Carotid Atherosclerotic Plaque: Noninvasive MR Characterization and Identification of Vulnerable Lesions
Abstract
Measurement of vessel stenosis by using ultrasonography or angiography remains the principal method for determining the severity of carotid atherosclerosis and the need for endarterectomy. The ipsilateral stroke rate, however—even in patients with severely stenotic vessels—is relatively low, which suggests that the amount of luminal narrowing may not represent the optimal means of assessing clinical risk. As a result, some patients may undergo unnecessary surgery. Improved imaging techniques are, therefore, needed to enable reliable identification of high-risk plaques that lead to cerebrovascular events. High-spatial-resolution magnetic resonance (MR) imaging has been described as one promising modality for this purpose, because the technique allows direct visualization of diseased vessel wall and can be used to characterize the morphology of individual atherosclerotic carotid plaques. The purpose of this report is to review the current state of carotid plaque MR imaging and the use of carotid MR to evaluate plaque morphology and composition.
References
- 1 Gorelick PB, Sacco RL, Smith DB, et al. Prevention of a first stroke: a review of guidelines and a multidisciplinary consensus statement from the National Stroke Association. JAMA 1999; 281:1112- 1120.
- 2 Hankey GJ. Stroke: how large a public health problem, and how can the neurologist help? Arch Neurol 1999; 56:748-754.
- 3 Dogan A, Dempsey RJ. Diagnostic modalities for carotid artery disease. Neurosurg Clin N Am 2000; 11:205-220.
- 4 North American Symptomatic Carotid Endarterectomy Trial Collaborators. Beneficial effect of carotid endarterectomy in symptomatic patients with high-grade stenosis. N Engl J Med 1991; 325:445-453.
- 5 Randomised trial of endarterectomy for recently symptomatic carotid stenosis: final results of the MRC European Carotid Surgery Trial (ECST).Lancet1998; 351:1379-1387.
- 6 Chaturvedi S. Public health impact of carotid endarterectomy. Neuroepidemiology 1999; 18:15-21.
- 7 Connors JJ, Seidenwurm D, Wojak JC, et al. Treatment of atherosclerotic disease at the cervical carotid bifurcation: current status and review of the literature. AJNR Am J Neuroradiol 2000; 21:444-450.
- 8 Brott T, Bogousslavsky J. Treatment of acute ischemic stroke. N Engl J Med 2000; 343:710-721.
- 9 Topol EJ, Nissen SE. Our preoccupation with coronary luminology: the dissociation between clinical and angiographic findings in ischemic heart disease. Circulation 1995; 92:2333-2342.
- 10 Wasserman BA, Haacke EM, Li D. Carotid plaque formation and its evaluation with angiography, ultrasound, and MR angiography. J Magn Reson Imaging 1994; 4:515-527.
- 11 Ambrose JA, Tannenbaum MA, Alexopoulos D, et al. Angiographic progression of coronary artery disease and the development of myocardial infarction. J Am Coll Cardiol 1988; 12:56-62.
- 12 Little WC, Constantinescu M, Applegate RJ, et al. Can coronary angiography predict the site of a subsequent myocardial infarction in patients with mild-to-moderate coronary artery disease? Circulation 1988; 78(5 pt 1):1157-1166.
- 13 Falk E. Why do plaques rupture? Circulation 1992; 86(suppl 6):III30-III42.
- 14 Bassiouny HS, Sakaguchi Y, Mikucki SA, et al. Juxtalumenal location of plaque necrosis and neoformation in symptomatic carotid stenosis. J Vasc Surg 1997; 26:585-594.
- 15 Edwards JH, Kricheff II, Riles T, Imparato A. Angiographically undetected ulceration of the carotid bifurcation as a cause of embolic stroke. Radiology 1979; 132:369-373.
- 16 Mann JM, Davies MJ. Vulnerable plaque: relation of characteristics to degree of stenosis in human coronary arteries. Circulation 1996; 94:928-931.
- 17 Gronholdt MM. Ultrasound and lipoproteins as predictors of lipid-rich, rupture-prone plaques in the carotid artery. Arterioscler Thromb Vasc Biol 1999; 19:2-13.
- 18 Kimura BJ, Bhargava V, DeMaria AN. Value and limitations of intravascular ultrasound imaging in characterizing coronary atherosclerotic plaque. Am Heart J 1995; 130:386-396.
- 19 Gold GE, Pauly JM, Glover GH, Moretto JC, Macovski A, Herfkens RJ. Characterization of atherosclerosis with a 1.5-T imaging system. J Magn Reson Imaging 1993; 3:399-407.
- 20 Martin AJ, Gotlieb AI, Henkelman RM. High-resolution MR imaging of human arteries. J Magn Reson Imaging 1995; 5:93-100.
- 21 Mohiaddin RH, Longmore DB. MRI studies of atherosclerotic vascular disease: structural evaluation and physiological measurements. Br Med Bull 1989; 45:968-990.
- 22 Merickel MB, Carman CS, Brookeman JR, Mugler JP, Brown MF, Ayers CR. Identification and 3-D quantification of atherosclerosis using magnetic resonance imaging. Comput Biol Med 1988; 18:89-102.
- 23 Pearlman JD, Southern JF, Ackerman JL. Nuclear magnetic resonance microscopy of atheroma in human coronary arteries. Angiology 1991; 42:726-733.
- 24 Toussaint JF, Southern JF, Fuster V, Kantor HL. T2-weighted contrast for NMR characterization of human atherosclerosis. Arterioscler Thromb Vasc Biol 1995; 15:1533-1542.
- 25 Toussaint JF, LaMuraglia GM, Southern JF, Fuster V, Kantor HL. Magnetic resonance images lipid, fibrous, calcified, hemorrhagic, and thrombotic components of human atherosclerosis in vivo. Circulation 1996; 94:932-938.
- 26 Fayad ZA, Fuster V. Characterization of atherosclerotic plaques by magnetic resonance imaging. Ann N Y Acad Sci 2000; 902:173-186.
- 27 Yuan C, Murakami JW, Hayes CE, et al. Phased-array magnetic resonance imaging of the carotid artery bifurcation: preliminary results in healthy volunteers and a patient with atherosclerotic disease. J Magn Reson Imaging 1995; 5:561-565.
- 28 Shinnar M, Fallon JT, Wehrli S, et al. The diagnostic accuracy of ex vivo MRI for human atherosclerotic plaque characterization. Arterioscler Thromb Vasc Biol 1999; 19:2756-2761.
- 29 Davies MJ, Woolf N. Atherosclerosis: what is it and why does it occur? Br Heart J 1993; 69(suppl 1):S3-S11.
- 30 Rubin JR, Goldstone J. Peripheral vascular disease: treatment and referral of the elderly—part I. Geriatrics 1985; 40:34-39.
- 31 Fuster V, Stein B, Ambrose JA, Badimon L, Badimon JJ, Chesebro JH. Atherosclerotic plaque rupture and thrombosis: evolving concepts. Circulation 1990; 82(suppl 3):II47-II59.
- 32 Libby P. The interface of atherosclerosis and thrombosis: basic mechanisms. Vasc Med 1998; 3:225-229.
- 33 Davies MJ, Thomas AC. Plaque fissuring: the cause of acute myocardial infarction, sudden ischaemic death, and crescendo angina. Br Heart J 1985; 53:363-373.
- 34 Falk E. Stable versus unstable atherosclerosis: clinical aspects. Am Heart J 1999; 138(5 pt 2):S421-S425.
- 35 Farb A, Burke AP, Tang AL, et al. Coronary plaque erosion without rupture into a lipid core. Circulation 1996; 93:1354-1363.
- 36 Arroyo LH, Lee RT. Mechanisms of plaque rupture: mechanical and biologic interactions. Cardiovasc Res 1999; 41:369-375.
- 37 Shah PK. Plaque disruption and thrombosis: potential role of inflammation and infection. Cardiol Clin 1999; 17:271-281.
- 38 Glagov S, Bassiouny HS, Giddens DP, Zarins CK. Pathobiology of plaque modeling and complication. Surg Clin North Am 1995; 75:545-556.
- 39 Glagov S, Weisenberg E, Zarins CK, Stankunavicius R, Kolettis GJ. Compensatory enlargement of human atherosclerotic coronary arteries. N Engl J Med 1987; 316:1371-1375.
- 40 Budinger T, Berson A, McVeigh E, et al. Magnetic resonance imaging of the cardiovascular system. J Cardiovasc Magn Res 1999; 1:53-58.
- 41 Falk E, Fernandez-Ortiz A. Role of thrombosis in atherosclerosis and its complications. Am J Cardiol 1995; 75:3B-11B.
- 42 Kullo IJ, Edwards WD, Schwartz RS. Vulnerable plaque: pathobiology and clinical implications. Ann Intern Med 1998; 129:1050-1060.
- 43 Roederer GO, Langlois YE, Jaeger KA, et al. A simple spectral parameter for accurate classification of severe carotid disease. Bruit 1984; 8:174-178.
- 44 Kohler T, Langlois Y, Roederer GO, et al. Sources of variability in carotid duplex examination: a prospective study. Ultrasound Med Biol 1985; 11:571-576.
- 45 Langlois YE, Roederer GO, Strandness DE, Jr. Vascular ultrasound: ultrasonic evaluation of the carotid bifurcation. Echocardiography 1987; 4:141-159.
- 46 Pignoli P. Ultrasound B-mode imaging for arterial wall thickness measurement. Atherosclerosis Rev 1984; 12:177-184.
- 47 Riley WA, Barnes RW, Evans GW, Burke GL. Ultrasonic measurement of the elastic modulus of the common carotid artery: the Atherosclerosis Risk in Communities (ARIC) Study. Stroke 1992; 23:952-956.
- 48 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.
- 49 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.
- 50 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; 151:478-487.
- 51 Aly S, Bishop CC. An objective characterization of atherosclerotic lesion: an alternative method to identify unstable plaque. Stroke 2000; 31:1921-1924.
- 52 Biasi GM, Mingazzini PM, Baronio L, et al. Carotid plaque characterization using digital image processing and its potential in future studies of carotid endarterectomy and angioplasty. J Endovasc Surg 1998; 5:240-246.
- 53 Noritomi T, Sigel B, Swami V, et al. Carotid plaque typing by multiple-parameter ultrasonic tissue characterization. Ultrasound Med Biol 1997; 23:643-650.
- 54 Bridal SL, Beyssen B, Fornes P, Julia P, Berger G. Multiparametric attenuation and backscatter images for characterization of carotid plaque. Ultrason Imaging 2000; 22:20-34.
- 55 Lee DJ, Sigel B, Swami VK, et al. Determination of carotid plaque risk by ultrasonic tissue characterization. Ultrasound Med Biol 1998; 24:1291-1299.
- 56 Raynaud JS, Bridal SL, Toussaint JF, et al. Characterization of atherosclerotic plaque components by high resolution quantitative MR and US imaging. J Magn Reson Imaging 1998; 8:622-629.
- 57 Bridal SL, Fornes P, Bruneval P, Berger G. Correlation of ultrasonic attenuation (30 to 50 MHz and constituents of atherosclerotic plaque. Ultrasound Med Biol 1997; 23:691-703.
- 58 Takiuchi S, Rakugi H, Masuyama T, et al. Clinical implications of ultrasonic tissue characterization for atherosclerotic carotid intima-media. Nippon Ronen Igakkai Zasshi 2000; 37:137-142. [Japanese].
- 59 Noritomi T, Sigel B, Gahtan V, et al. In vivo detection of carotid plaque thrombus by ultrasonic tissue characterization. J Ultrasound Med 1997; 16:107-111.
- 60 Chan KL. Quantitative characterization of carotid atheromatous plaques using ultrasonic rf A-scan data. Ultrasonics 1995; 33:163-164.
- 61 Urbani MP, Picano E, Parenti G, et al. In vivo radio frequency-based ultrasonic tissue characterization of the atherosclerotic plaque. Stroke 1993; 24:1507-1512.
- 62 Prati F, Arbustini E, Labellarte A, et al. Intravascular ultrasound insights into plaque composition. Z Kardiol 2000; 89(suppl 2):117-123.
- 63 Wolverson MK, Bashiti HM, Peterson GJ. Ultrasonic tissue characterization of atheromatous plaques using a high resolution real time scanner. Ultrasound Med Biol 1983; 9:599-609.
- 64 Widder B, Paulat K, Hackspacher J, et al. Morphological characterization of carotid artery stenoses by ultrasound duplex scanning. Ultrasound Med Biol 1990; 16:349-354.
- 65 Hiro T, Leung CY, Karimi H, Farvid AR, Tobis JM. Angle dependence of intravascular ultrasound imaging and its feasibility in tissue characterization of human atherosclerotic tissue. Am Heart J 1999; 137:476-481.
- 66 Gussenhoven EJ, Essed CE, Lancee CT, et al. Arterial wall characteristics determined by intravascular ultrasound imaging: an in vitro study. J Am Coll Cardiol 1989; 14:947-952.
- 67 Pourcelot L, Tranquart F, De Bray JM, Philippot M, Bonithon MC, Salez F. Ultrasound characterization and quantification of carotid atherosclerosis lesions. Minerva Cardioangiol 1999; 47:15-24.
- 68 Iannuzzi A, Wilcosky T, Mercuri M, Rubba P, Bryan FA, Bond MG. Ultrasonographic correlates of carotid atherosclerosis in transient ischemic attack and stroke. Stroke 1995; 26:614-619.
- 69 Geroulakos G, Domjan J, Nicolaides A, et al. Ultrasonic carotid artery plaque structure and the risk of cerebral infarction on computed tomography. J Vasc Surg 1994; 20:263-266.
- 70 Arnold JA, Modaresi KB, Thomas N, Taylor PR, Padayachee TS. Carotid plaque characterization by duplex scanning: observer error may undermine current clinical trials. Stroke 1999; 30:61-65.
- 71 de Bray JM, Baud JM, Delanoy P, et al. Reproducibility in ultrasonic characterization of carotid plaques. Cerebrovasc Dis 1998; 8:273-277.
- 72 Montauban van Swijndregt AD, Elbers HR, Moll FL, de Letter J, Ackerstaff RG. Ultrasonographic characterization of carotid plaques. Ultrasound Med Biol 1998; 24:489-493.
- 73 Ricotta JJ. Plaque characterization by B-mode scan. Surg Clin North Am 1990; 70:191-199.
- 74 Sabetai MM, Tegos TJ, Nicolaides AN, Dhanjil S, Pare GJ, Stevens JM. Reproducibility of computer-quantified carotid plaque echogenicity: can we overcome the subjectivity? Stroke 2000; 31:2189-2196.
- 75 Bluth EI. Evaluation and characterization of carotid plaque. Semin Ultrasound CT MR 1997; 18:57-65.
- 76 Bluth EI. Extracranial carotid arteries: intraplaque hemorrhage and surface ulceration. Minerva Cardioangiol 1998; 46:81-85.
- 77 European Carotid Plaque Study Group. Carotid artery plaque composition: relationship to clinical presentation and ultrasound B-mode imaging. Eur J Vasc Endovasc Surg 1995; 10:23-30.
- 78 Geroulakos G, Ramaswami G, Nicolaides A. Characterization of symptomatic and asymptomatic carotid plaques using high-resolution real-time ultrasonography. Br J Surg 1993; 80:1274-1277.
- 79 AbuRahma AF, Kyer PD, III, Robinson PA, Hannay RS. The correlation of ultrasonic carotid plaque morphology and carotid plaque hemorrhage: clinical implications. Surgery 1998; 124:721-728.
- 80 Estes JM, Quist WC, Lo Gerfo FW, Costello P. Noninvasive characterization of plaque morphology using helical computed tomography. J Cardiovasc Surg (Torino) 1998; 39:527-534.
- 81 Kaufman L, Crooks LE, Sheldon PE, Rowan W, Miller T. Evaluation of NMR imaging for detection and quantification of obstructions in vessels. Invest Radiol 1982; 17:554-560.
- 82 Herfkens RJ, Higgins CB, Hricak Nuclear magnetic resonance imaging of atherosclerotic disease. Radiology 1983; 148:161-166.
- 83 Vinitski S, Consigny PM, Shapiro MJ, Janes N, Smullens SN, Rifkin MD. Magnetic resonance chemical shift imaging and spectroscopy of atherosclerotic plaque. Invest Radiol 1991; 26:703-714.
- 84 Small DM, Shipley GG. Physical-chemical basis of lipid deposition in atherosclerosis. Science 1974; 185:222-229.
- 85 Hatsukami TS, Ross R, Polissar NL, Yuan C. Visualization of fibrous cap thickness and rupture in human atherosclerotic carotid plaque in vivo with high-resolution magnetic resonance imaging. Circulation 2000; 102:959-964.
- 86 Pachot-Clouard M, Vaufrey F, Darrasse L, Toussainti JF. Magnetization transfer characteristics in atherosclerotic plaque components assessed by adapted binomial preparation pulses. MAGMA 1998; 7:9-15.
- 87 Kerwin W, Ferguson MS, Small R, Hatsukami TS, Yuan C. Magnetization transfer as a contrast enhancing mechanism in magnetic resonance images of human atherosclerotic plaques (abstr). Atherosclerosis 2000; 151:25.
- 88 Toussaint JF, Southern JF, Fuster V, Kantor HL. Water diffusion properties of human atherosclerosis and thrombosis measured by pulse field gradient nuclear magnetic resonance. Arterioscler Thromb Vasc Biol 1997; 17:542-546.
- 89 Ingersleben GV, Schmiedl UP, Hatsukami TS, et al. Characterization of atherosclerotic plaques at the carotid bifurcation: correlation of high-resolution MR with histology. RadioGraphics 1997; 17:1417-1423.
- 90 Parker DL, Yuan C, Blatter DD. MR angiography by multiple thin slab 3D acquisition. Magn Reson Med 1991; 17:434-451.
- 91 Mitsumori LM, Yuan C, Ferguson MS, Hatsukami TS. In vivo identification of lipid cores in advanced carotid atherosclerotic plaques by high resolution MR imaging (abstr). Circulation 2000; 102(suppl):II252.
- 92 Hatsukami TS, Ferguson MS, Beach KW, et al. Carotid plaque morphology and clinical events. Stroke 1997; 28:95-100.
- 93 Erlichman M. Surface/specialty coil devices and gating techniques in magnetic resonance imaging. Health Technol Assess Rep 1990; 3:1-23.
- 94 Hayes CE, Mathis CM, Yuan C. Surface coil phased arrays for high-resolution imaging of the carotid arteries. J Magn Reson Imaging 1996; 6:109-112.
- 95 Fayad ZA, Fallon JT, Shinnar M, et al. Noninvasive in vivo high-resolution magnetic resonance imaging of atherosclerotic lesions in genetically engineered mice. Circulation 1998; 98:1541-1547.
- 96 Finn JP, Edelman RR. Black-blood and segmented k-space magnetic resonance angiography. Magn Reson Imaging Clin N Am 1993; 1:349-357.
- 97 Edelman RR, Chien D, Kim D, et al. Fast selective black blood MR imaging. Radiology 1991; 181:655-660.
- 98 Milner JS, Moore JA, Rutt BK, Steinman DA. Hemodynamics of human carotid artery bifurcations: computational studies with models reconstructed from magnetic resonance imaging of normal subjects. J Vasc Surg 1998; 28:143-156.
- 99 Steinman DA, Rutt BK. On the nature and reduction of plaque-mimicking flow artifacts in black blood MRI of the carotid bifurcation. Magn Reson Med 1998; 39:635-641.
- 100 Yuan C, Beach KW, Smith LH, Jr, Hatsukami TS. Measurement of atherosclerotic carotid plaque size in vivo using high resolution magnetic resonance imaging. Circulation 1998; 98:2666-2671.
- 101 Aoki S, Aoki K, Ohsawa S, Nakajima H, Kumagai H, Araki T. Dynamic MR imaging of the carotid wall. J Magn Reson Imaging 1999; 9:420-427.
- 102 Coombs BD, Ursell PC, Reilly LM, Rarp JH, Saloner D. Carotid bifurcation plaque structure: high resolution MRI with histologic correlation (abstr) In: Proceedings of the Sixth Meeting of the International Society for Magnetic Resonance in Medicine. Berkeley, Calif: International Society for Magnetic Resonance in Medicine, 1998; 591.
- 103 Du YP, Parker DL, Davis WL, Cao G. Reduction of partial-volume artifacts with zero-filled interpolation in three-dimensional MR angiography. J Magn Reson Imaging 1994; 4:733-741.
- 104 Johnson BA, Fram EK, Drayer BP, Dean BL, Keller PJ, Jacobowitz R. Evaluation of shared-view acquisition using repeated echoes (SHARE): a dual-echo fast spin-echo MR technique. AJNR Am J Neuroradiol 1994; 15:667-673.
- 105 Yuan C, Petty C, O’Brien KD, Hatsukami TS, Eary JF, Brown BG. In vitro and in situ magnetic resonance imaging signal features of atherosclerotic plaque-associated lipids. Arterioscler Thromb Vasc Biol 1997; 17:1496-1503.
- 106 Kuller LH. AHA Symposium/Epidemiology Meeting: atherosclerosis—discussion: why measure atherosclerosis? Circulation 1993; 87(suppl 3):II34-II37.
- 107 Probstfield JL, Byington RP, Egan DA, et al. Methodological issues facing studies of atherosclerotic change. Circulation 1993; 87(suppl 3):II74-II81.
- 108 Yuan C, Schmiedl UP, Maravilla KR, et al. MR imaging of human carotid plaques: assessment of reproducibility and reader variability (abstr). Radiology 1996; 201(P):134-135.
- 109 Kang XJ, Polissar NL, Han C, Lin E, Yuan C. Analysis of the measurement precision of arterial lumen and wall areas using high resolution magnetic resonance imaging. Magn Reson Med 2000; 44:968-972.
- 110 Beach KW, Hatsukami T, Detmer PR, et al. Carotid artery intraplaque hemorrhage and stenotic velocity. Stroke 1993; 24:314-319.
- 111 Eubank WB, Yuan C, Fisher ER, Luna JA, et al. Endarterectomy specimen shrinkage: comparison of T2-weighted MR imaging of specimen ex vivo to histological processes. J Vasc Interv Radiol 1998; 4:161-170.
- 112 Thackray BD, Burns DH, Ferguson MS, et al. A new method for studying plaque morphology. Am J Card Imaging 1995; 9:149-156.
- 113 Rhim EY, Yuan C, Kaneko E, Reichenbach DD, Nelson JA. MR imaging of normal and atherosclerotic arteries: analysis of contrast features. J Vasc Invest 1997; 3:42-51.
- 114 Balaban RS, Ceckler TL. Magnetization transfer contrast in magnetic resonance imaging. Magn Reson Q 1992; 8:116-137.
- 115 Corti R, Badimon JJ, Worthley SG, Helft G, Fayad ZA, Fuster V. Statin therapy reduces burden in human atherosclerotic lesions: longitudinal study using noninvasive MRI (abstr). Circulation 2000; 102:II459.
- 116 Libby P, Aikawa M, Schonbeck U. Cholesterol and atherosclerosis. Biochim Biophys Acta 2000; 1529:299-309.
- 117 O’Leary DH, Polak JF, Kronmal RA, Manolio TA, Burke GL, Wolfson SK, Jr. Carotid-artery intima and media thickness as a risk factor for myocardial infarction and stroke in older adults. N Engl J Med 1999; 340:14-22.