Multi-contrast atherosclerosis characterization (MATCH) of carotid plaque with a single 5-min scan: technical development and clinical feasibility
Tóm tắt
Multi-contrast weighted imaging is a commonly used cardiovascular magnetic resonance (CMR) protocol for characterization of carotid plaque composition. However, this approach is limited in several aspects including low slice resolution, long scan time, image mis-registration, and complex image interpretation. In this work, a 3D CMR technique, named Multi-contrast Atherosclerosis Characterization (MATCH), was developed to mitigate the above limitations. MATCH employs a 3D spoiled segmented fast low angle shot readout to acquire data with three different contrast weightings in an interleaved fashion. The inherently co-registered image sets, hyper T1-weighting, gray blood, and T2-weighting, are used to detect intra-plaque hemorrhage (IPH), calcification (CA), lipid-rich necrotic core (LRNC), and loose-matrix (LM). The MATCH sequence was optimized by computer simulations and testing on four healthy volunteers and then evaluated in a pilot study of six patients with carotid plaque, using the conventional multi-contrast protocol as a reference. On MATCH images, the major plaque components were easy to identify. Spatial co-registration between the three image sets with MATCH was particularly helpful for the reviewer to discern co-existent components in an image and appreciate their spatial relation. Based on Cohen’s kappa tests, moderate to excellent agreement in the image-based or artery-based component detection between the two protocols was obtained for LRNC, IPH, CA, and LM, respectively. Compared with the conventional multi-contrast protocol, the MATCH protocol yield significantly higher signal contrast ratio for IPH (3.1 ± 1.3 vs. 0.4 ± 0.3, p < 0.001) and CA (1.6 ± 1.5 vs. 0.7 ± 0.6, p = 0.012) with respect to the vessel wall. To the best of our knowledge, the proposed MATCH sequence is the first 3D CMR technique that acquires spatially co-registered multi-contrast image sets in a single scan for characterization of carotid plaque composition. Our pilot clinical study suggests that the MATCH-based protocol may outperform the conventional multi-contrast protocol in several respects. With further technical improvements and large-scale clinical validation, MATCH has the potential to become a CMR method for assessing the risk of plaque disruption in a clinical workup.
Tài liệu tham khảo
Barnett HJ, Gunton RW, Eliasziw M, Fleming L, Sharpe B, Gates P, Meldrum H: Causes and severity of ischemic stroke in patients with internal carotid artery stenosis. JAMA. 2000, 283: 1429-1436. 10.1001/jama.283.11.1429.
Golledge J, Greenhalgh RM, Davies AH: The symptomatic carotid plaque. Stroke. 2000, 31: 774-781. 10.1161/01.STR.31.3.774.
Inzitari D, Eliasziw M, Gates P, Sharpe BL, Chan RK, Meldrum HE, Barnett HJ: The causes and risk of stroke in patients with asymptomatic internal-carotid-artery stenosis: North American Symptomatic Carotid Endarterectomy Trial Collaborators. N Engl J Med. 2000, 342: 1693-1700. 10.1056/NEJM200006083422302.
Imparato AM, Riles TS, Gorstein F: The carotid bifurcation plaque: pathologic findings associated with cerebral ischemia. Stroke. 1979, 10: 238-245. 10.1161/01.STR.10.3.238.
Lusby RJ, Ferrell LD, Ehrenfeld WK, Stoney RJ, Wylie EJ: Carotid plaque hemorrhage: its role in production of cerebral ischemia. Arch Surg. 1982, 117: 1479-1488. 10.1001/archsurg.1982.01380350069010.
Virmani R, Burke AP, Farb A, Kolodgie FD: Pathology of the vulnerable plaque. J Am Coll Cardiol. 2006, 47: C13-C18. 10.1016/j.jacc.2005.10.065.
Fayad ZA, Fuster V: Characterization of atherosclerotic plaques by magnetic resonance imaging. Ann N Y Acad Sci. 2000, 902: 173-186. 10.1111/j.1749-6632.2000.tb06312.x.
Yuan C, Mitsumori LM, Beach KW, Maravilla KR: Carotid atherosclerotic plaque: noninvasive MR characterization and identification of vulnerable lesions. Radiology. 2001, 221: 285-299. 10.1148/radiol.2212001612.
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: 1368-1373. 10.1161/01.CIR.0000028591.44554.F9.
Clarke SE, Hammond RR, Mitchell JR, Rutt BK: Quantitative assessment of carotid plaque composition using multicontrast MRI and registered histology. Magn Reson Med. 2003, 50: 1199-1208. 10.1002/mrm.10618.
Saam T, Ferguson MS, Yarnykh VL, Takaya N, Xu D, Polissar NL, Hatsukami TS, Yuan C: Quantitative evaluation of carotid plaque composition by in vivo MRI. Arterioscler Thromb Vasc Biol. 2005, 25: 234-239.
Yuan C, Mitsumori LM, Ferguson MS, Polissar NL, Echelard D, Ortiz G, Small R, Davies JW, Kerwin WS, Hatsukami TS: In vivo accuracy of multispectral magnetic resonance imaging for identifying lipid-rich necrotic cores and intraplaque hemorrhage in advanced human carotid plaques. Circulation. 2001, 104: 2051-2056. 10.1161/hc4201.097839.
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: 410-420. 10.1002/jmri.10264.
Takaya N, Yuan C, Chu B, Saam T, Underhill H, Cai J, Tran N, Polissar NL, Isaac C, Ferguson MS, Garden GA, Cramer SC, Maravilla KR, Hashimoto B, Hatsukami TS: Association between carotid plaque characteristics and subsequent ischemic cerebrovascular events: a prospective assessment with MRI–initial results. Stroke. 2006, 37: 818-823. 10.1161/01.STR.0000204638.91099.91.
den Hartog AG, Bovens SM, Koning W, Hendrikse J, Luijten PR, Moll FL, Pasterkamp G, de Borst GJ: Current status of clinical magnetic resonance imaging for plaque characterisation in patients with carotid artery stenosis. Eur J Vasc Endovasc Surg. 2013, 45: 7-21. 10.1016/j.ejvs.2012.10.022.
Antiga L, Wasserman BA, Steinman DA: On the overestimation of early wall thickening at the carotid bulb by black blood MRI, with implications for coronary and vulnerable plaque imaging. Magn Reson Med. 2008, 60: 1020-1028. 10.1002/mrm.21758.
Balu N, Kerwin WS, Chu B, Liu F, Yuan C: Serial MRI of carotid plaque burden: influence of subject repositioning on measurement precision. Magn Reson Med. 2007, 57: 592-599. 10.1002/mrm.21160.
Luk-Pat GT, Gold GE, Olcott EW, Hu BS, Nishimura DG: High-resolution three-dimensional in vivo imaging of atherosclerotic plaque. Magn Reson Med. 1999, 42: 762-771. 10.1002/(SICI)1522-2594(199910)42:4<762::AID-MRM19>3.0.CO;2-M.
Crowe LA, Gatehouse P, Yang GZ, Mohiaddin RH, Varghese A, Charrier C, Keegan J, Firmin DN: Volume-selective 3D turbo spin echo imaging for vascular wall imaging and distensibility measurement. J Magn Reson Imaging. 2003, 17: 572-580. 10.1002/jmri.10294.
Bornstedt A, Bernhardt P, Hombach V, Kamenz J, Spiess J, Subgang A, Rasche V: Local excitation black blood imaging at 3T: application to the carotid artery wall. Magn Reson Med. 2008, 59: 1207-1211. 10.1002/mrm.21590.
Balu N, Yarnykh VL, Chu B, Wang J, Hatsukami T, Yuan C: Carotid plaque assessment using fast 3D isotropic resolution black-blood MRI. Magn Reson Med. 2011, 65: 627-637. 10.1002/mrm.22642.
Fan Z, Zhang Z, Chung YC, Weale P, Zuehlsdorff S, Carr J, Li D: Carotid arterial wall MRI at 3T using 3D variable-flip-angle turbo spin-echo (TSE) with flow-sensitive dephasing (FSD). J Magn Reson Imaging. 2010, 31: 645-654. 10.1002/jmri.22058.
Koktzoglou I, Li D: Submillimeter isotropic resolution carotid wall MRI with swallowing compensation: imaging results and semiautomated wall morphometry. J Magn Reson Imaging. 2007, 25: 815-823. 10.1002/jmri.20849.
Moody AR, Murphy RE, Morgan PS, Martel AL, Delay GS, Allder S, MacSweeney ST, Tennant WG, Gladman J, Lowe J, Hunt BJ: Characterization of complicated carotid plaque with magnetic resonance direct thrombus imaging in patients with cerebral ischemia. Circulation. 2003, 107: 3047-3052. 10.1161/01.CIR.0000074222.61572.44.
Wang J, Bornert P, Zhao H, Hippe DS, Zhao X, Balu N, Ferguson MS, Hatsukami TS, Xu J, Yuan C, Kerwin WS: Simultaneous noncontrast angiography and intraplaque hemorrhage (SNAP) imaging for carotid atherosclerotic disease evaluation. Magn Reson Med. 2013, 69: 337-345. 10.1002/mrm.24254.
Zhu DC, Vu AT, Ota H, DeMarco JK: An optimized 3D spoiled gradient recalled echo pulse sequence for hemorrhage assessment using inversion recovery and multiple echoes (3D SHINE) for carotid plaque imaging. Magn Reson Med. 2010, 64: 1341-1351. 10.1002/mrm.22517.
Cappendijk VC, Heeneman S, Kessels AG, Cleutjens KB, Schurink GW, Welten RJ, Mess WH, van Suylen RJ, Leiner T, Daemen MJ, van Engelshoven JM, Kooi ME: 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: 1347-1355. 10.1002/jmri.21360.
Koktzoglou I: Gray blood magnetic resonance for carotid wall imaging and visualization of deep-seated and superficial vascular calcifications. Magn Reson Med. 2013, 70: 75-85. 10.1002/mrm.24445.
Ota H, Yarnykh VL, Ferguson MS, Underhill HR, Demarco JK, Zhu DC, Oikawa M, Dong L, Zhao X, Collar A, Hatsukami TS, Yuan C: Carotid intraplaque hemorrhage imaging at 3.0-T MR imaging: comparison of the diagnostic performance of three T1-weighted sequences. Radiology. 2010, 254: 551-563. 10.1148/radiol.09090535.
Zhu DC, Ferguson MS, DeMarco JK: An optimized 3D inversion recovery prepared fast spoiled gradient recalled sequence for carotid plaque hemorrhage imaging at 3.0 T. Magn Reson Imaging. 2008, 26: 1360-1366. 10.1016/j.mri.2008.05.002.
Fan Z, Sheehan J, Bi X, Liu X, Carr J, Li D: 3D noncontrast MR angiography of the distal lower extremities using flow-sensitive dephasing (FSD)-prepared balanced SSFP. Magn Reson Med. 2009, 62: 1523-1532. 10.1002/mrm.22142.
Wang J, Yarnykh VL, Hatsukami T, Chu B, Balu N, Yuan C: Improved suppression of plaque-mimicking artifacts in black-blood carotid atherosclerosis imaging using a multislice motion-sensitized driven-equilibrium (MSDE) turbo spin-echo (TSE) sequence. Magn Reson Med. 2007, 58: 973-981. 10.1002/mrm.21385.
Koktzoglou I, Li D: Diffusion-prepared segmented steady-state free precession: Application to 3D black-blood cardiovascular magnetic resonance of the thoracic aorta and carotid artery walls. J Cardiovasc Magn Reson. 2007, 9: 33-42. 10.1080/10976640600843413.
Levitt M, Freeman R, Frenkel T: Broadband heteronuclear decoupling. J Magn Reson. 1982, 47: 328-330.
Noeske R, Seifert F, Rhein KH, Rinneberg H: Human cardiac imaging at 3 T using phased array coils. Magn Reson Med. 2000, 44: 978-982. 10.1002/1522-2594(200012)44:6<978::AID-MRM22>3.0.CO;2-9.
Kerwin WS: Carotid artery disease and stroke: assessing risk with vessel wall MRI. ISRN Cardiol. 2012, 2012: 180710-10.5402/2012/180710.
Chu B, Kampschulte A, Ferguson MS, Kerwin WS, Yarnykh VL, O’Brien KD, Polissar NL, Hatsukami TS, Yuan C: Hemorrhage in the atherosclerotic carotid plaque: a high-resolution MRI study. Stroke. 2004, 35: 1079-1084. 10.1161/01.STR.0000125856.25309.86.
Landis JR, Koch GG: The measurement of observer agreement for categorical data. Biometrics. 1977, 33: 159-174. 10.2307/2529310.
Wang J, Ferguson MS, Balu N, Yuan C, Hatsukami TS, Bornert P: Improved carotid intraplaque hemorrhage imaging using a slab-selective phase-sensitive inversion-recovery (SPI) sequence. Magn Reson Med. 2010, 64: 1332-1340. 10.1002/mrm.22539.
Boussel L, Arora S, Rapp J, Rutt B, Huston J, Parker D, Yuan C, Bassiouny H, Saloner D, Investigators M: Atherosclerotic plaque progression in carotid arteries: monitoring with high-spatial-resolution MR imaging–multicenter trial. Radiology. 2009, 252: 789-796. 10.1148/radiol.2523081798.
Fan Z, Zuehlsdorff S, Liu X, Li D: Prospective self-gating for swallowing motion: a feasibility study in carotid artery wall MRI using three-dimensional variable-flip-angle turbo spin-echo. Magn Reson Med. 2012, 67: 490-498. 10.1002/mrm.23295.
Gupta A, Baradaran H, Schweitzer AD, Kamel H, Pandya A, Delgado D, Dunning A, Mushlin AI, Sanelli PC: Carotid plaque MRI and stroke risk: a systematic review and meta-analysis. Stroke. 2013, 44: 3071-3077. 10.1161/STROKEAHA.113.002551.
Touze E, Toussaint JF, Coste J, Schmitt E, Bonneville F, Vandermarcq P, Gauvrit JY, Douvrin F, Meder JF, Mas JL, Oppenheim C: Reproducibility of high-resolution MRI for the identification and the quantification of carotid atherosclerotic plaque components: consequences for prognosis studies and therapeutic trials. Stroke. 2007, 38: 1812-1819. 10.1161/STROKEAHA.106.479139.
Kwee RM, van Engelshoven JM, Mess WH, ter Berg JW, Schreuder FH, Franke CL, Korten AG, Meems BJ, van Oostenbrugge RJ, Wildberger JE, Kooi ME: Reproducibility of fibrous cap status assessment of carotid artery plaques by contrast-enhanced MRI. Stroke. 2009, 40: 3017-3021. 10.1161/STROKEAHA.109.555052.
Takaya N, Cai J, Ferguson MS, Yarnykh VL, Chu B, Saam T, Polissar NL, Sherwood J, Cury RC, Anders RJ, Broschat KO, Hinton D, Furie KL, Hatsukami TS, Yuan C: Intra- and interreader reproducibility of magnetic resonance imaging for quantifying the lipid-rich necrotic core is improved with gadolinium contrast enhancement. J Magn Reson Imaging. 2006, 24: 203-210. 10.1002/jmri.20599.
Wasserman BA, Smith WI, Trout HH, Cannon RO, Balaban RS, Arai AE: Carotid artery atherosclerosis: in vivo morphologic characterization with gadolinium-enhanced double-oblique MR imaging initial results. Radiology. 2002, 223: 566-573. 10.1148/radiol.2232010659.
Yuan C, Kerwin WS, Ferguson MS, Polissar N, Zhang S, Cai J, Hatsukami TS: Contrast-enhanced high resolution MRI for atherosclerotic carotid artery tissue characterization. J Magn Reson Imaging. 2002, 15: 62-67. 10.1002/jmri.10030.