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Published in: The International Journal of Cardiovascular Imaging 4/2010

01-04-2010 | Review

Recent developments and new perspectives on imaging of atherosclerotic plaque: role of anatomical, cellular and molecular MRI Part I and II

Authors: Bernard C. M. te Boekhorst, Maarten J. Cramer, Gerard Pasterkamp, Cees J. A. van Echteld, Pieter A. F. M. Doevendans

Published in: The International Journal of Cardiovascular Imaging | Issue 4/2010

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Abstract

Atherosclerotic plaque disruption accounts for the major part of cardiovascular mortality and the risk of disruption appears to depend on plaque composition. Carotid plaques in patients, scheduled for endarterectomy, have been successfully characterised with MRI. MRI has the advantage of combining information about morphology and function. Unfortunately, the tortuosity and size of the coronary arteries, and the respiratory and cardiac motion hinder the in vivo characterisation of human coronary plaque. In addition to plaque composition several molecular markers of the different processes involved in atherosclerosis, such as integrins, matrix metalloproteinases and fibrin seem to correlate with risk of plaque rupture and clinical outcome. These molecular markers can be targeted with antibodies coupled to carriers, which are loaded with gadolinium for detection (molecular MRI). Several cellular/molecular MRI studies in animal models and some in human patients have been conducted with varying levels of success. The advent of clinical high field magnets, the development of contrast agent carriers with high relaxivity and the development of relatively new MR contrast techniques are promising in the field of plaque imaging. Future MRI studies will have to focus on the molecular target of the atherosclerotic process, which has the highest prognostic value with regard to acute coronary syndromes and on the most suitable contrast agent to visualize that target.
Literature
1.
go back to reference Fayad ZA, Fuster V (2001) Clinical imaging of the high-risk or vulnerable atherosclerotic plaque. Circ Res 89:305–316CrossRefPubMed Fayad ZA, Fuster V (2001) Clinical imaging of the high-risk or vulnerable atherosclerotic plaque. Circ Res 89:305–316CrossRefPubMed
2.
go back to reference Badimon L (2001) Atherosclerosis and thrombosis: lessons from animal models. Thromb Haemost 86:356–365PubMed Badimon L (2001) Atherosclerosis and thrombosis: lessons from animal models. Thromb Haemost 86:356–365PubMed
4.
go back to reference Mitsumori LM, Hatsukami TS, Ferguson MS, Kerwin WS, Cai J, Yuan C (2003) In vivo accuracy of multisequence MR imaging for identifying unstable fibrous caps in advanced human carotid plaques. J Magn Reson Imaging 17:410–420CrossRefPubMed Mitsumori LM, Hatsukami TS, Ferguson MS, Kerwin WS, Cai J, Yuan C (2003) In vivo accuracy of multisequence MR imaging for identifying unstable fibrous caps in advanced human carotid plaques. J Magn Reson Imaging 17:410–420CrossRefPubMed
5.
go back to reference Leiner T, Gerretsen S, Botnar R, Lutgens E, Cappendijk V, Kooi E, van EJ (2005) Magnetic resonance imaging of atherosclerosis. Eur Radiol 15:1087–1099CrossRefPubMed Leiner T, Gerretsen S, Botnar R, Lutgens E, Cappendijk V, Kooi E, van EJ (2005) Magnetic resonance imaging of atherosclerosis. Eur Radiol 15:1087–1099CrossRefPubMed
6.
go back to reference Vink A, Pasterkamp G (2002) Atherosclerotic plaque burden, plaque vulnerability and arterial remodeling: the role of inflammation. Minerva Cardioangiol 50:75–83PubMed Vink A, Pasterkamp G (2002) Atherosclerotic plaque burden, plaque vulnerability and arterial remodeling: the role of inflammation. Minerva Cardioangiol 50:75–83PubMed
7.
go back to reference Corti R, Fuster V (2003) New understanding, diagnosis, and prognosis of atherothrombosis and the role of imaging. Am J Cardiol 91:17A–26ACrossRefPubMed Corti R, Fuster V (2003) New understanding, diagnosis, and prognosis of atherothrombosis and the role of imaging. Am J Cardiol 91:17A–26ACrossRefPubMed
8.
go back to reference Ambrose JA, Tannenbaum MA, Alexopoulos D, Hjemdahl-Monsen CE, Leavy J, Weiss M, Borrico S, Gorlin R, Fuster V (1988) Angiographic progression of coronary artery disease and the development of myocardial infarction. J Am Coll Cardiol 12:56–62PubMedCrossRef Ambrose JA, Tannenbaum MA, Alexopoulos D, Hjemdahl-Monsen CE, Leavy J, Weiss M, Borrico S, Gorlin R, Fuster V (1988) Angiographic progression of coronary artery disease and the development of myocardial infarction. J Am Coll Cardiol 12:56–62PubMedCrossRef
9.
go back to reference de Korte CL, Pasterkamp G, van der Steen AF, Woutman HA, Bom N (2000) Characterization of plaque components with intravascular ultrasound elastography in human femoral and coronary arteries in vitro. Circulation 102:617–623PubMed de Korte CL, Pasterkamp G, van der Steen AF, Woutman HA, Bom N (2000) Characterization of plaque components with intravascular ultrasound elastography in human femoral and coronary arteries in vitro. Circulation 102:617–623PubMed
10.
go back to reference Jang IK, Tearney GJ, MacNeill B, Takano M, Moselewski F, Iftima N, Shishkov M, Houser S, Aretz HT, Halpern EF, Bouma BE (2005) In vivo characterization of coronary atherosclerotic plaque by use of optical coherence tomography. Circulation 111:1551–1555CrossRefPubMed Jang IK, Tearney GJ, MacNeill B, Takano M, Moselewski F, Iftima N, Shishkov M, Houser S, Aretz HT, Halpern EF, Bouma BE (2005) In vivo characterization of coronary atherosclerotic plaque by use of optical coherence tomography. Circulation 111:1551–1555CrossRefPubMed
11.
go back to reference van de Poll SW, Kastelijn K, Bakker Schut TC, Strijder C, Pasterkamp G, Puppels GJ, van der LA (2003) On-line detection of cholesterol and calcification by catheter based Raman spectroscopy in human atherosclerotic plaque ex vivo. Heart 89:1078–1082CrossRefPubMed van de Poll SW, Kastelijn K, Bakker Schut TC, Strijder C, Pasterkamp G, Puppels GJ, van der LA (2003) On-line detection of cholesterol and calcification by catheter based Raman spectroscopy in human atherosclerotic plaque ex vivo. Heart 89:1078–1082CrossRefPubMed
12.
go back to reference Wang J, Geng YJ, Guo B, Klima T, Lal BN, Willerson JT, Casscells W (2002) Near-infrared spectroscopic characterization of human advanced atherosclerotic plaques. J Am Coll Cardiol 39:1305–1313CrossRefPubMed Wang J, Geng YJ, Guo B, Klima T, Lal BN, Willerson JT, Casscells W (2002) Near-infrared spectroscopic characterization of human advanced atherosclerotic plaques. J Am Coll Cardiol 39:1305–1313CrossRefPubMed
13.
go back to reference Toutouzas K, Drakopoulou M, Mitropoulos J, Tsiamis E, Vaina S, Vavuranakis M, Markou V, Bosinakou E, Stefanadis C (2006) Elevated plaque temperature in non-culprit de novo atheromatous lesions of patients with acute coronary syndromes. J Am Coll Cardiol 47:301–306CrossRefPubMed Toutouzas K, Drakopoulou M, Mitropoulos J, Tsiamis E, Vaina S, Vavuranakis M, Markou V, Bosinakou E, Stefanadis C (2006) Elevated plaque temperature in non-culprit de novo atheromatous lesions of patients with acute coronary syndromes. J Am Coll Cardiol 47:301–306CrossRefPubMed
14.
go back to reference Waki H, Masuyama T, Mori H, Maeda T, Kitade K, Moriyasu K, Tsujimoto M, Fujimoto K, Koshimae N, Matsuura N (2003) Ultrasonic tissue characterization of the atherosclerotic carotid artery: histological correlates or carotid integrated backscatter. Circ J 67:1013–1016CrossRefPubMed Waki H, Masuyama T, Mori H, Maeda T, Kitade K, Moriyasu K, Tsujimoto M, Fujimoto K, Koshimae N, Matsuura N (2003) Ultrasonic tissue characterization of the atherosclerotic carotid artery: histological correlates or carotid integrated backscatter. Circ J 67:1013–1016CrossRefPubMed
15.
go back to reference Leber AW, Knez A, von ZF, Becker A, Nikolaou K, Paul S, Wintersperger B, Reiser M, Becker CR, Steinbeck G, Boekstegers P (2005) Quantification of obstructive and nonobstructive coronary lesions by 64-slice computed tomography: a comparative study with quantitative coronary angiography and intravascular ultrasound. J Am Coll Cardiol 46:147–154CrossRefPubMed Leber AW, Knez A, von ZF, Becker A, Nikolaou K, Paul S, Wintersperger B, Reiser M, Becker CR, Steinbeck G, Boekstegers P (2005) Quantification of obstructive and nonobstructive coronary lesions by 64-slice computed tomography: a comparative study with quantitative coronary angiography and intravascular ultrasound. J Am Coll Cardiol 46:147–154CrossRefPubMed
16.
go back to reference Ben-Haim S, Israel O (2006) PET/CT for atherosclerotic plaque imaging. J Nucl Med Mol Imaging 50:53–60 Ben-Haim S, Israel O (2006) PET/CT for atherosclerotic plaque imaging. J Nucl Med Mol Imaging 50:53–60
17.
go back to reference Choudhury RP, Fisher EA (2009) Molecular imaging in atherosclerosis, thrombosis, and vascular inflammation. Arterioscler Thromb Vasc Biol 29:983–991CrossRefPubMed Choudhury RP, Fisher EA (2009) Molecular imaging in atherosclerosis, thrombosis, and vascular inflammation. Arterioscler Thromb Vasc Biol 29:983–991CrossRefPubMed
18.
go back to reference Thompson BH, Stanford W (2005) Update on using coronary calcium screening by computed tomography to measure risk for coronary heart disease. Int J Cardiovasc Imaging 21:39–53CrossRefPubMed Thompson BH, Stanford W (2005) Update on using coronary calcium screening by computed tomography to measure risk for coronary heart disease. Int J Cardiovasc Imaging 21:39–53CrossRefPubMed
19.
go back to reference Dey D, Slomka P, Chien D, Fieno D, Abidov A, Saouaf R, Thomson L, Friedman JD, Berman DS (2006) Direct quantitative in vivo comparison of calcified atherosclerotic plaque on vascular MRI and CT by multimodality image registration. J Magn Reson Imaging 23:345–354CrossRefPubMed Dey D, Slomka P, Chien D, Fieno D, Abidov A, Saouaf R, Thomson L, Friedman JD, Berman DS (2006) Direct quantitative in vivo comparison of calcified atherosclerotic plaque on vascular MRI and CT by multimodality image registration. J Magn Reson Imaging 23:345–354CrossRefPubMed
20.
go back to reference Viles-Gonzalez JF, Poon M, Sanz J, Rius T, Nikolaou K, Fayad ZA, Fuster V, Badimon JJ (2004) In vivo 16-slice, multidetector-row computed tomography for the assessment of experimental atherosclerosis: comparison with magnetic resonance imaging and histopathology. Circulation 110:1467–1472CrossRefPubMed Viles-Gonzalez JF, Poon M, Sanz J, Rius T, Nikolaou K, Fayad ZA, Fuster V, Badimon JJ (2004) In vivo 16-slice, multidetector-row computed tomography for the assessment of experimental atherosclerosis: comparison with magnetic resonance imaging and histopathology. Circulation 110:1467–1472CrossRefPubMed
21.
go back to reference Leber AW, Becker A, Knez A, Von ZF, Sirol M, Nikolaou K, Ohnesorge B, Fayad ZA, Becker CR, Reiser M, Steinbeck G, Boekstegers P (2006) Accuracy of 64-slice computed tomography to classify and quantify plaque volumes in the proximal coronary system: a comparative study using intravascular ultrasound. J Am Coll Cardiol 47:672–677CrossRefPubMed Leber AW, Becker A, Knez A, Von ZF, Sirol M, Nikolaou K, Ohnesorge B, Fayad ZA, Becker CR, Reiser M, Steinbeck G, Boekstegers P (2006) Accuracy of 64-slice computed tomography to classify and quantify plaque volumes in the proximal coronary system: a comparative study using intravascular ultrasound. J Am Coll Cardiol 47:672–677CrossRefPubMed
22.
go back to reference Kolodgie FD, Petrov A, Virmani R, Narula N, Verjans JW, Weber DK, Hartung D, Steinmetz N, Vanderheyden JL, Vannan MA, Gold HK, Reutelingsperger CP, Hofstra L, Narula J (2003) Targeting of apoptotic macrophages and experimental atheroma with radiolabeled annexin V: a technique with potential for noninvasive imaging of vulnerable plaque. Circulation 108:3134–3139CrossRefPubMed Kolodgie FD, Petrov A, Virmani R, Narula N, Verjans JW, Weber DK, Hartung D, Steinmetz N, Vanderheyden JL, Vannan MA, Gold HK, Reutelingsperger CP, Hofstra L, Narula J (2003) Targeting of apoptotic macrophages and experimental atheroma with radiolabeled annexin V: a technique with potential for noninvasive imaging of vulnerable plaque. Circulation 108:3134–3139CrossRefPubMed
23.
go back to reference Tsimikas S, Shortal BP, Witztum JL, Palinski W (2000) In vivo uptake of radiolabeled MDA2, an oxidation-specific monoclonal antibody, provides an accurate measure of atherosclerotic lesions rich in oxidized LDL and is highly sensitive to their regression. Arterioscler Thromb Vasc Biol 20:689–697PubMed Tsimikas S, Shortal BP, Witztum JL, Palinski W (2000) In vivo uptake of radiolabeled MDA2, an oxidation-specific monoclonal antibody, provides an accurate measure of atherosclerotic lesions rich in oxidized LDL and is highly sensitive to their regression. Arterioscler Thromb Vasc Biol 20:689–697PubMed
24.
go back to reference Rudd JH, Myers KS, Bansilal S, Machac J, Pinto CA, Tong C, Rafique A, Hargeaves R, Farkouh M, Fuster V, Fayad ZA (2008) Atherosclerosis inflammation imaging with 18F-FDG PET: carotid, iliac, and femoral uptake reproducibility, quantification methods, and recommendations. J Nucl Med 49:871–878CrossRefPubMed Rudd JH, Myers KS, Bansilal S, Machac J, Pinto CA, Tong C, Rafique A, Hargeaves R, Farkouh M, Fuster V, Fayad ZA (2008) Atherosclerosis inflammation imaging with 18F-FDG PET: carotid, iliac, and femoral uptake reproducibility, quantification methods, and recommendations. J Nucl Med 49:871–878CrossRefPubMed
25.
go back to reference Massoud TF, Gambhir SS (2003) Molecular imaging in living subjects: seeing fundamental biological processes in a new light. Genes Dev 17:545–580CrossRefPubMed Massoud TF, Gambhir SS (2003) Molecular imaging in living subjects: seeing fundamental biological processes in a new light. Genes Dev 17:545–580CrossRefPubMed
26.
go back to reference Hockings PD, Roberts T, Galloway GJ, Reid DG, Harris DA, Vidgeon-Hart M, Groot PH, Suckling KE, Benson GM (2002) Repeated three-dimensional magnetic resonance imaging of atherosclerosis development in innominate arteries of low-density lipoprotein receptor-knockout mice. Circulation 106:1716–1721CrossRefPubMed Hockings PD, Roberts T, Galloway GJ, Reid DG, Harris DA, Vidgeon-Hart M, Groot PH, Suckling KE, Benson GM (2002) Repeated three-dimensional magnetic resonance imaging of atherosclerosis development in innominate arteries of low-density lipoprotein receptor-knockout mice. Circulation 106:1716–1721CrossRefPubMed
27.
go back to reference Booth RF, Honey AC, Martin JF, Lindon JC, Farrant RD, Carpenter TA, Hall LD (1990) Lipid characterization in an animal model of atherosclerosis using NMR spectroscopy and imaging. NMR Biomed 3:95–100CrossRefPubMed Booth RF, Honey AC, Martin JF, Lindon JC, Farrant RD, Carpenter TA, Hall LD (1990) Lipid characterization in an animal model of atherosclerosis using NMR spectroscopy and imaging. NMR Biomed 3:95–100CrossRefPubMed
28.
go back to reference Vinitski S, Consigny PM, Shapiro MJ, Janes N, Smullens SN, Rifkin MD (1991) Magnetic resonance chemical shift imaging and spectroscopy of atherosclerotic plaque. Invest Radiol 26:703–714CrossRefPubMed Vinitski S, Consigny PM, Shapiro MJ, Janes N, Smullens SN, Rifkin MD (1991) Magnetic resonance chemical shift imaging and spectroscopy of atherosclerotic plaque. Invest Radiol 26:703–714CrossRefPubMed
29.
go back to reference Toussaint JF, Southern JF, Fuster V, Kantor HL (1995) T2-weighted contrast for NMR characterization of human atherosclerosis. Arterioscler Thromb Vasc Biol 15:1533–1542PubMed Toussaint JF, Southern JF, Fuster V, Kantor HL (1995) T2-weighted contrast for NMR characterization of human atherosclerosis. Arterioscler Thromb Vasc Biol 15:1533–1542PubMed
30.
go back to reference Toussaint JF, LaMuraglia GM, Southern JF, Fuster V, Kantor HL (1996) Magnetic resonance images lipid, fibrous, calcified, hemorrhagic, and thrombotic components of human atherosclerosis in vivo. Circulation 94:932–938PubMed Toussaint JF, LaMuraglia GM, Southern JF, Fuster V, Kantor HL (1996) Magnetic resonance images lipid, fibrous, calcified, hemorrhagic, and thrombotic components of human atherosclerosis in vivo. Circulation 94:932–938PubMed
31.
go back to reference Shinnar M, Fallon JT, Wehrli S, Levin M, Dalmacy D, Fayad ZA, Badimon JJ, Harrington M, Harrington E, Fuster V (1999) The diagnostic accuracy of ex vivo MRI for human atherosclerotic plaque characterization. Arterioscler Thromb Vasc Biol 19:2756–2761PubMed Shinnar M, Fallon JT, Wehrli S, Levin M, Dalmacy D, Fayad ZA, Badimon JJ, Harrington M, Harrington E, Fuster V (1999) The diagnostic accuracy of ex vivo MRI for human atherosclerotic plaque characterization. Arterioscler Thromb Vasc Biol 19:2756–2761PubMed
32.
go back to reference Toussaint JF, Southern JF, Fuster V, Kantor HL (1997) Water diffusion properties of human atherosclerosis and thrombosis measured by pulse field gradient nuclear magnetic resonance. Arterioscler Thromb Vasc Biol 17:542–546PubMed Toussaint JF, Southern JF, Fuster V, Kantor HL (1997) Water diffusion properties of human atherosclerosis and thrombosis measured by pulse field gradient nuclear magnetic resonance. Arterioscler Thromb Vasc Biol 17:542–546PubMed
33.
go back to reference Rogers WJ, Prichard JW, Hu YL, Olson PR, Benckart DH, Kramer CM, Vido DA, Reichek N (2000) Characterization of signal properties in atherosclerotic plaque components by intravascular MRI. Arterioscler Thromb Vasc Biol 20:1824–1830PubMed Rogers WJ, Prichard JW, Hu YL, Olson PR, Benckart DH, Kramer CM, Vido DA, Reichek N (2000) Characterization of signal properties in atherosclerotic plaque components by intravascular MRI. Arterioscler Thromb Vasc Biol 20:1824–1830PubMed
34.
go back to reference Schneider JE, McAteer MA, Tyler DJ, Clarke K, Channon KM, Choudhury RP, Neubauer S (2004) High-resolution, multicontrast three-dimensional-MRI characterizes atherosclerotic plaque composition in ApoE-/- mice ex vivo. J Magn Reson Imaging 20:981–989CrossRefPubMed Schneider JE, McAteer MA, Tyler DJ, Clarke K, Channon KM, Choudhury RP, Neubauer S (2004) High-resolution, multicontrast three-dimensional-MRI characterizes atherosclerotic plaque composition in ApoE-/- mice ex vivo. J Magn Reson Imaging 20:981–989CrossRefPubMed
35.
go back to reference Schneiderman J, Wilensky RL, Weiss A, Samouha E, Muchnik L, Chen-Zion M, Ilovitch M, Golan E, Blank A, Flugelman M, Rozenman Y, Virmani R (2005) Diagnosis of thin-cap fibroatheromas by a self-contained intravascular magnetic resonance imaging probe in ex vivo human aortas and in situ coronary arteries. J Am Coll Cardiol 45:1961–1969CrossRefPubMed Schneiderman J, Wilensky RL, Weiss A, Samouha E, Muchnik L, Chen-Zion M, Ilovitch M, Golan E, Blank A, Flugelman M, Rozenman Y, Virmani R (2005) Diagnosis of thin-cap fibroatheromas by a self-contained intravascular magnetic resonance imaging probe in ex vivo human aortas and in situ coronary arteries. J Am Coll Cardiol 45:1961–1969CrossRefPubMed
36.
go back to reference MacNeill BD, Lowe HC, Takano M, Fuster V, Jang IK (2003) Intravascular modalities for detection of vulnerable plaque: current status. Arterioscler Thromb Vasc Biol 23:1333–1342CrossRefPubMed MacNeill BD, Lowe HC, Takano M, Fuster V, Jang IK (2003) Intravascular modalities for detection of vulnerable plaque: current status. Arterioscler Thromb Vasc Biol 23:1333–1342CrossRefPubMed
37.
go back to reference Correia LC, Atalar E, Kelemen MD, Ocali O, Hutchins GM, Fleg JL, Gerstenblith G, Zerhouni EA, Lima JA (1997) Intravascular magnetic resonance imaging of aortic atherosclerotic plaque composition. Arterioscler Thromb Vasc Biol 17:3626–3632PubMed Correia LC, Atalar E, Kelemen MD, Ocali O, Hutchins GM, Fleg JL, Gerstenblith G, Zerhouni EA, Lima JA (1997) Intravascular magnetic resonance imaging of aortic atherosclerotic plaque composition. Arterioscler Thromb Vasc Biol 17:3626–3632PubMed
38.
go back to reference Larose E, Yeghiazarians Y, Libby P, Yucel EK, Aikawa M, Kacher DF, Aikawa E, Kinlay S, Schoen FJ, Selwyn AP, Ganz P (2005) Characterization of human atherosclerotic plaques by intravascular magnetic resonance imaging. Circulation 112:2324–2331CrossRefPubMed Larose E, Yeghiazarians Y, Libby P, Yucel EK, Aikawa M, Kacher DF, Aikawa E, Kinlay S, Schoen FJ, Selwyn AP, Ganz P (2005) Characterization of human atherosclerotic plaques by intravascular magnetic resonance imaging. Circulation 112:2324–2331CrossRefPubMed
39.
go back to reference Larose E, Kinlay S, Selwyn AP, Yeghiazarians Y, Yucel EK, Kacher DF, Libby P, Ganz P (2008) Improved characterization of atherosclerotic plaques by gadolinium contrast during intravascular magnetic resonance imaging of human arteries. Atherosclerosis 196:919–925CrossRefPubMed Larose E, Kinlay S, Selwyn AP, Yeghiazarians Y, Yucel EK, Kacher DF, Libby P, Ganz P (2008) Improved characterization of atherosclerotic plaques by gadolinium contrast during intravascular magnetic resonance imaging of human arteries. Atherosclerosis 196:919–925CrossRefPubMed
40.
go back to reference Cappendijk VC, Cleutjens KB, Kessels AG, Heeneman S, Schurink GW, Welten RJ, Mess WH, Daemen MJ, van Engelshoven JM, Kooi ME (2005) Assessment of human atherosclerotic carotid plaque components with multisequence MR imaging: initial experience. Radiology 234:487–492CrossRefPubMed Cappendijk VC, Cleutjens KB, Kessels AG, Heeneman S, Schurink GW, Welten RJ, Mess WH, Daemen MJ, van Engelshoven JM, Kooi ME (2005) Assessment of human atherosclerotic carotid plaque components with multisequence MR imaging: initial experience. Radiology 234:487–492CrossRefPubMed
41.
go back to reference Cappendijk VC, Heeneman S, Kessels AG, Cleutjens KB, Schurink GW, Welten RJ, Mess WH, van Suylen RJ, Leiner T, Daemen MJ, van Engelshoven JM, Kooi ME (2008) Comparison of single-sequence T1w TFE MRI with multisequence MRI for the quantification of lipid-rich necrotic core in atherosclerotic plaque. J Magn Reson Imaging 27:1347–1355CrossRefPubMed Cappendijk VC, Heeneman S, Kessels AG, Cleutjens KB, Schurink GW, Welten RJ, Mess WH, van Suylen RJ, Leiner T, Daemen MJ, van Engelshoven JM, Kooi ME (2008) Comparison of single-sequence T1w TFE MRI with multisequence MRI for the quantification of lipid-rich necrotic core in atherosclerotic plaque. J Magn Reson Imaging 27:1347–1355CrossRefPubMed
42.
go back to reference Luo Y, Polissar N, Han C, Yarnykh V, Kerwin WS, Hatsukami TS, Yuan C (2003) Accuracy and uniqueness of three in vivo measurements of atherosclerotic carotid plaque morphology with black blood MRI. Magn Reson Med 50:75–82CrossRefPubMed Luo Y, Polissar N, Han C, Yarnykh V, Kerwin WS, Hatsukami TS, Yuan C (2003) Accuracy and uniqueness of three in vivo measurements of atherosclerotic carotid plaque morphology with black blood MRI. Magn Reson Med 50:75–82CrossRefPubMed
43.
go back to reference Cai JM, Hatsukami TS, Ferguson MS, Small R, Polissar NL, Yuan C (2002) Classification of human carotid atherosclerotic lesions with in vivo multicontrast magnetic resonance imaging. Circulation 106:1368–1373CrossRefPubMed Cai JM, Hatsukami TS, Ferguson MS, Small R, Polissar NL, Yuan C (2002) Classification of human carotid atherosclerotic lesions with in vivo multicontrast magnetic resonance imaging. Circulation 106:1368–1373CrossRefPubMed
44.
go back to reference Cai J, Hatsukami TS, Ferguson MS, Kerwin WS, Saam T, Chu B, Takaya N, Polissar NL, Yuan C (2005) In vivo quantitative measurement of intact fibrous cap and lipid-rich necrotic core size in atherosclerotic carotid plaque: comparison of high-resolution, contrast-enhanced magnetic resonance imaging and histology. Circulation 112:3437–3444CrossRefPubMed Cai J, Hatsukami TS, Ferguson MS, Kerwin WS, Saam T, Chu B, Takaya N, Polissar NL, Yuan C (2005) In vivo quantitative measurement of intact fibrous cap and lipid-rich necrotic core size in atherosclerotic carotid plaque: comparison of high-resolution, contrast-enhanced magnetic resonance imaging and histology. Circulation 112:3437–3444CrossRefPubMed
45.
go back to reference Chu B, Kampschulte A, Ferguson MS, Kerwin WS, Yarnykh VL, O’Brien KD, Polissar NL, Hatsukami TS, Yuan C (2004) Hemorrhage in the atherosclerotic carotid plaque: a high-resolution MRI study. Stroke 35:1079–1084CrossRefPubMed Chu B, Kampschulte A, Ferguson MS, Kerwin WS, Yarnykh VL, O’Brien KD, Polissar NL, Hatsukami TS, Yuan C (2004) Hemorrhage in the atherosclerotic carotid plaque: a high-resolution MRI study. Stroke 35:1079–1084CrossRefPubMed
46.
go back to reference Yuan C, Mitsumori LM, Ferguson MS, Polissar NL, Echelard D, Ortiz G, Small R, Davies JW, Kerwin WS, Hatsukami TS (2001) In vivo accuracy of multispectral magnetic resonance imaging for identifying lipid-rich necrotic cores and intraplaque hemorrhage in advanced human carotid plaques. Circulation 104:2051–2056CrossRefPubMed Yuan C, Mitsumori LM, Ferguson MS, Polissar NL, Echelard D, Ortiz G, Small R, Davies JW, Kerwin WS, Hatsukami TS (2001) In vivo accuracy of multispectral magnetic resonance imaging for identifying lipid-rich necrotic cores and intraplaque hemorrhage in advanced human carotid plaques. Circulation 104:2051–2056CrossRefPubMed
47.
go back to reference Saam T, Hatsukami TS, Takaya N, Chu B, Underhill H, Kerwin WS, Cai J, Ferguson MS, Yuan C (2007) The vulnerable, or high-risk, atherosclerotic plaque: noninvasive MR imaging for characterization and assessment. Radiology 244:64–77CrossRefPubMed Saam T, Hatsukami TS, Takaya N, Chu B, Underhill H, Kerwin WS, Cai J, Ferguson MS, Yuan C (2007) The vulnerable, or high-risk, atherosclerotic plaque: noninvasive MR imaging for characterization and assessment. Radiology 244:64–77CrossRefPubMed
48.
go back to reference Ota H, Yu W, Underhill HR, Oikawa M, Dong L, Zhao X, Polissar NL, Neradilek B, Gao T, Zhang Z, Yan Z, Guo M, Zhang Z, Hatsukami TS, Yuan C (2009) Hemorrhage and large lipid-rich necrotic cores are independently associated with thin or ruptured fibrous caps: an in vivo 3T MRI study. Arterioscl Thromb Vasc Biol 29:1696–1701CrossRefPubMed Ota H, Yu W, Underhill HR, Oikawa M, Dong L, Zhao X, Polissar NL, Neradilek B, Gao T, Zhang Z, Yan Z, Guo M, Zhang Z, Hatsukami TS, Yuan C (2009) Hemorrhage and large lipid-rich necrotic cores are independently associated with thin or ruptured fibrous caps: an in vivo 3T MRI study. Arterioscl Thromb Vasc Biol 29:1696–1701CrossRefPubMed
49.
go back to reference Yuan C, Zhang SX, Polissar NL, Echelard D, Ortiz G, Davis JW, Ellington E, Ferguson MS, Hatsukami TS (2002) Identification of fibrous cap rupture with magnetic resonance imaging is highly associated with recent transient ischemic attack or stroke. Circulation 105:181–185CrossRefPubMed Yuan C, Zhang SX, Polissar NL, Echelard D, Ortiz G, Davis JW, Ellington E, Ferguson MS, Hatsukami TS (2002) Identification of fibrous cap rupture with magnetic resonance imaging is highly associated with recent transient ischemic attack or stroke. Circulation 105:181–185CrossRefPubMed
50.
go back to reference Takaya N, Yuan C, Chu B, Saam T, Polissar NL, Jarvik GP, Isaac C, McDonough J, Natiello C, Small R, Ferguson MS, Hatsukami TS (2005) Presence of intraplaque hemorrhage stimulates progression of carotid atherosclerotic plaques: a high-resolution magnetic resonance imaging study. Circulation 111:2768–2775CrossRefPubMed Takaya N, Yuan C, Chu B, Saam T, Polissar NL, Jarvik GP, Isaac C, McDonough J, Natiello C, Small R, Ferguson MS, Hatsukami TS (2005) Presence of intraplaque hemorrhage stimulates progression of carotid atherosclerotic plaques: a high-resolution magnetic resonance imaging study. Circulation 111:2768–2775CrossRefPubMed
51.
go back to reference Kampschulte A, Ferguson MS, Kerwin WS, Polissar NL, Chu B, Saam T, Hatsukami TS, Yuan C (2004) Differentiation of intraplaque versus juxtaluminal hemorrhage/thrombus in advanced human carotid atherosclerotic lesions by in vivo magnetic resonance imaging. Circulation 110:3239–3244CrossRefPubMed Kampschulte A, Ferguson MS, Kerwin WS, Polissar NL, Chu B, Saam T, Hatsukami TS, Yuan C (2004) Differentiation of intraplaque versus juxtaluminal hemorrhage/thrombus in advanced human carotid atherosclerotic lesions by in vivo magnetic resonance imaging. Circulation 110:3239–3244CrossRefPubMed
52.
go back to reference Corti R, Osende JI, Fayad ZA, Fallon JT, Fuster V, Mizsei G, Dickstein E, Drayer B, Badimon JJ (2002) In vivo noninvasive detection and age definition of arterial thrombus by MRI. J Am Coll Cardiol 39:1366–1373CrossRefPubMed Corti R, Osende JI, Fayad ZA, Fallon JT, Fuster V, Mizsei G, Dickstein E, Drayer B, Badimon JJ (2002) In vivo noninvasive detection and age definition of arterial thrombus by MRI. J Am Coll Cardiol 39:1366–1373CrossRefPubMed
53.
go back to reference Zhang SH, Reddick RL, Piedrahita JA, Maeda N (1992) Spontaneous hypercholesterolemia and arterial lesions in mice lacking apolipoprotein E. Science 258:468–471CrossRefPubMed Zhang SH, Reddick RL, Piedrahita JA, Maeda N (1992) Spontaneous hypercholesterolemia and arterial lesions in mice lacking apolipoprotein E. Science 258:468–471CrossRefPubMed
54.
go back to reference Lutgens E, Daemen M, Kockx M, Doevendans P, Hofker M, Havekes L, Wellens H, de Muinck ED (1999) Atherosclerosis in APOE*3-Leiden transgenic mice: from proliferative to atheromatous stage. Circulation 99:276–283PubMed Lutgens E, Daemen M, Kockx M, Doevendans P, Hofker M, Havekes L, Wellens H, de Muinck ED (1999) Atherosclerosis in APOE*3-Leiden transgenic mice: from proliferative to atheromatous stage. Circulation 99:276–283PubMed
55.
go back to reference Kuhlencordt PJ, Gyurko R, Han F, Scherrer-Crosbie M, Aretz TH, Hajjar R, Picard MH, Huang PL (2001) Accelerated atherosclerosis, aortic aneurysm formation, and ischemic heart disease in apolipoprotein E/endothelial nitric oxide synthase double-knockout mice. Circulation 104:448–454CrossRefPubMed Kuhlencordt PJ, Gyurko R, Han F, Scherrer-Crosbie M, Aretz TH, Hajjar R, Picard MH, Huang PL (2001) Accelerated atherosclerosis, aortic aneurysm formation, and ischemic heart disease in apolipoprotein E/endothelial nitric oxide synthase double-knockout mice. Circulation 104:448–454CrossRefPubMed
56.
go back to reference Fayad ZA, Fallon JT, Shinnar M, Wehrli S, Dansky HM, Poon M, Badimon JJ, Charlton SA, Fisher EA, Breslow JL, Fuster V (1998) Noninvasive In vivo high-resolution magnetic resonance imaging of atherosclerotic lesions in genetically engineered mice. Circulation 98:1541–1547PubMed Fayad ZA, Fallon JT, Shinnar M, Wehrli S, Dansky HM, Poon M, Badimon JJ, Charlton SA, Fisher EA, Breslow JL, Fuster V (1998) Noninvasive In vivo high-resolution magnetic resonance imaging of atherosclerotic lesions in genetically engineered mice. Circulation 98:1541–1547PubMed
57.
go back to reference Wiesmann F, Szimtenings M, Frydrychowicz A, Illinger R, Hunecke A, Rommel E, Neubauer S, Haase A (2003) High-resolution MRI with cardiac and respiratory gating allows for accurate in vivo atherosclerotic plaque visualization in the murine aortic arch. Magn Reson Med 50:69–74CrossRefPubMed Wiesmann F, Szimtenings M, Frydrychowicz A, Illinger R, Hunecke A, Rommel E, Neubauer S, Haase A (2003) High-resolution MRI with cardiac and respiratory gating allows for accurate in vivo atherosclerotic plaque visualization in the murine aortic arch. Magn Reson Med 50:69–74CrossRefPubMed
58.
go back to reference Itskovich VV, Choudhury RP, Aguinaldo JG, Fallon JT, Omerhodzic S, Fisher EA, Fayad ZA (2003) Characterization of aortic root atherosclerosis in ApoE knockout mice: high-resolution in vivo and ex vivo MRM with histological correlation. Magn Reson Med 49:381–385CrossRefPubMed Itskovich VV, Choudhury RP, Aguinaldo JG, Fallon JT, Omerhodzic S, Fisher EA, Fayad ZA (2003) Characterization of aortic root atherosclerosis in ApoE knockout mice: high-resolution in vivo and ex vivo MRM with histological correlation. Magn Reson Med 49:381–385CrossRefPubMed
59.
go back to reference Choudhury RP, Aguinaldo JG, Rong JX, Kulak JL, Kulak AR, Reis ED, Fallon JT, Fuster V, Fisher EA, Fayad ZA (2002) Atherosclerotic lesions in genetically modified mice quantified in vivo by non-invasive high-resolution magnetic resonance microscopy. Atherosclerosis 162:315–321CrossRefPubMed Choudhury RP, Aguinaldo JG, Rong JX, Kulak JL, Kulak AR, Reis ED, Fallon JT, Fuster V, Fisher EA, Fayad ZA (2002) Atherosclerotic lesions in genetically modified mice quantified in vivo by non-invasive high-resolution magnetic resonance microscopy. Atherosclerosis 162:315–321CrossRefPubMed
60.
go back to reference Weiss RG (2001) Imaging the murine cardiovascular system with magnetic resonance. Circ Res 88:550–551PubMed Weiss RG (2001) Imaging the murine cardiovascular system with magnetic resonance. Circ Res 88:550–551PubMed
61.
go back to reference Wehrens XH, Kirchhoff S, Doevendans PA (2000) Mouse electrocardiography: an interval of 30 years. Cardiovasc Res 45:231–237CrossRefPubMed Wehrens XH, Kirchhoff S, Doevendans PA (2000) Mouse electrocardiography: an interval of 30 years. Cardiovasc Res 45:231–237CrossRefPubMed
62.
go back to reference Wendt M, Wacker FK (2000) Visualization, tracking, and navigation of instruments for magnetic resonance imaging-guided endovascular procedures. Top Magn Reson Imaging 11:163–172CrossRefPubMed Wendt M, Wacker FK (2000) Visualization, tracking, and navigation of instruments for magnetic resonance imaging-guided endovascular procedures. Top Magn Reson Imaging 11:163–172CrossRefPubMed
63.
go back to reference Kim WY, Stuber M, Bornert P, Kissinger KV, Manning WJ, Botnar RM (2002) Three-dimensional black-blood cardiac magnetic resonance coronary vessel wall imaging detects positive arterial remodeling in patients with nonsignificant coronary artery disease. Circulation 106:296–299CrossRefPubMed Kim WY, Stuber M, Bornert P, Kissinger KV, Manning WJ, Botnar RM (2002) Three-dimensional black-blood cardiac magnetic resonance coronary vessel wall imaging detects positive arterial remodeling in patients with nonsignificant coronary artery disease. Circulation 106:296–299CrossRefPubMed
64.
go back to reference Miao C, Chen S, Macedo R, Lai S, Liu K, Li D, Wasserman BA, Vogel-Claussen J, Lima JA, Bluemke DA (2009) Positive remodeling of the coronary arteries detected by magnetic resonance imaging in an asymptomatic population: MESA (Multi-Ethnic Study of Atherosclerosis). J Am Coll Cardiol 53:1708–1715CrossRefPubMed Miao C, Chen S, Macedo R, Lai S, Liu K, Li D, Wasserman BA, Vogel-Claussen J, Lima JA, Bluemke DA (2009) Positive remodeling of the coronary arteries detected by magnetic resonance imaging in an asymptomatic population: MESA (Multi-Ethnic Study of Atherosclerosis). J Am Coll Cardiol 53:1708–1715CrossRefPubMed
65.
go back to reference Itskovich VV, Samber DD, Mani V, Aguinaldo JG, Fallon JT, Tang CY, Fuster V, Fayad ZA (2004) Quantification of human atherosclerotic plaques using spatially enhanced cluster analysis of multicontrast-weighted magnetic resonance images. Magn Reson Med 52:515–523CrossRefPubMed Itskovich VV, Samber DD, Mani V, Aguinaldo JG, Fallon JT, Tang CY, Fuster V, Fayad ZA (2004) Quantification of human atherosclerotic plaques using spatially enhanced cluster analysis of multicontrast-weighted magnetic resonance images. Magn Reson Med 52:515–523CrossRefPubMed
66.
go back to reference Worthley SG, Helft G, Fuster V, Fayad ZA, Fallon JT, Osende JI, Roqué M, Shinnar M, Zaman AG, Rodriguez OJ, Verhallen P, Badimon JJ (2000) High resolution ex vivo magnetic resonance imaging of in situ coronary and aortic atherosclerotic plaque in a porcine model. Atherosclerosis 150:321–329CrossRefPubMed Worthley SG, Helft G, Fuster V, Fayad ZA, Fallon JT, Osende JI, Roqué M, Shinnar M, Zaman AG, Rodriguez OJ, Verhallen P, Badimon JJ (2000) High resolution ex vivo magnetic resonance imaging of in situ coronary and aortic atherosclerotic plaque in a porcine model. Atherosclerosis 150:321–329CrossRefPubMed
Metadata
Title
Recent developments and new perspectives on imaging of atherosclerotic plaque: role of anatomical, cellular and molecular MRI Part I and II
Authors
Bernard C. M. te Boekhorst
Maarten J. Cramer
Gerard Pasterkamp
Cees J. A. van Echteld
Pieter A. F. M. Doevendans
Publication date
01-04-2010
Publisher
Springer Netherlands
Published in
The International Journal of Cardiovascular Imaging / Issue 4/2010
Print ISSN: 1569-5794
Electronic ISSN: 1875-8312
DOI
https://doi.org/10.1007/s10554-009-9565-8

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