(Circulation. 2000;102:959.)
© 2000 American Heart Association, Inc.
Clinical Investigation and Reports |
Visualization of Fibrous Cap Thickness and Rupture in Human Atherosclerotic Carotid Plaque In Vivo With High-Resolution Magnetic Resonance Imaging
From the Surgical Service (T.S.H.), VA Puget Sound Health Care System, Seattle, Wash; The Mountain-Whisper-Light Statistical Consulting (N.L.P.), Seattle, Wash; and the Departments of Pathology (R.R.) and Radiology (C.Y.), University of Washington (Seattle).
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Abstract |
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Background—The results of studies of advanced lesions of atherosclerosis suggest that the thickness of the fibrous cap that overlies the necrotic core distinguishes the stable lesion from one that is at high risk for rupture and thromboembolic events. We have developed a high-resolution MRI technique that can identify the fine structure of the lesion, including the fibrous cap, in vivo. The aim of the present study was to determine the agreement between in vivo MRI and lesion architecture as seen on histology and gross tissue examination to identify fibrous cap thickness and rupture.
Methods and Results—Twenty-two subjects who were scheduled for
carotid endarterectomy underwent MRI with a
3-dimensional multiple overlapping thin slab angiography protocol. The
appearance of the fibrous cap was categorized as (1) an intact, thick,
(2) an intact, thin, or (3) a ruptured fibrous cap on MRI, gross, and
histological sections. Thirty-six sites were available
for comparison between MRI and histology. There was a high level of
agreement between MRI and histological findings: 89%
agreement, 
(95% CI)=0.83 (0.67 to 1.0), weighted =0.87.
Spearman’s correlation coefficient was 0.88 (significant to the 0.01
level).
Conclusions—These findings indicate that high-resolution MRI with a 3-dimensional multiple overlapping thin slab angiography protocol is capable of distinguishing intact, thick fibrous caps from intact thin and disrupted caps in atherosclerotic human carotid arteries in vivo. This noninvasive technique has the potential to permit studies that examine the relationship between fibrous cap changes and clinical outcome and to permit trials that evaluate therapy intended to "stabilize" the fibrous cap.
Key Words: atherosclerosis • magnetic resonance imaging • imaging
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Introduction |
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Rupture of the fibrous cap, with the resultant exposure of thrombogenic subendothelial plaque constituents, is believed to be the critical event that leads to thromboembolic complications in atherosclerotic coronary and carotid artery disease. Falk1 noted that the majority of coronary thrombotic events are precipitated by fibrous cap rupture, and Carr et al2 found that the prevalence of plaque rupture was significantly higher among patients with a past history of an ischemic neurological event.
The mechanisms that lead to fibrous cap disruption are not well defined, in part because of a lack of animal models that mimic advanced atherosclerotic disease with plaque rupture. Therefore, much of what is known about fibrous cap rupture is based on histological studies of plaques excised at the time of surgery or during postmortem examination. A shortcoming of histological studies is that conclusions regarding the relationship between plaque features and clinical events must be based on histological findings from a single point in time. A prospective, serial examination of the lesion is needed to better understand the processes involved in the development of the high-risk atherosclerotic plaque. To accomplish this goal in vivo, an accurate, reproducible, and preferably noninvasive imaging tool that can characterize the fibrous cap is required.
MRI is ideal for serial studies of lesions of atherosclerosis over time because it is noninvasive and is superior to other imaging modalities in distinguishing soft tissue contrast. A number of studies have demonstrated that MRI can be used to identify morphological and compositional features of atherosclerotic plaque both in vitro and in vivo.3 4 5 6 7 8 9 10 11 12 13 Soila et al14 and Maynor et al8 published early reports that lipid components of atherosclerotic plaque can be distinguished with MRI. Toussaint et al13 noted that other plaque constituents, such as calcification, fibrous intimal tissue, and hemorrhage, could be identified in vivo in a series of 7 patients.
This study represents the first report in the literature of a noninvasive, high-resolution imaging technique that is capable of identifying the fibrous cap in atherosclerotic carotid arteries in vivo. A comparison with the examination of excised carotid endarterectomy specimens demonstrates a high level of agreement among MRI, histology, and gross examinations of the specimen.
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Methods |
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Study Population
Between June 1997 and May 1998, 22 consecutive patients scheduled to undergo carotid endarterectomy at the University of Washington Medical Center or the VA Puget Sound Health Care System were recruited for the study after informed consent was obtained. The consent forms and protocol were approved by the institutional review board of each facility. Each patient underwent an MRI study of the extracranial carotid arteries within 1 week before surgery.
MRI Protocol
All of the studies were conducted with a 1.5-T whole body
scanner (SIGNA, Horizon EchoSpeed, version 5.6/5.7; GE Medical
Systems). A custom-made phased-array carotid coil was used to improve
the signal-to-noise performance of the scanner.15
A head holder was used to maintain the subjects in a comfortable and
stable position. A 3-dimensional (3D) multiple overlapping thin slab
angiography (MOTSA) sequence, originally designed to visualize flowing
blood, was used to visualize arterial wall fine structure
in this study. The imaging parameters were TR 34 or 22 ms,
TE 2.9 to 4.4 ms, slice thickness 1 to 2 mm, field of view 13 to
16 cm, and matrix size 256x160 or 256x256. The number of excitations
were 1 for a matrix of 256x160 and 2 for a matrix of 256x256. A flip
angle of 25° was applied in all cases and was chosen to provide
adequate signal and contrast between vessel wall and flowing blood. The
imaging parameters varied due to the different sizes of
patients and the scan time available for the studies. The scan time
varied from 1 to 5 minutes. A best voxel size of 0.254x0.254x1
mm (0.065 mL) was achieved with zero padded Fourier transform.
The MRI appearance of the fibrous cap was categorized by a reader
(C.Y.) who was blinded to the histological findings.
The categories were (1) intact, thick fibrous cap, (2) intact, thin
fibrous cap, or (3) ruptured fibrous cap (Table 1
). On the basis of preliminary studies
with this 3D MOTSA protocol, we hypothesized that plaques with an
intact, thick fibrous cap would demonstrate a uniform dark band between
the bright lumen and the gray plaque core contents. Plaques with
intact, thin fibrous caps would be identified by the absence of the
dark band between the bright lumen and the gray plaque core. Recent
fibrous cap rupture would be identified by the absence of the dark band
between the lumen and the plaque core and the presence of a bright gray
region adjacent to the lumen, corresponding to recent plaque
hemorrhage or mural thrombus. The lumen surface may or may not
appear irregular, depending on the extent of plaque rupture and mural
thrombus formation. Image quality was rated from 1 to 5, with 5
representing best quality. Sections with an MRI quality
rating of 
2 were excluded from the analysis.
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Histological Processing
The atherosclerotic carotid plaques were excised intact without
disruption of the luminal surface of the lesion. This was accomplished
by scoring the adventitia and outer media with a scalpel and removing
the plaque as an intact tube. The formalin-fixed specimens were
decalcified, paraffin embedded, sectioned every 0.5 to 1.0 mm, and
stained as previously described.16 Readers (T.S.H. and
R.R.) who were unaware of the MRI findings classified the fibrous cap
in each histological section by using the same
categories described earlier (Table 1
). Caps with a uniform
thickness of >0.25 mm were categorized as thick. Plaques that
demonstrated any region with a cap thickness of <0.25 mm were
classified as thin. Recent fibrous cap rupture was identified by
evidence of recent mural thrombus or plaque hemorrhage, as
previously defined,16 adjacent to a disrupted fibrous
cap.
Coregistration
To ensure that matching cross sections were compared between MRI
and histology examination, the common carotid bifurcation was used as
an internal fiducial marker. The carotid bifurcation was defined as the
last cross section on which a single common carotid artery lumen was
identified. Therefore, by definition, the next sequential cross section
contained the 2 lumina of the internal and external carotid arteries. A
region that encompassed cross sections 2 mm proximal and 2 mm
distal to the bifurcation point was used for 1 comparison. The proximal
extent of the plaque into the common carotid artery was also identified
for a second comparison between MRI and histology. This region
encompassed the proximal 2 mm of the plaque.
Data Analysis
The values were determined to measure the level of agreement
between MRI and histology categorization of the fibrous cap. Unweighted
values, standard error for unweighted , and Spearman’s
correlation coefficients were calculated with SPSS for Windows (Version
7.5.1). Weighted was calculated as described by Fleiss and
Cicchetti.17 Full weight was given to perfect agreement,
half-weight was given to disagreement by 1 grade, and zero weight was
given to other disagreements.
The association of the histological appearance of the
fibrous cap at the 2 measurement points (the proximal end of the plaque
in the common carotid artery and in the carotid bifurcation region) was
also analyzed with weighted Cohen’s . The weighted
value was 0.03, indicating virtually no dependence or agreement.
Agreement between the MRI-rated grade for the appearance of the cap in
the common carotid artery and in the carotid bifurcation region was
also analyzed with Cohen’s . Weighted was 0.08. Because
it appears that there is no association between histology for the 2
regions or between MRI ratings for the regions, the regions were
considered independent. Each region was used as a separate observation
without any adjustment for the zero or negligible statistical
dependence.
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Results |
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Two subjects were excluded from the analysis because the MRI quality was poor throughout (rating of 1 and 2). One additional subject with a heavily calcified carotid plaque was excluded because the histological sections were not interpretable. Among the remaining 19 patients, data from 2 carotid bifurcation regions were excluded because the MRI quality was poor in 1 patient and the histological section was not interpretable in another. Therefore, of 44 possible cases, 36 observations were available for comparison between MRI and histology examinations.
Examples of thick, thin, and ruptured fibrous caps are demonstrated in
Figures 1 to 4.
The MRI appearance of an intact, thick fibrous cap is shown in Figure
1A; there is a uniform dark band between the bright lumen and
the gray plaque core. The lesion in Figure 1B would be
categorized as having an intact, thin fibrous cap, given the absence of
the dark band adjacent to the lumen. Figures 2A and 2B
demonstrate the MRI and matched histological cross
sections of another plaque with a thick fibrous cap. There are areas of
dense calcification at the 12- and 3-o’clock positions on the MRI and
histological cross sections. In Figure 3, a
series of axial common carotid artery images from 1 patient illustrate
how the cap appearance is not uniform, even within 1 cross section.
Figures 4A to 4C show an example of a plaque with fibrous cap
rupture on gross section, histology, and MRI, respectively, and
provides an explanation for the nonuniform appearance of the cap in
Figure 3. On the gross and histological sections
(Figures 4A and 4B), there is an area of cap rupture (arrow 1)
next to a region where the fibrous cap is thick (arrow 3). The cap
rupture site corresponds to a region where the dark band is absent and
a hyperintense, bright region is seen adjacent to the lumen on MRI
(Figure 4C). Furthermore, there is a hyperintense region in the
plaque core on MRI that corresponds to a region of recent intraplaque
hemorrhage on the gross and histological cross
sections (arrow 2).
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There was a high level of agreement between MRI and
histological findings, with a (95% CI) value of
0.83 (0.67 to 1.0) and a weighted value of 0.87 (Table 2). Spearman’s correlation coefficient
was 0.88 (significant to the 0.01 level). The level of agreement was
similarly high for distinguishing intact from ruptured fibrous caps
(Table 3; [95% CI]=0.85 [0.65 to
1.0]).
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Discussion |
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According to the National Center for Health Statistics, cardiovascular disease is the leading cause of death in the United States, and >70% of these deaths are related to atherosclerosis. Atherosclerotic cerebrovascular disease is the third leading cause of death and the leading cause of major disability among adults. Improved methods of diagnosis, treatment, and prevention of coronary and cerebrovascular atherosclerosis would result in significant improvement in quality of life and major savings in health care costs.
Traditionally, the severity of arterial stenosis has been used to identify the high-risk atherosclerotic plaque. However, in 1988, Ambrose et al18 and Little et al19 demonstrated in angiographic studies that mild-to-moderate coronary artery stenoses may lead to acute myocardial infarction and suggested that lumen narrowing was not the sole predictor for thrombotic events. Based on histopathological studies, Davies and Thomas,20 Fuster et al,21 and Falk1 suggested that plaque erosion or disruption was the critical feature in these moderately stenotic, high-risk lesions. Falk1 noted that >75% of major coronary thrombotic events were precipitated by atherosclerotic plaque rupture, resulting in the exposure of thrombogenic subendothelial plaque constituents. In a study that involved 44 carotid endarterectomy specimens (25 from asymptomatic patients and 19 from symptomatic patients), Carr2 noted plaque rupture in 74% of plaques from symptomatic patients compared with 32% of plaques from asymptomatic patients. Fibrous cap thinning was noted in 95% of symptomatic lesions and 48% of asymptomatic lesions.
To improve the identification of these high-risk lesions and to better understand the relationship between fibrous cap rupture and thromboembolic events, an accurate, reproducible imaging method of characterizing the fibrous cap in vivo is required. A number of reports suggest that intravascular ultrasound is capable of identifying cap rupture in coronary arteries.22 23 24 25 26 However, the technique is not optimally suited for serial studies given its invasive nature and the risks associated with catheterization. Optical coherence tomography has great promise for the assessment of the microstructure of the plaque, given its high resolution, which is on the order of 10 to 15 µm.27 28 29 However, to achieve this resolution, the vessel lumen must be replaced with saline due to attenuation from the presence of blood. Also, the depth penetration with optical coherence tomography is limited to 2 to 3 mm, which would permit only partial interrogation of larger vessels with advanced atherosclerosis.
The present study provides the first evidence that the appearance
of the fibrous cap on noninvasive, high-resolution MRI closely agrees
with gross and histological findings in advanced
atherosclerotic carotid plaques. The values were 0.83 for
distinguishing intact thick fibrous, intact thin caps, and ruptured
caps and 0.85 for distinguishing intact and ruptured caps. Kappa values
of >0.7 indicate good agreement between 2 tests. In 1 of the 36
comparisons, the fibrous cap was deemed ruptured on histology and was
thought to be intact on MRI. Possible explanations for disagreement
between histology and MRI include disruption of the cap caused by
surgical manipulation or histological sectioning,
problems with misregistration of sections in the comparison of
histology with MRI, and insufficient image resolution to detect small
areas of fibrous cap disruption. Last, although the case numbers are
small, the observed sensitivity and specificity for the identification
of fibrous cap rupture were promising (89% and 96%, respectively).
Although suggestive, more research is needed to establish the
sensitivity, specificity, and positive and negative predictive values
of the MRI examination, because the 95% CIs for data in the
present study are wide.
For this study, a thickness of 0.25 mm was chosen as the level for distinguishing thick and thin fibrous caps. The threshold thickness that poses an increased risk for cap rupture has not been established in a prospective study of carotid arteries. However, in a study that compared morphological features in carotid endarterectomy specimens harvested from asymptomatic and symptomatic patients, Bassiouny et al30 found that the distance between the necrotic core and lumen was 0.27 mm in symptomatic lesions and 0.5 mm in asymptomatic lesions.
The 3D MOTSA imaging sequence used in this project was originally developed as a MR angiography (MRA) technique to study vessel lumen caliber.31 32 The technique, which is relatively simple to implement, provides enhanced signal from flowing blood and a mixture of T1 and proton density contrast weighting. In typical application, the imaging parameters for MRA are chosen to suppress background signal to increase the contrast between the blood and stationary surrounding soft tissues. However, we have previously shown that this time-of-flight (TOF) technique can be used to visualize not only flowing blood but also structures within the vessel wall.33 Although a number of investigators have shown that spin echo– or fast spin echo–based MR sequences such as T1-, proton density–, and T2-weighted imaging can identify plaque constituents such as the lipid core, intraplaque hemorrhage, and calcification.,3 5 13 34 35 36 to date, there have been no reports in the literature that suggest the fibrous cap can be identified with spin echo– or fast spin echo–based MR sequences.
The appearance of a dark band in TOF images has been incidentally noted in previous reports.37 38 In a study that examined the temporal changes of carotid wall enhancement after the injection of MR contrast material, Aoki et al38 described the presence of a hypointense inner rim on the TOF images and postulated that this represented the intima. Räsänen et al37 noted that fibrous intimal thickening noted on intravascular ultrasound was seen as a hypointense region on 3D TOF MRA, but the study did not have histological verification of these findings.
Von Ingersleben et al39 postulated that the hypointense region may be due to the layered, organized structure seen in collagen-rich, thick fibrous caps. The layered structure seen in this type of fibrous cap would shorten T2 times, thus leading to the dark appearance in the 3D MOTSA image. We would not expect to see a dark band with fibrous caps that have a less-organized structure, such as those that are undergoing degradation by matrix metalloproteinases. Although we did not examine the specimens for matrix metalloproteinase activity in the present study, we are currently testing the hypothesis that the dark band is absent with caps undergoing matrix degradation. If proved correct, these results will lend further support to the favorable prognosis associated with this MRI finding.
Difficulties with MRI interpretation may arise from motion artifacts due to patient movement, swallowing, and artery wall pulsation. We developed a custom-made support device that permits the subject to lie comfortably and to minimize movement. A technique that avoids the acquisition of data during patient swallowing by tracking the motion of the larynx is currently under evaluation, and vessel wall motion artifact from arterial pulsation can be reduced with cardiac gating. Dense calcification, if located adjacent to the lumen, will also appear as a dark region on MRI and may be confused with the appearance of a thick fibrous cap. However, this problem can be reconciled by examining the spin echo images, because calcification will appear dark on T1-, T2-, and proton density–weighted images, whereas the fibrous tissue will appear gray. Last, identification of finer structures within the diseased arterial wall will require higher image resolution. Further improvement in image resolution is possible with unilateral coil design, high matrix size imaging, modification of imaging parameters, and improved, faster hardware.
The eventual goal is to apply this noninvasive technique to the identification of high-risk coronary artery lesions. However, there are significant obstacles that must be addressed, such as cardiac motion and small vessel structure, through shortening of image acquisition times, gating, and improvement in resolution. Future directions include investigation of the biomechanical forces, such as shear and circumferential stress on the fibrous cap, with either ultrasound or MRI. Studies by Meairs and Hennerici40 and Iannuzzi et al41 suggest that ultrasound is capable of quantifying wall motion in carotid atherosclerosis and that there appears to be a relationship between lesion motion and a prior history of ischemic neurological events. Preliminary studies in our laboratory indicate that it is technically feasible to quantify flow and wall motion with MRI, but this work is in its early stages and needs considerable development and validation.
In summary, the present findings demonstrate a high level of agreement between high-resolution in vivo MRI, gross, and histological findings on the thickness and sites of potential rupture of the fibrous cap in advanced carotid artery atherosclerosis. MRI may have important applications in natural history studies and in clinical trials that examine the process of cap thinning and disruption and may ultimately provide an accurate, noninvasive diagnostic and prognostic tool to treat and prevent the sequelae of this insidious disease.
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Acknowledgments |
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This work was supported by NIH grants R01-HL-60213 and R29-HL-56874 and by the Whitaker Foundation. The authors wish to acknowledge Randy Small and Roderick Brown for their excellent work with the histological processing, Denise Echelard and Vern Terry for their help in acquiring the MRIs, and the late Dr Russell Ross, whose insight, expertise, and encouragement will be greatly missed.
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Footnotes |
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Reprint requests to Thomas S. Hatsukami, MD, VA Puget Sound Health Care System, Surgical Service (112), 1660 S Columbian Way, Seattle, WA 98108.
Received October 21, 1999; revision received March 23, 2000; accepted March 28, 2000.
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J. N. Redgrave, P. Gallagher, J. K. Lovett, and P. M. Rothwell Critical Cap Thickness and Rupture in Symptomatic Carotid Plaques: The Oxford Plaque Study Stroke, June 1, 2008; 39(6): 1722 - 1729. [Abstract] [Full Text] [PDF]
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 K. Yoshida, O. Narumi, M. Chin, K. Inoue, T. Tabuchi, K. Oda, M. Nagayama, N. Egawa, M. Hojo, Y. Goto, et al. Characterization of Carotid Atherosclerosis and Detection of Soft Plaque with Use of Black-Blood MR Imaging AJNR Am. J. Neuroradiol., May 1, 2008; 29(5): 868 - 874. [Abstract] [Full Text] [PDF]
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 T. Saam, H. R. Underhill, B. Chu, N. Takaya, J. Cai, N. L. Polissar, C. Yuan, and T. S. Hatsukami Prevalence of American Heart Association type VI carotid atherosclerotic lesions identified by magnetic resonance imaging for different levels of stenosis as measured by duplex ultrasound. J. Am. Coll. Cardiol., March 11, 2008; 51(10): 1014 - 1021. [Abstract] [Full Text] [PDF]
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 J. C. Wu, F. M. Bengel, and S. S. Gambhir Cardiovascular Molecular Imaging Radiology, August 1, 2007; 244(2): 337 - 355. [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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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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D. Saloner, G. Acevedo-Bolton, M. Wintermark, and J. H. Rapp MRI of Geometric and Compositional Features of Vulnerable Carotid Plaque Stroke, February 1, 2007; 38(2): 637 - 641. [Abstract] [Full Text] [PDF]
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 B. G. Rubin Impact of Plaque Characterization on Carotid Interventions Perspectives in Vascular Surgery and Endovascular Therapy, December 1, 2006; 18(4): 312 - 315. [Abstract] [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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G. Stoll and M. Bendszus Inflammation and Atherosclerosis: Novel Insights Into Plaque Formation and Destabilization Stroke, July 1, 2006; 37(7): 1923 - 1932. [Abstract] [Full Text] [PDF]
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B. Chu, C. Yuan, N. Takaya, J. R. Shewchuk, A. W. Clowes, and T. S. Hatsukami Serial High-Spatial-Resolution, Multisequence Magnetic Resonance Imaging Studies Identify Fibrous Cap Rupture and Penetrating Ulcer Into Carotid Atherosclerotic Plaque Circulation, March 28, 2006; 113(12): e660 - e661. [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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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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 P. Raggi, A. Taylor, Z. Fayad, D. O'Leary, S. Nissen, D. Rader, and L. J. Shaw Atherosclerotic Plaque Imaging: Contemporary Role in Preventive Cardiology Arch Intern Med, November 14, 2005; 165(20): 2345 - 2353. [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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A. van der Lugt From Case Study to Prospective Study Stroke, November 1, 2005; 36(11): 2337 - 2338. [Full Text] [PDF]
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 E. K. Fishman Multidetector-row computed tomography to detect coronary artery disease: the importance of heart rate Eur. Heart J. Suppl., August 1, 2005; 7(suppl_G): G4 - G12. [Abstract] [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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L. V. Hofmann, R. P. Liddell, J. Eng, B. A. Wasserman, A. Arepally, D. S. Lee, and D. A. Bluemke Human Peripheral Arteries: Feasibility of Transvenous Intravascular MR Imaging of the Arterial Wall Radiology, May 1, 2005; 235(2): 617 - 622. [Abstract] [Full Text] [PDF]
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