Skip to main content
Top
Published in: The International Journal of Cardiovascular Imaging 7/2015

01-10-2015 | Original Paper

Ex vivo differential phase contrast and magnetic resonance imaging for characterization of human carotid atherosclerotic plaques

Authors: Romana Meletta, Nicole Borel, Paul Stolzmann, Alberto Astolfo, Jan Klohs, Marco Stampanoni, Markus Rudin, Roger Schibli, Stefanie D. Krämer, Adrienne Müller Herde

Published in: The International Journal of Cardiovascular Imaging | Issue 7/2015

Login to get access

Abstract

Non-invasive detection of specific atherosclerotic plaque components related to vulnerability is of high clinical relevance to prevent cerebrovascular events. The feasibility of magnetic resonance imaging (MRI) for characterization of plaque components was already demonstrated. We aimed to evaluate the potential of ex vivo differential phase contrast X-ray tomography (DPC) to accurately characterize human carotid plaque components in comparison to high field multicontrast MRI and histopathology. Two human plaque segments, obtained from carotid endarterectomy, classified according to criteria of the American Heart Association as stable and unstable plaque, were examined by ex vivo DPC tomography and multicontrast MRI (T1-, T2-, and proton density-weighted imaging, magnetization transfer contrast, diffusion-weighted imaging). To identify specific plaque components, the plaques were subsequently sectioned and stained for fibrous and cellular components, smooth muscle cells, hemosiderin, and fibrin. Histological data were then matched with DPC and MR images to define signal criteria for atherosclerotic plaque components. Characteristic structures, such as the lipid and necrotic core covered by a fibrous cap, calcification and hemosiderin deposits were delineated by histology and found with excellent sensitivity, resolution and accuracy in both imaging modalities. DPC tomography was superior to MRI regarding resolution and soft tissue contrast. Ex vivo DPC tomography allowed accurate identification of structures and components of atherosclerotic plaques at different lesion stages, in good correlation with histopathological findings.
Appendix
Available only for authorised users
Literature
1.
go back to reference World Health Organization, Mackay J, Mensah GA, Mendis S, Greenlund K (2004) The atlas of heart disease and stroke. World Health Organization, Geneva World Health Organization, Mackay J, Mensah GA, Mendis S, Greenlund K (2004) The atlas of heart disease and stroke. World Health Organization, Geneva
2.
go back to reference Go AS, Mozaffarian D, Roger VL, Benjamin EJ, Berry JD, Blaha MJ, Dai S, Ford ES, Fox CS, Franco S, Fullerton HJ, Gillespie C, Hailpern SM, Heit JA, Howard VJ, Huffman MD, Judd SE, Kissela BM, Kittner SJ, Lackland DT, Lichtman JH, Lisabeth LD, Mackey RH, Magid DJ, Marcus GM, Marelli A, Matchar DB, McGuire DK, Mohler ER, III, Moy CS, Mussolino ME, Neumar RW, Nichol G, Pandey DK, Paynter NP, Reeves MJ, Sorlie PD, Stein J, Towfighi A, Turan TN, Virani SS, Wong ND, Woo D, Turner MB, American Heart Association Statistics C, Stroke Statistics S (2014) Heart disease and stroke statistics–2014 update: a report from the American Heart Association. Circulation 129:e28–e292. doi:10.1161/01.cir.0000441139.02102.80 Go AS, Mozaffarian D, Roger VL, Benjamin EJ, Berry JD, Blaha MJ, Dai S, Ford ES, Fox CS, Franco S, Fullerton HJ, Gillespie C, Hailpern SM, Heit JA, Howard VJ, Huffman MD, Judd SE, Kissela BM, Kittner SJ, Lackland DT, Lichtman JH, Lisabeth LD, Mackey RH, Magid DJ, Marcus GM, Marelli A, Matchar DB, McGuire DK, Mohler ER, III, Moy CS, Mussolino ME, Neumar RW, Nichol G, Pandey DK, Paynter NP, Reeves MJ, Sorlie PD, Stein J, Towfighi A, Turan TN, Virani SS, Wong ND, Woo D, Turner MB, American Heart Association Statistics C, Stroke Statistics S (2014) Heart disease and stroke statistics–2014 update: a report from the American Heart Association. Circulation 129:e28–e292. doi:10.​1161/​01.​cir.​0000441139.​02102.​80
5.
go back to reference Stampanoni M, Groso A, Isenegger A, Mikuljan G, Chen Q, Bertrand A, Henein S, Betemps R, Frommherz U, Bohler P, Meister D, Lange M, Abela R (2006) Trends in synchrotron-based tomographic imaging: the SLS experience. Dev X-Ray Tomogr 5:6318. doi:10.1117/12.679497 Stampanoni M, Groso A, Isenegger A, Mikuljan G, Chen Q, Bertrand A, Henein S, Betemps R, Frommherz U, Bohler P, Meister D, Lange M, Abela R (2006) Trends in synchrotron-based tomographic imaging: the SLS experience. Dev X-Ray Tomogr 5:6318. doi:10.​1117/​12.​679497
6.
go back to reference Weitkamp T, Diaz A, David C, Pfeiffer F, Stampanoni M, Cloetens P, Ziegler E (2005) X-ray phase imaging with a grating interferometer. Opt Express 13:6296–6304CrossRefPubMed Weitkamp T, Diaz A, David C, Pfeiffer F, Stampanoni M, Cloetens P, Ziegler E (2005) X-ray phase imaging with a grating interferometer. Opt Express 13:6296–6304CrossRefPubMed
7.
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 94:932–938CrossRefPubMed 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 94:932–938CrossRefPubMed
8.
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 19:2756–2761CrossRefPubMed 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 19:2756–2761CrossRefPubMed
9.
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
12.
go back to reference Müller A, Mu L, Meletta R, Beck K, Rancic Z, Drandarov K, Kaufmann PA, Ametamey SM, Schibli R, Borel N, Krämer SD (2014) Towards non-invasive imaging of vulnerable atherosclerotic plaques by targeting co-stimulatory molecules. Int J Cardiol 174:503–515. doi:10.1016/j.ijcard.2014.04.071 CrossRefPubMed Müller A, Mu L, Meletta R, Beck K, Rancic Z, Drandarov K, Kaufmann PA, Ametamey SM, Schibli R, Borel N, Krämer SD (2014) Towards non-invasive imaging of vulnerable atherosclerotic plaques by targeting co-stimulatory molecules. Int J Cardiol 174:503–515. doi:10.​1016/​j.​ijcard.​2014.​04.​071 CrossRefPubMed
13.
go back to reference Stary HC, Chandler AB, Dinsmore RE, Fuster V, Glagov S, Insull W Jr, Rosenfeld ME, Schwartz CJ, Wagner WD, Wissler RW (1995) A definition of advanced types of atherosclerotic lesions and a histological classification of atherosclerosis. A report from the Committee on Vascular Lesions of the Council on Arteriosclerosis, American Heart Association. Arterioscler Thromb Vasc Biol 15:1512–1531CrossRefPubMed Stary HC, Chandler AB, Dinsmore RE, Fuster V, Glagov S, Insull W Jr, Rosenfeld ME, Schwartz CJ, Wagner WD, Wissler RW (1995) A definition of advanced types of atherosclerotic lesions and a histological classification of atherosclerosis. A report from the Committee on Vascular Lesions of the Council on Arteriosclerosis, American Heart Association. Arterioscler Thromb Vasc Biol 15:1512–1531CrossRefPubMed
15.
go back to reference Lacolley P, Regnault V, Nicoletti A, Li Z, Michel JB (2012) The vascular smooth muscle cell in arterial pathology: a cell that can take on multiple roles. Cardiovasc Res 95:194–204. doi:10.1093/cvr/cvs135 CrossRefPubMed Lacolley P, Regnault V, Nicoletti A, Li Z, Michel JB (2012) The vascular smooth muscle cell in arterial pathology: a cell that can take on multiple roles. Cardiovasc Res 95:194–204. doi:10.​1093/​cvr/​cvs135 CrossRefPubMed
16.
go back to reference Riviere C, Boudghene FP, Gazeau F, Roger J, Pons JN, Laissy JP, Allaire E, Michel JB, Letourneur D, Deux JF (2005) Iron oxide nanoparticle-labeled rat smooth muscle cells: cardiac MR imaging for cell graft monitoring and quantitation. Radiology 235:959–967. doi:10.1148/radiol.2353032057 CrossRefPubMed Riviere C, Boudghene FP, Gazeau F, Roger J, Pons JN, Laissy JP, Allaire E, Michel JB, Letourneur D, Deux JF (2005) Iron oxide nanoparticle-labeled rat smooth muscle cells: cardiac MR imaging for cell graft monitoring and quantitation. Radiology 235:959–967. doi:10.​1148/​radiol.​2353032057 CrossRefPubMed
18.
go back to reference Coombs BD, Rapp JH, Ursell PC, Reilly LM, Saloner D (2001) Structure of plaque at carotid bifurcation: high-resolution MRI with histological correlation. Stroke 32:2516–2521CrossRefPubMed Coombs BD, Rapp JH, Ursell PC, Reilly LM, Saloner D (2001) Structure of plaque at carotid bifurcation: high-resolution MRI with histological correlation. Stroke 32:2516–2521CrossRefPubMed
19.
go back to reference Li T, Li X, Zhao X, Zhou W, Cai Z, Yang L, Guo A, Zhao S (2012) Classification of human coronary atherosclerotic plaques using ex vivo high-resolution multicontrast-weighted MRI compared with histopathology. AJR Am J Roentgenol 198:1069–1075. doi:10.2214/AJR.11.6496 CrossRefPubMed Li T, Li X, Zhao X, Zhou W, Cai Z, Yang L, Guo A, Zhao S (2012) Classification of human coronary atherosclerotic plaques using ex vivo high-resolution multicontrast-weighted MRI compared with histopathology. AJR Am J Roentgenol 198:1069–1075. doi:10.​2214/​AJR.​11.​6496 CrossRefPubMed
20.
21.
go back to reference Worthley SG, Helft G, Fuster V, Fayad ZA, Fallon JT, Osende JI, Roque 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, Roque 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
22.
go back to reference Gury-Paquet L, Millon A, Salami F, Cernicanu A, Scoazec JY, Douek P, Boussel L (2012) Carotid plaque high-resolution MRI at 3 T: evaluation of a new imaging score for symptomatic plaque assessment. Magn Reson Imaging 30:1424–1431. doi:10.1016/j.mri.2012.04.024 CrossRefPubMed Gury-Paquet L, Millon A, Salami F, Cernicanu A, Scoazec JY, Douek P, Boussel L (2012) Carotid plaque high-resolution MRI at 3 T: evaluation of a new imaging score for symptomatic plaque assessment. Magn Reson Imaging 30:1424–1431. doi:10.​1016/​j.​mri.​2012.​04.​024 CrossRefPubMed
23.
go back to reference Worthley SG, Helft G, Fuster V, Fayad ZA, Rodriguez OJ, Zaman AG, Fallon JT, Badimon JJ (2000) Noninvasive in vivo magnetic resonance imaging of experimental coronary artery lesions in a porcine model. Circulation 101:2956–2961CrossRefPubMed Worthley SG, Helft G, Fuster V, Fayad ZA, Rodriguez OJ, Zaman AG, Fallon JT, Badimon JJ (2000) Noninvasive in vivo magnetic resonance imaging of experimental coronary artery lesions in a porcine model. Circulation 101:2956–2961CrossRefPubMed
24.
go back to reference Yuan C, Kerwin WS, Ferguson MS, Polissar N, Zhang S, Cai J, Hatsukami TS (2002) Contrast-enhanced high resolution MRI for atherosclerotic carotid artery tissue characterization. J Magn Reson Imaging 15:62–67CrossRefPubMed Yuan C, Kerwin WS, Ferguson MS, Polissar N, Zhang S, Cai J, Hatsukami TS (2002) Contrast-enhanced high resolution MRI for atherosclerotic carotid artery tissue characterization. J Magn Reson Imaging 15:62–67CrossRefPubMed
26.
go back to reference Hetterich H, Fill S, Herzen J, Willner M, Zanette I, Weitkamp T, Rack A, Schuller U, Sadeghi M, Brandl R, Adam-Neumair S, Reiser M, Pfeiffer F, Bamberg F, Saam T (2013) Grating-based X-ray phase-contrast tomography of atherosclerotic plaque at high photon energies. Z Med Phys 23:194–203. doi:10.1016/j.zemedi.2012.12.001 CrossRefPubMed Hetterich H, Fill S, Herzen J, Willner M, Zanette I, Weitkamp T, Rack A, Schuller U, Sadeghi M, Brandl R, Adam-Neumair S, Reiser M, Pfeiffer F, Bamberg F, Saam T (2013) Grating-based X-ray phase-contrast tomography of atherosclerotic plaque at high photon energies. Z Med Phys 23:194–203. doi:10.​1016/​j.​zemedi.​2012.​12.​001 CrossRefPubMed
27.
go back to reference Hetterich H, Willner M, Fill S, Herzen J, Bamberg F, Hipp A, Schuller U, Adam-Neumair S, Wirth S, Reiser M, Pfeiffer F, Saam T (2014) Phase-contrast CT: qualitative and quantitative evaluation of atherosclerotic carotid artery plaque. Radiology 271:870–878. doi:10.1148/radiol.14131554 CrossRefPubMed Hetterich H, Willner M, Fill S, Herzen J, Bamberg F, Hipp A, Schuller U, Adam-Neumair S, Wirth S, Reiser M, Pfeiffer F, Saam T (2014) Phase-contrast CT: qualitative and quantitative evaluation of atherosclerotic carotid artery plaque. Radiology 271:870–878. doi:10.​1148/​radiol.​14131554 CrossRefPubMed
28.
go back to reference Saam T, Herzen J, Hetterich H, Fill S, Willner M, Stockmar M, Achterhold K, Zanette I, Weitkamp T, Schuller U, Auweter S, Adam-Neumair S, Nikolaou K, Reiser MF, Pfeiffer F, Bamberg F (2013) Translation of atherosclerotic plaque phase-contrast CT imaging from synchrotron radiation to a conventional lab-based X-ray source. PLoS One 8:e73513. doi:10.1371/journal.pone.0073513 PubMedCentralCrossRefPubMed Saam T, Herzen J, Hetterich H, Fill S, Willner M, Stockmar M, Achterhold K, Zanette I, Weitkamp T, Schuller U, Auweter S, Adam-Neumair S, Nikolaou K, Reiser MF, Pfeiffer F, Bamberg F (2013) Translation of atherosclerotic plaque phase-contrast CT imaging from synchrotron radiation to a conventional lab-based X-ray source. PLoS One 8:e73513. doi:10.​1371/​journal.​pone.​0073513 PubMedCentralCrossRefPubMed
29.
go back to reference Fujimoto S, Kondo T, Kodama T, Fujisawa Y, Groarke J, Kumamaru KK, Takamura K, Matsunaga E, Miyauchi K, Daida H, Rybicki FJ (2014) A novel method for non-invasive plaque morphology analysis by coronary computed tomography angiography. Int J Cardiovasc Imaging 30:1373–1382. doi:10.1007/s10554-014-0461-5 CrossRefPubMed Fujimoto S, Kondo T, Kodama T, Fujisawa Y, Groarke J, Kumamaru KK, Takamura K, Matsunaga E, Miyauchi K, Daida H, Rybicki FJ (2014) A novel method for non-invasive plaque morphology analysis by coronary computed tomography angiography. Int J Cardiovasc Imaging 30:1373–1382. doi:10.​1007/​s10554-014-0461-5 CrossRefPubMed
Metadata
Title
Ex vivo differential phase contrast and magnetic resonance imaging for characterization of human carotid atherosclerotic plaques
Authors
Romana Meletta
Nicole Borel
Paul Stolzmann
Alberto Astolfo
Jan Klohs
Marco Stampanoni
Markus Rudin
Roger Schibli
Stefanie D. Krämer
Adrienne Müller Herde
Publication date
01-10-2015
Publisher
Springer Netherlands
Published in
The International Journal of Cardiovascular Imaging / Issue 7/2015
Print ISSN: 1569-5794
Electronic ISSN: 1875-8312
DOI
https://doi.org/10.1007/s10554-015-0706-y

Other articles of this Issue 7/2015

The International Journal of Cardiovascular Imaging 7/2015 Go to the issue