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(Circulation. 1996;94:932-938.)
© 1996 American Heart Association, Inc.
Articles |
Magnetic Resonance Images Lipid, Fibrous, Calcified, Hemorrhagic, and Thrombotic Components of Human Atherosclerosis In Vivo
Service de Cardiologie, Hopital Cochin, Paris, Service Hospitalier Frederic Joliot, CEA, Orsay, France (J-F.T.); the Cardiac Unit and NMR Center (J-F.T., H.L.K.), Division of Vascular Surgery (G.M.LaM.), and Pathology Department (J.F.S.), Massachusetts General Hospital, Boston; and the Cardiovascular Institute, Mount Sinai Medical Center, New York, NY (V.F.).
Correspondence to J.F. Toussaint, MD, PhD, Service Hospitalier Frederic Joliot, Groupe de RMN, CEA, 4 Place du General Leclerc, 91401 Orsay, Cedex, France. E-mail toussain@uriens.shfj.cea.fr.
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Abstract |
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Background Although MRI can discriminate the lipid core from the collagenous cap of atherosclerotic lesions in vitro with T2 contrast, it has not yet produced detailed in vivo images of these human plaque components.
Methods and Results We imaged seven lesions from six patients who required surgical carotid endarterectomy and calculated T2 in vivo before surgery in various plaque regions. Using the same acquisition parameters, we repeated these measurements in vitro on the resected fragment and compared MR images with histology. T2 values calculated in vivo correlate with in vitro measurements for each plaque component; the in vitro discrimination we demonstrated previously with T2 contrast can therefore be performed similarly in vivo.
Conclusions MRI is the first noninvasive imaging technique that allows the discrimination of lipid cores, fibrous caps, calcifications, normal media, and adventitia in human atheromatous plaques in vivo. This technique also characterizes intraplaque hemorrhage and acute thrombosis. This result may support further investigations that include MRI of plaque progression, stabilization, and rupture in human atherosclerosis.
Key Words: magnetic resonance imaging • lipids • fibrous cap • thrombosis • carotid arteries
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Introduction |
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Despite recent trends showing a reduction in the incidence of atherosclerosis, this disease remains the major cause of death in industrialized countries. However, although current technologies for studying the disease in vivo can provide long-term prognostic parameters, they do not help physicians to predict the evolution of a given lesion.1 Our understanding of disease progression over decades (slow progression) and of the occurrence of acute events (rapid progression)2 essentially relies on pathological studies.3 4 5 The most common decision-guiding technique used in the clinical field, x-ray angiography, fails to describe the heterogeneity of atheromatous arterial wall. Indeed, no imaging technique has permitted the in vivo discrimination of collagenous cap and atheromatous core, the two main components of atherosclerotic plaques thought to be essential to plaque stability6 7 and thrombogenicity.8 Their visualization may therefore improve our understanding of plaque susceptibility to rupture9 and their role in acute ischemic events10 or conversely in plaque stabilization.11
MRI allows noninvasive tissue characterization by virtue of its dependence on biophysical and biochemical parameters such as chemical composition and concentration, molecular motion, diffusion, physical state, or water content. Previous investigations12 13 have demonstrated that MRI allows in vitro discrimination of wall components in normal and atheromatous arteries, including media, adventitia, perivascular fat, lipid-rich core, collagenous cap, and calcifications at high (9.4-T) and low (1.5-T) field strengths. Although various MR approaches have been used to image the lipid component,14 15 16 a robust description based on conventional parameters has been developed that has proved its ability to distinguish in vitro lipid-rich cores and collagenous caps in a single image by T2 contrast with a high contrast-to-noise ratio,13 even in early lesions.17 A recent study showed the usefulness of this technique in describing progression of experimental atherosclerosis and its ability to image in vivo plaque components such as fibrous caps, necrotic cores, and intraplaque hemorrhage resulting from balloon injury to the abdominal aorta in six cholesterol-fed rabbits.18
We undertook this investigation to compare T2 contrast in vivo and in vitro to apply these previous results to studies of human plaque structure in vivo. Using magnetic resonance at 1.5 T, we studied atherosclerotic lesions from patients requiring carotid endarterectomy and calculated the T2 of various plaque components in vivo before surgery and in vitro after surgery. By comparing both measurements and histology, we specifically tested the ability of MRI to discriminate collagenous caps and lipid cores in vivo.
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Methods |
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Patients
We have used MRI to noninvasively image advanced lesions in carotid arteries from six consecutive patients (67±1.9 [mean±SD] years old) referred for endarterectomy. A total of seven lesions were studied (one patient had a severe stenosis of both internal carotid arteries). The decision to proceed with surgery was based on the presence of a severe carotid stenosis identified by ultrasound, which was confirmed by MR angiography or x-ray angiography. Three patients were asymptomatic: one had a recent series of near syncopal episodes, and two had recent transient ischemic attacks. Surgical endarterectomy by double Ender's spatula under systemic heparinization was performed <4 days after in vivo MRI. Informed consent was obtained from each patient before the in vivo MR study. This investigation was approved by the Massachusetts General Hospital Subcommittee on Human Studies.
In Vivo Images
The MR images of the arterial wall characterizing atherosclerosis were obtained from T1w and T2w SE sequences and CSI (with lipid suppression). We acquired in vivo images at 1.5 T on a standard system (Signa, General Electric Corp) with a General Electric–designed neck coil. MR angiography was first performed to determine lesion level and maximal extension. We used a time-of-flight gradient echo sequence (TE, 6 ms; TR, 40 ms; flip angle, 30°). Two-dimensional slices were generated from multiple 3D slabs with maximum-intensity projection. Plaque images were obtained through three successive data sets: (1) a scout of ungated sagittal 3-mm-thick SE slices, centered on the stenosed carotid (TR, 500 ms; TE, 12 ms; FOV, 25 cm; matrix, 256x128; one average); (2) a set of oblique coronal 3-mm-thick slices in the main direction of the stenosed vessel (TR, 1 cardiac cycle; TE, 23 ms; FOV, 16 cm; matrix, 256x192; one average) to align the next set; (3) axial oblique slices in a direction perpendicular to flow. The MR images of the arterial wall characterizing atherosclerosis were performed at the location of greatest stenosis of the common carotid and internal carotid arteries and at three levels on each side of the major stenosis location. T1w image parameters were as follows: TR, 500 ms; TE, 18 ms; FOV, 12 cm; matrix, 256x192; one average. Parameters of the ECG-gated T2w images allowed T2 determination from a double-echo sequence (TE, 20 and 55 ms; TR, 1 cardiac cycle; slice thickness, 5 mm; FOV, 10 cm; matrix, 256x256; two averages, with an in-plane resolution of 390 µm). Regions of interest for T2 calculation were defined from the MR images with a minimum of 10 pixels per analyzed region. A CSI image was also acquired at the level of the main stenosis by adding a lipid suppression pulse, with all other parameters kept equal.
In Vitro Images
After surgery, samples were immediately frozen at -60°C,13 except for two thrombosed arteries, which were imaged <2 hours after removal. Great care was taken to determine the effects of freezing and storage conditions. Soila et al19 demonstrated that relaxation constants of atheromatous plaques sampled during surgery were not altered over 6 days when samples were kept at 4°C in a sterile environment and rewarmed to 37°C before imaging. In a preliminary work, we compared two preservation methods13 : arteries were stored at 4°C and compared with arteries stored at -60°C. Both were similarly imaged at 37°C after 20 minutes of rewarming. T2 contrast was identical in both groups, suggesting that low-temperature storage did not alter the respective T2s once the samples were rewarmed for a sufficient time. We applied the same method for this study.
We identified vessel orientation by staining the superior and external sides with black ink, which does not modify the magnetic parameters of arterial wall. Samples were imaged in vitro within 24 hours of surgery after being placed in NMR tubes filled with saline to prevent dehydration; they were rewarmed and imaged at 37°C. Orientation planes and parameters were identical to those used for in vivo axial and longitudinal images (T1w image: TR, 500 ms; TE, 18 ms; T2w image: TE, 20 to 55 ms; TR, set equal to the respective patient cardiac cycle duration; slice thickness, 5 mm; FOV, 10 cm; matrix size, 256x256; two averages).
Histology
Arteries were cut every 5 mm at a level corresponding to each imaging plane in the magnet and step-sectioned every 200 µm. Sections were photographed. We stained the two slices adjacent to each section, using Masson's derived trichrome to stain collagenous regions and Sudan black for lipid core identification.13
Statistical Analysis
Data are expressed as mean±SD. In vivo measurements were compared by ANOVA with a significance level of 95%. Student's two-tailed paired t test was used to compare in vivo and in vitro T2s. A value of P<.05 was considered significant. Linear regression was used to correlate in vitro and in vivo measurements.
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Results |
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T2 was measured in vivo and in vitro in successive wall regions shown by MRI from the lumen to the outer layer. These regions were subsequently characterized by histology as being fibrous cap, lipid core, media, and adventitia. On the seven T2w successive parallel axial MR slices, each patient had at least three short and three long T2 regions in which measurements could be compared with in vitro images and histology, resulting in a total of 18 to 24 T2 measurements for each component. The Table
gives the results of these measurements. For each component (lipid core, collagenous cap, normal media, and normal adventitia), T2 calculated in vitro is close to its in vivo value. This is shown in the scatterplot of T2 calculations in Fig 1; similar relations are obtained for medial and adventitial T2s. A significant difference is demonstrated in vivo and in vitro between collagenous cap and lipid core, between normal media and lipid core, and between media and adventitia (see the Table).
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, solid line; n=19) and lipid core measurements (
, dotted line; n=18) with average values and SDs. With linear regression, T2s closely correlate in both fibrous caps (r2=.51, P<.001) and atheromatous cores (r2=.44, P=.002).
The ability of NMR to discriminate fibrous cap from lipid-rich core is illustrated in Fig 2, which characterizes a carotid lesion from a 65-year-old patient. Fig 2A and 2B shows the axial in vivo image of the left common carotid artery 12 mm below the level of maximum stenosis. The three layers of the lesion indicated by the white arrow (two bright layers with long T2 surrounding a layer with short T2) are similarly demonstrated in the in vitro image (Fig 2C). From lumen to adventitia, this result corresponds to a succession of collagenous cap, lipid core (black arrow), and media.13 With trichrome and Sudan black staining, histology (Fig 2D and 2E) shows the lipid infiltration in the central layer (arrows), corresponding to the central shortest T2 layer of the MR images. MRI characterizes adventitia in vivo by the black, thin layer surrounding vessels in T2w images; this result agrees with in vitro data showing a similar T2 contrast between media and adventitia.13
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Fig 3 shows the lesion of a 66-year-old asymptomatic patient with severe stenosis involving the proximal right internal carotid artery. As expected from previous investigations,20 the in vivo morphological measurements (9.4-mm length, 4.4-mm thickening in the outer wall, 3.1-mm thickening in the inner wall; Fig 3B) are similar to the in vitro measurements in Fig 3C (T1w, SE; 9.1-mm length, 4.5-mm outer wall, 2.1-mm inner wall) and to the histological evaluation. A calcification, shown as a signal void,13 21 is demonstrated in the lower part of the wall (white arrow, Fig 3B and 3C). On the axial sections (Fig 3D and 3E), two different regions appear. The double arrow shows a region with low T2 (29.4 ms). A more homogeneous layer with a T2 of 49.1 ms is present on the luminal side (arrowhead). The in vitro image (Fig 3F) demonstrates a similar pattern with two regions: a heterogeneous region with short T2 (31.3 ms) and calcifications, and the opposite side (C in Fig 3F), which is more homogeneous with higher intensity and longer T2 (52.7 ms). This distribution is consistent with a lipid-rich and calcified region encompassing the right side (double arrow) and a fibrous region on the left side (C in Fig 3F) of the artery.13 The microscopic appearance of this plaque (Fig 3G) demonstrates the presence of a white dense collagenous region (C in Fig 3G) over an atheromatous lipid core (A in Fig 3G) with calcified components. With lipid suppression, the CSI image of the same slice as in Fig 3D yields a contrast-to-noise ratio only slightly reduced in the lipid core (6.7 versus 7.5; 12% reduction) compared with nonfrequency selective images, whereas the contrast-to-noise ratio was reduced by 80% (5.7 versus 29.1) in subcutaneous fat. For the six patients, the reduction of contrast-to-noise ratio by CSI was 11.5±6.5% in the atheromatous core and 82.4±4.9% in subcutaneous fat.
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Two patients had complex lesions with intraplaque hemorrhage. Fig 4 shows the MR angiography and MRI of the suboccluded left internal carotid artery of a 68-year-old asymptomatic patient. On the axial images, the plaque shows a striated pattern in its central part in vivo and in vitro (Fig 4F and 4G): on the luminal side is a long T2 layer (45.3 ms), whereas the black double arrow indicates a low-intensity layer with a T2 of 22.8 ms, shorter than mean lipid core value. Histology depicts an intraplaque hemorrhage corresponding to the deep short T2 layer. For the two hemorrhagic lesions, T2 in the central zone was 21.5±1.7 ms.
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Two patients had large luminal thromboses. Fig 5 shows the subocclusive thrombus of the left common carotid artery of a 70-year-old patient. The patient was referred after recent transient ischemic attacks with a very severe stenosis on the early Doppler study, and alternating patency and occlusion was visible on successive ultrasound and x-ray angiography studies. Fig 5A shows a bright area at the site of occlusion. In this area, a long T2 region surrounds a superficial shorter T2 layer. The perioperative histological analysis revealed a fresh thrombus of the left bifurcation, upstream of a severe stenosis of the proximal internal carotid artery. Fig 5B shows the T2w in vitro image of this thrombus. Two layers are clearly distinguished: a shorter T2 region in the luminal superficial zone and a longer T2 region in the deeper layer. Histology shows the bilayer pattern with intact red cells in the most recent dark-red superficial layer (arrow) and elements of thrombus organization in the deep, older region.
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Discussion |
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In this investigation, we discriminated atherosclerotic plaque components in vivo using 1H-NMR imaging in a clinical imager with routinely available pulse sequences. Our data from seven carotid lesions demonstrate that the water resonance in lipid core has a short T2 in vivo, as has been shown in vitro.13 In the same study, we had also demonstrated that the major contributor to the MR signal in the atheromatous core is water and not lipid, with a ratio of 10/1. In vivo spectroscopic measurements have not yet confirmed the same property; however, the similitude of the lipid core T2s in vivo and in vitro shown here and the 6.5-times-poorer signal from atheromatous core lipids compared with subcutaneous fat (water CSI with lipid suppression) strongly suggest that the content of liquid lipids in the atheromatous core is as small in vivo as in vitro.13 The relative content of these lipids such as cholesteryl esters decreases further with stenosis severity,22 as solid cholesterol cleft content increases. Therefore, sequences with water as the principal signal source for atherosclerosis imaging benefit from a larger signal-to-noise ratio than techniques based on direct lipid analysis. Furthermore, such water proton sequences allow the simultaneous description of other major components such as fibrous cap, media, and adventitia.
With increasing acquisition speed, other methods that directly visualize atheromatous lipids (by use of diffusion-weighted sequences15 or long T2 suppression16 ) may help to define lipid-rich regions. Determination of the diffusion coefficient, which is decreased in atheromatous core,23 may also enhance atherosclerosis characterization. However, these techniques have yet to be tested in vivo.
The T2 measurements we performed in this study substantially differ from our previous data, which showed larger values.13 However, these earlier results were obtained under different conditions: we used a long spectroscopic Hahn SE sequence with echo times ranging from 10 µs to 1000 ms, whereas in the present study we used two images with TEs of 20 and 55 ms. In a multiexponential relaxation system, the much longer echo times used in the Hahn SE sequence increase the relative contribution of the longest T2 species of each component and therefore lengthen the resulting relaxation constant.
We have used T1w images to identify calcifications. Calcified regions appear as low-intensity zones in all NMR sequences owing to low water content.21 24 The contrast-to-noise ratio for calcified regions compared with other components is higher in T1w than T2w images (see Fig 6 in Reference 13). Imaging calcification simultaneously with other components such as caps and cores, as demonstrated here, remains critical to a better understanding of their role in plaque aging,25 stabilization,7 or arterial dysfunction.26
Intraplaque Hemorrhage and Thrombosis
We have been able to identify intraplaque hemorrhage using methods similar to those reported in animal models.18 This result is also consistent with data from human myocardium27 and experimental brain hemorrhage,28 which demonstrated that the signal loss on T2w images is due to magnetic susceptibility of hemosiderin and ferritin, two iron-storing proteins present in macrophages. Such proteins and other degradation metabolites of hemoglobin in scavenger macrophages29 may be involved in a similar way in human plaque hemorrhage18 and are responsible for the imaging susceptibility-induced pattern shown in Fig 4
.
The two different components inside the thrombus shown in Fig 5 are consistent with in vivo data obtained in aortic thrombi.30 The shorter T2 region of the luminal side corresponds to the most recent layer as shown by histology (Fig 5D); this layer has the largest content of intact red blood cells31 filled with iron-rich products from deoxyhemoglobin breakdown. These metabolites produce a large magnetic susceptibility effect and decrease T2.32 During later thrombus organization, they are degraded, internalized by macrophages,31 and replaced with fibrosis,30 a process that diminishes the intensity of the susceptibility effect, as seen in the deeper layer with a longer T2.
Perspectives
MRI provides a unique method of discriminating the main components of human plaques in the carotid artery. Chemical shift imaging, along with diffusion, and dynamic studies30 are likely to help further characterization of atherothrombosis in vivo. Technical improvements are aimed at obtaining high resolution, high signal-to-noise ratios, small FOVs, motion compensation, and 3D reconstruction of plaque structure in clinically available NMR systems.21 These may be provided by localized gradient coils,33 specialized receiver coils,34 high magnetic field strength, and improved in vivo NMR microscopy.35
The capability to discriminate atheromatous components allows large-scale clinical studies of plaque progression, regression, and stabilization and their effect on clinical events. This could also improve our understanding of the slow evolution of atherosclerosis in the early decades of life and may provide a basis for screening young patients. Longitudinal studies of vascular interventional therapies may also benefit from these results.36 The combination of MR angiography for luminal morphometry, 3D velocity mapping for the analysis of peristenotic blood flow streamlines,37 and local vortices,38 time-of-flight echo-planar MRI for the determination of flow reserve in terminal arteries,39 perfusion measurement based on T1 changes,40 and tissue characterization sequences may provide a complete description of the atherosclerotic process and its dynamic consequences. Finally, identification of intraplaque hemorrhage and acute thrombosis allows study of the cascade of events leading from plaque rupture to arterial thrombosis, acute ischemia, and infarction,41 which may provide newer methods for the prediction and prevention of these life-threatening events.
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Selected Abbreviations and Acronyms |
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Acknowledgments |
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We gratefully acknowledge the support of the Harold M. English Fund from the Harvard Medical School, La Bourse Accelli de la Societe Francaise de Cardiologie, and Le Fonds d'Etudes et de Recherche du Corps Medical des Hopitaux de Paris. We thank Drs Erling Falk and Anne Leroy-Willig for very helpful discussions. We are grateful for the photographic assistance of Michele Forrestall and Steve Conley. We thank Tom Brady and the staff and members of the MGH-NMR Center for the use of the NMR systems and for beneficial discussions.
Received December 28, 1995; revision received February 26, 1996; accepted February 27, 1996.
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H. R. Underhill, V. L. Yarnykh, T. S. Hatsukami, J. Wang, N. Balu, C. E. Hayes, M. Oikawa, W. Yu, D. Xu, B. Chu, et al. Carotid Plaque Morphology and Composition: Initial Comparison between 1.5- and 3.0-T Magnetic Field Strengths Radiology, August 1, 2008; 248(2): 550 - 560. [Abstract] [Full Text] [PDF]
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P. Gao, Z.-q. Chen, Y.-h. Bao, L.-q. Jiao, and F. Ling Correlation Between Carotid Intraplaque Hemorrhage and Clinical Symptoms: Systematic Review of Observational Studies Stroke, August 1, 2007; 38(8): 2382 - 2390. [Abstract] [Full Text] [PDF]
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T. Saam, T. S. Hatsukami, N. Takaya, B. Chu, H. Underhill, W. S. Kerwin, J. Cai, M. S. Ferguson, and C. Yuan The Vulnerable, or High-Risk, Atherosclerotic Plaque: Noninvasive MR Imaging for Characterization and Assessment Radiology, July 1, 2007; 244(1): 64 - 77. [Abstract] [Full Text] [PDF]
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Y. Qiao, I. Ronen, J. Viereck, F. L. Ruberg, and J. A. Hamilton Identification of Atherosclerotic Lipid Deposits by Diffusion-Weighted Imaging Arterioscler Thromb Vasc Biol, June 1, 2007; 27(6): 1440 - 1446. [Abstract] [Full Text] [PDF]
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E. Touze, J.-F. Toussaint, J. Coste, E. Schmitt, F. Bonneville, P. Vandermarcq, J.-Y. Gauvrit, F. Douvrin, J.-F. Meder, J.-L. Mas, et al. Reproducibility of High-Resolution MRI for the Identification and the Quantification of Carotid Atherosclerotic Plaque Components: Consequences for Prognosis Studies and Therapeutic Trials Stroke, June 1, 2007; 38(6): 1812 - 1819. [Abstract] [Full Text] [PDF]
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I. Koktzoglou, Y.-C. Chung, T. J. Carroll, O. P. Simonetti, M. D. Morasch, and D. Li Three-dimensional Black-Blood MR Imaging of Carotid Arteries with Segmented Steady-State Free Precession: Initial Experience Radiology, April 1, 2007; 243(1): 220 - 228. [Abstract] [Full Text] [PDF]
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B. S. Pessanha, K. Potter, F. D. Kolodgie, A. Farb, R. Kutys, E. K. Mont, A. P. Burke, T. J. O'Leary, and R. Virmani Characterization of Intimal Changes in Coronary Artery Specimens with MR Microscopy Radiology, October 1, 2006; 241(1): 107 - 115. [Abstract] [Full Text] [PDF]
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T. Saam, J. Cai, L. Ma, Y.-Q. Cai, M. S. Ferguson, N. L. Polissar, T. S. Hatsukami, and C. Yuan Comparison of Symptomatic and Asymptomatic Atherosclerotic Carotid Plaque Features with in Vivo MR Imaging. Radiology, August 1, 2006; 240(2): 464 - 472. [Abstract] [Full Text] [PDF]
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C. M. Matter, M. T. Wyss, P. Meier, N. Spath, T. von Lukowicz, C. Lohmann, B. Weber, A. R. de Molina, J. C. Lacal, S. M. Ametamey, et al. 18F-Choline Images Murine Atherosclerotic Plaques Ex Vivo Arterioscler Thromb Vasc Biol, March 1, 2006; 26(3): 584 - 589. [Abstract] [Full Text] [PDF]
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N. Takaya, C. Yuan, B. Chu, T. Saam, H. Underhill, J. Cai, N. Tran, N. L. Polissar, C. Isaac, M. S. Ferguson, et al. Association Between Carotid Plaque Characteristics and Subsequent Ischemic Cerebrovascular Events: A Prospective Assessment With MRI--Initial Results Stroke, March 1, 2006; 37(3): 818 - 823. [Abstract] [Full Text] [PDF]
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N. Nighoghossian, L. Derex, and P. Douek The Vulnerable Carotid Artery Plaque: Current Imaging Methods and New Perspectives Stroke, December 1, 2005; 36(12): 2764 - 2772. [Abstract] [Full Text] [PDF]
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J. Cai, T. S. Hatsukami, M. S. Ferguson, W. S. Kerwin, T. Saam, B. Chu, N. Takaya, N. L. Polissar, and C. Yuan 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, November 29, 2005; 112(22): 3437 - 3444. [Abstract] [Full Text] [PDF]
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B. A. Wasserman, R. J. Wityk, H. H. Trout III, and R. Virmani Low-Grade Carotid Stenosis: Looking Beyond the Lumen With MRI Stroke, November 1, 2005; 36(11): 2504 - 2513. [Abstract] [Full Text] [PDF]
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E. Larose, Y. Yeghiazarians, P. Libby, E.K. Yucel, M. Aikawa, D. F. Kacher, E. Aikawa, S. Kinlay, F. J. Schoen, A. P. Selwyn, et al. Characterization of Human Atherosclerotic Plaques by Intravascular Magnetic Resonance Imaging Circulation, October 11, 2005; 112(15): 2324 - 2331. [Abstract] [Full Text] [PDF]
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V. Fuster, P. R. Moreno, Z. A. Fayad, R. Corti, and J. J. Badimon Atherothrombosis and High-Risk Plaque: Part I: Evolving Concepts J. Am. Coll. Cardiol., September 20, 2005; 46(6): 937 - 954. [Abstract] [Full Text] [PDF]
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M. Sirol, V. Fuster, J. J. Badimon, J. T. Fallon, J.-F. Toussaint, and Z. A. Fayad Chronic Thrombus Detection With In Vivo Magnetic Resonance Imaging and a Fibrin-Targeted Contrast Agent Circulation, September 13, 2005; 112(11): 1594 - 1600. [Abstract] [Full Text] [PDF]
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R. L. Wolf, S. L. Wehrli, A. M. Popescu, J. H. Woo, H. K. Song, A. C. Wright, E. R. Mohler III, J. D. Harding, E. L. Zager, R. M. Fairman, et al. Mineral Volume and Morphology in Carotid Plaque Specimens Using High-Resolution MRI and CT Arterioscler Thromb Vasc Biol, August 1, 2005; 25(8): 1729 - 1735. [Abstract] [Full Text] [PDF]
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M. Y. Desai, A. Rodriguez, B. A. Wasserman, G. Gerstenblith, S. Agarwal, M. Kennedy, D. A Bluemke, and J. A.C. Lima Association of Cholesterol Subfractions and Carotid Lipid Core Measured by MRI Arterioscler Thromb Vasc Biol, June 1, 2005; 25(6): e110 - e111. [Full Text] [PDF]
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N. Takaya, C. Yuan, B. Chu, T. Saam, N. L. Polissar, G. P. Jarvik, C. Isaac, J. McDonough, C. Natiello, R. Small, et al. Presence of Intraplaque Hemorrhage Stimulates Progression of Carotid Atherosclerotic Plaques: A High-Resolution Magnetic Resonance Imaging Study Circulation, May 31, 2005; 111(21): 2768 - 2775. [Abstract] [Full Text] [PDF]
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J.K. Lovett, J.N.E. Redgrave, and P.M. Rothwell A Critical Appraisal of the Performance, Reporting, and Interpretation of Studies Comparing Carotid Plaque Imaging With Histology Stroke, May 1, 2005; 36(5): 1085 - 1091. [Abstract] [Full Text] [PDF]
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A. Yonemura, Y. Momiyama, Z. A. Fayad, M. Ayaori, R. Ohmori, K. Higashi, T. Kihara, S. Sawada, N. Iwamoto, M. Ogura, et al. Effect of lipid-lowering therapy with atorvastatin on atherosclerotic aortic plaques detected by noninvasive magnetic resonance imaging J. Am. Coll. Cardiol., March 1, 2005; 45(5): 733 - 742. [Abstract] [Full Text] [PDF]
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T. Saam, J.M. Cai, Y.Q. Cai, N.Y. An, A. Kampschulte, D. Xu, W.S. Kerwin, N. Takaya, N.L. Polissar, T.S. Hatsukami, et al. Carotid Plaque Composition Differs Between Ethno-Racial Groups: An MRI Pilot Study Comparing Mainland Chinese and American Caucasian Patients Arterioscler Thromb Vasc Biol, March 1, 2005; 25(3): 611 - 616. [Abstract] [Full Text] [PDF]
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T. Saam, M.S. Ferguson, V.L. Yarnykh, N. Takaya, D. Xu, N.L. Polissar, T.S. Hatsukami, and C. Yuan Quantitative Evaluation of Carotid Plaque Composition by In Vivo MRI Arterioscler Thromb Vasc Biol, January 1, 2005; 25(1): 234 - 239. [Abstract] [Full Text] [PDF]
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J. Viereck, F. L. Ruberg, Y. Qiao, A. S. Perez, K. Detwiller, M. Johnstone, and J. A. Hamilton MRI of Atherothrombosis Associated With Plaque Rupture Arterioscler Thromb Vasc Biol, January 1, 2005; 25(1): 240 - 245. [Abstract] [Full Text] [PDF]
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A. Kampschulte, M.S. Ferguson, W.S. Kerwin, N. L. Polissar, B. Chu, T. Saam, T.S. Hatsukami, and C. Yuan Differentiation of Intraplaque Versus Juxtaluminal Hemorrhage/Thrombus in Advanced Human Carotid Atherosclerotic Lesions by In Vivo Magnetic Resonance Imaging Circulation, November 16, 2004; 110(20): 3239 - 3244. [Abstract] [Full Text] [PDF]
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J. R. Davies, J. H. Rudd, and P. L. Weissberg Molecular and Metabolic Imaging of Atherosclerosis J. Nucl. Med., November 1, 2004; 45(11): 1898 - 1907. [Abstract] [Full Text] [PDF]
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B. Chu, T. S. Hatsukami, N. L. Polissar, X.-Q. Zhao, L. W. Kraiss, D. L. Parker, J. C. Waterton, J. S. Raichlen, W. Hamar, and C. Yuan Determination of Carotid Artery Atherosclerotic Lesion Type and Distribution in Hypercholesterolemic Patients With Moderate Carotid Stenosis Using Noninvasive Magnetic Resonance Imaging Stroke, November 1, 2004; 35(11): 2444 - 2448. [Abstract] [Full Text] [PDF]
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E. Trogan, Z. A. Fayad, V. V. Itskovich, J.-G. S. Aguinaldo, V. Mani, J. T. Fallon, I. Chereshnev, and E. A. Fisher Serial Studies of Mouse Atherosclerosis by In Vivo Magnetic Resonance Imaging Detect Lesion Regression After Correction of Dyslipidemia Arterioscler Thromb Vasc Biol, September 1, 2004; 24(9): 1714 - 1719. [Abstract] [Full Text] [PDF]
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M. Sirol, V. V. Itskovich, V. Mani, J. G. S. Aguinaldo, J. T. Fallon, B. Misselwitz, H.-J. Weinmann, V. Fuster, J.-F. Toussaint, and Z. A. Fayad Lipid-Rich Atherosclerotic Plaques Detected by Gadofluorine-Enhanced In Vivo Magnetic Resonance Imaging Circulation, June 15, 2004; 109(23): 2890 - 2896. [Abstract] [Full Text] [PDF]
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R. M. Botnar, A. S. Perez, S. Witte, A. J. Wiethoff, J. Laredo, J. Hamilton, W. Quist, E. C. Parsons Jr, A. Vaidya, A. Kolodziej, et al. In Vivo Molecular Imaging of Acute and Subacute Thrombosis Using a Fibrin-Binding Magnetic Resonance Imaging Contrast Agent Circulation, April 27, 2004; 109(16): 2023 - 2029. [Abstract] [Full Text] [PDF]
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C. M. Kramer, L. A. Cerilli, K. Hagspiel, J. M. DiMaria, F. H. Epstein, and J. A. Kern Magnetic Resonance Imaging Identifies the Fibrous Cap in Atherosclerotic Abdominal Aortic Aneurysm Circulation, March 2, 2004; 109(8): 1016 - 1021. [Abstract] [Full Text] [PDF]
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S. Zhang, J. Cai, Y. Luo, C. Han, N. L. Polissar, T. S. Hatsukami, and C. Yuan Measurement of Carotid Wall Volume and Maximum Area with Contrast-enhanced 3D MR Imaging: Initial Observations Radiology, July 1, 2003; 228(1): 200 - 205. [Abstract] [Full Text] [PDF]
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A. R. Moody, R. E. Murphy, P. S. Morgan, A. L. Martel, G.S. Delay, S. Allder, S. T. MacSweeney, W. G. Tennant, J. Gladman, J. Lowe, et al. Characterization of Complicated Carotid Plaque With Magnetic Resonance Direct Thrombus Imaging in Patients With Cerebral Ischemia Circulation, June 24, 2003; 107(24): 3047 - 3052. [Abstract] [Full Text] [PDF]
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R. E. Murphy, A. R. Moody, P. S. Morgan, A. L. Martel, G.S. Delay, S. Allder, S. T. MacSweeney, W. G. Tennant, J. Gladman, J. Lowe, 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, June 24, 2003; 107(24): 3053 - 3058. [Abstract] [Full Text] [PDF]
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R. F. Redberg, R. A. Vogel, M. H. Criqui, D. M. Herrington, J. A. C. Lima, and M. J. Roman Task force #3--what is the spectrum of current and emerging techniques for the noninvasive measurement of atherosclerosis? J. Am. Coll. Cardiol., June 4, 2003; 41(11): 1886 - 1898. [Full Text] [PDF]
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P. W. F. Wilson, S. C. Smith Jr, R. S. Blumenthal, G. L. Burke, and N. D. Wong Task force #4--how do we select patients for atherosclerosis imaging? J. Am. Coll. Cardiol., June 4, 2003; 41(11): 1898 - 1906. [Full Text] [PDF]
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S. G. Worthley, G. Helft, V. Fuster, Z. A. Fayad, M. Shinnar, L. A. Minkoff, C. Schechter, J. T. Fallon, and J. J. Badimon A Novel Nonobstructive Intravascular MRI Coil: In Vivo Imaging of Experimental Atherosclerosis Arterioscler Thromb Vasc Biol, February 1, 2003; 23(2): 346 - 350. [Abstract] [Full Text] [PDF]
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Z. A. Fayad, V. Fuster, K. Nikolaou, and C. Becker Computed Tomography and Magnetic Resonance Imaging for Noninvasive Coronary Angiography and Plaque Imaging: Current and Potential Future Concepts Circulation, October 8, 2002; 106(15): 2026 - 2034. [Full Text] [PDF]
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J.-M. Cai, T. S. Hatsukami, M. S. Ferguson, R. Small, N. L. Polissar, and C. Yuan Classification of Human Carotid Atherosclerotic Lesions With In Vivo Multicontrast Magnetic Resonance Imaging Circulation, September 10, 2002; 106(11): 1368 - 1373. [Abstract] [Full Text] [PDF]
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V. Fuster, R. Corti, Z.A. Fayad, and J.J. Badimon Understanding the pathophysiology of the arterial wall: which method should we choose? Magnetic resonance imaging Eur. Heart J. Suppl., September 1, 2002; 4(suppl_F): F41 - F46. [Abstract] [PDF]
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A. F. AbuRahma, J. T. Wulu Jr, and B. Crotty Carotid Plaque Ultrasonic Heterogeneity and Severity of Stenosis Stroke, July 1, 2002; 33(7): 1772 - 1775. [Abstract] [Full Text] [PDF]
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R. P. Choudhury, V. Fuster, J. J. Badimon, E. A. Fisher, and Z. A. Fayad MRI and Characterization of Atherosclerotic Plaque: Emerging Applications and Molecular Imaging Arterioscler Thromb Vasc Biol, July 1, 2002; 22(7): 1065 - 1074. [Abstract] [Full Text] [PDF]
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B. A. Wasserman, W. I. Smith, H. H. Trout III, R. O. Cannon III, R. S. Balaban, and A. E. Arai Carotid Artery Atherosclerosis: In Vivo Morphologic Characterization with Gadolinium-enhanced Double-oblique MR Imaging—Initial Results Radiology, May 1, 2002; 223(2): 566 - 573. [Abstract] [Full Text] [PDF]
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J. Wang, Y.-J. Geng, B. Guo, T. Klima, B. N. Lal, J. T. Willerson, and W. Casscells Near-infrared spectroscopic characterization of human advanced atherosclerotic plaques J. Am. Coll. Cardiol., April 17, 2002; 39(8): 1305 - 1313. [Abstract] [Full Text] [PDF]
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R. Corti, J. I. Osende, Z. A. Fayad, J. T. Fallon, V. Fuster, G. Mizsei, E. Dickstein, B. Drayer, and J. J. Badimon In vivo noninvasive detection and age definition of arterial thrombus by MRI J. Am. Coll. Cardiol., April 17, 2002; 39(8): 1366 - 1373. [Abstract] [Full Text] [PDF]
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L. J. Walker, A. Ismail, W. McMeekin, D. Lambert, A. D. Mendelow, and D. Birchall Computed Tomography Angiography for the Evaluation of Carotid Atherosclerotic Plaque: Correlation With Histopathology of Endarterectomy Specimens Stroke, April 1, 2002; 33(4): 977 - 981. [Abstract] [Full Text] [PDF]
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 C. Di Mario Vulnerable plaques: let's stop sinking on submerged icebergs? Eur. Heart J., March 1, 2002; 23(5): 349 - 351. [Full Text] [PDF]
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B. D. Coombs, J. H. Rapp, P. C. Ursell, L. M. Reilly, and D. Saloner Structure of Plaque at Carotid Bifurcation: High-Resolution MRI With Histological Correlation Stroke, November 1, 2001; 32(11): 2516 - 2521. [Abstract] [Full Text] [PDF]
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C. Yuan, L. M. Mitsumori, M. S. Ferguson, N. L. Polissar, D. Echelard, G. Ortiz, R. Small, J. W. Davies, W. S. Kerwin, and T. S. Hatsukami In Vivo Accuracy of Multispectral Magnetic Resonance Imaging for Identifying Lipid-Rich Necrotic Cores and Intraplaque Hemorrhage in Advanced Human Carotid Plaques Circulation, October 23, 2001; 104(17): 2051 - 2056. [Abstract] [Full Text] [PDF]
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X.-Q. Zhao, C. Yuan, T. S. Hatsukami, E. H. Frechette, X.-J. Kang, K. R. Maravilla, and B. G. Brown Effects of Prolonged Intensive Lipid-Lowering Therapy on the Characteristics of Carotid Atherosclerotic Plaques In Vivo by MRI: A Case-Control Study Arterioscler Thromb Vasc Biol, October 1, 2001; 21(10): 1623 - 1629. [Abstract] [Full Text] [PDF]
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S. Flacke, S. Fischer, M. J. Scott, R. J. Fuhrhop, J. S. Allen, M. McLean, P. Winter, G. A. Sicard, P. J. Gaffney, S. A. Wickline, et al. Novel MRI Contrast Agent for Molecular Imaging of Fibrin: Implications for Detecting Vulnerable Plaques Circulation, September 11, 2001; 104(11): 1280 - 1285. [Abstract] [Full Text] [PDF]
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M. T. Johnstone, R. M. Botnar, A. S. Perez, R. Stewart, W. C. Quist, J. A. Hamilton, and W. J. Manning In Vivo Magnetic Resonance Imaging of Experimental Thrombosis in a Rabbit Model Arterioscler Thromb Vasc Biol, September 1, 2001; 21(9): 1556 - 1560. [Abstract] [Full Text] [PDF]
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Z. A. Fayad and V. Fuster Clinical Imaging of the High-Risk or Vulnerable Atherosclerotic Plaque Circ. Res., August 17, 2001; 89(4): 305 - 316. [Abstract] [Full Text] [PDF]
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M. Kawasaki, H. Takatsu, T. Noda, Y. Ito, A. Kunishima, M. Arai, K. Nishigaki, G. Takemura, N. Morita, S. Minatoguchi, et al. Noninvasive quantitative tissue characterization and two-dimensional color-coded map of human atherosclerotic lesions using ultrasound integrated backscatter: Comparison between histology and integrated backscatter images J. Am. Coll. Cardiol., August 1, 2001; 38(2): 486 - 492. [Abstract] [Full Text] [PDF]
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R. Corti, Z. A. Fayad, V. Fuster, S. G. Worthley, G. Helft, J. Chesebro, M. Mercuri, and J. J. Badimon Effects of Lipid-Lowering by Simvastatin on Human Atherosclerotic Lesions: A Longitudinal Study by High-Resolution, Noninvasive Magnetic Resonance Imaging Circulation, July 17, 2001; 104(3): 249 - 252. [Abstract] [Full Text] [PDF]
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M.-L. M. Gronholdt, B. G. Nordestgaard, T. V. Schroeder, S. Vorstrup, and H. Sillesen Ultrasonic Echolucent Carotid Plaques Predict Future Strokes Circulation, July 3, 2001; 104(1): 68 - 73. [Abstract] [Full Text] [PDF]
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K. A. Shunk, J.e. Garot, E. Atalar, and J. A. C. Lima Transesophageal magnetic resonance imaging of the aortic arch and descending thoracic aorta in patients with aortic atherosclerosis J. Am. Coll. Cardiol., June 15, 2001; 37(8): 2031 - 2035. [Abstract] [Full Text] [PDF]
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K. J. Hunt, G. W. Evans, A. R. Folsom, A. R. Sharrett, L. E. Chambless, C. H. Tegeler, and G. Heiss Acoustic Shadowing on B-Mode Ultrasound of the Carotid Artery Predicts Ischemic Stroke : The Atherosclerosis Risk in Communities (ARIC) Study Stroke, May 1, 2001; 32(5): 1120 - 1126. [Abstract] [Full Text] [PDF]
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M. Stuber, R. M. Botnar, K. V. Kissinger, and W. J. Manning Free-Breathing Black-Blood Coronary MR Angiography: Initial Results Radiology, April 1, 2001; 219(1): 278 - 283. [Abstract] [Full Text]
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G.e. Helft, S. G. Worthley, V. Fuster, A. G. Zaman, C. Schechter, J. I. Osende, O. J. Rodriguez, Z. A. Fayad, J. T. Fallon, and J. J. Badimon Atherosclerotic aortic component quantification by noninvasive magnetic resonance imaging: an in vivo study in rabbits J. Am. Coll. Cardiol., March 15, 2001; 37(4): 1149 - 1154. [Abstract] [Full Text] [PDF]
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S. G. Ruehm, C. Corot, P. Vogt, S. Kolb, and J. F. Debatin Magnetic Resonance Imaging of Atherosclerotic Plaque With Ultrasmall Superparamagnetic Particles of Iron Oxide in Hyperlipidemic Rabbits Circulation, January 23, 2001; 103(3): 415 - 422. [Abstract] [Full Text] [PDF]
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R. M. Botnar, M. Stuber, K. V. Kissinger, W. Y. Kim, E. Spuentrup, and W. J. Manning Noninvasive Coronary Vessel Wall and Plaque Imaging With Magnetic Resonance Imaging Circulation, November 21, 2000; 102(21): 2582 - 2587. [Abstract] [Full Text] [PDF]
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X. Yang and E. Atalar Intravascular MR Imaging-guided Balloon Angioplasty With an MR Imaging Guide Wire: Feasibility Study in Rabbits Radiology, November 1, 2000; 217(2): 501 - 506. [Abstract] [Full Text]
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T. S. Hatsukami, R. Ross, N. L. Polissar, and C. Yuan Visualization of Fibrous Cap Thickness and Rupture in Human Atherosclerotic Carotid Plaque In Vivo With High-Resolution Magnetic Resonance Imaging Circulation, August 29, 2000; 102(9): 959 - 964. [Abstract] [Full Text] [PDF]
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Z. A. Fayad, V. Fuster, J. T. Fallon, T. Jayasundera, S. G. Worthley, G. Helft, J. G. Aguinaldo, J. J. Badimon, and S. K. Sharma Noninvasive In Vivo Human Coronary Artery Lumen and Wall Imaging Using Black-Blood Magnetic Resonance Imaging Circulation, August 1, 2000; 102(5): 506 - 510. [Abstract] [Full Text] [PDF]
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G. Pasterkamp, E. Falk, H. Woutman, and C. Borst Techniques characterizing the coronary atherosclerotic plaque: influence on clinical decision making? J. Am. Coll. Cardiol., July 1, 2000; 36(1): 13 - 21. [Abstract] [Full Text] [PDF]
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 B. Axisa, A. R. Naylor, N. London, P. R. F. Bell, and M. M. Thompson The Influence of Carotid Plaque Morphology on the Development of Cerebral Symptoms Vascular and Endovascular Surgery, July 1, 2000; 34(4): 309 - 318. [Abstract] [PDF]
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W. J. Rogers, J. W. Prichard, Y.-L. Hu, P. R. Olson, D. H. Benckart, C. M. Kramer, D. A. Vido, and N. Reichek Characterization of Signal Properties in Atherosclerotic Plaque Components by Intravascular MRI Arterioscler Thromb Vasc Biol, July 1, 2000; 20(7): 1824 - 1830. [Abstract] [Full Text] [PDF]
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S. G. Worthley, G. Helft, V. Fuster, Z. A. Fayad, O. J. Rodriguez, A. G. Zaman, J. T. Fallon, and J. J. Badimon Noninvasive In Vivo Magnetic Resonance Imaging of Experimental Coronary Artery Lesions in a Porcine Model Circulation, June 27, 2000; 101(25): 2956 - 2961. [Abstract] [Full Text] [PDF]
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Z. A. Fayad, T. Nahar, J. T. Fallon, M. Goldman, J. G. Aguinaldo, J. J. Badimon, M. Shinnar, J. H. Chesebro, and V. Fuster In Vivo Magnetic Resonance Evaluation of Atherosclerotic Plaques in the Human Thoracic Aorta : A Comparison With Transesophageal Echocardiography Circulation, May 30, 2000; 101(21): 2503 - 2509. [Abstract] [Full Text] [PDF]
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R Erbel, A Schmermund, S Mohlenkamp, S Sack, and D Baumgart Electron-beam computed tomography for detection of early signs of coronary arteriosclerosis Eur. Heart J., May 1, 2000; 21(9): 720 - 732. [PDF]
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 P. A. Tunick, G. A. Krinsky, V. S. Lee, and I. Kronzon Diagnostic Imaging of Thoracic Aortic Atherosclerosis Am. J. Roentgenol., April 1, 2000; 174(4): 1119 - 1125. [Full Text] [PDF]
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 S Manzi, L H Kuller, D Edmundowicz, and K Sutton-Tyrrell Vascular imaging: changing the face of cardiovascular research Lupus, March 1, 2000; 9(3): 176 - 182. [Abstract] [PDF]
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S. Aoki, H. Nakajima, H. Kumagai, and T. Araki Dynamic Contrast-Enhanced MR Angiography and MR Imaging of the Carotid Artery: High-Resolution Sequences in Different Acquisition Planes AJNR Am. J. Neuroradiol., February 1, 2000; 21(2): 381 - 385. [Abstract] [Full Text]
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 R A Coulden, H Moss, M J Graves, D J Lomas, D S Appleton, and P L Weissberg High resolution magnetic resonance imaging of atherosclerosis and the response to balloon angioplasty Heart, February 1, 2000; 83(2): 188 - 191. [Abstract] [Full Text]
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