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Review Article

Carotid intima-media thickness as a surrogate marker for cardiovascular disease in intervention studies

Pages 2181-2190 | Accepted 20 Sep 2006, Published online: 06 Oct 2006

References

  • De Backer G, Ambrosioni E, Borch-Johnsen K, et al. European guidelines on cardiovascular disease prevention in clinical practice [Third Joint Task Force of European and Other Societies on Cardiovascular Disease Prevention in Clinical Practice]. Eur Heart J 2003;24:1601–10
  • Association AH. Heart disease and stroke statistics – 2005 update. Dallas (TX): American Heart Association; 2005
  • Boissel JP, Collet JP, Moleur P, Haugh M. Surrogate endpoints: a basis for a rational approach. Eur J Clin Pharmacol 1992;43: 235–44
  • Prentice RL. Surrogate endpoints in clinical trials: definition and operational criteria. Stat Med 1989;8:431–40
  • Berger VW. Does the Prentice criterion validate surrogate endpoints? Stat Med 2004;23:1571–8
  • Ip JH, Fuster V, Chesebro JH. Exploration of the atherosclerotic plaque. Biomed Pharmacother 1990;44:343–52
  • Azen SP, Mack WJ, Cashin-Hemphill L, et al. Progression of coronary artery disease predicts clinical coronary events. Long-term follow-up from the Cholesterol Lowering Atherosclerosis Study. Circulation 1996;93:34–41
  • Waters D, Craven TE, Lesperance J. Prognostic significance of progression of coronary atherosclerosis. Circulation 1993;87:1067–75
  • Glagov S, Weisenberg E, Zarins CK, et al. Compensatory enlargement of human atherosclerotic coronary arteries. New Engl J Med 1987;316:1371–5
  • Topol EJ, Nissen SE. Our preoccupation with coronary luminology. The dissociation between clinical and angiographic findings in ischemic heart disease. Circulation 1995;92: 2333–42
  • Pearson TA. New tools for coronary risk assessment: what are their advantages and limitations? Circulation 2002;105:886–92
  • Fayad ZA, Fuster V. Clinical imaging of the high-risk or vulnerable atherosclerotic plaque. Circ Res 2001;89:305–16
  • Nicholls SJ, Sipahi I. Emerging role of intravascular ultrasound in the assessment of experimental anti-atherosclerotic therapies. Curr Med Chem 2006;13:1727–34
  • Sipahi I, Nicholls SJ, Tuzcu EM. Recent trends in coronary intravascular ultrasound: tracking atherosclerosis, pursuit of vulnerable plaques, and beyond. J Nucl Cardiol 2006;13:91–6
  • Schoenhagen P, Nissen SE. Intravascular ultrasonography: using imaging end points in coronary atherosclerosis trials. Cleve Clin J Med 2005;72:487–9, 493–6
  • Guedes A, Tardif JC. Intravascular ultrasound assessment of atherosclerosis. Curr Atheroscler Rep 2004;6:219–24
  • Van Mieghem CA, McFadden EP, de Feyter PJ, et al. Noninvasive detection of subclinical coronary atherosclerosis coupled with assessment of changes in plaque characteristics using novel invasive imaging modalities: the Integrated Biomarker and Imaging Study (IBIS). J Am Coll Cardiol 2006;47:1134–42
  • Nissen SE, Nicholls SJ, Sipahi I, et al; ASTEROID Investigators. Effect of very high-intensity statin therapy on regression of coronary atherosclerosis: the ASTEROID trial. J Am Med Assoc 2006;295:1556–65
  • Nissen SE. Effect of intensive lipid lowering on progression of coronary atherosclerosis: evidence for an early benefit from the Reversal of Atherosclerosis with Aggressive Lipid Lowering (REVERSAL) trial. Am J Cardiol 2005;96:61F–68F
  • Nissen SE, Tsunoda T, Tuzcu EM, et al. Effect of recombinant ApoA-I Milano on coronary atherosclerosis in patients with acute coronary syndromes: a randomized controlled trial. J Am Med Assoc 2003;290:2292–300
  • Tardif JC, Gregoire J, L’Allier PL, et al; Avasimibe and Progression of Lesions on UltraSound (A-PLUS) Investigators. Effects of the acyl coenzyme A:cholesterol acyltransferase inhibitor avasimibe on human atherosclerotic lesions. Circulation 2004;110:3372–7
  • Nicholls SJ, Sipahi I, Schoenhagen P, et al; ACTIVATE Investigators. Intravascular ultrasound assessment of novel antiatherosclerotic therapies: rationale and design of the Acyl-CoA:Cholesterol Acyltransferase Intravascular Atherosclerosis Treatment Evaluation (ACTIVATE) study. Am Heart J 2006;152:67–74
  • Ainsworth CD, Blake CC, Tamayo A, et al. 3D ultrasound measurement of change in carotid plaque volume: a tool for rapid evaluation of new therapies. Stroke 2005;36:1904–9
  • Landry A, Spence JD, Fenster A. Quantification of carotid plaque volume measurements using 3D ultrasound imaging. Ultrasound Med Biol 2005;31: 751–62
  • Al-Shali K, House AA, Hanley AJ, et al. Differences between carotid wall morphological phenotypes measured by ultrasound in one, two and three dimensions. Atherosclerosis 2005;178:319–25
  • Painter RC, de Rooij SR, Hutten BA, et al. Reduced intima media thickness in adults after prenatal exposure to the Dutch famine. Atherosclerosis 2006 [Epub ahead of print]
  • Chaturvedi N, Coady E, Mayet J, et al. Indian Asian men have less peripheral arterial disease than European men for equivalent levels of coronary disease. Atherosclerosis 2006 [Epub ahead of print]
  • Vriend JW, de Groot E, de Waal TT, et al. Increased carotid and femoral intima-media thickness in patients after repair of aortic coarctation: influence of early repair. Am Heart J 2006;151:242–7
  • Kastelein JJ, Sager PT, de Groot E, Veltri E. Comparison of ezetimibe plus simvastatin versus simvastatin monotherapy on atherosclerosis progression in familial hypercholesterolemia. Design and rationale of the Ezetimibe and Simvastatin in Hypercholesterolemia Enhances Atherosclerosis Regression (ENHANCE) trial. Am Heart J 2005;149:234–9
  • Terpstra WF, May JF, Smit AJ, et al. Effects of amlodipine and lisinopril on intima-media thickness in previously untreated, elderly hypertensive patients (the ELVERA trial). J Hypertens 2004;22:1309–16
  • van Wissen S, Smilde TJ, de Groot E, et al. The significance of femoral intima-media thickness and plaque scoring in the Atorvastatin versus Simvastatin on Atherosclerosis Progression (ASAP) study. Eur J Cardiovasc Prev Rehabil 2003;10:451–5
  • Terpstra WF, May JF, Smit AJ, et al. Effects of nifedipine on carotid and femoral arterial wall thickness in previously untreated hypertensive patients. Blood Press Suppl 2003;1: 22–9
  • Cheng KS, Mikhailidis DP, Hamilton G, Seifalian AM. A review of the carotid and femoral intima-media thickness as an indicator of the presence of peripheral vascular disease and cardiovascular risk factors. Cardiovasc Res 2002;54:528–38
  • Bots ML, Witteman JC, Grobbee DE. Carotid intima-media wall thickness in elderly women with and without atherosclerosis of the abdominal aorta. Atherosclerosis 1993;102:99–105
  • Allan PL, Mowbray PI, Lee AJ, Fowkes FG. Relationship between carotid intima-media thickness and symptomatic and asymptomatic peripheral arterial disease. The Edinburgh Artery Study. Stroke 1997;28:348–53
  • Mattace Raso F, Rosato M, Talerico A, et al. Intimalmedial thickness of the common carotid arteries and lower limbs atherosclerosis in the elderly. Minerva Cardioangiol 1999;47:321–7
  • Geroulakos G, O’Gorman DJ, Kalodiki E, et al. The carotid intima-media thickness as a marker of the presence of severe symptomatic coronary artery disease. Eur Heart J 1994;15: 781–5
  • Visona A, Pesavento R, Lusiani L, et al. Intimal medial thickening of common carotid artery as indicator of coronary artery disease. Angiology 1996;47:61–6
  • Khoury Z, Schwartz R, Gottlieb S, et al. Relation of coronary artery disease to atherosclerotic disease in the aorta, carotid, and femoral arteries evaluated by ultrasound. Am J Cardiol 1997;80:1429–33
  • Balbarini A, Buttitta F, Limbruno U, et al. Usefulness of carotid intima-media thickness measurement and peripheral B-mode ultrasound scan in the clinical screening of patients with coronary artery disease. Angiology 2000;51:269–79
  • Bots ML, Grobbee DE. Intima media thickness as a surrogate marker for generalised atherosclerosis. Cardiovasc Drugs Ther 2002;16:341–51
  • Jacoby DS, Mohler IE, Rader DJ. Noninvasive atherosclerosis imaging for predicting cardiovascular events and assessing therapeutic interventions. Curr Atheroscler Rep 2004; 6:20–6
  • de Groot E, Hovingh GK, Wiegman A, et al. Measurement of arterial wall thickness as a surrogate marker for atherosclerosis. Circulation 2004;109:11133–8
  • Poredos P. Intima-media thickness: indicator of cardiovascular risk and measure of the extent of atherosclerosis. Vasc Med 2004;9:46–54
  • Bots ML, Evans GW, Riley WA, Grobbee DE. Carotid intima-media thickness measurements in intervention studies: design options, progression rates, and sample size considerations: a point of view. Stroke 2003;34:2985–94
  • O’Leary DH, Polak JF, Wolfson Jr SK, et al. Use of sonography to evaluate carotid atherosclerosis in the elderly. The Cardiovascular Health Study [CHS Collaborative Research Group]. Stroke 1991;22:1155–63
  • Group AS. High-resolution B-mode ultrasound reading methods in the Atherosclerosis Risk in Communities (ARIC) cohort. J Neuroimaging 1991;1:168–72
  • Bots ML, Mulder PG, Hofman A, et al. Reproducibility of carotid vessel wall thickness measurements [The Rotterdam Study]. J Clin Epidemiol 1994;47:921–30
  • Riley WA, Barnes RW, Applegate WB, et al. Reproducibility of noninvasive ultrasonic measurement of carotid atherosclerosis [The Asymptomatic Carotid Artery Plaque Study]. Stroke 1992;23:1062–8
  • Pitt B, Byington RP, Furberg CD, et al. Effect of amlodipine on the progression of atherosclerosis and the occurrence of clinical events. Circulation 2000;102:1503–10
  • Bots ML, Evans GW, Riley W, et al. The Osteoporosis Prevention and Arterial effects of tiboLone (OPAL) study: design and baseline characteristics. Control Clin Trials 2003;24:752–75
  • Durga J, Bots ML, Schouten EG, et al. Low concentrations of folate, not hyperhomocysteinemia, are associated with carotid intima-media thickness. Atherosclerosis 2005;179:285–92
  • Crouse 3rd JR, Grobbee DE, O’Leary DH, et al. Measuring Effects on intima media Thickness: an Evaluation Of Rosuvastatin in subclinical atherosclerosis – the rationale and methodology of the METEOR study. Cardiovasc Drugs Ther 2004;18: 231–8
  • Kastelein JJP, Bots ML, Riley WA, et al. Design of a study comparing torcetrapib/atorvastatin with atorvastatin alone on carotid atherosclerosis in patients with familial hypercholesterolemia. Poster presented at the 75th European Atherosclerosis Society congress, 23–26 April, Prague, Czech Republic 2005
  • Wendelhag I, Gustavsson T, Suurkula M, et al. Ultrasound measurement of wall thickness in the carotid artery: fundamental principles and description of a computerized analysing system. Clin Physiol 1991;11:565–77
  • Gamble G, Beaumont B, Smith H, et al. B-mode ultrasound images of the carotid artery wall: correlation of ultrasound with histological measurements. Atherosclerosis 1993;102:163–73
  • Wong M, Edelstein J, Wollman J, Bond MG. Ultrasonic-pathological comparison of the human arterial wall. Verification of intima-media thickness. Arterioscler Thromb 1993;13:482–6
  • Montauban van Swijndregt AD, The SH, Gussenhoven EJ, et al. An in vitro evaluation of the line pattern of the near and far walls of carotid arteries using B-mode ultrasound. Ultrasound Med Biol 1996;22:1007–15
  • Dijk JM, van der Graaf Y, Bots ML, et al. Carotid intima-media thickness and the risk of new vascular events in patients with manifest atherosclerotic disease: the SMART study. Eur Heart J 2006;27:1971–8
  • Salonen R, Salonen JT. Determinants of carotid intima-media thickness: a population-based ultrasonography study in eastern Finnish men. J Intern Med 1991;229:225–31
  • Bots ML, Hoes AW, Koudstaal PJ, et al. Common carotid intima-media thickness and risk of stroke and myocardial infarction: the Rotterdam Study. Circulation 1997;96:1432–7
  • 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;146:483–94
  • 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 Epidemiol 2000;151:478–87
  • 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. New Engl J Med 1999;340: 14–22
  • Lorenz MW, von Kegler S, Steinmetz H, et al. Carotid intima-media thickening indicates a higher vascular risk across a wide age range: prospective data from the Carotid Atherosclerosis Progression Study (CAPS). Stroke 2006;37:87–92
  • Hodis HN, Mack WJ, LaBree L, et al. The role of carotid arterial intima-media thickness in predicting clinical coronary events. Ann Intern Med 1998;128:262–9
  • Gottdiener JS, Bednarz J, Devereux R, et al. American Society of Echocardiography recommendations for use of echocardiography in clinical trials. J Am Soc Echocardiogr 2004;17: 1086–119
  • Espeland MA, O’Leary D H, Terry JG, et al. Carotid intimal-media thickness as a surrogate for cardiovascular disease events in trials of HMG-CoA reductase inhibitors. Curr Control Trials Cardiovasc Med 2005;6:3
  • Wang JG, Staessen JA, Li Y, et al. Carotid intima-media thickness and antihypertensive treatment: a meta-analysis of randomized controlled trials. Stroke 2006;37:1933–40
  • 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. Diabetes Care 2004;27:2887–92
  • Elkeles RS, Diamond JR, Poulter C, et al. Cardiovascular outcomes in type 2 diabetes. A double-blind placebo-controlled study of bezafibrate: the St. Mary’s, Ealing, Northwick Park Diabetes Cardiovascular Disease Prevention (SENDCAP) Study. Diabetes Care 1998;21: 641–8
  • 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 Care 2000;23:1310–5
  • Yamasaki Y, Kim YS, Kawamori R. Rationale and protocol of a trial for prevention of diabetic atherosclerosis by using anti-platelet drugs: Study of Diabetic Atherosclerosis Prevention by Cilostazol (DAPC Study). Cardiovasc Diabetol 2006;5:16 [Epub ahead of print]
  • Kodama M, Yamasaki Y, Sakamoto K, et al. Antiplatelet drugs attenuate progression of carotid intima-media thickness in subjects with type 2 diabetes. Thromb Res 2000;97:239–45
  • Cesarone MR, Laurora G, DeSanctis MT, et al. Effects of triflusal on arteriosclerosis progression assessed with high-resolution arterial ultrasound. Angiology 1999;50:455–63
  • de Kleijn MJ, Bots ML, Bak AA, et al. Hormone replacement therapy in perimenopausal women and 2-year change of carotid intima-media thickness. Maturitas 1999;32:195–204
  • Angerer P, Stork S, Kothny W, et al. Effect of oral postmenopausal hormone replacement on progression of atherosclerosis: a randomized, controlled trial. Arterioscler Thromb Vasc Biol 2001;21:262–8
  • Byington RP, Furberg CD, Herrington DM, et al. Effect of estrogen plus progestin on progression of carotid atherosclerosis in postmenopausal women with heart disease: HERS B-mode substudy [Heart and Estrogen/Progestin Replacement Study Research Group]. Arterioscler Thromb Vasc Biol 2002;22:1692–7
  • Hodis HN, Mack WJ, Lobo RA, et al. Estrogen in the prevention of atherosclerosis. A randomized, double-blind, placebo-controlled trial. Ann Intern Med 2001;135:939–53
  • Bots ML, Evans GW, Riley W, et al; OPAL Investigators. The effect of tibolone and continuous combined conjugated equine oestrogens plus medroxyprogesterone acetate on progression of carotid intima-media thickness: the Osteoporosis Prevention and Arterial effects of tiboLone (OPAL) study. Eur Heart J 2006;27:746–55
  • Yokoyama H, Katakami N, Yamasaki Y. Recent advances of intervention to inhibit progression of carotid intima-media thickness in patients with type 2 diabetes mellitus. Stroke 2006;37: 2420–7
  • Magliano D, McNeil J, Branley P, et al. The Melbourne Atherosclerosis Vitamin E Trial (MAVET): a study of high dose vitamin E in smokers. Eur J Cardiovasc Prev Rehabil 2006;13:341–7
  • Anderssen SA, Hjelstuen AK, Hjermann I, et al. Fluvastatin and lifestyle modification for reduction of carotid intima-media thickness and left ventricular mass progression in drug-treated hypertensives. Atherosclerosis 2005;178:387–97
  • Salonen RM, Nyyssonen K, Kaikkonen J, et al; Antioxidant Supplementation in Atherosclerosis Prevention Study Group. Six-year effect of combined vitamin C and E supplementation on atherosclerotic progression: the Antioxidant Supplementation in Atherosclerosis Prevention (ASAP) Study. Circulation 2003;107:947–53
  • Hodis HN, Mack WJ, LaBree L, et al; VEAPS Research Group. Alpha-tocopherol supplementation in healthy individuals reduces low-density lipoprotein oxidation but not atherosclerosis: the Vitamin E Atherosclerosis Prevention Study (VEAPS). Circulation 2002;106:1453–9
  • Azen SP, Qian D, Mack WJ, et al. Effect of supplementary antioxidant vitamin intake on carotid arterial wall intima-media thickness in a controlled clinical trial of cholesterol lowering. Circulation 1996;94:2369–72
  • Kastelein JJ, Wiegman A, de Groot E. Surrogate markers of atherosclerosis: impact of statins. Atheroscler Suppl 2003;4: 31–6
  • Amarenco P, Labreuche J, Lavallee P, Touboul PJ. Statins in stroke prevention and carotid atherosclerosis: systematic review and up-to-date meta-analysis. Stroke 2004;35:2902–9
  • Grobbee DE, Bots ML. Atherosclerotic disease regression with statins: studies using vascular markers. Int J Cardiol 2004;96:447–59
  • Smilde TJ, van Wissen S, Wollersheim H, et al. Effect of aggressive versus conventional lipid lowering on atherosclerosis progression in familial hypercholesterolaemia (ASAP): a prospective, randomised, double-blind trial. Lancet 2001;357:577–81
  • de Sauvage Nolting PR, de Groot E, Zwinderman AH, et al. Regression of carotid and femoral artery intima-media thickness in familial hypercholesterolemia: treatment with simvastatin. Arch Intern Med 2003;163:1837–41
  • Taylor AJ, Kent SM, Flaherty PJ, et al. ARBITER: Arterial Biology for the Investigation of the Treatment Effects of Reducing Cholesterol: a randomized trial comparing the effects of atorvastatin and pravastatin on carotid intima medial thickness. Circulation 2002;106:2055–60
  • Kent SM, Coyle LC, Flaherty PJ, et al. Marked low-density lipoprotein cholesterol reduction below current national cholesterol education program targets provides the greatest reduction in carotid atherosclerosis. Clin Cardiol 2004; 27:17–21
  • Taylor AJ, Sullenberger LE, Lee HJ, et al. Arterial Biology for the Investigation of the Treatment Effects of Reducing Cholesterol (ARBITER) 2: A double-blind, placebo-controlled study of extended-release niacin on atherosclerosis progression in secondary prevention patients treated with statins. Circulation 2004;110:3512–7
  • The Scandinavian Simvastatin Survival Study Group. Randomised trial of cholesterol lowering in 4444 patients with coronary heart disease: the Scandinavian Simvastatin Survival Study (4S). Lancet 1994;344:1383–9
  • Downs JR, Clearfield M, Weis S, et al. Primary prevention of acute coronary events with lovastatin in men and women with average cholesterol levels: results of AFCAPS/TexCAPS [Air Force/Texas Coronary Atherosclerosis Prevention Study]. J Am Med Assoc 1998;279:1615–22
  • Cannon CP, Braunwald E, McCabe CH, et al. Intensive versus moderate lipid lowering with statins after acute coronary syndromes. New Engl J Med 2004;350:1495–504
  • Clark RW, Sutfin TA, Ruggeri RB, et al. Raising high-density lipoprotein in humans through inhibition of cholesteryl ester transfer protein: an initial multidose study of torcetrapib. Arterioscler Thromb Vasc Biol 2004;24:490–7
  • Brousseau ME, Schaefer EJ, Wolfe ML, et al. Effects of an inhibitor of cholesteryl ester transfer protein on HDL cholesterol. New Engl J Med 2004;350:1505–15
  • Bots ML, Riley WA, Evans GW, et al. Design of a study on the effect of torcetrapib/atorvastatin versus atorvastatin alone on carotid intima-media thickness in patients with mixed hyperlipidemia. Poster presented at the 75th European Atherosclerosis Society congress, 23–26 April, Prague, Czech Republic 2005
  • Furberg CD, Adams Jr HP, Applegate WB, et al. Effect of lovastatin on early carotid atherosclerosis and cardiovascular events [Asymptomatic Carotid Artery Progression Study (ACAPS) Research Group]. Circulation 1994;90:1679–87
  • Salonen R, Nyyssonen K, Porkkala E, et al. Kuopio Atherosclerosis Prevention Study (KAPS). A population-based primary preventive trial of the effect of LDL lowering on atherosclerotic progression in carotid and femoral arteries. Circulation 1995;92:1758–64
  • Crouse 3rd JR, Byington RP, Bond MG, et al. Pravastatin, Lipids, and Atherosclerosis in the Carotid Arteries (PLAC-II). Am J Cardiol 1995;75:455–9
  • Mercuri M, Bond MG, Sirtori CR, et al. Pravastatin reduces carotid intima-media thickness progression in an asymptomatic hypercholesterolemic Mediterranean population: the Carotid Atherosclerosis Italian Ultrasound Study. Am J Med 1996;101:627–34
  • de Groot E, Jukema JW, Montauban van Swijndregt AD, et al. B-mode ultrasound assessment of pravastatin treatment effect on carotid and femoral artery walls and its correlations with coronary arteriographic findings: a report of the Regression Growth Evaluation Statin Study (REGRESS). J Am Coll Cardiol 1998;31:1561–7
  • Hedblad B, Wikstrand J, Janzon L, et al. Low-dose metoprolol CR/XL and fluvastatin slow progression of carotid intima-media thickness: main results from the Beta-Blocker Cholesterol-Lowering Asymptomatic Plaque Study (BCAPS). Circulation 2001;103:1721–6
  • Sawayama Y, Shimizu C, Maeda N, et al. Effects of probucol and pravastatin on common carotid atherosclerosis in patients with asymptomatic hypercholesterolemia [Fukuoka Atherosclerosis Trial (FAST)]. J Am Coll Cardiol 2002;39:610–6
  • MacMahon S, Sharpe N, Gamble G, et al. Effects of lowering average of below-average cholesterol levels on the progression of carotid atherosclerosis: results of the LIPID Atherosclerosis Substudy [LIPID Trial Research Group]. Circulation 1998;97:1784–90
  • Hodis HN, Mack WJ, LaBree L, et al. Reduction in carotid arterial wall thickness using lovastatin and dietary therapy: a randomized controlled clinical trial. Ann Intern Med 1996;124:548–56

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