Ultrasound imaging for risk assessment in atherosclerosis

International Journal of Molecular Sciences

Volumn 16, Issue 5, 2015, Pages 9749-9769

  Steinl, David C ^a   Kaufmann, Beat A ^a  

^a UNIVERSITY HOSPITAL BASEL   (Switzerland)

Author keywords

Atherosclerosis; Contrast enhanced; Micro bubbles; Molecular imaging; Ultrasound

Indexed keywords

CONTRAST MEDIUM; FIBRIN; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 6; INTERLEUKIN 8; LOW DENSITY LIPOPROTEIN CHOLESTEROL; MONOCYTE CHEMOTACTIC PROTEIN 1; PADGEM PROTEIN; THROMBOPLASTIN; TUMOR NECROSIS FACTOR ALPHA; VASCULAR CELL ADHESION MOLECULE 1; VON WILLEBRAND FACTOR;

ANATOMICAL CONCEPTS; APOPTOSIS; ARTERIAL WALL THICKNESS; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; B SCAN; BIOMECHANICS; BLOOD CLOTTING; BLOOD VESSEL WALL; CAROTID ARTERY; CONTRAST ENHANCEMENT; ECHOGRAPHY; ELASTOGRAPHY; HUMAN; INTRAVASCULAR ULTRASOUND; META ANALYSIS (TOPIC); MICROBUBBLE; MOLECULAR IMAGING; NEOVASCULARIZATION (PATHOLOGY); NONHUMAN; PATHOGENESIS; PROTEIN EXPRESSION; PULSE WAVE; REVIEW; RISK ASSESSMENT; VASCULITIS; DIAGNOSTIC IMAGING; PATHOLOGY;

ATHEROSCLEROSIS; BIOMECHANICAL PHENOMENA; CONTRAST MEDIA; DIAGNOSTIC IMAGING; HUMANS; RISK ASSESSMENT; ULTRASONOGRAPHY;

EID: 84929359025     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms16059749     Document Type: Review

References (107)

1. Ross, R. Atherosclerosis—An inflammatory disease. N. Engl. J. Med. 1999, 340, 115–126.
2. Wildgruber, M.; Swirski, F.K.; Zernecke, A. Molecular imaging of inflammation in atherosclerosis. Theranostics 2013, 3, 865–884.
3. Enos, W.F.; Holmes, R.H.; Beyer, J. Coronary disease among United-States soldiers killed in action in korea. JAMA J. Am. Med. Assoc. 1953, 152, 1090–1093.
4. Strong, J.P.; Malcom, G.T.; McMahan, C.A.; Tracy, R.E.; Newman, W.P., 3rd; Herderick, E.E.; Cornhill, J.F. Prevalence and extent of atherosclerosis in adolescents and young adults: Implications for prevention from the pathobiological determinants of atherosclerosis in youth study. JAMA 1999, 281, 727–735.
5. Health Status, OECD Database 2014. Available online: https://stats.oecd.org/index.aspx? DataSetCode=HEALTH_STAT (accessed on 20 April 2015).
6. Murray, C.J.L.; Vos, T.; Lozano, R.; Naghavi, M.; Flaxman, A.D.; Michaud, C.; Ezzati, M.; Shibuya, K.; Salomon, J.A.; Abdalla, S., et al. Disability-adjusted life years (dalys) for 291 diseases and injuries in 21 regions, 1990–2010: A systematic analysis for the global burden of disease study 2010. Lancet 2012, 380, 2197–2223.
7. Ginghina, C.; Bejan, I.; Ceck, C.D. Modern risk stratification in coronary heart disease. J. Med. Life 2011, 4, 377–386.
8. Witztum, J.L.; Steinberg, D. Role of oxidized low-density-lipoprotein in atherogenesis. J. Clin. Investig. 1991, 88, 1785–1792.
9. Kunsch, C.; Medford, R.M. Oxidative stress as a regulator of gene expression in the vasculature. Circ. Res. 1999, 85, 753–766.
10. Stocker, R.; Keaney, J.F. Role of oxidative modifications in atherosclerosis. Physiol. Rev. 2004, 84, 1381–1478.
11. Marui, N.; Offermann, M.K.; Swerlick, R.; Kunsch, C.; Rosen, C.A.; Ahmad, M.; Alexander, R.W.; Medford, R.M. Vascular cell-adhesion molecule-1 (VCAM-1) gene-transcription and expression are regulated through an antioxidant sensitive mechanism in human vascular endothelial-cells. J. Clin. Investig. 1993, 92, 1866–1874.
12. Bevilacqua, M.P. Endothelial-leukocyte adhesion molecules. Annu. Rev. Immunol. 1993, 11, 767–804.
13. Huo, Y.Q.; Hafezi-Moghadam, A.; Ley, K. Role of vascular cell adhesion molecule-1 and fibronectin connecting segment-1 in monocyte rolling and adhesion on early atherosclerotic lesions. Circ. Res. 2000, 87, 153–159.
14. Moore, K.J.; Sheedy, F.J.; Fisher, E.A. Macrophages in atherosclerosis: A dynamic balance. Nat. Rev. Immunol. 2013, 13, 709–721.
15. Falk, E.; Shah, P.K.; Fuster, V. Coronary plaque disruption. Circulation 1995, 92, 657–671.
16. Theilmeier, G.; Michiels, C.; Spaepen, E.; Vreys, I.; Collen, D.; Vermylen, J.; Hoylaerts, M.F. Endothelial von willebrand factor recruits platelets to atherosclerosis-prone sites in response to hypercholesterolemia. Blood 2002, 99, 4486–4493.
17. Steffel, J.; Hermann, M.; Greutert, H.; Gay, S.; Luscher, T.F.; Ruschitzka, F.; Tanner, F.C. Celecoxib decreases endothelial tissue factor expression through inhibition of c-Jun terminal NH2 kinase phosphorylation. Circulation 2005, 111, 1685–1689.
18. Nilsson, P.M.; Boutouyrie, P.; Cunha, P.; Kotsis, V.; Narkiewicz, K.; Parati, G.; Rietzschel, E.; Scuteri, A.; Laurent, S. Early vascular ageing in translation: From laboratory investigations to clinical applications in cardiovascular prevention. J. Hypertens. 2013, 31, 1517–1526.
19. Glagov, S.; Weisenberg, E.; Zarins, C.K.; Stankunavicius, R.; Kolettis, G.J. Compensatory enlargement of human atherosclerotic coronary arteries. N. Engl. J. Med. 1987, 316, 1371–1375.
20. Aggoun, Y.; Bonnet, D.; Sidi, D.; Girardet, J.P.; Brucker, E.; Polak, M.; Safar, M.E.; Levy, B.I. Arterial mechanical changes in children with familial hypercholesterolemia. Arterioscler. Thromb. Vasc. Biol. 2000, 20, 2070–2075.
21. Doyle, B.; Caplice, N. Plaque neovascularization and antiangiogenic therapy for atherosclerosis. J. Am. Coll. Cardiol. 2007, 49, 2073–2080.
22. Amato, M.; Montorsi, P.; Ravani, A.; Oldani, E.; Galli, S.; Ravagnani, P.M.; Tremoli, E.; Baldassarre, D. Carotid intima-media thickness by B-mode ultrasound as surrogate of coronary atherosclerosis: Correlation with quantitative coronary angiography and coronary intravascular ultrasound findings. Eur. Heart J. 2007, 28, 2094–2101.
23. Stork, S.; Feelders, R.A.; van den Beld, A.W.; Steyerberg, E.W.; Savelkoul, H.F.J.; Lamberts, S.W.J.; Grobbee, D.E.; Bots, M.L. Prediction of mortality risk in the elderly. Am. J. Med. 2006, 119, 519–525.
24. Mathiesen, E.B.; Johnsen, S.H.; Wilsgaard, T.; Bonaa, K.H.; Lochen, M.L.; Njolstad, I. Carotid plaque area and intima-media thickness in prediction of first-ever ischemic stroke a 10-year follow-up of 6584 men and women: The tromso study. Stroke 2011, 42, 972–978.
25. Allen, J.D.; Ham, K.L.; Dumont, D.M.; Sileshi, B.; Trahey, G.E.; Dahl, J.J. The development and potential of acoustic radiation force impulse (ARFI) imaging for carotid artery plaque characterization. Vasc. Med. 2011, 16, 302–311.
26. Gray-Weale, A.C.; Graham, J.C.; Burnett, J.R.; Byrne, K.; Lusby, R.J. Carotid artery atheroma: Comparison of preoperative B-mode ultrasound appearance with carotid endarterectomy specimen pathology. J. Cardiovasc. Surg. 1988, 29, 676–681.
27. Mathiesen, E.B.; Bonaa, K.H.; Joakimsen, O. Echolucent plaques are associated with high risk of ischemic cerebrovascular events in carotid stenosis: The tromso study. Circulation 2001, 103, 2171–2175.
28. Reiter, M.; Effenberger, I.; Sabeti, S.; Mlekusch, W.; Schlager, O.; Dick, P.; Puchner, S.; Amighi, J.; Bucek, R.A.; Minar, E., et al. Increasing carotid plaque echolucency is predictive of cardiovascular events in high-risk patients. Radiology 2008, 248, 1050–1055.
29. Nambi, V.; Chambless, L.; Folsom, A.R.; He, M.; Hu, Y.J.; Mosley, T.; Volcik, K.; Boerwinkle, E.; Ballantyne, C.M. Carotid intima-media thickness and presence or absence of plaque improves prediction of coronary heart disease risk the aric (atherosclerosis risk in communities) study. J. Am. Coll. Cardiol. 2010, 55, 1600–1607.
30. Bots, M.L.; Hoes, A.W.; Koudstaal, P.J.; Hofman, A.; Grobbee, D.E. Common carotid intima-media thickness and risk of stroke and myocardial infarction—The rotterdam study. Circulation 1997, 96, 1432–1437.
31. Peters, S.A.; den Ruijter, H.M.; Grobbee, D.E.; Bots, M.L. 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, 20–25.
32. Den Ruijter, H.M.; Peters, S.A.; Anderson, T.J.; Britton, A.R.; Dekker, J.M.; Eijkemans, M.J.; Engstrom, G.; Evans, G.W.; de Graaf, J.; Grobbee, D.E., et al. Common carotid intima-media thickness measurements in cardiovascular risk prediction: A meta-analysis. JAMA 2012, 308, 796–803.
33. Finn, A.V.; Kolodgie, F.D.; Virmani, R. Correlation between carotid intimal/medial thickness and atherosclerosis: A point of view from pathology. Arterioscler. Thromb. Vasc. Biol. 2010, 30, 177–181.
34. Molinari, F.; Zeng, G.; Suri, J.S. An integrated approach to computer-based automated tracing and its validation for 200 common carotid arterial wall ultrasound images: A new technique. J. Ultrasound Med. 2010, 29, 399–418.
35. Sillesen, H.; Muntendam, P.; Adourian, A.; Entrekin, R.; Garcia, M.; Falk, E.; Fuster, V. Carotid plaque burden as a measure of subclinical atherosclerosis: Comparison with other tests for subclinical arterial disease in the high risk plaque bioimage study. JACC Cardiovasc. Imaging 2012, 5, 681–689.
36. Baber, U.; Mehran, R.; Sartori, S.; Schoos, M.M.; Sillesen, H.; Muntendam, P.; Garcia, M.J.; Gregson, J.; Pocock, S.; Falk, E., et al. Prevalence, impact, and predictive value of detecting subclinical coronary and carotid atherosclerosis in asymptomatic adults: The bioimage study. J. Am. Coll. Cardiol. 2015, 65, 1065–1074.
37. Yamagishi, M.; Terashima, M.; Awano, K.; Kijima, M.; Nakatani, S.; Daikoku, S.; Ito, K.; Yasumura, Y.; Miyatake, K. Morphology of vulnerable coronary plaque: Insights from follow-up of patients examined by intravascular ultrasound before an acute coronary syndrome. J. Am. Coll. Cardiol. 2000, 35, 106–111.
38. Nishimura, R.A.; Edwards, W.D.; Warnes, C.A.; Reeder, G.S.; Holmes, D.R.; Tajik, A.J.; Yock, P.G. Intravascular ultrasound imaging-in vitro validation and pathological correlation. J. Am. Coll. Cardiol. 1990, 16, 145–154.
39. Prati, F.; Arbustini, E.; Labellarte, A.; Dal Bello, B.; Sommariva, L.; Mallus, M.T.; Pagano, A.; Boccanelli, A. Correlation between high frequency intravascular ultrasound and histomorphology in human coronary arteries. Heart (Br. Card. Soc.) 2001, 85, 567–570.
40. Palmer, N.D.; Northridge, D.; Lessells, A.; McDicken, W.N.; Fox, K.A.A. In vitro analysis of coronary atheromatous lesions by intravascular ultrasound-reproducibility and histological correlation of lesion morphology. Eur. Heart J. 1999, 20, 1701–1706.
41. Potkin, B.N.; Bartorelli, A.L.; Gessert, J.M.; Neville, R.F.; Almagor, Y.; Roberts, W.C.; Leon, M.B. Coronary-artery imaging with intravascular high-frequency ultrasound. Circulation 1990, 81, 1575–1585.
42. Mintz, G.S.; Nissen, S.E.; Anderson, W.D.; Bailey, S.R.; Erbel, R.; Fitzgerald, P.J.; Pinto, F.J.; Rosenfield, K.; Siegel, R.J.; Tuzcu, E.M., et al. American college of cardiology clinical expert consensus document on standards for acquisition, measurement and reporting of intravascular ultrasound studies (ivus). A report of the american college of cardiology task force on clinical expert consensus documents. J. Am. Coll. Cardiol. 2001, 37, 1478–1492.
43. Schoenhagen, P.; Stone, G.W.; Nissen, S.E.; Grines, C.L.; Griffin, J.; Clemson, B.S.; Vince, D.G.; Ziada, K.; Crowe, T.; Apperson-Hanson, C., et al. Coronary plaque morphology and frequency of ulceration distant from culprit lesions in patients with unstable and stable presentation. Arterioscler. Thromb. Vasc. Biol. 2003, 23, 1895–1900.
44. Wuyts, F.L.; Vanhuyse, V.J.; Langewouters, G.J.; Decraemer, W.F.; Raman, E.R.; Buyle, S. Elastic properties of human aortas in relation to age and atherosclerosis—A structural model. Phys. Med. Biol. 1995, 40, 1577–1597.
45. Van Sloten, T.T.; Schram, M.T.; van den Hurk, K.; Dekker, J.M.; Nijpels, G.; Henry, R.M.; Stehouwer, C.D. Local stiffness of the carotid and femoral artery is associated with incident cardiovascular events and all-cause mortality: The hoorn study. J. Am. Coll. Cardiol. 2014, 63, 1739–1747.
46. Cecelja, M.; Chowienczyk, P. Dissociation of aortic pulse wave velocity with risk factors for cardiovascular disease other than hypertension: A systematic review. Hypertension 2009, 54, 1328–1336.
47. De Korte, C.L.; Pasterkamp, G.; van der Steen, A.F.; Woutman, H.A.; Bom, N. Characterization of plaque components with intravascular ultrasound elastography in human femoral and coronary arteries in vitro. Circulation 2000, 102, 617–623.
48. Schaar, J.A.; van der Steen, A.F.; Mastik, F.; Baldewsing, R.A.; Serruys, P.W. Intravascular palpography for vulnerable plaque assessment. J. Am. Coll. Cardiol. 2006, 47, C86–C91.
49. De Korte, C.L.; Sierevogel, M.J.; Mastik, F.; Strijder, C.; Schaar, J.A.; Velema, E.; Pasterkamp, G.; Serruys, P.W.; van der Steen, A.F. Identification of atherosclerotic plaque components with intravascular ultrasound elastography in vivo: A yucatan pig study. Circulation 2002, 105, 1627–1630.
50. Schaar, J.A.; Regar, E.; Mastik, F.; McFadden, E.P.; Saia, F.; Disco, C.; de Korte, C.L.; de Feyter, P.J.; van der Steen, A.F.; Serruys, P.W. Incidence of high-strain patterns in human coronary arteries: Assessment with three-dimensional intravascular palpography and correlation with clinical presentation. Circulation 2004, 109, 2716–2719.
51. Kruizinga, P.; Mastik, F.; van den Oord, S.C.; Schinkel, A.F.; Bosch, J.G.; de Jong, N.; van Soest, G.; van der Steen, A.F. High-definition imaging of carotid artery wall dynamics. Ultrasound Med. Biol. 2014, 40, 2392–2403.
52. Svedlund, S.; Gan, L.M. Longitudinal common carotid artery wall motion is associated with plaque burden in man and mouse. Atherosclerosis 2011, 217, 120–124.
53. Widman, E.; Caidahl, K.; Heyde, B.; D’Hooge, J.; Larsson, M. Ultrasound speckle tracking strain estimation of in vivo carotid artery plaque with in vitro sonomicrometry validation. Ultrasound Med. Biol. 2015, 41, 77–88.
54. Tsai, W.C.; Sun, Y.T.; Liu, Y.W.; Ho, C.S.; Chen, J.Y.; Wang, M.C.; Tsai, L.M. Usefulness of vascular wall deformation for assessment of carotid arterial stiffness and association with previous stroke in elderly. Am. J. Hypertens. 2013, 26, 770–777.
55. Gramiak, R.; Shah, P.M. Echocardiography of the aortic root. Investig. Radiol. 1968, 3, 356–366.
56. Jayaweera, A.R.; Edwards, N.; Glasheen, W.P.; Villanueva, F.S.; Abbott, R.D.; Kaul, S. In vivo myocardial kinetics of air-filled albumin microbubbles during myocardial contrast echocardiography. Comparison with radiolabeled red blood cells. Circ. Res. 1994, 74, 1157–1165.
57. Demos, S.M.; Onyuksel, H.; Gilbert, J.; Roth, S.I.; Kane, B.; Jungblut, P.; Pinto, J.V.; McPherson, D.D.; Klegerman, M.E. In vitro targeting of antibody-conjugated echogenic liposomes for site-specific ultrasonic image enhancement. J. Pharm. Sci. 1997, 86, 167–171.
58. de Jong, N.; Frinking, P.J.; Bouakaz, A.; Goorden, M.; Schourmans, T.; Jingping, X.; Mastik, F. Optical imaging of contrast agent microbubbles in an ultrasound field with a 100-MHz camera. Ultrasound Med. Biol. 2000, 26, 487–492.
59. Dayton, P.A.; Morgan, K.E.; Klibanov, A.L.; Brandenburger, G.H.; Ferrara, K.W. Optical and acoustical observations of the effects of ultrasound on contrast agents. IEEE Trans. Ultrasonics Ferroelectr. Freq. Control 1999, 46, 220–232.
60. Kaufmann, B.A.; Wei, K.; Lindner, J.R. Contrast echocardiography. Curr. Probl. Cardiol. 2007, 32, 51–96.
61. Barger, A.C.; Beeuwkes, R. 3rd; Lainey, L.L.; Silverman, K.J. Hypothesis: Vasa vasorum and neovascularization of human coronary arteries. A possible role in the pathophysiology of atherosclerosis. N. Engl. J. Med. 1984, 310, 175–177.
62. Sluimer, J.C.; Kolodgie, F.D.; Bijnens, A.; Maxfield, K.; Pacheco, E.; Kutys, B.; Duimel, H.; Frederik, P.M.; van Hinsbergh, V.W.M.; Virmani, R., et al. Thin-walled microvessels in human coronary atherosclerotic plaques show incomplete endothelial junctions relevance of compromised structural integrity for intraplaque microvascular leakage. J. Am. Coll. Cardiol. 2009, 53, 1517–1527.
63. Kolodgie, F.D.; Gold, H.K.; Burke, A.P.; Fowler, D.R.; Kruth, H.S.; Weber, D.K.; Farb, A.; Guerrero, L.J.; Hayase, M.; Kutys, R., et al. Intraplaque hemorrhage and progression of coronary atheroma. N. Engl. J. Med. 2003, 349, 2316–2325.
64. Coli, S.; Magnoni, M.; Sangiorgi, G.; Marrocco-Trischitta, M.M.; Melisurgo, G.; Mauriello, A.; Spagnoli, L.; Chiesa, R.; Cianflone, D.; Maseri, A. Contrast-enhanced ultrasound imaging of intraplaque neovascularization in carotid arteries: Correlation with histology and plaque echogenicity. J. Am. Coll. Cardiol. 2008, 52, 223–230.
65. Staub, D.; Partovi, S.; Schinkel, A.F.; Coll, B.; Uthoff, H.; Aschwanden, M.; Jaeger, K.A.; Feinstein, S.B. Correlation of carotid artery atherosclerotic lesion echogenicity and severity at standard us with intraplaque neovascularization detected at contrast-enhanced us. Radiology 2011, 258, 618–626.
66. Hoogi, A.; Adam, D.; Hoffman, A.; Kerner, H.; Reisner, S.; Gaitini, D. Carotid plaque vulnerability: Quantification of neovascularization on contrast-enhanced ultrasound with histopathologic correlation. AJR Am. J. Roentgenol. 2011, 196, 431–436.
67. Staub, D.; Patel, M.B.; Tibrewala, A.; Ludden, D.; Johnson, M.; Espinosa, P.; Coll, B.; Jaeger, K.A.; Feinstein, S.B. Vasa vasorum and plaque neovascularization on contrast-enhanced carotid ultrasound imaging correlates with cardiovascular disease and past cardiovascular events. Stroke 2010, 41, 41–47.
68. Saito, K.; Nagatsuka, K.; Ishibashi-Ueda, H.; Watanabe, A.; Kannki, H.; Iihara, K. Contrast-enhanced ultrasound for the evaluation of neovascularization in atherosclerotic carotid artery plaques. Stroke 2014, 45, 3073–3075.
69. Ten Kate, G.L.; Renaud, G.G.; Akkus, Z.; van den Oord, S.C.; ten Cate, F.J.; Shamdasani, V.; Entrekin, R.R.; Sijbrands, E.J.; de Jong, N.; Bosch, J.G., et al. Far-wall pseudoenhancement during contrast-enhanced ultrasound of the carotid arteries: Clinical description and in vitro reproduction. Ultrasound Med. Biol. 2012, 38, 593–600.
70. Renaud, G.; Bosch, J.G.; Ten Kate, G.L.; Shamdasani, V.; Entrekin, R.; de Jong, N.; van der Steen, A.F. Counter-propagating wave interaction for contrast-enhanced ultrasound imaging. Phys. Med. Biol. 2012, 57, L9–L18.
71. Staub, D.; Schinkel, A.F.L.; Coll, B.; Coli, S.; van der Steen, A.F.W.; Reed, J.D.; Krueger, C.; Thomenius, K.E.; Adam, D.; Sijbrands, E.J., et al. Contrast-enhanced ultrasound imaging of the vasa vasorum from early atherosclerosis to the identification of unstable plaques. JACC Cardiovasc. Imaging 2010, 3, 761–771.
72. Lindner, J.R.; Song, J.; Xu, F.; Klibanov, A.L.; Singbartl, K.; Ley, K.; Kaul, S. Noninvasive ultrasound imaging of inflammation using microbubbles targeted to activated leukocytes. Circulation 2000, 102, 2745–2750.
73. Lindner, J.R.; Coggins, M.P.; Kaul, S.; Klibanov, A.L.; Brandenburger, G.H.; Ley, K. Microbubble persistence in the microcirculation during ischemia/reperfusion and inflammation is caused by integrin-and complement-mediated adherence to activated leukocytes. Circulation 2000, 101, 668–675.
74. Khanicheh, E.; Mitterhuber, M.; Kinslechner, K.; Xu, L.; Lindner, J.R.; Kaufmann, B.A. Factors affecting the endothelial retention of targeted microbubbles: Influence of microbubble shell design and cell surface projection of the endothelial target molecule. J. Am. Soc. Echocardiogr. 2012, 25, 460–466.
75. Takalkar, A.M.; Klibanov, A.L.; Rychak, J.J.; Lindner, J.R.; Ley, K. Binding and detachment dynamics of microbubbles targeted to P-selectin under controlled shear flow. J. Control. Release 2004, 96, 473–482.
76. Lindner, J.R. Molecular imaging with contrast ultrasound and targeted microbubbles. J. Nucl. Cardiol. 2004, 11, 215–221.
77. Lankford, M.; Behm, C.Z.; Yeh, J.; Klibanov, A.L.; Robinson, P.; Lindner, J.R. Effect of microbubble ligation to cells on ultrasound signal enhancement: Implications for targeted imaging. Investig. Radiol. 2006, 41, 721–728.
78. Lindner, J.R. Molecular imaging of vascular phenotype in cardiovascular disease: New diagnostic opportunities on the horizon. J. Am. Soc. Echocardiogr. 2010, 23, 343–350.
79. Fenyo, I.M.; Gafencu, A.V. The involvement of the monocytes/macrophages in chronic inflammation associated with atherosclerosis. Immunobiology 2013, 218, 1376–1384.
80. Tsutsui, J.M.; Xie, F.; Cano, M.; Chomas, J.; Phillips, P.; Radio, S.J.; Lof, J.; Porter, T.R. Detection of retained microbubbles in carotid arteries with real-time low mechanical index imaging in the setting of endothelial dysfunction. J. Am. Coll. Cardiol. 2004, 44, 1036–1046.
81. Anderson, D.R.; Tsutsui, J.M.; Xie, F.; Radio, S.J.; Porter, T.R. The role of complement in the adherence of microbubbles to dysfunctional arterial endothelium and atherosclerotic plaque. Cardiovasc. Res. 2007, 73, 597–606.
82. McEver, R.P.; Cummings, R.D. Perspectives series: Cell adhesion in vascular biology. Role of PSGL-1 binding to selectins in leukocyte recruitment. J. Clin. Investig. 1997, 100, 485–491.
83. Ramos, C.L.; Huo, Y.; Jung, U.; Ghosh, S.; Manka, D.R.; Sarembock, I.J.; Ley, K. Direct demonstration of P-selectin-and VCAM-1-dependent mononuclear cell rolling in early atherosclerotic lesions of apolipoprotein E-deficient mice. Circ. Res. 1999, 84, 1237–1244.
84. Kaufmann, B.A.; Carr, C.L.; Belcik, J.T.; Xie, A.; Yue, Q.; Chadderdon, S.; Caplan, E.S.; Khangura, J.; Bullens, S.; Bunting, S., et al. Molecular imaging of the initial inflammatory response in atherosclerosis: Implications for early detection of disease. Arterioscler. Thromb. Vasc. Biol. 2010, 30, 54–59.
85. Villanueva, F.S.; Lu, E.; Bowry, S.; Kilic, S.; Tom, E.; Wang, J.; Gretton, J.; Pacella, J.J.; Wagner, W.R. Myocardial ischemic memory imaging with molecular echocardiography. Circulation 2007, 115, 345–352.
86. Kaufmann, B.A.; Lewis, C.; Xie, A.; Mirza-Mohd, A.; Lindner, J.R. Detection of recent myocardial ischaemia by molecular imaging of P-selectin with targeted contrast echocardiography. Eur. Heart J. 2007, 28, 2011–2017.
87. Walpola, P.L.; Gotlieb, A.I.; Cybulsky, M.I.; Langille, B.L. Expression of ICAM-1 and VCAM-1 and monocyte adherence in arteries exposed to altered shear stress. Arterioscler. Thromb. Vasc. Biol. 1995, 15, 2–10.
88. Dansky, H.M.; Barlow, C.B.; Lominska, C.; Sikes, J.L.; Kao, C.; Weinsaft, J.; Cybulsky, M.I.; Smith, J.D. Adhesion of monocytes to arterial endothelium and initiation of atherosclerosis are critically dependent on vascular cell adhesion molecule-1 gene dosage. Arterioscler. Thromb. Vasc. Biol. 2001, 21, 1662–1667.
89. Iiyama, K.; Hajra, L.; Iiyama, M.; Li, H.; DiChiara, M.; Medoff, B.D.; Cybulsky, M.I. Patterns of vascular cell adhesion molecule-1 and intercellular adhesion molecule-1 expression in rabbit and mouse atherosclerotic lesions and at sites predisposed to lesion formation. Circ. Res. 1999, 85, 199–207.
90. Villanueva, F.S.; Jankowski, R.J.; Klibanov, S.; Pina, M.L.; Alber, S.M.; Watkins, S.C.; Brandenburger, G.H.; Wagner, W.R. Microbubbles targeted to intercellular adhesion molecule-1 bind to activated coronary artery endothelial cells. Circulation 1998, 98, 1–5.
91. Hamilton, A.J.; Huang, S.L.; Warnick, D.; Rabbat, M.; Kane, B.; Nagaraj, A.; Klegerman, M.; McPherson, D.D. Intravascular ultrasound molecular imaging of atheroma components in vivo. J. Am. Coll. Cardiol. 2004, 43, 453–460.
92. Kaufmann, B.A.; Sanders, J.M.; Davis, C.; Xie, A.; Aldred, P.; Sarembock, I.J.; Lindner, J.R. Molecular imaging of inflammation in atherosclerosis with targeted ultrasound detection of vascular cell adhesion molecule-1. Circulation 2007, 116, 276–284.
93. Wu, J.; Leong-Poi, H.; Bin, J.; Yang, L.; Liao, Y.; Liu, Y.; Cai, J.; Xie, J.; Liu, Y. Efficacy of contrast-enhanced us and magnetic microbubbles targeted to vascular cell adhesion molecule-1 for molecular imaging of atherosclerosis. Radiology 2011, 260, 463–471.
94. Liu, Y.; Davidson, B.P.; Yue, Q.; Belcik, T.; Xie, A.; Inaba, Y.; McCarty, O.J.; Tormoen, G.W.; Zhao, Y.; Ruggeri, Z.M., et al. Molecular imaging of inflammation and platelet adhesion in advanced atherosclerosis effects of antioxidant therapy with nadph oxidase inhibition. Circ. Cardiovasc. Imaging 2013, 6, 74–82.
95. Khanicheh, E.; Qi, Y.; Xie, A.; Mitterhuber, M.; Xu, L.; Mochizuki, M.; Daali, Y.; Jaquet, V.; Krause, K.H.; Ruggeri, Z.M., et al. Molecular imaging reveals rapid reduction of endothelial activation in early atherosclerosis with apocynin independent of antioxidative properties. Arterioscler. Thromb. Vasc. Biol. 2013, 33, 2187–2192.
96. Khanicheh, E.; Mitterhuber, M.; Xu, L.; Haeuselmann, S.P.; Kuster, G.M.; Kaufmann, B.A. Noninvasive ultrasound molecular imaging of the effect of statins on endothelial inflammatory phenotype in early atherosclerosis. PLoS ONE 2013, 8, e58761.
97. Unger, E.C.; McCreery, T.P.; Sweitzer, R.H.; Shen, D.; Wu, G. In vitro studies of a new thrombus-specific ultrasound contrast agent. Am. J. Cardiol. 1998, 81, 58g–61g.
98. Wu, W.; Wang, Y.; Shen, S.; Wu, J.; Guo, S.; Su, L.; Hou, F.; Wang, Z.; Liao, Y.; Bin, J. In vivo ultrasound molecular imaging of inflammatory thrombosis in arteries with cyclic Arg-Gly-Aspmodified microbubbles targeted to glycoprotein IIB/IIIA. Investig. Radiol. 2013, 48, 803–812.
99. Wang, X.; Hagemeyer, C.E.; Hohmann, J.D.; Leitner, E.; Armstrong, P.C.; Jia, F.; Olschewski, M.; Needles, A.; Peter, K.; Ahrens, I. Novel single-chain antibody-targeted microbubbles for molecular ultrasound imaging of thrombosis: Validation of a unique noninvasive method for rapid and sensitive detection of thrombi and monitoring of success or failure of thrombolysis in mice. Circulation 2012, 125, 3117–3126.
100. Alonso, A.; Della Martina, A.; Stroick, M.; Fatar, M.; Griebe, M.; Pochon, S.; Schneider, M.; Hennerici, M.; Allemann, E.; Meairs, S. Molecular imaging of human thrombus with novel abciximab immunobubbles and ultrasound. Stroke 2007, 38, 1508–1514.
101. Wang, X.; Palasubramaniam, J.; Gkanatsas, Y.; Hohmann, J.D.; Westein, E.; Kanojia, R.; Alt, K.; Huang, D.; Jia, F.; Ahrens, I., et al. Towards effective and safe thrombolysis and thromboprophylaxis: Preclinical testing of a novel antibody-targeted recombinant plasminogen activator directed against activated platelets. Circ. Res. 2014, 114, 1083–1093.
102. Burger, P.C.; Wagner, D.D. Platelet P-selectin facilitates atherosclerotic lesion development. Blood 2003, 101, 2661–2666.
103. Massberg, S.; Brand, K.; Gruner, S.; Page, S.; Muller, E.; Muller, I.; Bergmeier, W.; Richter, T.; Lorenz, M.; Konrad, I., et al. A critical role of platelet adhesion in the initiation of atherosclerotic lesion formation. J. Exp. Med. 2002, 196, 887–896.
104. Henn, V.; Slupsky, J.R.; Grafe, M.; Anagnostopoulos, I.; Forster, R.; Muller-Berghaus, G.; Kroczek, R.A. Cd40 ligand on activated platelets triggers an inflammatory reaction of endothelial cells. Nature 1998, 391, 591–594.
105. McCarty, O.J.; Conley, R.B.; Shentu, W.; Tormoen, G.W.; Zha, D.; Xie, A.; Qi, Y.; Zhao, Y.; Carr, C.; Belcik, T., et al. Molecular imaging of activated von willebrand factor to detect high-risk atherosclerotic phenotype. JACC Cardiovasc. Imaging 2010, 3, 947–955.
106. Couture, O.; Bannouf, S.; Montaldo, G.; Aubry, J.F.; Fink, M.; Tanter, M. Ultrafast imaging of ultrasound contrast agents. Ultrasound Med. Biol. 2009, 35, 1908–1916.
107. Mauldin, F.W., Jr.; Dhanaliwala, A.H.; Patil, A.V.; Hossack, J.A. Real-time targeted molecular imaging using singular value spectra properties to isolate the adherent microbubble signal. Phys. Med. Biol. 2012, 57, 5275–5293.