of risk factor modification and glycaemic control on retarding atherosclerosis progression has been assessed by several invasive and non-invasive imaging methods that will be reviewed in this article.
Jacoby RM, Nesto RWAcute myocardial infarction in the diabetic patient: pathophysiology, clinical course and prognosis. J Am Coll Cardiol1992 ;20:736-44.
2.
American Diabetes Association: Diabetes statistics [article online], 2004. Available from http://www.diabetes.org/diabetes-statistics.jsp (Accessed 11 March 2007).
3.
Haffner SM, Stern MP, Hazuda HP et al. Cardiovascular risk factors in confirmed prediabetic individuals. Does the clock for coronary heart disease start ticking before the onset of clinical diabetes?JAMA1990;263:2893-8.
4.
Raggi P., Callister TQ, Shaw LJProgression of coronary artery calcium and risk of first myocardial infarction in patients receiving cholesterol-lowering therapy. Arterioscler Thromb Vasc Biol2004;24:1272-7.
5.
Raggi P., Cooil B., Shaw LJ et al. Progression of coronary calcium on serial electron beam tomographic scanning is greater in patients with future myocardial infarction. Am J Cardiol2003;92:827-9.
6.
Waters D., Higginson L., Gladstone P. et al. Effects of monotherapy with an HMG-CoA reductase inhibitor on the progression of coronary atherosclerosis as assessed by serial quantitative arteriography. The Canadian Coronary Atherosclerosis Intervention Trial. Circulation1994;89:959-68.
7.
Brown BG, Zhao XQ, Chait A. et al. Simvastatin and niacin, antioxidant vitamins, or the combination for the prevention of coronary disease. N Engl J Med2001;345:1583-92.
8.
Topol EJ, Nissen SEOur preoccupation with coronary luminology. The dissociation between clinical and angiographic findings in ischemic heart disease. Circulation1995;92:2333-42.
9.
Effect of fenofibrate on progression of coronary-artery disease in type 2 diabetes: the Diabetes Atherosclerosis Intervention Study, a randomised study. Lancet2001;357:905-10.
10.
Vakkilainen J., Steiner G., Ansquer JC et al. Relationships between low-density lipoprotein particle size, plasma lipoproteins, and progression of coronary artery disease: the Diabetes Atherosclerosis Intervention Study (DAIS). Circulation2003;107:1733-7.
11.
Nissen SE, Nicholls SJ, Sipahi I. et al. Effect of very high-intensity statin therapy on regression of coronary atherosclerosis: the ASTEROID trial. JAMA2006;295:1556-65.
12.
Nissen SE, Tuzcu EM, Schoenhagen P. et al. Effect of intensive compared with moderate lipid-lowering therapy on progression of coronary atherosclerosis: a randomized controlled trial . JAMA2004; 291:1071-80.
13.
Nicholls SJ , Tuzcu EM, Sipahi I. et al. Statins, high-density lipoprotein cholesterol, and regression of coronary atherosclerosis. JAMA2007;297:499-508.
14.
Ricote M., Huang J., Fajas L. et al. Expression of the peroxisome proliferator-activated receptor gamma (PPARgamma) in human atherosclerosis and regulation in macrophages by colony stimulating factors and oxidized low density lipoprotein. Proc Natl Acad Sci USA1998; 95:7614-19.
15.
Law RE, Goetze S., Xi XP et al. Expression and function of PPARgamma in rat and human vascular smooth muscle cells. Circulation2000; 101:1311-18.
16.
Choi D., Kim SK, Choi SH et al. Preventative effects of rosiglitazone on restenosis after coronary stent implantation in patients with type 2 diabetes. Diabetes Care2004;27:2654-60.
17.
Takagi T., Akasaka T., Yamamuro A. et al. Troglitazone reduces neointimal tissue proliferation after coronary stent implantation in patients with non-insulin dependent diabetes mellitus: a serial intravascular ultrasound study. J Am Coll Cardiol2000;36:1529-35.
18.
Takagi T., Akasaka T., Yamamuro A. et al. Impact of insulin resistance on neointimal tissue proliferation after coronary stent implantation. Intravascular ultrasound studies. J Diabetes Complications2002; 16:50-5.
19.
Takagi T., Yamamuro A., Tamita K. et al. Pioglitazone reduces neointimal tissue proliferation after coronary stent implantation in patients with type 2 diabetes mellitus: an intravascular ultrasound scanning study. Am Heart J2003 ;146:E5.
20.
Pignoli P., Tremoli E., Poli A. et al. Intimal plus medial thickness of the arterial wall: a direct measurement with ultrasound imaging. Circulation1986;74:1399-406.
21.
Wong M., Edelstein J., Wollman J. et al. Ultrasonic-pathological comparison of the human arterial wall. Verification of intima-media thickness. Arterioscler Thromb1993;13:482-6.
22.
Persson J., Formgren J., Israelsson B. et al. Ultrasound-determined intima-media thickness and atherosclerosis. Direct and indirect validation. Arterioscler Thromb1994;14:261-4.
23.
O'Leary DH, Polak JF, Kronmal RA et al. Carotid-artery intima and media thickness as a risk factor for myocardial infarction and stroke in older adults. Cardiovascular Health Study Collaborative Research Group. N Engl J Med1999;340:14-22.
24.
Chambless LE, Folsom AR, Clegg LX et al. Carotid wall thickness is predictive of incident clinical stroke: the Atherosclerosis Risk in Communities (ARIC) study. Am J Epidemiol2000;151:478-87.
25.
Hodis HN, Mack WJ, LaBree L. et al. The role of carotid arterial intima-media thickness in predicting clinical coronary events. Ann Intern Med1998 ;128:262-9.
26.
Bots ML, Hoes AW, Koudstaal PJ et al. Common carotid intima-media thickness and risk of stroke and myocardial infarction: the Rotterdam Study. Circulation1997;96:1432-7.
27.
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 Care2005;28:1158-62.
28.
Holaj R., Spacil J., Petrasek J. et al. Intima-media thickness of the common carotid artery is the significant predictor of angiographically proven coronary artery disease. Can J Cardiol2003;19:670-6.
29.
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 Thromb1991; 11:1786-94.
30.
Mitsuhashi N., Onuma T., Kubo S. et al. Coronary artery disease and carotid artery intima-media thickness in Japanese type 2 diabetic patients. Diabetes Care2002;25:1308-12.
31.
Temelkova-Kurktschiev TS, Koehler C., Henkel E. et al. Postchallenge plasma glucose and glycemic spikes are more strongly associated with atherosclerosis than fasting glucose or HbA1c level. Diabetes Care2000;23:1830-4.
32.
Teno S., Uto Y., Nagashima H. et al. Association of postprandial hypertriglyceridemia and carotid intima-media thickness in patients with type 2 diabetes. Diabetes Care2000;23:1401-06.
33.
Guvener N., Tutuncu NB, Oto A. et al. Major determinants of the carotid intima-media thickness in type 2 diabetic patients: age and body mass index. Endocr J2000;47:525-33.
34.
Yamamoto M. , Egusa G., Yamakido M.Carotid atherosclerosis and serum lipoprotein(a) concentrations in patients with NIDDM. Diabetes Care1997;20:829-31.
35.
Agewall S., Wikstrand J., Ljungman S. et al. Urinary albumin excretion is associated with the intima-media thickness of the carotid artery in hypertensive males with non-insulin-dependent diabetes mellitus. J Hypertens1995;13:463-9.
36.
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). Stroke1997 ;28:1710-16.
37.
Leinonen ES , Hiukka A., Hurt-Camejo E. et al. Low-grade inflammation, endothelial activation and carotid intima-media thickness in type 2 diabetes. J Intern Med2004;256:119-27.
38.
Hayaishi-Okano R., Yamasaki Y., Katakami N. et al. Elevated C-reactive protein associates with early-stage carotid atherosclerosis in young subjects with type 1 diabetes . Diabetes Care2002;25:1432-8.
39.
Bonora E., Tessari R., Micciolo R. et al. Intimal-medial thickness of the carotid artery in nondiabetic and NIDDM patients. Relationship with insulin resistance. Diabetes Care1997;20:627-31.
40.
Folsom AR, Eckfeldt JH, Weitzman S. et al. Relation of carotid artery wall thickness to diabetes mellitus, fasting glucose and insulin, body size, and physical activity. Atherosclerosis Risk in Communities (ARIC) Study Investigators. Stroke1994;25:66-73.
41.
Espeland MA , Evans GW, Wagenknecht LE et al. Site-specific progression of carotid artery intimal-medial thickness. Atherosclerosis2003; 171:137-43.
42.
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 Epidemiol1997;146:483-94.
43.
Wagenknecht LE, Zaccaro D., Espeland MA et al. Diabetes and progression of carotid atherosclerosis: the insulin resistance atherosclerosis study. Arterioscler Thromb Vasc Biol2003;23:1035-41.
44.
Wagenknecht LE, D'Agostino RB Jr., Haffner SM et al. Impaired glucose tolerance, type 2 diabetes, and carotid wall thickness: the Insulin Resistance Atherosclerosis Study. Diabetes Care1998;21:1812-18.
45.
Nathan DM, Lachin J., Cleary P. et al. Intensive diabetes therapy and carotid intima-media thickness in type 1 diabetes mellitus. N Engl J Med2003;348:2294-303.
46.
Fiorina P., Folli F., Bertuzzi F. et al. Long-term beneficial effect of islet transplantation on diabetic macro-/microangiopathy in type 1 diabetic kidney-transplanted patients. Diabetes Care2003;26:1129-36.
47.
Hodis HN, Mack WJ, Zheng L. et al. Effect of peroxisome proliferatoractivated receptor gamma agonist treatment on subclinical atherosclerosis in patients with insulin-requiring type 2 diabetes. Diabetes Care2006;29:1545-53.
48.
Minamikawa J., Tanaka S., Yamauchi M. et al. Potent inhibitory effect of troglitazone on carotid arterial wall thickness in type 2 diabetes. J Clin Endocrinol Metab1998;83:1818-20.
49.
Koshiyama H. , Shimono D., Kuwamura N. et al. Rapid communication: inhibitory effect of pioglitazone on carotid arterial wall thickness in type 2 diabetes. J Clin Endocrinol Metab2001;86:3452-6.
50.
Nakamura T. , Matsuda T., Kawagoe Y. et al. Effect of pioglitazone on carotid intima-media thickness and arterial stiffness in type 2 diabetic nephropathy patients. Metabolism2004;53:1382-6.
51.
Mazzone T., Meyer PM, Feinstein SB et al. Effect of pioglitazone compared with glimepiride on carotid intima-media thickness in type 2 diabetes: a randomized trial. JAMA2006;296:2572-81.
52.
Beishuizen ED , van de Ree MA, Jukema JW 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.
53.
Diabete Care2004;27:2887-92. 53. Yamasaki Y., Kim YS, Kawamori R.Rationale and protocol of a trial for prevention of diabetic atherosclerosis by using antiplatelet drugs: study of Diabetic Atherosclerosis Prevention by Cilostazol (DAPC study). Cardiovascular Diabetology2006;5:16-20.
54.
Kodama M., Yamasaki Y., Sakamoto K. et al. Antiplatelet drugs attenuate progression of carotid intima-media thickness in subjects with type 2 diabetes. Thromb Res2000;97:239-45.
55.
Ahn CW, Lee HC, Park SW et al. Decrease in carotid intima media thickness after 1 year of cilostazol treatment in patients with type 2 diabetes mellitus. Diabetes Res Clin Pract2001 ;52 :45-53.
56.
Yamasaki Y. , Kodama M., Nishizawa H. et al. Carotid intima-media thickness in Japanese type 2 diabetic subjects: predictors of progression and relationship with incident coronary heart disease. Diabetes Care2000; 23:1310-15.
57.
Stary HCThe development of calcium deposits in atherosclerotic lesions and their persistence after lipid regression. Am J Cardiol lesions and their persistence after lipid regression. Am J Cardiol2001;88:16E-19E.
Rumberger JA , Sheedy PF, 2nd, Breen JF et al. Electron beam computed tomography and coronary artery disease: scanning for coronary artery calcification. Mayo Clin Proc1996;71:369-77.
60.
Agatston AS , Janowitz WR, Hildner FJ et al. Quantification of coronary artery calcium using ultrafast computed tomography. J Am Coll Cardiol1990;15:827-32.
61.
Naghavi M., Libby P., Falk E. et al. From vulnerable plaque to vulnerable patient: a call for new definitions and risk assessment strategies: Part I. Circulation2003;108:1664-72.
62.
Virmani R., Kolodgie FD, Burke AP et al. Lessons from sudden coronary death: a comprehensive morphological classification scheme for atherosclerotic lesions. Arterioscler Thromb Vasc Biol2000;20:1262-75.
63.
Shaw LJ, Raggi P., Schisterman E. et al. Prognostic value of cardiac risk factors and coronary artery calcium screening for all-cause mortality. Radiology2003;228:826-33.
64.
Kondos GT, Hoff JA, Sevrukov A. et al. Electron-beam tomography coronary artery calcium and cardiac events: a 37-month follow-up of 5635 initially asymptomatic low- to intermediate-risk adults. Circulation2003;107:2571-6.
65.
Greenland P. , LaBree L., Azen SP et al. Coronary artery calcium score combined with Framingham score for risk prediction in asymptomatic individuals. JAMA2004;291:210-15.
66.
Taylor AJ, Bindeman J., Feuerstein I. et al. Coronary calcium independently predicts incident premature coronary heart disease over measured cardiovascular risk factors: mean three-year outcomes in the Prospective Army Coronary Calcium (PACC) project. J Am Coll Cardiol2005;46:807-14.
67.
Greenland P., Bonow RO, Brundage BH et al. ACCF/AHA 2007 clinical expert consensus document on coronary artery calcium scoring by computed tomography in global cardiovascular risk assessment and in evaluation of patients with chest pain: a report of the American College of Cardiology Foundation Clinical Expert Consensus Task Force (ACCF/AHA Writing Committee to Update the 2000 Expert Consensus Document on Electron Beam Computed Tomography) developed in collaboration with the Society of Atherosclerosis Imaging and Prevention and the Society of Cardiovascular Computed Tomography. J Am Coll Cardiol2007 ;49:378-402.
68.
Raggi P., Shaw LJ, Berman DS et al. Prognostic value of coronary artery calcium screening in subjects with and without diabetes. J Am Coll Cardiol2004;43:1663-9.
69.
Anand DV, Lim E., Hopkins D. et al. Risk stratification in uncomplicated type 2 diabetes: prospective evaluation of the combined use of coronary artery calcium imaging and selective myocardial perfusion scintigraphy. Eur Heart J2006;27:713-21.
70.
Qu W., Le TT, Azen SP et al. Value of coronary artery calcium scanning by computed tomography for predicting coronary heart disease in diabetic subjects. Diabetes Care2003;26:905-10.
71.
Raggi P., Cooil B., Ratti C. et al. Progression of coronary artery calcium and occurrence of myocardial infarction in patients with and without diabetes mellitus. Hypertension2005;46:238-43.
72.
Mehrotra R. , Budoff M., Hokanson JE et al. Progression of coronary artery calcification in diabetics with and without chronic kidney disease. Kidney Int2005;68:1258-66.
73.
Maahs DM, Ogden LG, Kinney GL et al. Low plasma adiponectin levels predict progression of coronary artery calcification. Circulation2005;111:747-53.
74.
Budoff MJ, Yu D., Nasir K. et al. Diabetes and progression of coronary calcium under the influence of statin therapy. Am Heart J2005;149:695-700.
75.
Callister TQ , Raggi P., Cooil B. et al. Effect of HMG-CoA reductase inhibitors on coronary artery disease as assessed by electron-beam computed tomography . N Engl J Med1998;339:1972-8.
76.
Galassi A., Spiegel DM, Bellasi A. et al. Accelerated vascular calcification and relative hypoparathyroidism in incident haemodialysis diabetic patients receiving calcium binders. Nephrol Dial Transplant2006;21:3215-22.
77.
Block GA, Raggi P., Bellasi A. et al. Mortality effect of coronary calcification and phosphate binder choice in incident hemodialysis patients. Kidney Int2007;71:438-41.
78.
Prior JO, Quinones MJ, Hernandez-Pampaloni M. et al. Coronary circulatory dysfunction in insulin resistance, impaired glucose tolerance, and type 2 diabetes mellitus. Circulation2005;111:2291-8.
79.
Lautamaki R. , Airaksinen KE, Seppanen M. et al. Insulin improves myocardial blood flow in patients with type 2 diabetes and coronary artery disease. Diabetes2006;55:511-16.
80.
McMahon GT, Plutzky J., Daher E. et al. Effect of a peroxisome proliferator-activated receptor-gamma agonist on myocardial blood flow in type 2 diabetes. Diabetes Care2005;28:1145-50.
81.
Scognamiglio R., Negut C., de Kreutzenberg SV et al. Effects of different insulin regimes on postprandial myocardial perfusion defects in type 2 diabetic patients. Diabetes Care2006;29:95-100.