Detecting the vulnerable plaque in patients

Journal of Internal Medicine

Volumn 278, Issue 5, 2015, Pages 520-530

  Goncalves I ^a   den Ruijter, H ^b   Nahrendorf, M ^c   Pasterkamp, G ^b  

^a LUND UNIVERSITY HOSPITAL   (Sweden)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

Atherosclerosis; Noninvasive imaging; Vulnerable plaque

Indexed keywords

BIOLOGICAL MARKER;

ACUTE CORONARY SYNDROME; ACUTE HEART INFARCTION; ANGIOGRAPHY; ARTERIAL WALL THICKNESS; ARTIFACT; ATHEROSCLEROTIC PLAQUE; BLOOD VESSEL CALCIFICATION; CEREBROVASCULAR ACCIDENT; COMPUTER ASSISTED EMISSION TOMOGRAPHY; COMPUTER ASSISTED TOMOGRAPHY; ECHOGRAPHY; HUMAN; MOLECULAR IMAGING; MULTIMODAL IMAGING; NON INVASIVE PROCEDURE; NUCLEAR MAGNETIC RESONANCE IMAGING; POSITRON EMISSION TOMOGRAPHY; PREDICTIVE VALUE; PRIMARY PREVENTION; PRIORITY JOURNAL; REVIEW; SENSITIVITY AND SPECIFICITY; SIGNAL NOISE RATIO; BLOOD; COMPLICATION; DIAGNOSTIC IMAGING; PATHOLOGY; PLAQUE, ATHEROSCLEROTIC; PROCEDURES; REPRODUCIBILITY; RUPTURE, SPONTANEOUS; STROKE;

ACUTE CORONARY SYNDROME; BIOMARKERS; DIAGNOSTIC IMAGING; HUMANS; PLAQUE, ATHEROSCLEROTIC; PREDICTIVE VALUE OF TESTS; REPRODUCIBILITY OF RESULTS; RUPTURE, SPONTANEOUS; STROKE;

EID: 84944688084     PISSN: 09546820     EISSN: 13652796     Source Type: Journal    
DOI: 10.1111/joim.12414     Document Type: Review

References (95)

1. Leuschner F, Nahrendorf M. Molecular imaging of coronary atherosclerosis and myocardial infarction: considerations for the bench and perspectives for the clinic. Circ Res 2011; 108: 593-606.
2. Sanz J, Fayad ZA. Imaging of atherosclerotic cardiovascular disease. Nature 2008; 451: 953-7.
3. Lorenz MW, Polak JF, Kavousi M et al. Carotid intima-media thickness progression to predict cardiovascular events in the general population (the PROG-IMT collaborative project): a meta-analysis of individual participant data. Lancet 2012; 379: 2053-62.
4. Den Ruijter HM, Peters SA, Anderson TJ et al. Common carotid intima-media thickness measurements in cardiovascular risk prediction: a meta-analysis. JAMA 2012; 308: 796-803.
5. Peters SA, den Ruijter HM, Grobbee DE, Bots ML. Results from a carotid intima-media thickness trial as a decision tool for launching a large-scale morbidity and mortality trial. Circ Cardiovasc Imaging 2013; 6: 20-5.
6. Gray-Weale AC, Graham JC, Burnett JR, Byrne K, Lusby RJ. Carotid artery atheroma: comparison of preoperative B-mode ultrasound appearance with carotid endarterectomy specimen pathology. J Cardiovasc Surg (Torino) 1988; 29: 676-81.
7. Elatrozy T, Nicolaides A, Tegos T, Griffin M. The objective characterisation of ultrasonic carotid plaque features. Eur J Vasc Endovasc Surg 1998; 16: 223-30.
8. El-Barghouty N, Nicolaides A, Bahal V, Geroulakos G, Androulakis A. The identification of the high risk carotid plaque. Eur J Vasc Endovasc Surg 1996; 11: 470-478.
9. Gronholdt ML, Nordestgaard BG, Schroeder TV, Vorstrup S, Sillesen H. Ultrasonic echolucent carotid plaques predict future strokes. Circulation 2001; 104: 68-73.
10. Liapis CD, Kakisis JD, Kostakis AG. Carotid stenosis. Factors affecting symptomatology. Stroke 2001; 32: 2782-2786.
11. Mathiesen EB, Bonaa KH, Joakimsen O. Echolucent plaques are associated with high risk of ischemic cerebrovascular events in carotid stenosis: the tromso study. Circulation 2001; 103: 2171-5.
12. Polak JF, Shemanski L, O'Leary DH et al. Hypoechoic plaque at US of the carotid artery: an independent risk factor for incident stroke in adults aged 65 years or older. Cardiovascular Health Study. Radiology 1998; 208: 649-54.
13. Kardoulas DG, Katsamouris AN, Gallis PT et al. Ultrasonographic and histologic characteristics of symptom-free and symptomatic carotid plaque. Cardiovasc Surg 1996; 4: 580-90.
14. Gronholdt ML, Nordestgaard BG, Bentzon J et al. Macrophages are associated with lipid-rich carotid artery plaques, echolucency on B-mode imaging, and elevated plasma lipid levels. J Vasc Surg 2002; 35: 137-45.
15. Goncalves I, Moses J, Pedro LM et al. Echolucency of carotid plaques correlates with plaque cellularity. Eur J Vasc Endovasc Surg 2003; 26: 32-8.
16. Goncalves I, Lindholm MW, Pedro LM et al. Elastin and calcium rather than collagen or lipid content are associated with echogenicity of human carotid plaques. Stroke 2004; 35: 2795-800.
17. Crouse JR 3rd, Raichlen JS, Riley WA et al. Effect of rosuvastatin on progression of carotid intima-media thickness in low-risk individuals with subclinical atherosclerosis: the METEOR Trial. JAMA 2007; 297: 1344-53.
18. Lind L, Peters SA, den Ruijter HM et al. Effect of rosuvastatin on the echolucency of the common carotid intima-media in low-risk individuals: the METEOR trial. J Am Soc Echocardiogr 2012; 25: 1120-1127.e1.
19. Feinstein SB. Contrast ultrasound imaging of the carotid artery vasa vasorum and atherosclerotic plaque neovascularization. J Am Coll Cardiol 2006; 48: 236-43.
20. Rubin JR, Bondi JA, Rhodes RS. Duplex scanning versus conventional arteriography for the evaluation of carotid artery plaque morphology. Surgery 1987; 102: 749-55.
21. Madani A, Beletsky V, Tamayo A, Munoz C, Spence JD. High-risk asymptomatic carotid stenosis: ulceration on 3D ultrasound vs TCD microemboli. Neurology 2011; 77: 744-50.
22. Pedro LM, Pedro MM, Goncalves I et al. Computer-assisted carotid plaque analysis: characteristics of plaques associated with cerebrovascular symptoms and cerebral infarction. Eur J Vasc Endovasc Surg 2000; 19: 118-23.
23. Bassiouny HS, Sakaguchi Y, Mikucki SA et al. Juxtalumenal location of plaque necrosis and neoformation in symptomatic carotid stenosis. J Vasc Surg 1997; 26: 589-594.
24. Saam T, Ferguson MS, Yarnykh VL et al. Quantitative evaluation of carotid plaque composition by in vivo MRI. Arterioscler Thromb Vasc Biol 2005; 25: 234-9.
25. Gupta A, Baradaran H, Schweitzer AD et al. Carotid plaque MRI and stroke risk: a systematic review and meta-analysis. Stroke 2013; 44: 3071-7.
26. 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: 932-8.
27. Hatsukami TS, Thackray BD, Primozich JF et al. Echolucent regions in carotid plaque: preliminary analysis comparing three-dimensional histologic reconstructions to sonographic findings. Ultrasound Med Biol 1994; 20: 743-749.
28. Fayad ZA, Fuster V. Characterization of atherosclerotic plaques by magnetic resonance imaging. Ann N Y Acad Sci 2000; 902: 173-86.
29. Teng Z, Sadat U, Ji G et al. Lumen irregularity dominates the relationship between mechanical stress condition, fibrous-cap thickness, and lumen curvature in carotid atherosclerotic plaque. J Biomech Eng 2011; 133: 034501.
30. Trivedi RA, U-King-Im J, Graves MJ et al. Multi-sequence in vivo MRI can quantify fibrous cap and lipid core components in human carotid atherosclerotic plaques. Eur J Vasc Endovasc Surg 2004; 28: 207-13.
31. 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: 3047-52.
32. 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: 3239-44.
33. Kerwin W, Hooker A, Spilker M et al. Quantitative magnetic resonance imaging analysis of neovasculature volume in carotid atherosclerotic plaque. Circulation 2003; 107: 851-6.
34. Kerwin WS, O'Brien KD, Ferguson MS, Polissar N, Hatsukami TS, Yuan C. Inflammation in carotid atherosclerotic plaque: a dynamic contrast-enhanced MR imaging study. Radiology 2006; 241: 459-68.
35. Takaya N, Yuan C, Chu B et al. Association between carotid plaque characteristics and subsequent ischemic cerebrovascular events: a prospective assessment with MRI-initial results. Stroke 2006; 37: 818-23.
36. Altaf N, Daniels L, Morgan PS 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 2008; 47: 337-42.
37. Singh N, Moody AR, Gladstone DJ et al. Moderate carotid artery stenosis: MR imaging-depicted intraplaque hemorrhage predicts risk of cerebrovascular ischemic events in asymptomatic men. Radiology 2009; 252: 502-8.
38. Takaya N, Yuan C, Chu B et al. Presence of intraplaque hemorrhage stimulates progression of carotid atherosclerotic plaques: a high-resolution magnetic resonance imaging study. Circulation 2005; 111: 2768-75.
39. Underhill HR, Yuan C, Yarnykh VL et al. Predictors of surface disruption with MR imaging in asymptomatic carotid artery stenosis. AJNR Am J Neuroradiol 2010; 31: 487-93.
40. Huang Y, Teng Z, Sadat U, Graves MJ, Bennett MR, Gillard JH. The influence of computational strategy on prediction of mechanical stress in carotid atherosclerotic plaques: comparison of 2D structure-only, 3D structure-only, one-way and fully coupled fluid-structure interaction analyses. J Biomech 2014; 47: 1465-71.
41. Canton G, Chiu B, Chen H et al. A framework for the co-registration of hemodynamic forces and atherosclerotic plaque components. Physiol Meas 2013; 34: 977-90.
42. Thrysoe SA, Oikawa M, Yuan C et al. Longitudinal distribution of mechanical stresses in carotid plaques of symptomatic patients. Stroke 2010; 41: 1041-3.
43. Huang Y, Teng Z, Sadat U, He J, Graves MJ, Gillard JH. In vivo MRI-based simulation of fatigue process: a possible trigger for human carotid atherosclerotic plaque rupture. Biomed Eng Online 2013; 12: 36.
44. Duivenvoorden R, van Wijk D, Klimas M, Kastelein JJ, Stroes ES, Nederveen AJ. Detection of liquid phase cholesteryl ester in carotid atherosclerosis by 1H-MR spectroscopy in humans. JACC Cardiovasc Imaging 2013; 6: 1277-84.
45. Agatston AS, Janowitz WR, Hildner FJ, Zusmer NR, Viamonte M Jr, Detrano R. Quantification of coronary artery calcium using ultrafast computed tomography. J Am Coll Cardiol 1990; 15: 827-832.
46. Breen JF, Sheedy PF 2nd, Schwartz RS et al. Coronary artery calcification detected with ultrafast CT as an indication of coronary artery disease. Radiology 1992; 185: 435-9.
47. Becker CR, Nikolaou K, Muders M et al. Ex vivo coronary atherosclerotic plaque characterization with multi-detector-row CT. Eur Radiol 2003; 13: 2094-8.
48. Becker CR, Knez A, Ohnesorge B, Schoepf UJ, Reiser MF. Imaging of noncalcified coronary plaques using helical CT with retrospective ECG gating. AJR Am J Roentgenol 2000; 175: 423-4.
49. Hoffmann U, Moselewski F, Nieman K et al. Noninvasive assessment of plaque morphology and composition in culprit and stable lesions in acute coronary syndrome and stable lesions in stable angina by multidetector computed tomography. J Am Coll Cardiol 2006; 47: 1655-62.
50. Motoyama S, Sarai M, Harigaya H et al. Computed tomographic angiography characteristics of atherosclerotic plaques subsequently resulting in acute coronary syndrome. J Am Coll Cardiol 2009; 54: 49-57.
51. Seifarth H, Schlett CL, Nakano M et al. Histopathological correlates of the napkin-ring sign plaque in coronary CT angiography. Atherosclerosis 2012; 224: 90-6.
52. Otsuka K, Fukuda S, Tanaka A et al. Napkin-ring sign on coronary CT angiography for the prediction of acute coronary syndrome. JACC Cardiovasc Imaging 2013; 6: 448-57.
53. Nahrendorf M, Jaffer FA, Kelly KA et al. Noninvasive vascular cell adhesion molecule-1 imaging identifies inflammatory activation of cells in atherosclerosis. Circulation 2006; 114: 1504-11.
54. Nahrendorf M, Keliher E, Panizzi P et al. 18F-4V for PET-CT imaging of VCAM-1 expression in atherosclerosis. JACC Cardiovasc Imaging 2009; 2: 1213-22.
55. Winter PM, Morawski AM, Caruthers SD et al. Molecular imaging of angiogenesis in early-stage atherosclerosis with alpha(v)beta3-integrin-targeted nanoparticles. Circulation 2003; 108: 2270-4.
56. Spuentrup E, Katoh M, Wiethoff AJ et al. Molecular coronary MR imaging of human thrombi using EP-2104R, a fibrin-targeted contrast agent: experimental study in a swine model. RoFo 2007; 179: 1166-73.
57. von zur Muhlen C, von Elverfeldt D, Moeller JA et al. Magnetic resonance imaging contrast agent targeted toward activated platelets allows in vivo detection of thrombosis and monitoring of thrombolysis. Circulation 2008; 118: 258-67.
58. Klink A, Lancelot E, Ballet S et al. Magnetic resonance molecular imaging of thrombosis in an arachidonic acid mouse model using an activated platelet targeted probe. Arterioscler Thromb Vasc Biol 2010; 30: 403-10.
59. Kooi ME, Cappendijk VC, Cleutjens KB et al. Accumulation of ultrasmall superparamagnetic particles of iron oxide in human atherosclerotic plaques can be detected by in vivo magnetic resonance imaging. Circulation 2003; 107: 2453-8.
60. Rudd JH, Warburton EA, Fryer TD et al. Imaging atherosclerotic plaque inflammation with [18F]-fluorodeoxyglucose positron emission tomography. Circulation 2002; 105: 2708-11.
61. Tawakol A, Migrino RQ, Bashian GG et al. In vivo 18F-fluorodeoxyglucose positron emission tomography imaging provides a noninvasive measure of carotid plaque inflammation in patients. J Am Coll Cardiol 2006; 48: 1818-24.
62. Briley-Saebo KC, Shaw PX, Mulder WJ et al. Targeted molecular probes for imaging atherosclerotic lesions with magnetic resonance using antibodies that recognize oxidation-specific epitopes. Circulation 2008; 117: 3206-15.
63. Luehmann HP, Pressly ED, Detering L et al. PET/CT imaging of chemokine receptor CCR5 in vascular injury model using targeted nanoparticle. J Nucl Med 2014; 55: 629-34.
64. Nahrendorf M, Waterman P, Thurber G et al. Hybrid in vivo FMT-CT imaging of protease activity in atherosclerosis with customized nanosensors. Arterioscler Thromb Vasc Biol 2009; 29: 1444-51.
65. Ronald JA, Chen JW, Chen Y et al. Enzyme-sensitive magnetic resonance imaging targeting myeloperoxidase identifies active inflammation in experimental rabbit atherosclerotic plaques. Circulation 2009; 120: 592-9.
66. Joshi NV, Vesey AT, Williams MC et al. 18F-fluoride positron emission tomography for identification of ruptured and high-risk coronary atherosclerotic plaques: a prospective clinical trial. Lancet 2014; 383: 705-13.
67. De Saint-Hubert M, Bauwens M, Deckers N et al. In vivo molecular imaging of apoptosisand necrosis in atherosclerotic plaques using microSPECT-CT and microPET-CT imaging. Mol Imaging Biol 2014; 16: 246-54.
68. Derlin T, Habermann CR, Lengyel Z et al. Feasibility of 11C-acetate PET/CT for imaging of fatty acid synthesis in the atherosclerotic vessel wall. J Nucl Med 2011; 52: 1848-54.
69. Wykrzykowska J, Lehman S, Williams G et al. Imaging of inflamed and vulnerable plaque in coronary arteries with 18F-FDG PET/CT in patients with suppression of myocardial uptake using a low-carbohydrate, high-fat preparation. J Nucl Med 2009; 50: 563-8.
70. Tawakol A, Fayad ZA, Mogg R 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 2013; 62: 909-17.
71. Figueroa AL, Abdelbaky A, Truong QA et al. Measurement of arterial activity on routine FDG PET/CT images improves prediction of risk of future CV events. JACC Cardiovasc Imaging 2013; 6: 1250-9.
72. Majmudar MD, Nahrendorf M. Cardiovascular molecular imaging: the road ahead. J Nucl Med 2012; 53: 673-6.
73. Davies MJ. Acute coronary thrombosis - the role of plaque disruption and its initiation and prevention. Eur Heart J 1995; 16(Suppl L): 3-7.
74. Pasterkamp G, Schoneveld AH, van der Wal AC et al. Inflammation of the atherosclerotic cap and shoulder of the plaque is a common and locally observed feature in unruptured plaques of femoral and coronary arteries. Arterioscler Thromb Vasc Biol 1999; 19: 54-8.
75. Cheng JM, Garcia-Garcia HM, de Boer SP et al. In vivo detection of high-risk coronary plaques by radiofrequency intravascular ultrasound and cardiovascular outcome: results of the ATHEROREMO-IVUS study. Eur Heart J 2014; 35: 639-47.
76. Stone GW, Maehara A, Lansky AJ et al. A prospective natural-history study of coronary atherosclerosis. N Engl J Med 2011; 364: 226-35.
77. Zavodni AE, Wasserman BA, McClelland RL et al. Carotid artery plaque morphology and composition in relation to incident cardiovascular events: the Multi-Ethnic Study of Atherosclerosis (MESA). Radiology 2014; 271: 381-9.
78. Saam T, Hetterich H, Hoffmann V 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 2013; 62: 1081-91.
79. Criqui MH, Denenberg JO, Ix JH et al. Calcium density of coronary artery plaque and risk of incident cardiovascular events. JAMA 2014; 311: 271-8.
80. Kato K, Yonetsu T, Kim SJ et al. Comparison of nonculprit coronary plaque characteristics between patients with and without diabetes: a 3-vessel optical coherence tomography study. JACC Cardiovasc Interv 2012; 5: 1150-8.
81. Reith S, Battermann S, Hoffmann R, Marx N, Burgmaier M. Optical coherence tomography derived differences of plaque characteristics in coronary culprit lesions between type 2 diabetic patients with and without acute coronary syndrome. Catheter Cardiovasc Interv 2014; 84: 700-7.
82. Edsfeldt A, Goncalves I, Grufman H et al. Impaired fibrous repair: a possible contributor to atherosclerotic plaque vulnerability in patients with type II diabetes. Arterioscler Thromb Vasc Biol 2014; 34: 2143-50.
83. Ozaki Y, Tanaka A, Komukai K et al. High-density lipoprotein cholesterol level is associated with fibrous cap thickness in acute coronary syndrome. Circ J 2013; 77: 2982-9.
84. Semb AG, Rollefstad S, Provan SA et al. Carotid plaque characteristics and disease activity in rheumatoid arthritis. J Rheumatol 2013; 40: 359-68.
85. Ostling G, Persson M, Hedblad B, Goncalves I. Comparison of grey scale median (GSM) measurement in ultrasound images of human carotid plaques using two different softwares. Clin Physiol Funct Imaging 2013; 33: 431-5.
86. Scholtes VP, Peeters W, van Lammeren GW et al. Type 2 diabetes is not associated with an altered plaque phenotype among patients undergoing carotid revascularization. A histological analysis of 1455 carotid plaques. Atherosclerosis 2014; 235: 418-23.
87. Hellings WE, Peeters W, Moll FL et al. Composition of carotid atherosclerotic plaque is associated with cardiovascular outcome: a prognostic study. Circulation 2010; 121: 1941-50.
88. Vrijenhoek JE, Den Ruijter HM, De Borst GJ et al. Sex is associated with the presence of atherosclerotic plaque hemorrhage and modifies the relation between plaque hemorrhage and cardiovascular outcome. Stroke 2013; 44: 3318-23.
89. de Kleijn DP, Moll FL, Hellings WE et al. Local atherosclerotic plaques are a source of prognostic biomarkers for adverse cardiovascular events. Arterioscler Thromb Vasc Biol 2010; 30: 612-9.
90. Hattori K, Ozaki Y, Ismail TF et al. Impact of statin therapy on plaque characteristics as assessed by serial OCT, grayscale and integrated backscatter-IVUS. JACC Cardiovasc Imaging 2012; 5: 169-77.
91. Crisby M, Nordin-Fredriksson G, Shah PK, Yano J, Zhu J, Nilsson J. Pravastatin treatment increases collagen content and decreases lipid content, inflammation, metalloproteinases, and cell death in human carotid plaques: implications for plaque stabilization. Circulation 2001; 103: 926-933.
92. McManus DD, Gore J, Yarzebski J, Spencer F, Lessard D, Goldberg RJ. Recent trends in the incidence, treatment, and outcomes of patients with STEMI and NSTEMI. Am J Med 2011; 124: 40-7.
93. Koton S, Schneider AL, Rosamond WD et al. Stroke incidence and mortality trends in US communities, 1987 to 2011. JAMA 2014; 312: 259-68.
94. van Lammeren GW, den Ruijter HM, Vrijenhoek JE et al. Time-dependent changes in atherosclerotic plaque composition in patients undergoing carotid surgery. Circulation 2014; 129: 2269-76.
95. Schmucker J, Wienbergen H, Seide S et al. Smoking ban in public areas is associated with a reduced incidence of hospital admissions due to ST-elevation myocardial infarctions in non-smokers. Results from the Bremen STEMI Registry. Eur J Prev Cardiol 2014; 21: 1180-6.