Contemporary carotid imaging: From degree of stenosis to plaque vulnerability

Journal of Neurosurgery

Volumn 124, Issue 1, 2016, Pages 27-42

  Brinjikji, Waleed ^a   Huston, John ^a   Rabinstein, Alejandro A ^a   Kim, Gyeong Moon ^b   Lerman, Amir ^a   Lanzino, Giuseppe ^a  

^a MAYO CLINIC   (United States)

^b Sungkyunkwan University School of Medicine   (South Korea)

Author keywords

Carotid artery; MRI; Risk; Ultrasound; Vascular disorders

Indexed keywords

CAROTID ARTERY; CAROTID ARTERY OBSTRUCTION; CAROTID ARTERY STENTING; CAROTID ATHEROSCLEROSIS; CAROTID ENDARTERECTOMY; CAROTID PLAQUE IMAGING; COMPUTER ASSISTED TOMOGRAPHY; CONTRAST ENHANCEMENT; ECHOGRAPHY; HISTOPATHOLOGY; HUMAN; META ANALYSIS (TOPIC); MOLECULAR IMAGING; NEUROIMAGING; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOGENESIS; PATIENT RISK; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; SENSITIVITY AND SPECIFICITY; SYSTEMATIC REVIEW (TOPIC); TRANSCRANIAL DOPPLER ULTRASONOGRAPHY; CAROTID STENOSIS; PATHOLOGY; PLAQUE, ATHEROSCLEROTIC;

CAROTID ARTERIES; CAROTID STENOSIS; HUMANS; MAGNETIC RESONANCE IMAGING; MOLECULAR IMAGING; PLAQUE, ATHEROSCLEROTIC; POSITRON-EMISSION TOMOGRAPHY;

EID: 84966350064     PISSN: 00223085     EISSN: 19330693     Source Type: Journal    
DOI: 10.3171/2015.1.JNS142452     Document Type: Review

References (130)

1. Ajduk M, Pavić L, Bulimbasić S, Sarlija M, Pavić P, Patrlj L, et al: Multidetector-row computed tomography in evaluation of atherosclerotic carotid plaques complicated with intraplaque hemorrhage. Ann Vasc Surg 23:186-193, 2009
2. Aldemir E, Apaydin M, Varer M, Uluc E: Echolucency of carotid plaques and cerebrovascular events. J Clin Ultrasound 40:399-404, 2012
3. Altaf N, Daniels L, Morgan PS, Auer D, MacSweeney ST, Moody AR, et al: Detection of intraplaque hemorrhage by magnetic resonance imaging in symptomatic patients with mild to moderate carotid stenosis predicts recurrent neurological events. J Vasc Surg 47:337-342, 2008
4. Anzidei M, Napoli A, Geiger D, Cavallo Marincola B, Zini C, Zaccagna F, et al: Preliminary experience with MRA in evaluating the degree of carotid stenosis and plaque morphology using high-resolution sequences after gadofosveset trisodium (Vasovist) administration: comparison with CTA and DSA. Radiol Med (Torino) 115:634-647, 2010
5. Arnold JA, Modaresi KB, Thomas N, Taylor PR, Padayachee TS: Carotid plaque characterization by duplex scanning: observer error may undermine current clinical trials. Stroke 30:61-65, 1999
6. Ballotta E, Angelini A, Mazzalai F, Piatto G, Toniato A, Baracchini C: Carotid endarterectomy for symptomatic lowgrade carotid stenosis. J Vasc Surg 59:25-31, 2014
7. Barger AC, Beeuwkes R III, Lainey LL, Silverman KJ: Hypothesis: vasa vasorum and neovascularization of human coronary arteries. A possible role in the pathophysiology of atherosclerosis. N Engl J Med 310:175-177, 1984
8. Barnett HJ, Taylor DW, Eliasziw M, Fox AJ, Ferguson GG, Haynes RB, et al: Benefit of carotid endarterectomy in patients with symptomatic moderate or severe stenosis. N Engl J Med 339:1415-1425, 1998
9. Beer AJ, Pelisek J, Heider P, Saraste A, Reeps C, Metz S, et al: PET/CT imaging of integrin avb3 expression in human carotid atherosclerosis. JACC Cardiovasc Imaging 7: 178-187, 2014
10. Blomberg BA, Thomassen A, Takx RA, Hildebrandt MG, Simonsen JA, Buch-Olsen KM, et al: Delayed 18F-fluorodeoxyglucose PET/CT imaging improves quantitation of atherosclerotic plaque inflammation: results from the CAMONA study. J Nucl Cardiol 21:588-597, 2014
11. Calcagno C, Ramachandran S, Izquierdo-Garcia D, Mani V, Millon A, Rosenbaum D, et al: The complementary roles of dynamic contrast-enhanced MRI and 18F-fluorodeoxyglucose PET/CT for imaging of carotid atherosclerosis. Eur J Nucl Med Mol Imaging 40:1884-1893, 2013
12. Cappendijk VC, Cleutjens KB, Heeneman S, Schurink GW, Welten RJ, Kessels AG, et al: In vivo detection of hemorrhage in human atherosclerotic plaques with magnetic resonance imaging. J Magn Reson Imaging 20:105-110, 2004
13. Cappendijk VC, Kessels AG, Heeneman S, Cleutjens KB, Schurink GW, Welten RJ, et al: Comparison of lipid-rich necrotic core size in symptomatic and asymptomatic carotid atherosclerotic plaque: Initial results. J Magn Reson Imaging 27:1356-1361, 2008
14. Carr SC, Farb A, Pearce WH, Virmani R, Yao JS: Activated inflammatory cells are associated with plaque rupture in carotid artery stenosis. Surgery 122:757-764, 1997
15. Chan JM, Monaco C, Wylezinska-Arridge M, Tremoleda JL, Gibbs RG: Imaging of the vulnerable carotid plaque: biological targeting of inflammation in atherosclerosis using iron oxide particles and MRI. Eur J Vasc Endovasc Surg 47:462-469, 2014
16. Chen W, Dilsizian V: Targeted PET/CT imaging of vulnerable atherosclerotic plaques: microcalcification with sodium fluoride and inflammation with fluorodeoxyglucose. Curr Cardiol Rep 15:364, 2013
17. Chu B, Kampschulte A, Ferguson MS, Kerwin WS, Yarnykh VL, O'Brien KD, et al: Hemorrhage in the atherosclerotic carotid plaque: a high-resolution MRI study. Stroke 35:1079-1084, 2004
18. Clevert DA, Sommer WH, Helck A, Saam T, Reiser M: Improved carotid atherosclerotic plaques imaging with contrast-enhanced ultrasound (CEUS). Clin Hemorheol Microcirc 48:141-148, 2011
19. Coli S, Magnoni M, Sangiorgi G, Marrocco-Trischitta MM, Melisurgo G, Mauriello A, et al: Contrast-enhanced ultrasound imaging of intraplaque neovascularization in carotid arteries: correlation with histology and plaque echogenicity. J Am Coll Cardiol 52:223-230, 2008
20. Das M, Braunschweig T, Mühlenbruch G, Mahnken AH, Krings T, Langer S, et al: Carotid plaque analysis: comparison of dual-source computed tomography (CT) findings and histopathological correlation. Eur J Vasc Endovasc Surg 38:14-19, 2009
21. Della-Morte D, Moussa I, Elkind MS, Sacco RL, Rundek T: The short-term effect of atorvastatin on carotid plaque morphology assessed by computer-assisted gray-scale densitometry: a pilot study. Neurol Res 33:991-994, 2011
22. den Hartog AG, Bovens SM, Koning W, Hendrikse J, Luijten PR, Moll FL, et al: Current status of clinical magnetic resonance imaging for plaque characterisation in patients with carotid artery stenosis. Eur J Vasc Endovasc Surg 45:7-21, 2013
23. Deyama J, Nakamura T, Takishima I, Fujioka D, Kawabata K, Obata JE, et al: Contrast-enhanced ultrasound imaging of carotid plaque neovascularization is useful for identifying high-risk patients with coronary artery disease. Circ J 77:1499-1507, 2013
24. Droste DW, Jürgens R, Nabavi DG, Schuierer G, Weber S, Ringelstein EB: Echocontrast-enhanced ultrasound of extracranial internal carotid artery high-grade stenosis and occlusion. Stroke 30:2302-2306, 1999
25. Eliasziw M, Streifler JY, Fox AJ, Hachinski VC, Ferguson GG, Barnett HJ: Significance of plaque ulceration in symptomatic patients with high-grade carotid stenosis. North American Symptomatic Carotid Endarterectomy Trial. Stroke 25:304-308, 1994
26. Etesami M, Hoi Y, Steinman DA, Gujar SK, Nidecker AE, Astor BC, et al: Comparison of carotid plaque ulcer detection using contrast-enhanced and time-of-flight MRA techniques. AJNR Am J Neuroradiol 34:177-184, 2013
27. European Carotid Surgery Trialists' Collaborative Group: Randomised trial of endarterectomy for recently symptomatic carotid stenosis: final results of the MRC European Carotid Surgery Trial (ECST). Lancet 351:1379-1387, 1998
28. Fairhead JF, Rothwell PM: The need for urgency in identification and treatment of symptomatic carotid stenosis is already established. Cerebrovasc Dis 19:355-358, 2005
29. Falk E: Why do plaques rupture? Circulation 86 (6 Suppl):III30-III42, 1992
30. Ferrer JM, Samsó JJ, Serrando JR, Valenzuela VF, Montoya SB, Docampo MM: Use of ultrasound contrast in the diagnosis of carotid artery occlusion. J Vasc Surg 31:736-741, 2000
31. Folco EJ, Sheikine Y, Rocha VZ, Christen T, Shvartz E, Sukhova GK, et al: Hypoxia but not inflammation augments glucose uptake in human macrophages: Implications for imaging atherosclerosis with 18fluorine-labeled 2-deoxy-Dglucose positron emission tomography. J Am Coll Cardiol 58:603-614, 2011
32. Freilinger TM, Schindler A, Schmidt C, Grimm J, Cyran C, Schwarz F, et al: Prevalence of nonstenosing, complicated atherosclerotic plaques in cryptogenic stroke. JACC Cardiovasc Imaging 5:397-405, 2012
33. Gaens ME, Backes WH, Rozel S, Lipperts M, Sanders SN, Jaspers K, et al: Dynamic contrast-enhanced MR imaging of carotid atherosclerotic plaque: model selection, reproducibility, and validation. Radiology 266:271-279, 2013
34. Glagov S, Weisenberg E, Zarins CK, Stankunavicius R, Kolettis GJ: Compensatory enlargement of human atherosclerotic coronary arteries. N Engl J Med 316:1371-1375, 1987
35. Griswold MA, Jakob PM, Heidemann RM, Nittka M, Jellus V, Wang J, et al: Generalized autocalibrating partially parallel acquisitions (GRAPPA). Magn Reson Med 47:1202-1210, 2002
36. Gupta A, Baradaran H, Schweitzer AD, Kamel H, Pandya A, Delgado D, et al: Carotid plaque MRI and stroke risk: a systematic review and meta-analysis. Stroke 44:3071-3077, 2013
37. Halliday A, Mansfield A, Marro J, Peto C, Peto R, Potter J, et al: Prevention of disabling and fatal strokes by successful carotid endarterectomy in patients without recent neurological symptoms: randomised controlled trial. Lancet 363:1491-1502, 2004
38. Handa N, Matsumoto M, Maeda H, Hougaku H, Kamada T: Ischemic stroke events and carotid atherosclerosis. Results of the Osaka Follow-up Study for Ultrasonographic Assessment of Carotid Atherosclerosis (the OSACA Study). Stroke 26:1781-1786, 1995
39. Heidemann RM, Griswold MA, Haase A, Jakob PM: VD-AUTO-SMASH imaging. Magn Reson Med 45:1066-1074, 2001
40. Hermann S, Starsichova A, Waschkau B, Kuhlmann M, Wenning C, Schober O, et al: Non-FDG imaging of atherosclerosis: will imaging of MMPs assess plaque vulnerability? J Nucl Cardiol 19:609-617, 2012
41. Hobson RW II, Weiss DG, Fields WS, Goldstone J, Moore WS, Towne JB, et al: Efficacy of carotid endarterectomy for asymptomatic carotid stenosis. N Engl J Med 328:221-227, 1993
42. Horie N, Morikawa M, Ishizaka S, Takeshita T, So G, Hayashi K, et al: Assessment of carotid plaque stability based on the dynamic enhancement pattern in plaque components with multidetector CT angiography. Stroke 43:393-398, 2012
43. Huang PT, Huang FG, Zou CP, Sun HY, Tian XQ, Yang Y, et al: Contrast-enhanced sonographic characteristics of neovascularization in carotid atherosclerotic plaques. J Clin Ultrasound 36:346-351, 2008
44. Jaipersad AS, Shantsila A, Silverman S, Lip GY, Shantsila E: Evaluation of carotid plaque neovascularization using contrast ultrasound. Angiology 64:447-450, 2013
45. Jonasson L, Holm J, Skalli O, Bondjers G, Hansson GK: Regional accumulations of T cells, macrophages, and smooth muscle cells in the human atherosclerotic plaque. Arteriosclerosis 6:131-138, 1986
46. Joshi NV, Vesey AT, Williams MC, Shah AS, Calvert PA, Craighead FH, et al: 18F-fluoride positron emission tomography for identification of ruptured and high-risk coronary atherosclerotic plaques: a prospective clinical trial. Lancet 383:705-713, 2014
47. Kadoglou NP, Sailer N, Moumtzouoglou A, Kapelouzou A, Gerasimidis T, Liapis CD: Aggressive lipid-lowering is more effective than moderate lipid-lowering treatment in carotid plaque stabilization. J Vasc Surg 51:114-121, 2010
48. Kern R, Szabo K, Hennerici M, Meairs S: Characterization of carotid artery plaques using real-time compound B-mode ultrasound. Stroke 35:870-875, 2004
49. Kerwin WS, Oikawa M, Yuan C, Jarvik GP, Hatsukami TS: MR imaging of adventitial vasa vasorum in carotid atherosclerosis. Magn Reson Med 59:507-514, 2008
50. Kim HS, Woo JS, Kim BY, Jang HH, Hwang SJ, Kwon SJ, et al: Biochemical and clinical correlation of intraplaque neovascularization using contrast-enhanced ultrasound of the carotid artery. Atherosclerosis 233:579-583, 2014
51. Kirsch JD, Mathur M, Johnson MH, Gowthaman G, Scoutt LM: Advances in transcranial Doppler US: imaging ahead. Radiographics 33:E1-E14, 2013
52. Kurata M, Nose M, Shimazu Y, Aoba T, Kohada Y, Yorioka S, et al: Microvasculature of carotid atheromatous plaques: hemorrhagic plaques have dense microvessels with fenestrations to the arterial lumen. J Stroke Cerebrovasc Dis 23:1440-1446, 2014
53. Kwee RM, Truijman MT, Mess WH, Teule GJ, ter Berg JW, Franke CL, et al: Potential of integrated [18F] fluorodeoxyglucose positron-emission tomography/CT in identifying vulnerable carotid plaques. AJNR Am J Neuroradiol 32:950-954, 2011
54. Kyriacou EC, Pattichis C, Pattichis M, Loizou C, Christodoulou C, Kakkos SK, et al: A review of noninvasive ultrasound image processing methods in the analysis of carotid plaque morphology for the assessment of stroke risk. IEEE Trans Inf Technol Biomed 14:1027-1038, 2010
55. Leschka S, Scheffel H, Desbiolles L, Plass A, Gaemperli O, Valenta I, et al: Image quality and reconstruction intervals of dual-source CT coronary angiography: recommendations for ECG-pulsing windowing. Invest Radiol 42:543-549, 2007
56. Lindner JR, Dayton PA, Coggins MP, Ley K, Song J, Ferrara K, et al: Noninvasive imaging of inflammation by ultrasound detection of phagocytosed microbubbles. Circulation 102:531-538, 2000
57. Markus HS, Brown MM: Differentiation between different pathological cerebral embolic materials using transcranial Doppler in an in vitro model. Stroke 24:1-5, 1993
58. Marnane M, Merwick A, Sheehan OC, Hannon N, Foran P, Grant T, et al: Carotid plaque inflammation on 18F-fluorodeoxyglucose positron emission tomography predicts early stroke recurrence. Ann Neurol 71:709-718, 2012
59. Masteling MG, Zeebregts CJ, Tio RA, Breek JC, Tietge UJ, de Boer JF, et al: High-resolution imaging of human atherosclerotic carotid plaques with micro 18F-FDG PET scanning exploring plaque vulnerability. J Nucl Cardiol 18:1066-1075, 2011
60. Mathiesen EB, Boønaa KH, Joakimsen O: Echolucent plaques are associated with high risk of ischemic cerebrovascular events in carotid stenosis: the Tromsoø study. Circulation 103:2171-2175, 2001
61. Menezes LJ, Kotze CW, Agu O, Richards T, Brookes J, Goh VJ, et al: Investigating vulnerable atheroma using combined (18)F-FDG PET/CT angiography of carotid plaque with immunohistochemical validation. J Nucl Med 52:1698-1703, 2011
62. Michel JB, Delbosc S, Ho-Tin-Noé B, Leseche G, Nicoletti A, Meilhac O, et al: From intraplaque haemorrhages to plaque vulnerability: biological consequences of intraplaque haemorrhages. J Cardiovasc Med (Hagerstown) 13:628- 634, 2012
63. Milei J, Parodi JC, Fernandez Alonso G, Barone A, Beigelman R, Ferreira LM, et al: Carotid atherosclerosis. Immunocytochemical analysis of the vascular and cellular composition in endarterectomies. Cardiologia 41:535-542, 1996
64. Millon A, Boussel L, Brevet M, Mathevet JL, Canet-Soulas E, Mory C, et al: Clinical and histological significance of gadolinium enhancement in carotid atherosclerotic plaque. Stroke 43:3023-3028, 2012
65. Mizoguchi M, Tahara N, Tahara A, Nitta Y, Kodama N, Oba T, et al: Pioglitazone attenuates atherosclerotic plaque inflammation in patients with impaired glucose tolerance or diabetes a prospective, randomized, comparator-controlled study using serial FDG PET/CT imaging study of carotid artery and ascending aorta. JACC Cardiovasc Imaging 4:1110-1118, 2011
66. Moustafa RR, Izquierdo-Garcia D, Fryer TD, Graves MJ, Rudd JH, Gillard JH, et al: Carotid plaque inflammation is associated with cerebral microembolism in patients with recent transient ischemic attack or stroke: a pilot study. Circ Cardiovasc Imaging 3:536-541, 2010
67. Mughal MM, Khan MK, DeMarco JK, Majid A, Shamoun F, Abela GS: Symptomatic and asymptomatic carotid artery plaque. Expert Rev Cardiovasc Ther 9:1315-1330, 2011
68. Müller A, Beck K, Rancic Z, Müller C, Fischer CR, Betzel T, et al: Imaging atherosclerotic plaque inflammation via folate receptor targeting using a novel 18F-folate radiotracer. Mol Imaging 13:1-11, 2014
69. Muraki M, Mikami T, Yoshimoto T, Fujimoto S, Tokuda K, Kaneko S, et al: New criteria for the sonographic diagnosis of a plaque ulcer in the extracranial carotid artery. AJR Am J Roentgenol 198:1161-1166, 2012
70. Nakamura T, Tsutsumi Y, Shimizu Y, Uchiyama S: Ulcerated carotid plaques with ultrasonic echolucency are causatively associated with thromboembolic cerebrovascular events. J Stroke Cerebrovasc Dis 22:93-99, 2013
71. Niccoli Asabella A, Ciccone MM, Cortese F, Scicchitano P, Gesualdo M, Zito A, et al: Higher reliability of 18F-FDG target background ratio compared to standardized uptake value in vulnerable carotid plaque detection: a pilot study. Ann Nucl Med 28:571-579, 2014
72. North American Symptomatic Carotid Endarterectomy Trial Collaborators: Beneficial effect of carotid endarterectomy in symptomatic patients with high-grade carotid stenosis. N Engl J Med 325:445-453, 1991
73. Piscaglia F, Nolsoøe C, Dietrich CF, Cosgrove DO, Gilja OH, Bachmann Nielsen M, et al: The EFSUMB Guidelines and Recommendations on the Clinical Practice of Contrast Enhanced Ultrasound (CEUS): update 2011 on non-hepatic applications. Ultraschall Med 33:33-59, 2012
74. Qiao Y, Etesami M, Astor BC, Zeiler SR, Trout HH III, Wasserman BA: Carotid plaque neovascularization and hemorrhage detected by MR imaging are associated with recent cerebrovascular ischemic events. AJNR Am J Neuroradiol 33:755-760, 2012
75. Qureshi AI, Alexandrov AV, Tegeler CH, Hobson RW II, Dennis Baker J, Hopkins LN: Guidelines for screening of extracranial carotid artery disease. J Neuroimaging 17:19-47, 2007
76. Reiter M, Horvat R, Puchner S, Rinner W, Polterauer P, Lammer J, et al: Plaque imaging of the internal carotid artery-correlation of B-flow imaging with histopathology. AJNR Am J Neuroradiol 28:122-126, 2007
77. Ritter MA, Dittrich R, Thoenissen N, Ringelstein EB, Nabavi DG: Prevalence and prognostic impact of microembolic signals in arterial sources of embolism. A systematic review of the literature. J Neurol 255:953-961, 2008
78. Ritter MA, Theismann K, Schmiedel M, Ringelstein EB, Dittrich R: Vascularization of carotid plaque in recently symptomatic patients is associated with the occurrence of transcranial microembolic signals. Eur J Neurol 20:1218- 1221, 2013
79. Rudd JH, Myers KS, Bansilal S, Machac J, Pinto CA, Tong C, et al: Atherosclerosis inflammation imaging with 18FFDG PET: carotid, iliac, and femoral uptake reproducibility, quantification methods, and recommendations. J Nucl Med 49:871-878, 2008
80. Rudd JH, Myers KS, Bansilal S, Machac J, Rafique A, Farkouh M, et al: (18)Fluorodeoxyglucose positron emission tomography imaging of atherosclerotic plaque inflammation is highly reproducible: implications for atherosclerosis therapy trials. J Am Coll Cardiol 50:892-896, 2007
81. Saam T, Ferguson MS, Yarnykh VL, Takaya N, Xu D, Polissar NL, et al: Quantitative evaluation of carotid plaque composition by in vivo MRI. Arterioscler Thromb Vasc Biol 25:234-239, 2005
82. Saam T, Hatsukami TS, Takaya N, Chu B, Underhill H, Kerwin WS, et al: The vulnerable, or high-risk, atherosclerotic plaque: noninvasive MR imaging for characterization and assessment. Radiology 244:64-77, 2007
83. Saam T, Hetterich H, Hoffmann V, Yuan C, Dichgans M, Poppert H, et al: Meta-analysis and systematic review of the predictive value of carotid plaque hemorrhage on cerebrovascular events by magnetic resonance imaging. J Am Coll Cardiol 62:1081-1091, 2013
84. Saba L, Caddeo G, Sanfilippo R, Montisci R, Mallarini G: CT and ultrasound in the study of ulcerated carotid plaque compared with surgical results: potentialities and advantages of multidetector row CT angiography. AJNR Am J Neuroradiol 28:1061-1066, 2007
85. Saba L, Caddeo G, Sanfilippo R, Montisci R, Mallarini G: Efficacy and sensitivity of axial scans and different reconstruction methods in the study of the ulcerated carotid plaque using multidetector-row CT angiography: comparison with surgical results. AJNR Am J Neuroradiol 28:716-723, 2007
86. Saba L, Lai ML, Montisci R, Tamponi E, Sanfilippo R, Faa G, et al: Association between carotid plaque enhancement shown by multidetector CT angiography and histologically validated microvessel density. Eur Radiol 22:2237-2245, 2012
87. Saba L, Mallarini G: Carotid plaque enhancement and symptom correlations: an evaluation by using multidetector row CT angiography. AJNR Am J Neuroradiol 32:1919- 1925, 2011
88. Saba L, Mallarini G: Fissured fibrous cap of vulnerable carotid plaques and symptomaticity: are they correlated? Preliminary results by using multi-detector-row CT angiography. Cerebrovasc Dis 27:322-327, 2009
89. Saba L, Tamponi E, Raz E, Lai L, Montisci R, Piga M, et al: Correlation between fissured fibrous cap and contrast enhancement: preliminary results with the use of CTA and histologic validation. AJNR Am J Neuroradiol 35:754- 759, 2014
90. Saito H, Kuroda S, Hirata K, Magota K, Shiga T, Tamaki N, et al: Validity of dual MRI and F-FDG PET imaging in predicting vulnerable and inflamed carotid plaque. Cerebrovasc Dis 35:370-377, 2013
91. Shalhoub J, Monaco C, Owen DR, Gauthier T, Thapar A, Leen EL, et al: Late-phase contrast-enhanced ultrasound reflects biological features of instability in human carotid atherosclerosis. Stroke 42:3634-3636, 2011
92. Sheikine Y, Akram K: FDG-PET imaging of atherosclerosis: Do we know what we see? Atherosclerosis 211:371- 380, 2010
93. Sibley CT, Vavere AL, Gottlieb I, Cox C, Matheson M, Spooner A, et al: MRI-measured regression of carotid atherosclerosis induced by statins with and without niacin in a randomised controlled trial: the NIA plaque study. Heart 99:1675-1680, 2013
94. Silvera SS, Aidi HE, Rudd JH, Mani V, Yang L, Farkouh M, et al: Multimodality imaging of atherosclerotic plaque activity and composition using FDG-PET/CT and MRI in carotid and femoral arteries. Atherosclerosis 207:139-143, 2009
95. Singh AS, Atam V, Jain N, Yathish BE, Patil MR, Das L: Association of carotid plaque echogenicity with recurrence of ischemic stroke. N Am J Med Sci 5:371-376, 2013
96. Singh N, Moody AR, Gladstone DJ, Leung G, Ravikumar R, Zhan J, et al: Moderate carotid artery stenosis: MR imaging-depicted intraplaque hemorrhage predicts risk of cerebrovascular ischemic events in asymptomatic men. Radiology 252:502-508, 2009
97. Spence JD, Tamayo A, Lownie SP, Ng WP, Ferguson GG: Absence of microemboli on transcranial Doppler identifies low-risk patients with asymptomatic carotid stenosis. Stroke 36:2373-2378, 2005
98. Spencer MP, Thomas GI, Nicholls SC, Sauvage LR: Detection of middle cerebral artery emboli during carotid endarterectomy using transcranial Doppler ultrasonography. Stroke 21:415-423, 1990
99. Stary HC, Blankenhorn DH, Chandler AB, Glagov S, Insull W Jr, Richardson M, et al: A definition of the intima of human arteries and of its atherosclerosis-prone regions. Circulation 85:391-405, 1992
100. Stary HC, Chandler AB, Dinsmore RE, Fuster V, Glagov S, Insull W Jr, et al: A definition of advanced types of atherosclerotic lesions and a histological classification of atherosclerosis. Circulation 92:1355-1374, 1995
101. Stary HC, Chandler AB, Glagov S, Guyton JR, Insull W Jr, Rosenfeld ME, et al: A definition of initial, fatty streak, and intermediate lesions of atherosclerosis. Circulation 89:2462-2478, 1994
102. Staub D, Patel MB, Tibrewala A, Ludden D, Johnson M, Espinosa P, et al: Vasa vasorum and plaque neovascularization on contrast-enhanced carotid ultrasound imaging correlates with cardiovascular disease and past cardiovascular events. Stroke 41:41-47, 2010
103. Steinberg D, Witztum JL: Lipoproteins and atherogenesis. Current concepts. JAMA 264:3047-3052, 1990
104. Tahara N, Kai H, Ishibashi M, Nakaura H, Kaida H, Baba K, et al: Simvastatin attenuates plaque inflammation: evaluation by fluorodeoxyglucose positron emission tomography. J Am Coll Cardiol 48:1825-1831, 2006
105. Tawakol A, Fayad ZA, Mogg R, Alon A, Klimas MT, Dansky H, et al: Intensification of statin therapy results in a rapid reduction in atherosclerotic inflammation: results of a multicenter fluorodeoxyglucose-positron emission tomography/computed tomography feasibility study. J Am Coll Cardiol 62:909-917, 2013
106. Tawakol A, Migrino RQ, Bashian GG, Bedri S, Vermylen D, Cury RC, et al: In vivo 18F-fluorodeoxyglucose positron emission tomography imaging provides a noninvasive measure of carotid plaque inflammation in patients. J Am Coll Cardiol 48:1818-1824, 2006
107. ten Kate GL, Renaud GG, Akkus Z, van den Oord SC, ten Cate FJ, Shamdasani V, et al: Far-wall pseudoenhancement during contrast-enhanced ultrasound of the carotid arteries: clinical description and in vitro reproduction. Ultrasound Med Biol 38:593-600, 2012
108. ten Kate GL, van den Oord SC, Sijbrands EJ, van der Lugt A, de Jong N, Bosch JG, et al: Current status and future developments of contrast-enhanced ultrasound of carotid atherosclerosis. J Vasc Surg 57:539-546, 2013
109. ten Kate GL, van Dijk AC, van den Oord SC, Hussain B, Verhagen HJ, Sijbrands EJ, et al: Usefulness of contrastenhanced ultrasound for detection of carotid plaque ulceration in patients with symptomatic carotid atherosclerosis. Am J Cardiol 112:292-298, 2013
110. Topakian R, King A, Kwon SU, Schaafsma A, Shipley M, Markus HS: Ultrasonic plaque echolucency and emboli signals predict stroke in asymptomatic carotid stenosis. Neurology 77:751-758, 2011
111. Truijman MT, Kwee RM, van Hoof RH, Hermeling E, van Oostenbrugge RJ, Mess WH, et al: Combined 18F-FDG PET-CT and DCE-MRI to assess inflammation and microvascularization in atherosclerotic plaques. Stroke 44:3568- 3570, 2013
112. Underhill HR, Yuan C, Zhao XQ, Kraiss LW, Parker DL, Saam T, et al: Effect of rosuvastatin therapy on carotid plaque morphology and composition in moderately hypercholesterolemic patients: a high-resolution magnetic resonance imaging trial. Am Heart J 155:584.e1-584.e8, 2008
113. van Gils MJ, Vukadinovic D, van Dijk AC, Dippel DW, Niessen WJ, van der Lugt A: Carotid atherosclerotic plaque progression and change in plaque composition over time: a 5-year follow-up study using serial CT angiography. AJNR Am J Neuroradiol 33:1267-1273, 2012
114. van Zuilen EV, Moll FL, Vermeulen FE, Mauser HW, van Gijn J, Ackerstaff RG: Detection of cerebral microemboli by means of transcranial Doppler monitoring before and after carotid endarterectomy. Stroke 26:210-213, 1995
115. Vavuranakis M, Sigala F, Vrachatis DA, Papaioannou TG, Filis K, Kavantzas N, et al: Quantitative analysis of carotid plaque vasa vasorum by CEUS and correlation with histology after endarterectomy. Vasa 42:184-195, 2013
116. Walker MD, Marler JR, Goldstein M, Grady PA, Toole JF, Baker WF, et al: Endarterectomy for asymptomatic carotid artery stenosis. JAMA 273:1421-1428, 1995
117. Watanabe Y, Nagayama M: MR plaque imaging of the carotid artery. Neuroradiology 52:253-274, 2010
118. Watanabe Y, Nagayama M, Suga T, Yoshida K, Yamagata S, Okumura A, 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 28:478-485, 2008
119. Wilhjelm JE, Jensen MS, Jespersen SK, Sahl B, Falk E: Visual and quantitative evaluation of selected image combination schemes in ultrasound spatial compound scanning. IEEE Trans Med Imaging 23:181-190, 2004
120. Wintermark M, Arora S, Tong E, Vittinghoff E, Lau BC, Chien JD, et al: Carotid plaque computed tomography imaging in stroke and nonstroke patients. Ann Neurol 64:149-157, 2008
121. Wintermark M, Jawadi SS, Rapp JH, Tihan T, Tong E, Glidden DV, et al: High-resolution CT imaging of carotid artery atherosclerotic plaques. AJNR Am J Neuroradiol 29:875-882, 2008
122. Xiong L, Deng YB, Zhu Y, Liu YN, Bi XJ: Correlation of carotid plaque neovascularization detected by using contrast-enhanced US with clinical symptoms. Radiology 251:583-589, 2009
123. Yim YJ, Choe YH, Ko Y, Kim ST, Kim KH, Jeon P, 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 27:1341-1346, 2008
124. Yoshida K, Sadamasa N, Narumi O, Chin M, Yamagata S, Miyamoto S: Symptomatic low-grade carotid stenosis with intraplaque hemorrhage and expansive arterial remodeling is associated with a high relapse rate refractory to medical treatment. Neurosurgery 70:1143-1151, 2012
125. Yoshimura S, Yamada K, Kawasaki M, Asano T, Kanematsu M, Miyai M, et al: Selection of carotid artery stenting or endarterectomy based on magnetic resonance plaque imaging reduced periprocedural adverse events. J Stroke Cerebrovasc Dis 22:1082-1087, 2013
126. Yoshimura S, Yamada K, Kawasaki M, Asano T, Kanematsu M, Takamatsu M, et al: High-intensity signal on time-of-flight magnetic resonance angiography indicates carotid plaques at high risk for cerebral embolism during stenting. Stroke 42:3132-3137, 2011
127. Yuan C, Mitsumori LM, Ferguson MS, Polissar NL, Echelard D, Ortiz G, et al: In vivo accuracy of multispectral magnetic resonance imaging for identifying lipid-rich necrotic cores and intraplaque hemorrhage in advanced human carotid plaques. Circulation 104:2051-2056, 2001
128. Zhao XQ, Dong L, Hatsukami T, Phan BA, Chu B, Moore A, et al: MR imaging of carotid plaque composition during lipid-lowering therapy a prospective assessment of effect and time course. JACC Cardiovasc Imaging 4:977-986, 2011
129. Zhou Y, Xing Y, Li Y, Bai Y, Chen Y, Sun X, et al: An assessment of the vulnerability of carotid plaques: a comparative study between intraplaque neovascularization and plaque echogenicity. BMC Med Imaging 13:13, 2013
130. Zhu Y, Deng YB, Liu YN, Bi XJ, Sun J, Tang QY, et al: Use of carotid plaque neovascularization at contrastenhanced US to predict coronary events in patients with coronary artery disease. Radiology 268:54-60, 2013