Diagnostics Accuracy of Magnetic Resonance Imaging in Detection of Atherosclerotic Plaque Characteristics in Carotid Arteries Compared to Histology: A Systematic Review
Language English Country United States Media print-electronic
Document type Systematic Review, Journal Article, Comparative Study
Grant support
Ostravská Univerzita v Ostravě
PubMed
38981139
PubMed Central
PMC11803704
DOI
10.1002/jmri.29522
Knihovny.cz E-resources
- Keywords
- atherosclerosis, carotid plaque, carotid stenosis, diagnostic accuracy, intraplaque hemorrhage, lipid‐rich necrotic core,
- MeSH
- Carotid Arteries * diagnostic imaging pathology MeSH
- Plaque, Atherosclerotic * diagnostic imaging pathology MeSH
- Humans MeSH
- Magnetic Resonance Imaging * methods MeSH
- Carotid Artery Diseases * diagnostic imaging pathology MeSH
- Reproducibility of Results MeSH
- Sensitivity and Specificity MeSH
- Check Tag
- Humans MeSH
- Male MeSH
- Female MeSH
- Publication type
- Journal Article MeSH
- Comparative Study MeSH
- Systematic Review MeSH
Carotid plaque composition represents one of the main risk factors of future ischemic stroke. MRI provides excellent soft tissue contrast that can distinguish plaque characteristics. Our objective was to analyze the diagnostic accuracy of MRI imaging in the detection of carotid plaque characteristics compared to histology in patients with symptomatic and asymptomatic carotid atherosclerosis through a systematic review. After prospective registration in PROSPERO (ID CRD42022329690), Medline Ovid, Embase.com, Cochrane Library, and Web of Science Core were searched without any search limitation up to May 27, 2022 to identify eligible articles. Of the 8168 studies, 53 (37 × 1.5 T MRI, 17 × 3 T MRI) evaluated MRI accuracy in the detection of 13 specific carotid plaque characteristics in 169 comparisons. MRI demonstrated high diagnostic accuracy for detection of calcification (3 T MRI: mean sensitivity 92%/mean specificity 90%; 1.5 T MRI: mean sensitivity 81%/mean specificity 91%), fibrous cap (1.5 T: 89%/87%), unstable plaque (1.5 T: 89%/87%), intraplaque hemorrhage (1.5 T: 86%/88%), and lipid-rich necrotic core (1.5 T: 89%/79%). MRI also proved to have a high level of tissue discrimination for the carotid plaque characteristics investigated, allowing potentially for a better risk assessment and follow-up of patients who may benefit from more aggressive treatments. These results emphasize the role of MRI as the first-line imaging modality for comprehensive assessment of carotid plaque morphology, particularly for unstable plaque. EVIDENCE LEVEL: 2 TECHNICAL EFFICACY: Stage 2.
Medical Library Lausanne University Hospital and University of Lausanne Lausanne Switzerland
Neurology Unit Department of Internal Medicine Riviera Chablais Hospital Rennaz Switzerland
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Feeley TM, Leen EJ, Colgan MP, Moore DJ, Hourihane DO'B, Shanik GD. Histologic characteristics of carotid artery plaque. J Vasc Surg 1991;13(5):719‐724. PubMed
Lusis AJ. Atherosclerosis. Nature 2000;407(6801):233‐241. PubMed PMC
Traub O, Berk BC. Laminar shear stress. Arterioscler Thromb Vasc Biol 1998;18(5):677‐685. PubMed
Arroyo L. Mechanisms of plaque rupture mechanical and biologic interactions. Cardiovasc Res 1999;41(2):369‐375. PubMed
Kerwin WS, Hatsukami T, Yuan C, Zhao XQ. MRI of carotid atherosclerosis. Am J Roentgenol 2013;200(3):W304‐W313. PubMed PMC
Lukanova DV, Nikolov NK, Genova KZ, Stankev MD, Georgieva EV. The accuracy of noninvasive imaging techniques in diagnosis of carotid plaque morphology. Open Access Maced J Med Sci 2015;3(2):224‐230. PubMed PMC
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(5):932‐938. PubMed
Gupta A, Baradaran H, Schweitzer AD, et al. Carotid plaque MRI and stroke risk. Stroke 2013;44(11):3071‐3077. PubMed
Kamtchum‐Tatuene J, Noubiap JJ, Wilman AH, Saqqur M, Shuaib A, Jickling GC. Prevalence of high‐risk plaques and risk of stroke in patients with asymptomatic carotid stenosis. JAMA Neurol 2020;77(12):1524‐1535. PubMed PMC
Schindler A, Schinner R, Altaf N, et al. Prediction of stroke risk by detection of hemorrhage in carotid plaques. JACC Cardiovasc Imaging 2020;13(2):395‐406. PubMed
Page MJ, McKenzie JE, Bossuyt PM, et al. The PRISMA 2020 statement: An updated guideline for reporting systematic reviews. BMJ 2021;372:n71. PubMed PMC
Cohen JF, Korevaar DA, Altman DG, et al. STARD 2015 guidelines for reporting diagnostic accuracy studies: Explanation and elaboration. BMJ Open 2016;6(11):e012799. PubMed PMC
Pakizer D, Sirimarco G, Elmers J, et al. Search strategies related to: Sensitivity and specificity of atherosclerotic plaque components in carotid arteries detectable by CT, MRI, PET, and sonography – Comparison with histology: A systematic review and meta‐analysis (version 1). Zenodo 2022. 10.5281/zenodo.7229512. DOI
Liberopoulos K, Kaponis A, Kokkinis K, et al. Comparative study of magnetic resonance angiography, digital subtraction angiography, duplex ultrasound examination with surgical and histological findings of atherosclerotic carotid bifurcation disease. Int Angiol 1996;15(2):131‐137. PubMed
Albuquerque LC, Narvaes LB, Maciel AA, et al. Intraplaque hemorrhage assessed by high‐resolution magnetic resonance imaging and C‐reactive protein in carotid atherosclerosis. J Vasc Surg 2007;46(6):1130‐1137. PubMed
Altaf N, Akwei S, Auer DP, MacSweeney ST, Lowe J. Magnetic resonance detected carotid plaque hemorrhage is associated with inflammatory features in symptomatic carotid plaques. Ann Vasc Surg 2013;27(5):655‐661. PubMed
Du Y, Yang L, Wang Y, Zhao Y, Li D, Yu W. Carotid intraplaque hemorrhage imaging using MRI: Comparison of the diagnostic performance between multi‐contrast atherosclerosis characterization and magnetization‐prepared rapid acquisition gradient‐echo with histology. Chin J Radiol 2017;51(6):412‐416.
Li D, Qiao H, Han Y, et al. Histological validation of simultaneous non‐contrast angiography and intraplaque hemorrhage imaging (SNAP) for characterizing carotid intraplaque hemorrhage. Eur Radiol 2021;31(5):3106‐3115. PubMed
Ota H, Tamura H, Itabashi R, et al. Quantitative characterization of carotid plaque components using MR apparent diffusion coefficients and longitudinal relaxation rates at 3T: A comparison with histology. J Magn Reson Imaging 2018;48(6):1657‐1667. PubMed
Ota H, Yarnykh VL, Ferguson MS, et al. Carotid intraplaque hemorrhage imaging at 3.0‐T MR imaging: Comparison of the diagnostic performance of three T1‐weighted sequences. Radiology 2010;254(2):551‐563. PubMed PMC
Liu J, Sun J, Balu N, et al. Semiautomatic carotid intraplaque hemorrhage volume measurement using 3D carotid MRI. J Magn Reson Imaging 2019;50(4):1055‐1062. PubMed PMC
Qiao H, Li D, Cao J, et al. Quantitative evaluation of carotid atherosclerotic vulnerable plaques using in vivo T1 mapping cardiovascular magnetic resonaonce: Validation by histology. J Cardiovasc Magn Reson 2020;22(1):1‐11. PubMed PMC
Dai Y, Lv P, Lin J, et al. Comparison study between multicontrast atherosclerosis characterization (MATCH) and conventional multicontrast MRI of carotid plaque with histology validation. J Magn Reson Imaging 2017;45(3):764‐770. PubMed
Young VE, Patterson AJ, Sadat U, et al. Diffusion‐weighted magnetic resonance imaging for the detection of lipid‐rich necrotic core in carotid atheroma in vivo. Neuroradiology 2010;52(10):929‐936. PubMed
Chai JT, Biasiolli L, Li L, et al. Quantification of lipid‐rich core in carotid atherosclerosis using magnetic resonance T2 mapping. JACC Cardiovasc Imaging 2017;10(7):747‐756. PubMed PMC
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(9):959‐964. PubMed
Kawahara I, Nakamoto M, Kitigawa N, et al. Potential of magnetic resonance plaque imaging using superparamagnetic particles of iron oxide for the detection of carotid plaque. Neurol Med Chir 2008;48(4):157‐162. PubMed
Dong L, Li B, Wang Z, Lu D, Wang Y, Zhang Z. Feasibility study of rapid three dimensional MR angiography in visualization of carotid atherosclerotic plaque. Chin J Radiol 2017;51(4):299‐303.
D'Onofrio M, Mansueto G, Faccioli N, et al. Doppler ultrasound and contrast‐enhanced magnetic resonance angiography in assessing carotid artery stenosis. Radiol Med 2006;111(1):93‐103. PubMed
Millon A, Boussel L, Brevet M, et al. Clinical and histological significance of gadolinium enhancement in carotid atherosclerotic plaque. Stroke 2012;43(11):3023‐3028. PubMed
Millon A, Mathevet JL, Boussel L, et al. High‐resolution magnetic resonance imaging of carotid atherosclerosis identifies vulnerable carotid plaques. J Vasc Surg 2013;57(4):1046‐1051. PubMed
Sigovan M, Bidet C, Bros S, et al. 3D black blood MR angiography of the carotid arteries. A simple sequence for plaque hemorrhage and stenosis evaluation. Magn Reson Imaging 2017;42:95‐100. PubMed PMC
Wang Z, Fan Z, Liu W, et al. Incremental diagnostic value of neck vessel wall imaging technique with T1‐weighted three‐dimensional variable‐flip‐angle turbo spin‐echo before revascularization in patients with carotid atherosclerotic disease. Chin J Radiol 2019;53(8):661‐667.
Yim YJ, Choe YH, Ko Y, et al. High signal intensity halo around the carotid artery on maximum intensity projection images of time‐of‐flight MR angiography: A new sign for intraplaque hemorrhage. J Magn Reson Imaging 2008;27(6):1341‐1346. PubMed
Kawahara I, Morikawa M, Honda M, et al. High‐resolution magnetic resonance imaging using gadolinium‐based contrast agent for atherosclerotic carotid plaque. Surg Neurol 2007;68(1):60‐65. PubMed
Qiao Y, Etesami M, Malhotra S, et al. Identification of intraplaque hemorrhage on MR angiography images: A comparison of contrast‐enhanced mask and time‐of‐flight techniques. Am J Neuroradiol 2011;32(3):454‐459. PubMed PMC
Papini GDE, Di Leo G, Tritella S, et al. Evaluation of inflammatory status of atherosclerotic carotid plaque before thromboendarterectomy using delayed contrast‐enhanced subtracted images after magnetic resonance angiography. Eur J Radiol 2011;80(3):e373‐e380. PubMed
Wang Q, Wang Y, Cai J, et al. Oblique‐sagittal black‐blood contrast‐enhanced magnetic resonance imaging in preoperative evaluation for carotid endarterectomy. Nan Fang Yi Ke Da Xue Xue Bao 2011;31(3):385‐391. PubMed
Yu W, Underhill HR, Ferguson MS, et al. The added value of longitudinal black‐blood cardiovascular magnetic resonance angiography in the cross sectional identification of carotid atherosclerotic ulceration. J Cardiovasc Magn Reson 2009;11(1):1‐10. PubMed PMC
Yuan C, Kerwin WS, Ferguson MS, et al. Contrast‐enhanced high resolution MRI for atherosclerotic carotid artery tissue characterization. J Magn Reson Imaging 2002;15(1):62‐67. PubMed
Ideguchi R, Uetani M, Morikawa M, et al. Usefulness of dynamic contrast‐enhanced MR imaging study for carotid atherosclerotic plaque. Jpn J Clin Radiol 2009;54(9):1119‐1124.
Tapis P, El‐Koussy M, Hewer E, Mono ML, Reinert M. Plaque vulnerability in patients with high‐ and moderate‐grade carotid stenosis – Comparison of plaque features on MRI with histopathological findings. Swiss Med Wkly 2020;150:w20174. PubMed
Chu B, Kampschulte A, Ferguson MS, et al. Hemorrhage in the atherosclerotic carotid plaque: A high‐resolution MRI study. Stroke 2004;35(5):1079‐1084. PubMed
Cappendijk VC, Cleutjens KBJM, Heeneman S, et al. In vivo detection of hemorrhage in human atherosclerotic plaques with magnetic resonance imaging. J Magn Reson Imaging 2004;20(1):105‐110. PubMed
Narumi S, Sasaki M, Miyazawa H, et al. T1‐weighted magnetic resonance carotid plaque imaging: A comparison between conventional and fast spin‐Echo techniques. J Stroke Cerebrovasc Dis 2017;26(2):273‐279. PubMed
Saam T, Ferguson MS, Yarnykh VL, et al. Quantitative evaluation of carotid plaque composition by in vivo MRI. Arterioscler Thromb Vasc Biol 2005;25(1):234‐239. PubMed
Cappendijk VC, Heeneman S, Kessels AGH, et al. Comparison of single‐sequence T1w TFE MRI with multisequence MRI for the quantification of lipid‐rich necrotic core in atherosclerotic plaque. J Magn Reson Imaging 2008;27(6):1347‐1355. PubMed
Esposito L, Sievers M, Sander D, et al. Detection of unstable carotid artery stenosis using MRI. J Neurol 2007;254(12):1714‐1722. PubMed
Yuan C, Mitsumori LM, Beach KW, Maravilla KR. Carotid atherosclerotic plaque: Noninvasive MR characterization and identification of vulnerable lesions. Radiology 2001;221(2):285‐299. PubMed
Honda M, Kitagawa N, Tsutsumi K, Nagata I, Morikawa M, Hayashi T. High‐resolution magnetic resonance imaging for detection of carotid plaques. Neurosurgery 2006;58(2):338‐346. PubMed
Cai JM, Hatsukami TS, Ferguson MS, Small R, Polissar NL, Yuan C. Classification of human carotid atherosclerotic lesions with in vivo multicontrast magnetic resonance imaging. Circulation 2002;106(11):1368‐1373. PubMed
Yoshida K, Goto M, Funaki T, et al. Noninvasive carotid plaque characterization by black blood MRI. No Shinkei Geka 2005;33(3):235‐241. PubMed
Wintermark M, Jawadi SS, Rapp JH, et al. High‐resolution CT imaging of carotid artery atherosclerotic plaques. Am J Neuroradiol 2008;29(5):875‐882. PubMed PMC
Schroeder S, Kuettner A, Leitritz M, et al. Reliability of differentiating human coronary plaque morphology using contrast‐enhanced multislice spiral computed tomography. J Comput Assist Tomogr 2004;28(4):449‐454. PubMed
Mujaj B, Lorza AMA, van Engelen A, et al. Comparison of CT and CMR for detection and quantification of carotid artery calcification: The Rotterdam study. J Cardiovasc Magn Reson 2017;19(1):28. PubMed PMC
Homssi M, Saha A, Delgado D, et al. Extracranial carotid plaque calcification and cerebrovascular ischemia: A systematic review and meta‐analysis. Stroke 2023;54(10):2621‐2628. PubMed PMC
Kan Y, He W, Ning B, Li H, Wei S, Yu T. The correlation between calcification in carotid plaque and stroke: Calcification may be a risk factor for stroke. Int J Clin Exp Pathol 2019;12(3):750‐758. PubMed PMC
Watson MG, Byrne HM, Macaskill C, Myerscough MR. A two‐phase model of early fibrous cap formation in atherosclerosis. J Theor Biol 2018;456:123‐136. PubMed
Yuan C, Zhang S, Polissar NL, et al. Identification of fibrous cap rupture with magnetic resonance imaging is highly associated with recent transient ischemic attack or stroke. Circulation 2002;105(2):181‐185. PubMed
Cappendijk VC, Cleutjens KBJM, Kessels AGH, et al. Assessment of human atherosclerotic carotid plaque components with multisequence MR imaging: Initial experience. Radiology 2005;234(2):487‐492. PubMed
Watanabe Y, Nagayama M, Suga T, et al. Characterization of atherosclerotic plaque of carotid arteries with histopathological correlation: Vascular wall MR imaging vs. color Doppler ultrasonography (US). J Magn Reson Imaging 2008;28(2):478‐485. PubMed
Fan Z, Yu W, Xie Y, et al. Multi‐contrast atherosclerosis characterization (MATCH) of carotid plaque with a single 5‐min scan: Technical development and clinical feasibility. J Cardiovasc Magn Reson 2014;16(1):53. PubMed PMC
Takaya N, Yuan C, Chu B, et al. Presence of intraplaque hemorrhage stimulates progression of carotid atherosclerotic plaques. Circulation 2005;111(21):2768‐2775. PubMed
Mujaj B, Bos D, Muka T, et al. Antithrombotic treatment is associated with intraplaque haemorrhage in the atherosclerotic carotid artery: A cross‐sectional analysis of the Rotterdam study. Eur Heart J 2018;39(36):3369‐3376. PubMed PMC
Redgrave JNE, Lovett JK, Gallagher PJ, Rothwell PM. Histological assessment of 526 symptomatic carotid plaques in relation to the nature and timing of ischemic symptoms. Circulation 2006;113(19):2320‐2328. PubMed
Deng F, Mu C, Yang L, et al. Carotid plaque magnetic resonance imaging and recurrent stroke risk. Medicine 2020;99(13):e19377. PubMed PMC
de Weert TT, Ouhlous M, Zondervan PE, et al. In vitro characterization of atherosclerotic carotid plaque with multidetector computed tomography and histopathological correlation. Eur Radiol 2005;15(9):1906‐1914. PubMed
Underhill HR, Hatsukami TS, Fayad ZA, Fuster V, Yuan C. MRI of carotid atherosclerosis: Clinical implications and future directions. Nat Rev Cardiol 2010;7(3):165‐173. PubMed
Underhill HR, Yarnykh VL, Hatsukami TS, et al. Carotid plaque morphology and composition: Initial comparison between 1.5‐ and 3.0‐T magnetic field strengths. Radiology 2008;248(2):550‐560. PubMed PMC
McNally JS, Yoon HC, Kim SE, et al. Carotid MRI detection of intraplaque hemorrhage at 3T and 1.5T. J Neuroimaging 2015;25(3):390‐396. PubMed PMC
de Buck MHS, Jezzard P, Frost R, et al. 10‐channel phased‐array coil for carotid wall MRI at 3T. PLoS One 2023;18(8):e0288529. PubMed PMC
Wang Y, Liu X, Wang J, et al. Simultaneous T1, T2, and T2* mapping of carotid plaque: The SIMPLE* technique. Radiology 2023;307(3):e222061. PubMed
Geroulakos G, Ramaswami G, Nicolaides A, et al. Characterization of symptomatic and asymptomatic carotid plaques using high‐resolution real‐time ultrasonography. Br J Surg 1993;80(10):1274‐1277. PubMed
Smith LC, Funnell JP, Richards T, Best LMJ. Carotid plaque ulceration: Unquantified predictor of stroke. BJS Open 2023;7(3):zrad058. PubMed PMC
Yuan J, Usman A, Das T, Patterson AJ, Gillard JH, Graves MJ. Imaging carotid atherosclerosis plaque ulceration: Comparison of advanced imaging modalities and recent developments. Am J Neuroradiol 2017;38(4):664‐671. PubMed PMC
Milei J, Parodi JC, Alonso GF, Barone A, Grana D, Matturri L. Carotid rupture and intraplaque hemorrhage: Immunophenotype and role of cells involved. Am Heart J 1998;136(6):1096‐1105. PubMed
Saba L, Saam T, Jäger HR, et al. Imaging biomarkers of vulnerable carotid plaques for stroke risk prediction and their potential clinical implications. Lancet Neurol 2019;18(6):559‐572. PubMed
Bos D, Arshi B, van den Bouwhuijsen QJA, et al. Atherosclerotic carotid plaque composition and incident stroke and coronary events. J Am Coll Cardiol 2021;77(11):1426‐1435. PubMed
Naylor R, Rantner B, Ancetti S, et al. Editor's choice – European Society for Vascular Surgery (ESVS) 2023 Clinical Practice Guidelines on the Management of Atherosclerotic Carotid and Vertebral Artery Disease. Eur J Vasc Endovasc Surg 2023;65(1):7‐111. PubMed
Gupta A, Mushlin AI, Kamel H, Navi BB, Pandya A. Cost‐effectiveness of carotid plaque MR imaging as a stroke risk stratification tool in asymptomatic carotid artery stenosis. Radiology 2015;277(3):763‐772. PubMed PMC
Wang Y, Cai C, Du YM, et al. Assessment of stroke risk using MRI‐VPD with automatic segmentation of carotid plaques and classification of plaque properties based on deep learning. J Radiat Res Appl Sci 2023;16(3):100630.
Bitar R, Moody AR, Leung G, et al. In vivo 3D high‐spatial‐resolution MR imaging of intraplaque hemorrhage. Radiology 2008;249(1):259‐267. PubMed
Kampschulte A, Ferguson MS, Kerwin WS, et al. Differentiation of intraplaque versus juxtaluminal hemorrhage/thrombus in advanced human carotid atherosclerotic lesions by in vivo magnetic resonance imaging. Circulation 2004;110(20):3239‐3244. PubMed
Saito H, Kuroda S, Hirata K, et al. Validity of dual MRI and 18F‐FDG PET imaging in predicting vulnerable and inflamed carotid plaque. Cerebrovasc Dis 2013;35(4):370‐377. PubMed
Liu W, Xie Y, Wang C, et al. Atherosclerosis T1‐weighted characterization (CATCH): Evaluation of the accuracy for identifying intraplaque hemorrhage with histological validation in carotid and coronary artery specimens. J Cardiovasc Magn Reson 2018;20(1):1‐9. PubMed PMC
Puppini G, Furlan F, Cirota N, et al. Characterisation of carotid atherosclerotic plaque: Comparison between magnetic resonance imaging and histology. Radiol Med 2006;111(7):921‐930. PubMed
Takemoto K, Ueba T, Takano K, et al. Quantitative evaluation using the plaque/muscle ratio index panels predicts plaque type and risk of embolism in patients undergoing carotid artery stenting. Clin Neurol Neurosurg 2013;115(8):1298‐1303. PubMed
Honda M, Kawahara I, Kitagawa N, et al. Asymptomatic carotid artery plaques: Use of magnetic resonance imaging to characterize vulnerable plaques in 6 cases. Surg Neurol 2007;67(1):35‐39. PubMed
Mitsumori LM, Hatsukami TS, Ferguson MS, Kerwin WS, Cai J, Yuan C. In vivo accuracy of multisequence MR imaging for identifying unstable fibrous caps in advanced human carotid plaques. J Magn Reson Imaging 2003;17(4):410‐420. PubMed
Watanabe Y, Nagayama M, Sakata A, et al. Evaluation of fibrous cap rupture of atherosclerotic carotid plaque with thin‐slice source images of time‐of‐flight MR angiography. Ann Vasc Dis 2014;7(2):127‐133. PubMed PMC
Moody AR, Murphy RE, Morgan PS, et al. Characterization of complicated carotid plaque with magnetic resonance direct thrombus imaging in patients with cerebral ischemia. Circulation 2003;107(24):3047‐3052. PubMed
Yoshida K, Narumi O, Chin M, et al. Characterization of carotid atherosclerosis and detection of soft plaque with use of black‐blood MR imaging. Am J Neuroradiol 2008;29(5):868‐874. PubMed PMC
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