Molecular MRI of atherosclerosis

Molecules

Volumn 18, Issue 11, 2013, Pages 14042-14069

  Phinikaridou, Alkystis ^a   Andia, Marcelo E ^a,b   Lacerda, Sara ^a   Lorrio, Silvia ^a   Makowski, Marcus R ^a,c   Botnar, René M ^a,d,e  

^a ST THOMAS HOSPITAL   (United Kingdom)

^b PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^c CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^d WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^e KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Atherosclerosis; Contrast agent; Molecular imaging; MRI

Indexed keywords

CONTRAST MEDIUM; DIAGNOSTIC AGENT;

ANIMAL; ATHEROSCLEROSIS; CORONARY ARTERY DISEASE; HUMAN; METHODOLOGY; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOLOGY; REVIEW;

ANIMALS; ATHEROSCLEROSIS; CONTRAST MEDIA; CORONARY ARTERY DISEASE; HUMANS; MAGNETIC RESONANCE IMAGING;

EID: 84888621253     PISSN: None     EISSN: 14203049     Source Type: Journal    
DOI: 10.3390/molecules181114042     Document Type: Review

References (121)

1. Rosamond, W.; Flegal, K.; Furie, K.; Go, A.; Greenlund, K.; Haase, N.; Hailpern, S.M.; Ho, M.; Howard, V.; Kissela, B.; et al. Heart disease and stroke statistics-2008 update: A report from the american heart association statistics committee and stroke statistics subcommittee. Circulation 2008, 117, e25-e146.
2. Lloyd-Jones, D.; Adams, R.; Carnethon, M.; De Simone, G.; Ferguson, T.B.; Flegal, K.; Ford, E.; Furie, K.; Go, A.; Greenlund, K.; et al. Heart disease and stroke statistics-2009 update: A report from the american heart association statistics committee and stroke statistics subcommittee. Circulation 2009, 119, 480-486.
3. Virmani, R.; Burke, A.P.; Farb, A.; Kolodgie, F.D. Pathology of the vulnerable plaque. J. Am. Coll. Cardiol. 2006, 47, C13-C18.
4. Falk, E. Pathogenesis of atherosclerosis. J. Am. Coll. Cardiol. 2006, 47, C7-C12.
5. Narula, J.; Strauss, H.W. The popcorn plaques. Nat. Med. 2007, 13, 532-534.
6. Kubo, T.; Imanishi, T.; Takarada, S.; Kuroi, A.; Ueno, S.; Yamano, T.; Tanimoto, T.; Matsuo, Y.; Masho, T.; Kitabata, H.; et al. Assessment of culprit lesion morphology in acute myocardial infarction: Ability of optical coherence tomography compared with intravascular ultrasound and coronary angioscopy. J. Am. Coll. Cardiol. 2007, 50, 933-939.
7. Schoenhagen, P.; Ziada, K.M.; Kapadia, S.R.; Crowe, T.D.; Nissen, S.E.; Tuzcu, E.M. Extent and direction of arterial remodeling in stable versus unstable coronary syndromes: An intravascular ultrasound study. Circulation 2000, 101, 598-603.
8. Pundziute, G.; Schuijf, J.D.; Jukema, J.W.; Boersma, E.; Scholte, A.J.; Kroft, L.J.; van der Wall, E.E.; Bax, J.J. Noninvasive assessment of plaque characteristics with multislice computed tomography coronary angiography in symptomatic diabetic patients. Diabetes Care 2007, 30, 1113-1119.
9. Yeon, S.B.; Sabir, A.; Clouse, M.; Martinezclark, P.O.; Peters, D.C.; Hauser, T.H.; Gibson, C.M.; Nezafat, R.; Maintz, D.; Manning, W.J.; et al. Delayed-enhancement cardiovascular magnetic resonance coronary artery wall imaging: Comparison with multislice computed tomography and quantitative coronary angiography. J. Am. Coll. Cardiol. 2007, 50, 441-447.
10. Maintz, D.; Ozgun, M.; Hoffmeier, A.; Fischbach, R.; Kim, W.Y.; Stuber, M.; Manning, W.J.; Heindel, W.; Botnar, R.M. Selective coronary artery plaque visualization and differentiation by contrast-enhanced inversion prepared mri. Eur. Heart J. 2006, 27, 1732-1736.
11. Fayad, Z.A.; Fuster, V.; Fallon, J.T.; Jayasundera, T.; Worthley, S.G.; Helft, G.; Aguinaldo, J.G.; Badimon, J.J.; Sharma, S.K. Noninvasive in vivo human coronary artery lumen and wall imaging using black-blood magnetic resonance imaging. Circulation 2000, 102, 506-510.
12. Kim, W.Y.; Stuber, M.; Bornert, P.; Kissinger, K.V.; Manning, W.J.; Botnar, R.M. Three-dimensional black-blood cardiac magnetic resonance coronary vessel wall imaging detects positive arterial remodeling in patients with nonsignificant coronary artery disease. Circulation 2002, 106, 296-299.
13. Johnson, G.A.; Benveniste, H.; Black, R.D.; Hedlund, L.W.; Maronpot, R.R.; Smith, B.R. Histology by magnetic resonance microscopy. Magn. Reson. Quart. 1993, 9, 1-30.
14. Hays, A.G.; Hirsch, G.A.; Kelle, S.; Gerstenblith, G.; Weiss, R.G.; Stuber, M. Noninvasive visualization of coronary artery endothelial function in healthy subjects and in patients with coronary artery disease. J. Am. Coll. Cardiol. 2010, 56, 1657-1665.
15. Hays, A.G.; Kelle, S.; Hirsch, G.A.; Soleimanifard, S.; Yu, J.; Agarwal, H.K.; Gerstenblith, G.; Schar, M.; Stuber, M.; Weiss, R.G. Regional coronary endothelial function is closely related to local early coronary atherosclerosis in patients with mild coronary artery disease: Pilot study. Circ. Cardiovasc. Imaging 2012, 5, 341-348.
16. Phinikaridou, A.; Andia, M.E.; Protti, A.; Indermuehle, A.; Shah, A.; Smith, A.; Warley, A.; Botnar, R.M. Noninvasive magnetic resonance imaging evaluation of endothelial permeability in murine atherosclerosis using an albumin-binding contrast agent. Circulation 2012, 126, 707-719.
17. Ross, R. Atherosclerosis-An inflammatory disease. N. Engl. J. Med. 1999, 340, 115-126.
18. Libby, P.; Ridker, P.M.; Maseri, A. Inflammation and atherosclerosis. Circulation 2002, 105, 1135-1143.
19. Falk, E. Why do plaques rupture? Circulation 1992, 86, III30-III42.
20. Falk, E.; Shah, P.K.; Fuster, V. Coronary plaque disruption. Circulation 1995, 92, 657-671.
21. Welt, F.G.; Rogers, C. Inflammation and restenosis in the stent era. Arterioscler. Thromb. Vasc. Biol. 2002, 22, 1769-1776.
22. Jeremias, A.; Spies, C.; Herity, N.A.; Pomerantsev, E.; Yock, P.G.; Fitzgerald, P.J.; Yeung, A.C. Coronary artery compliance and adaptive vessel remodelling in patients with stable and unstable coronary artery disease. Heart 2000, 84, 314-319.
23. Katsuda, S.; Kaji, T. Atherosclerosis and extracellular matrix. J. Atheroscler. Thromb. 2003, 10, 267-274.
24. Rekhter, M.D. Collagen synthesis in atherosclerosis: Too much and not enough. Cardiovasc. Res. 1999, 41, 376-384.
25. Krettek, A.; Sukhova, G.K.; Libby, P. Elastogenesis in human arterial disease: A role for macrophages in disordered elastin synthesis. Arterioscler. Thromb. Vasc. Biol. 2003, 23, 582-587.
26. Strauss, B.H.; Chisholm, R.J.; Keeley, F.W.; Gotlieb, A.I.; Logan, R.A.; Armstrong, P.W. Extracellular matrix remodeling after balloon angioplasty injury in a rabbit model of restenosis. Circ. Res. 1994, 75, 650-658.
27. Brasselet, C.; Durand, E.; Addad, F.; Al Haj Zen, A.; Smeets, M.B.; Laurent-Maquin, D.; Bouthors, S.; Bellon, G.; de Kleijn, D.; Godeau, G.; et al. Collagen and elastin cross-linking: A mechanism of constrictive remodeling after arterial injury. Am. J. Physiol. Heart Circ. Physiol. 2005, 289, H2228-H2233.
28. Stone, G.W.; Maehara, A.; Lansky, A.J.; de Bruyne, B.; Cristea, E.; Mintz, G.S.; Mehran, R.; McPherson, J.; Farhat, N.; Marso, S.P.; et al. A prospective natural-history study of coronary atherosclerosis. N. Engl. J. Med. 2011, 364, 226-235.
29. Calvert, P.A.; Obaid, D.R.; O'Sullivan, M.; Shapiro, L.M.; McNab, D.; Densem, C.G.; Schofield, P.M.; Braganza, D.; Clarke, S.C.; Ray, K.K.; et al. Association between ivus findings and adverse outcomes in patients with coronary artery disease: The viva (vh-ivus in vulnerable atherosclerosis) study. J. Am. Coll. Cardiol. Img. 2011, 4, 894-901.
30. Motoyama, S.; Sarai, M.; Harigaya, H.; Anno, H.; Inoue, K.; Hara, T.; Naruse, H.; Ishii, J.; Hishida, H.; Wong, N.D.; et al. Computed tomographic angiography characteristics of atherosclerotic plaques subsequently resulting in acute coronary syndrome. J. Am. Coll. Cardiol. 2009, 54, 49-57.
31. Sluimer, J.C.; Kolodgie, F.D.; Bijnens, A.P.; Maxfield, K.; Pacheco, E.; Kutys, B.; Duimel, H.; Frederik, P.M.; van Hinsbergh, V.W.; 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.
32. Lee, R.T.; Schoen, F.J.; Loree, H.M.; Lark, M.W.; Libby, P. Circumferential stress and matrix metalloproteinase 1 in human coronary atherosclerosis. Implications for plaque rupture. Arterioscler. Thromb. Vasc. Biol. 1996, 16, 1070-1073.
33. Hansson, G.K.; Robertson, A.K.; Soderberg-Naucler, C. Inflammation and atherosclerosis. Annu. Rev. Pathol. 2006, 1, 297-329.
34. 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.
35. Tavora, F.; Cresswell, N.; Li, L.; Ripple, M.; Burke, A. Immunolocalisation of fibrin in coronary atherosclerosis: Implications for necrotic core development. Pathology 2010, 42, 15-22.
36. Gossl, M.; Versari, D.; Mannheim, D.; Ritman, E.L.; Lerman, L.O.; Lerman, A. Increased spatial vasa vasorum density in the proximal lad in hypercholesterolemia-implications for vulnerable plaque-development. Atherosclerosis 2007, 192, 246-252.
37. Cheruvu, P.K.; Finn, A.V.; Gardner, C.; Caplan, J.; Goldstein, J.; Stone, G.W.; Virmani, R.; Muller, J.E. Frequency and distribution of thin-cap fibroatheroma and ruptured plaques in human coronary arteries: A pathologic study. J. Am. Coll. Cardiol. 2007, 50, 940-949.
38. Virmani, R.; Kolodgie, F.D.; Burke, A.P.; Finn, A.V.; Gold, H.K.; Tulenko, T.N.; Wrenn, S.P.; Narula, J. Atherosclerotic plaque progression and vulnerability to rupture: Angiogenesis as a source of intraplaque hemorrhage. Arterioscler. Thromb. Vasc. Biol. 2005, 25, 2054-2061.
39. Dollery, C.M.; Libby, P. Atherosclerosis and proteinase activation. Cardiovasc. Res. 2006, 69, 625-635.
40. Newby, A.C. Metalloproteinase expression in monocytes and macrophages and its relationship to atherosclerotic plaque instability. Arterioscler. Thromb. Vasc. Biol. 2008, 28, 2108-2114.
41. Re, G.; Azzimondi, G.; Lanzarini, C.; Bassein, L.; Vaona, I.; Guarnieri, C. Plasma lipoperoxidative markers in ischaemic stroke suggest brain embolism. Eur. J. Emerg. Med. 1997, 4, 5-9.
42. Brennan, M.L.; Penn, M.S.; Van Lente, F.; Nambi, V.; Shishehbor, M.H.; Aviles, R.J.; Goormastic, M.; Pepoy, M.L.; McErlean, E.S.; Topol, E.J.; et al. Prognostic value of myeloperoxidase in patients with chest pain. N. Engl. J. Med. 2003, 349, 1595-1604.
43. Sugiyama, S.; Okada, Y.; Sukhova, G.K.; Virmani, R.; Heinecke, J.W.; Libby, P. Macrophage myeloperoxidase regulation by granulocyte macrophage colony-stimulating factor in human atherosclerosis and implications in acute coronary syndromes. Am. J. Pathol. 2001, 158, 879-891.
44. Xiao, Q.; Danton, M.J.; Witte, D.P.; Kowala, M.C.; Valentine, M.T.; Degen, J.L. Fibrinogen deficiency is compatible with the development of atherosclerosis in mice. J. Clin Invest. 1998, 101, 1184-1194.
45. Bini, A.; Fenoglio, J.J., Jr.; Mesa-Tejada, R.; Kudryk, B.; Kaplan, K.L. Identification and distribution of fibrinogen, fibrin, and fibrin(ogen) degradation products in atherosclerosis. Use of monoclonal antibodies. Arteriosclerosis 1989, 9, 109-121.
46. Sirol, M.; Itskovich, V.V.; Mani, V.; Aguinaldo, J.G.; Fallon, J.T.; Misselwitz, B.; Weinmann, H.J.; Fuster, V.; Toussaint, J.F.; Fayad, Z.A. Lipid-rich atherosclerotic plaques detected by gadofluorine-enhanced in vivo magnetic resonance imaging. Circulation 2004, 109, 2890-2896.
47. Weinmann, H.J.; Brasch, R.C.; Press, W.R.; Wesbey, G.E. Characteristics of gadolinium-dtpa complex: A potential nmr contrast agent. Am. J. Roentgenol 1984, 142, 619-624.
48. Laniado, M.; Weinmann, H.J.; Schorner, W.; Felix, R.; Speck, U. First use of gddtpa/dimeglumine in man. Physiol. Chem. Phys. Med. NMR 1984, 16, 157-165.
49. Caravan, P.; Ellison, J.J.; McMurry, T.J.; Lauffer, R.B. Gadolinium(iii) chelates as mri contrast agents: Structure, dynamics, and applications. Chem. Rev. 1999, 99, 2293-2352.
50. Weissleder, R.; Elizondo, G.; Wittenberg, J.; Rabito, C.A.; Bengele, H.H.; Josephson, L. Ultrasmall superparamagnetic iron oxide: Characterization of a new class of contrast agents for mr imaging. Radiology 1990, 175, 489-493.
51. Blume, U.; Orbell, J.; Waltham, M.; Smith, A.; Razavi, R.; Schaeffter, T., 3D T(1)-mapping for the characterization of deep vein thrombosis. Magn. Reson. Mater. Phys. Biol. Med. 2009, 22, 375-383.
52. Deoni, S.C.; Rutt, B.K.; Peters, T.M. Rapid combined t1 and t2 mapping using gradient recalled acquisition in the steady state. Magn. Reson. Med. 2003, 49, 515-526.
53. Bach-Gansmo, T. Ferrimagnetic susceptibility contrast agents. Acta Radiol. Suppl. 1993, 387, 1-30.
54. Nivorozhkin, A.L.; Kolodziej, A.F.; Caravan, P.; Greenfield, M.T.; Lauffer, R.B.; McMurry, T.J. Enzyme-activated gd(3+) magnetic resonance imaging contrast agents with a prominent receptor-induced magnetization enhancement. Angew. Chem. Int. Ed. Engl. 2001, 40, 2903-2906.
55. Caravan, P. Strategies for increasing the sensitivity of gadolinium based mri contrast agents. Chem. Soc. Rev. 2006, 35, 512-523.
56. Solomon, I. Relaxation processes in a system of 2 spins. Phys. Rev. 1955, 99, 559-565.
57. Caravan, P.; Farrar, C.T.; Frullano, L.; Uppal, R. Influence of molecular parameters and increasing magnetic field strength on relaxivity of gadolinium- and manganese-based t(1) contrast agents. Contrast. Media. Mol. Imaging 2009, 4, 89-100.
58. Ferrucci, J.T.; Stark, D.D., Iron oxide-enhanced mr imaging of the liver and spleen: Review of the first 5 years. Am. J. Roentgenol. 1990, 155, 943-950.
59. Small, W.C.; Nelson, R.C.; Bernardino, M.E. Dual contrast enhancement of both t1- and t2-weighted sequences using ultrasmall superparamagnetic iron oxide. Magn. Reson. Imaging 1993, 11, 645-654.
60. Taupitz, M.; Wagner, S.; Schnorr, J.; Kravec, I.; Pilgrimm, H.; Bergmann-Fritsch, H.; Hamm, B. Phase i clinical evaluation of citrate-coated monocrystalline very small superparamagnetic iron oxide particles as a new contrast medium for magnetic resonance imaging. Invest. Radiol 2004, 39, 394-405.
61. von Bary, C.; Preissel, A.; Wagner, S.; Makowski, M.; Schachoff, S.; Keithahn, A.; Spuentrup, E.; Schoemig, A.; Robinson, S.; Lazewatsky, J.; et al. 211 MRI of coronary vessel wall injury in a swine model of coronary intervention using an eletrostatically stabilized vsop nanoparticle. J. Cardiovasc. Magn. Resonance 2008, 10 (Suppl. 1), A72.
62. Choudhury, R.P.; Fuster, V.; Fayad, Z.A. Molecular, cellular and functional imaging of atherothrombosis. Nat. Rev. Drug Discov. 2004, 3, 913-925.
63. Pouliquen, D.; Le Jeune, J.J.; Perdrisot, R.; Ermias, A.; Jallet, P. Iron oxide nanoparticles for use as an mri contrast agent: Pharmacokinetics and metabolism. Magn. Reson. Imaging 1991, 9, 275-283.
64. Schmitz, S.A.; Coupland, S.E.; Gust, R.; Winterhalter, S.; Wagner, S.; Kresse, M.; Semmler, W.; Wolf, K.J. Superparamagnetic iron oxide-enhanced mri of atherosclerotic plaques in watanabe hereditable hyperlipidemic rabbits. Invest. Radiol. 2000, 35, 460-471.
65. Taupitz, M.; Schnorr, J.; Abramjuk, C.; Wagner, S.; Pilgrimm, H.; Hunigen, H.; Hamm, B. New generation of monomer-stabilized very small superparamagnetic iron oxide particles (vsop) as contrast medium for mr angiography: Preclinical results in rats and rabbits. J. Magn. Reson. Imaging 2000, 12, 905-911.
66. Ruehm, S.G.; Corot, C.; Vogt, P.; Kolb, S.; Debatin, J.F. Magnetic resonance imaging of atherosclerotic plaque with ultrasmall superparamagnetic particles of iron oxide in hyperlipidemic rabbits. Circulation 2001, 103, 415-422.
67. Kooi, M.E.; Cappendijk, V.C.; Cleutjens, K.B.; Kessels, A.G.; Kitslaar, P.J.; Borgers, M.; Frederik, P.M.; Daemen, M.J.; van Engelshoven, J.M., Accumulation of ultrasmall superparamagnetic particles of iron oxide in human atherosclerotic plaques can be detected by in vivo magnetic resonance imaging. Circulation 2003, 107, 2453-2458.
68. Pirko, I.; Johnson, A.; Ciric, B.; Gamez, J.; Macura, S.I.; Pease, L.R.; Rodriguez, M. In vivo magnetic resonance imaging of immune cells in the central nervous system with superparamagnetic antibodies. Faseb J. 2004, 18, 179-182.
69. Yuan, C.; Kerwin, W.S.; Ferguson, M.S.; Polissar, N.; Zhang, S.; Cai, J.; Hatsukami, T.S. Contrast-enhanced high resolution mri for atherosclerotic carotid artery tissue characterization. J. Magn. Reson. Imaging 2002, 15, 62-67.
70. Kramer, C.M.; Cerilli, L.A.; Hagspiel, K.; DiMaria, J.M.; Epstein, F.H.; Kern, J.A. Magnetic resonance imaging identifies the fibrous cap in atherosclerotic abdominal aortic aneurysm. Circulation 2004, 109, 1016-1021.
71. Weinmann, H.J.; Ebert, W.; Misselwitz, B.; Schmitt-Willich, H. Tissue-specific mr contrast agents. Eur J. Radiol. 2003, 46, 33-44.
72. Lobbes, M.B.; Heeneman, S.; Passos, V.L.; Welten, R.; Kwee, R.M.; van der Geest, R.J.; Wiethoff, A.J.; Caravan, P.; Misselwitz, B.; Daemen, M.J.; et al. Gadofosveset-enhanced magnetic resonance imaging of human carotid atherosclerotic plaques: A proof-of-concept study. Invest. Radiol. 2010, 45, 275-281.
73. Jaffer, F.A.; Nahrendorf, M.; Sosnovik, D.; Kelly, K.A.; Aikawa, E.; Weissleder, R. Cellular imaging of inflammation in atherosclerosis using magnetofluorescent nanomaterials. Mol. Imaging 2006, 5, 85-92.
74. McAteer, M.A.; Schneider, J.E.; Ali, Z.A.; Warrick, N.; Bursill, C.A.; von zur Muhlen, C.; Greaves, D.R.; Neubauer, S.; Channon, K.M.; Choudhury, R.P. Magnetic resonance imaging of endothelial adhesion molecules in mouse atherosclerosis using dual-targeted microparticles of iron oxide. Arterioscler. Thromb. Vasc. Biol. 2008, 28, 77-83.
75. Mulder, W.J.; Strijkers, G.J.; Griffioen, A.W.; van Bloois, L.; Molema, G.; Storm, G.; Koning, G.A.; Nicolay, K. A liposomal system for contrast-enhanced magnetic resonance imaging of molecular targets. Bioconjug. Chem. 2004, 15, 799-806.
76. Nahrendorf, M.; Jaffer, F.A.; Kelly, K.A.; Sosnovik, D.E.; Aikawa, E.; Libby, P.; Weissleder, R. Noninvasive vascular cell adhesion molecule-1 imaging identifies inflammatory activation of cells in atherosclerosis. Circulation 2006, 114, 1504-1511.
77. Mulder, W.J.; Strijkers, G.J.; Briley-Saboe, K.C.; Frias, J.C.; Aguinaldo, J.G.; Vucic, E.; Amirbekian, V.; Tang, C.; Chin, P.T.; Nicolay, K.; et al. Molecular imaging of macrophages in atherosclerotic plaques using bimodal peg-micelles. Magn. Reson. Med. 2007, 58, 1164-1170.
78. Amirbekian, V.; Lipinski, M.J.; Briley-Saebo, K.C.; Amirbekian, S.; Aguinaldo, J.G.; Weinreb, D.B.; Vucic, E.; Frias, J.C.; Hyafil, F.; Mani, V.; et al. Detecting and assessing macrophages in vivo to evaluate atherosclerosis noninvasively using molecular mri. Proc. Natl. Acad. Sci. USA 2007, 104, 961-966.
79. Korosoglou, G.; Weiss, R.G.; Kedziorek, D.A.; Walczak, P.; Gilson, W.D.; Schar, M.; Sosnovik, D.E.; Kraitchman, D.L.; Boston, R.C.; Bulte, J.W.; et al. Noninvasive detection of macrophage-rich atherosclerotic plaque in hyperlipidemic rabbits using "positive contrast" magnetic resonance imaging. J. Am. Coll. Cardiol. 2008, 52, 483-491.
80. Makowski, M.R.; Wiethoff, A.J.; Blume, U.; Cuello, F.; Warley, A.; Jansen, C.H.; Nagel, E.; Razavi, R.; Onthank, D.C.; Cesati, R.R.; et al. Assessment of atherosclerotic plaque burden with an elastin-specific magnetic resonance contrast agent. Nat. Med. 2011, 17, 383-388.
81. von Bary, C.; Makowski, M.; Preissel, A.; Keithahn, A.; Warley, A.; Spuentrup, E.; Buecker, A.; Lazewatsky, J.; Cesati, R.; Onthank, D.; et al. Mri of coronary wall remodeling in a swine model of coronary injury using an elastin-binding contrast agent. Circ. Cardiovasc. Imaging 2011, 4, 147-155.
82. Sanders, H.M.; Strijkers, G.J.; Mulder, W.J.; Huinink, H.P.; Erich, S.J.; Adan, O.C.; Sommerdijk, N.A.; Merkx, M.; Nicolay, K. Morphology, binding behavior and mr-properties of paramagnetic collagen-binding liposomes. Contrast Media Mol. Imaging 2009, 4, 81-88.
83. Klink, A.; Heynens, J.; Herranz, B.; Lobatto, M.E.; Arias, T.; Sanders, H.M.; Strijkers, G.J.; Merkx, M.; Nicolay, K.; Fuster, V.; et al. In vivo characterization of a new abdominal aortic aneurysm mouse model with conventional and molecular magnetic resonance imaging. J. Am. Coll. Cardiol. 2011, 58, 2522-2530.
84. Chen, W.; Cormode, D.P.; Vengrenyuk, Y.; Herranz, B.; Feig, J.E.; Klink, A.; Mulder, W.J.; Fisher, E.A.; Fayad, Z.A. Collagen-specific peptide conjugated hdl nanoparticles as mri contrast agent to evaluate compositional changes in atherosclerotic plaque regression. JACC Cardiovasc. Imaging 2013, 6, 373-384.
85. Moody, A.R. Magnetic resonance direct thrombus imaging. J. Thromb. Haemost. 2003, 1, 1403-1409.
86. Moody, A.R.; Murphy, R.E.; Morgan, P.S.; Martel, A.L.; Delay, G.S.; Allder, S.; MacSweeney, S.T.; Tennant, W.G.; Gladman, J.; Lowe, J.; et al. Characterization of complicated carotid plaque with magnetic resonance direct thrombus imaging in patients with cerebral ischemia. Circulation 2003, 107, 3047-3052.
87. Murphy, R.E.; Moody, A.R.; Morgan, P.S.; Martel, A.L.; Delay, G.S.; Allder, S.; MacSweeney, S.T.; Tennant, W.G.; Gladman, J.; Lowe, J.; et al. Prevalence of complicated carotid atheroma as detected by magnetic resonance direct thrombus imaging in patients with suspected carotid artery stenosis and previous acute cerebral ischemia. Circulation 2003, 107, 3053-3058.
88. van Beek, E.J.; Wild, J.M.; Fink, C.; Moody, A.R.; Kauczor, H.U.; Oudkerk, M. Mri for the diagnosis of pulmonary embolism. J. Magn. Reson. Imaging 2003, 18, 627-640.
89. Toussaint, J.F.; LaMuraglia, G.M.; Southern, J.F.; Fuster, V.; Kantor, H.L. Magnetic resonance images lipid, fibrous, calcified, hemorrhagic, and thrombotic components of human atherosclerosis in vivo. Circulation 1996, 94, 932-938.
90. Yuan, C.; Petty, C.; O'Brien, K.D.; Hatsukami, T.S.; Eary, J.F.; Brown, B.G. In vitro and in situ magnetic resonance imaging signal features of atherosclerotic plaque-associated lipids. Arterioscler. Thromb. Vasc. Biol. 1997, 17, 1496-1503.
91. Fayad, Z.A.; Fallon, J.T.; Shinnar, M.; Wehrli, S.; Dansky, H.M.; Poon, M.; Badimon, J.J.; Charlton, S.A.; Fisher, E.A.; Breslow, J.L.; et al. Noninvasive in vivo high-resolution magnetic resonance imaging of atherosclerotic lesions in genetically engineered mice. Circulation 1998, 98, 1541-1547.
92. Rapoport, S.; Sostman, H.D.; Pope, C.; Camputaro, C.M.; Holcomb, W.; Gore, J.C. Venous clots: Evaluation with mr imaging. Radiology 1987, 162, 527-530.
93. Moody, A.R.; Morgan, P.S.; Fraser, D.; Hunt, B.J. T1 Reducing Properties of Methaemoglobin: Application to Direct MR Thrombus Imaging. In Proceedings of the ISMRM 8th scientific meeting, Denver, CO, USA, 2000.
94. McGuinness, C.L.; Humphries, J.; Waltham, M.; Burnand, K.G.; Collins, M.; Smith, A. Recruitment of labelled monocytes by experimental venous thrombi. Thromb. Haemost. 2001, 85, 1018-1024.
95. Modarai, B.; Burnand, K.G.; Humphries, J.; Waltham, M.; Smith, A., The role of neovascularisation in the resolution of venous thrombus. Thromb. Haemost. 2005, 93, 801-809.
96. Fraser, D.G.W.; Moody, A.R.; Morgan, P.S.; Martel, A.L.; Davidson, I. Diagnosis of lower-limb deep venous thrombosis: A prospective blinded study of magnetic resonance direct thrombus imaging. Ann. Intern. Med. 2002, 136, 89-98.
97. Moody, A.R. Direct imaging of deep-vein thrombosis with magnetic resonance imaging. Lancet 1997, 350, 1073-1073.
98. Kelly, J.; Hunt, B.J.; Moody, A. Magnetic resonance direct thrombus imaging: A novel technique for imaging venous thromboemboli. Thromb. Haemost. 2003, 89, 773-782.
99. Moody, A.R.; Pollock, J.G.; O'Connor, A.R.; Bagnall, M. Lower-limb deep venous thrombosis: Direct mr imaging of the thrombus. Radiology 1998, 209, 349-355.
100. Schmitz, S.A.; O'Regan, D.P.; Gibson, D.; Cunningham, C.; Fitzpatrick, J.; Allsop, J.; Larkman, D.J.; Hajnal, J.V. Magnetic resonance direct thrombus imaging at 3 t field strength in patients with lower limb deep vein thrombosis: A feasibility study. Clin. Radiol. 2006, 61, 282-286.
101. Saha, P.; Andia, M.E.; Modarai, B.; Blume, U.; Humphries, J.; Patel, A.S.; Phinikaridou, A.; Evans, C.E.; Mattock, K.; Grover, S.P.; et al. Magnetic resonance t1 relaxation time of venous thrombus is determined by iron processing and predicts susceptibility to lysis. Circulation 2013, 128, 729-736.
102. Griffioen, A.W.; Molema, G., Angiogenesis: Potentials for pharmacologic intervention in the treatment of cancer, cardiovascular diseases, and chronic inflammation. Pharmacol. Rev. 2000, 52, 237-268.
103. Purushothaman, K.R.; Sanz, J.; Zias, E.; Fuster, V.; Moreno, P.R. Atherosclerosis neovascularization and imaging. Curr. Mol. Med. 2006, 6, 549-556.
104. Libby, P. Inflammation in atherosclerosis. Nature 2002, 420, 868-874.
105. Winter, P.M.; Neubauer, A.M.; Caruthers, S.D.; Harris, T.D.; Robertson, J.D.; Williams, T.A.; Schmieder, A.H.; Hu, G.; Allen, J.S.; Lacy, E.K.; et al. Endothelial alpha(v)beta3 integrintargeted fumagillin nanoparticles inhibit angiogenesis in atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 2006, 26, 2103-2109.
106. Cai, K.; Caruthers, S.D.; Huang, W.; Williams, T.A.; Zhang, H.; Wickline, S.A.; Lanza, G.M.; Winter, P.M. Mr molecular imaging of aortic angiogenesis. JACC Cardiovasc. Imaging 2010, 3, 824-832.
107. Kerwin, W.S.; O'Brien, K.D.; Ferguson, M.S.; Polissar, N.; Hatsukami, T.S.; Yuan, C. Inflammation in carotid atherosclerotic plaque: A dynamic contrast-enhanced mr imaging study. Radiology 2006, 241, 459-468.
108. Lancelot, E.; Amirbekian, V.; Brigger, I.; Raynaud, J.S.; Ballet, S.; David, C.; Rousseaux, O.; Le Greneur, S.; Port, M.; Lijnen, H.R.; et al. Evaluation of matrix metalloproteinases in atherosclerosis using a novel noninvasive imaging approach. Arterioscler. Thromb. Vasc. Biol. 2008, 28, 425-432.
109. Hyafil, F.; Vucic, E.; Cornily, J.C.; Sharma, R.; Amirbekian, V.; Blackwell, F.; Lancelot, E.; Corot, C.; Fuster, V.; Galis, Z.S.; et al. Monitoring of arterial wall remodelling in atherosclerotic rabbits with a magnetic resonance imaging contrast agent binding to matrix metalloproteinases. Eur. Heart J. 2011, 32, 1561-1571.
110. Ronald, J.A.; Chen, J.W.; Chen, Y.; Hamilton, A.M.; Rodriguez, E.; Reynolds, F.; Hegele, R.A.; Rogers, K.A.; Querol, M.; Bogdanov, A.; et al. Enzyme-sensitive magnetic resonance imaging targeting myeloperoxidase identifies active inflammation in experimental rabbit atherosclerotic plaques. Circulation 2009, 120, 592-599.
111. Yu, X.; Song, S.K.; Chen, J.; Scott, M.J.; Fuhrhop, R.J.; Hall, C.S.; Gaffney, P.J.; Wickline, S.A.; Lanza, G.M. High-resolution mri characterization of human thrombus using a novel fibrin-targeted paramagnetic nanoparticle contrast agent. Magn. Reson. Med. 2000, 44, 867-872.
112. Flacke, S.; Fischer, S.; Scott, M.J.; Fuhrhop, R.J.; Allen, J.S.; McLean, M.; Winter, P.; Sicard, G.A.; Gaffney, P.J.; Wickline, S.A.; et al. Novel mri contrast agent for molecular imaging of fibrin: Implications for detecting vulnerable plaques. Circulation 2001, 104, 1280-1285.
113. Botnar, R.M.; Perez, A.S.; Witte, S.; Wiethoff, A.J.; Laredo, J.; Hamilton, J.; Quist, W.; Parsons, E.C., Jr.; Vaidya, A.; Kolodziej, A.; et al. In vivo molecular imaging of acute and subacute thrombosis using a fibrin-binding magnetic resonance imaging contrast agent. Circulation 2004, 109, 2023-2029.
114. Botnar, R.M.; Buecker, A.; Wiethoff, A.J.; Parsons, E.C., Jr.; Katoh, M.; Katsimaglis, G.; Weisskoff, R.M.; Lauffer, R.B.; Graham, P.B.; Gunther, R.W.; et al. In vivo magnetic resonance imaging of coronary thrombosis using a fibrin-binding molecular magnetic resonance contrast agent. Circulation 2004, 110, 1463-1466.
115. Spuentrup, E.; Buecker, A.; Katoh, M.; Wiethoff, A.J.; Parsons, E.C., Jr.; Botnar, R.M.; Weisskoff, R.M.; Graham, P.B.; Manning, W.J.; Gunther, R.W. Molecular magnetic resonance imaging of coronary thrombosis and pulmonary emboli with a novel fibrin-targeted contrast agent. Circulation 2005, 111, 1377-1382.
116. Makowski, M.R.; Forbes, S.C.; Blume, U.; Warley, A.; Jansen, C.H.; Schuster, A.; Wiethoff, A.J.; Botnar, R.M. In vivo assessment of intraplaque and endothelial fibrin in apoe(-/-) mice by molecular mri. Atherosclerosis 2012, 222, 43-49.
117. Spuentrup, E.; Botnar, R.M.; Wiethoff, A.; Ibrahim, T.; Sebastin, K.; Katho, M.; Oezgun, M.; Nagel, E.; Vymazal, J.; Graham, P.; et al. Mr imaging of thrombi using ep-2104r, a fibrin specific contrast agent: Initial results in patients. European Radiol. 2008, 18, 1995-2005.
118. Sirol, M.; Moreno, P.; Purushothaman, K.; Vucic, E.; Amirbekian, V.; Weinmann, H.; Muntner, P.; Fuster, V.; Fayad, Z. Increased neovascularization in advanced lipid-rich atherosclerotic lesions detected by gadofluorine-m-enhanced mri: Implications for plaque vulnerability. Circ. Cardiovasc. Imaging 2009, 2, 391-396.
119. Frias, J.C.; Williams, K.J.; Fisher, E.A.; Fayad, Z.A. Recombinant hdl-like nanoparticles: A specific contrast agent for mri of atherosclerotic plaques. J. Am. Chem. Soc. 2004, 126, 16316-16317.
120. Chen, W.; Vucic, E.; Leupold, E.; Mulder, W.J.; Cormode, D.P.; Briley-Saebo, K.C.; Barazza, A.; Fisher, E.A.; Dathe, M.; Fayad, Z.A. Incorporation of an apoe-derived lipopeptide in high-density lipoprotein mri contrast agents for enhanced imaging of macrophages in atherosclerosis. Contrast Media Mol. Imaging 2008, 3, 233-242.
121. Winter, P.M.; Morawski, A.M.; Caruthers, S.D.; Fuhrhop, R.W.; Zhang, H.; Williams, T.A.; Allen, J.S.; Lacy, E.K.; Robertson, J.D.; Lanza, G.M.; et al. Molecular imaging of angiogenesis in early-stage atherosclerosis with alpha(v)beta3-integrin-targeted nanoparticles. Circulation 2003, 108, 2270-2274.