Download MRI of the vulnerable carotid plaque

Investigations and research
MRI of the vulnerable carotid plaque
C.Yuan
N. Balu
B.C. Chu
T. Hatsukami
Vascular Imaging Laboratory, Department of Radiology,
University of Washington, Seattle, WA, USA.
1
Stroke due to atherosclerotic disease is a major
cause of disability and death all over the world.
Atherosclerotic plaque rupture in the internal
carotid arteries and subsequent thrombosis and/
or embolism is believed to be the major factor in
stroke or transient ischemic attack (TIA).
Carotid atherosclerosis is marked by plaque
deposition, mainly at the bifurcation of the
common carotid artery into the internal and
external carotid arteries. Increased sequestration
of circulating cholesterol into the vessel wall leads
to the development of lipid pools and eventually
large lipid cores. Ensuing inflammation and
angiogenesis cause intraplaque hemorrhage and
necrosis to form a thrombogenic necrotic core
separated from the lumen by a well-defined
fibrous cap. Identification of the plaque that is
vulnerable to rupture at this stage is of primary
importance if thrombosis or embolism is to be
prevented. The steps involved in the progression
to possible stroke are shown in Figure 1.
Traditionally, luminal stenosis has been used as
a measure of carotid atherosclerotic disease.
Recent studies have shown that luminal stenosis
may not be the only causation of symptoms, but
that plaque composition may also impact disease
outcome. Although angiography is still used to
decide whether patients will receive surgical
treatment (endarterectomy) or other interventions,
it is increasingly recognized that a large
proportion of vulnerable plaques cannot be seen
by angiography. Non-invasive high-resolution
MRI can identify these angiographically silent
but potentially vulnerable plaques.

Figure 1. Schematic of stages of the
atherosclerotic plaque:
• Initial lipid deposition leads to a
fatty streak.
• Further lipid deposition leads to
the formation of the lipid core
formation with an intact overlying
fibrous cap.
• Calcifications may develop. Note
that the luminal area is preserved
by outward plaque growth (vessel
wall remodeling) in these early
stages.
• Luminal compromise occurs in
later stages. Intraplaque
hemorrhage may occur. Small
ruptures expose the thrombogenic
core to the blood stream.
• A thrombus may develop, leading
to symptomatic occlusion or
embolism.
Components such as lipid/necrotic core and
hemorrhage, along with inflammation, are
currently considered vulnerability markers
regardless of plaque size. MRI can easily visualize
and quantify these components. These are
valuable capabilities, not only in diagnosis but
also in the study of atherosclerosis progression
and in pharmaceutical clinical trials.
This article reviews the currently established
procedure for plaque characterization by MRI.
It addresses the technical advances in coils,
sequences, imaging protocols and postprocessing methods for quantification, followed
by examples of the MR appearance of plaque
components. The article concludes with a
discussion of the current state of the art imaging
as implemented on a Philips Achieva 3T scanner.
 This article reviews the
currently established
procedure for plaque
characterization by MRI.
MRI of the carotid atherosclerotic
plaque
The widely accepted AHA classification of
atherosclerotic plaques is based on plaque
composition [1]. A modified AHA classification
[2] based on the MR appearance of plaque
components was shown to have good correlation
MEDICAMUNDI 52/1 2008/07
57
with the traditional AHA classification, suggesting
that MRI is a reliable way to characterize plaque
composition.
 Detecting vulnerable
plaque in vivo is the
primary purpose of
atherosclerotic plaque
imaging.
The detection of the vulnerable plaque in vivo is
considered to be the primary purpose of
atherosclerotic plaque imaging. Histological
studies of vulnerable plaques indicate that plaque
composition is a primary determinant of plaque
vulnerability [3, 4]. Histological criteria for the
vulnerable plaque are known from cross-sectional
studies. Imaging markers corresponding to many
of those criteria have been identified in the last
decade [5-8]. MRI possesses unique features
which can reveal a wide range of information,
including excellent soft tissue contrast, ability
to visualize plaque morphology and tissue
constituents, and the ability to quantify those
components [9]. Several markers of plaque
vulnerability can be identified by MRI [10]:
• Large lipid-rich necrotic core
• Intra-plaque hemorrhage
• Surface disruption
• Inflammation
• Surface calcific nodules
Technical advances
Plaque characterization requires high spatial
resolution with good blood-suppression and
enhancement. MR plaque characterization has
been made possible by recent advances in the
design of coils, sequences and post-processing
algorithms targeted to these needs.
Coils
 Quantification of plaque
components requires
high resolution and good
signal-to-noise ratio.
Quantification of plaque components requires
both high resolution and good signal-to-noise
ratio (SNR). Therefore, receiver coils need to be
tailored specifically to the needs of carotid
imaging. Small field-of-view surface phased array
coils have been shown to be ideally suited for
this purpose. Array coils for carotid imaging are
designed to provide good SNR at a depth of
about 4 cm from the surface. Hayes et al.
demonstrated a four-channel phased array coil
construction that performs well for carotid
imaging [11]. This has continued to be a standard
setting design. A suitable head restrainer and
positioner is an integral part of the coil design
to ensure patient comfort and reproducible
patient positioning for serial studies.
Sequences
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A comprehensive assessment of plaque
morphology and composition requires a multicontrast time-efficient protocol with good
blood-suppression and enhancement, high
resolution and high SNR. Currently established
multi-contrast protocols use a combination of
bright blood (Time-of-Flight (TOF) MRA),
black-blood and contrast-enhanced imaging.
The vessel wall and plaque components are best
characterized on high-resolution black-blood
sequences while TOF provides complimentary
angiography. Contrast-enhanced MRI improves
delineation of plaque components. Dynamic
contrast-enhanced MRI (DCE) provides
information about functional characteristics such
as inflammation and neovasculature. Sequences
targeted at specific plaque components may also
be added to the protocol.
Blood-suppression techniques
Excellent blood suppression is mandatory for
plaque characterization. Several new timeefficient techniques have been developed for
black-blood imaging:
• Multi-slice double inversion recovery (MDIR)
• Quadruple inversion recovery (QIR)
• Motion-sensitized driven equilibrium (MSDE)
Multi-slice double inversion recovery (MDIR)
Double inversion recovery (DIR), in which a
non-selective inversion followed by a sliceselective re-inversion nulls the blood signal after
an inversion delay, provides adequate bloodsuppression. However, the DIR preparation was
initially developed as a single-slice technique
and is time-inefficient. Several multi-slice DIR
mechanisms have been recently proposed to
improve scan time. The technique proposed by
Yarnykh et al., which uses a slab-selective
re-inversion pulse to acquire up to eight slices
per TR interval with good blood suppression
[12], has been found to be SAR efficient and is
thus desirable for high-field imaging.
Quadruple inversion recovery (QIR)
The DIR inversion time (TI) is blood T1
dependent. The TI therefore changes when
T1-shortening contrast agents such as
gadolinium are injected. This requires separate
sequence parameter optimization for pre- and
post-contrast scans. In this case, the image
contrast will be a function of both sequence
parameters and contrast enhancement. The
QIR technique solves this problem by
employing two DIR blocks with two different
TIs [13]. By adjusting the TIs, nulling of the
blood signal can be achieved over a wide range
of T1, covering both pre- and post-contrast
blood T1. Thus the same sequence parameters
can be used for pre- and post-contrast scans
allowing quantitative measurements of contrast
enhancement in the vessel wall.
Motion-sensitized driven equilibrium (MSDE)
Slow and re-circulating blood flows produce
plaque-mimicking artifacts near the carotid

Figure 2. A plaque-mimicking flow
artifact (arrow) is visible in the image
obtained with DIR in an oblique
black-blood MRA (left), but is
removed with the application of an
MSDE pre-pulse (center). The images
on the right show an axial section
obtained with MDIR, QIR and MSDE
preparations, respectively. There is
well-defined distinction between
the vessel lumen and wall on MSDE
(center) compared with MDIR (left).
2
bifurcation, sometimes even with DIR and
MDIR preparation, because blood in the imaging
slab is not completely replaced by fresh blood
inflow. Recently a new black-blood preparation
referred to as Driven-Equilibrium Fourier
Transform (DEFT) [14] or Motion-Sensitized
Driven Equilibrium (MSDE) [15] has been
introduced to surmount this problem. The
MSDE preparation refocuses stationary spins
while destroying moving spins, and has been
shown to provide better suppression of slow
flowing blood when compared with DIR [15]
(Figure 2).
Contrast-enhanced MRI
Contrast-enhanced MRI improves plaque tissue
contrast and provides additional information
about the presence of macrophages [16] and
neovasculature [17]. This information is obtained
from modeling the transfer kinetics of contrast
into the plaque and is otherwise not obtainable
from standard contrast weightings. Thus both
a post-contrast T1 weighted sequence and
dynamic CE-MRI (DCE) can be included in a
standardized protocol. This use of contrast agents
is for research purposes only and not for the
purposes of diagnoses.
Image processing
Image processing methods and software are for
research purposes only and not FDA approved.
They are used for investigational studies and are
not commercially available. Quantitative plaque
analysis is important for identification of
vulnerable plaque. Vessel wall and plaque
components have to be identified and segmented
from multi-contrast images before quantification
is possible. Furthermore, precision and
reproducibility of measurements is important
where small treatment effects have to be
discerned in limited study populations. Image
misregistration is a major impediment to
reproducible measurements, especially in clinical
trials or natural history studies that contain
several imaging sessions spanning months or
years. Specialized algorithms to overcome these
problems have been collected into a plaque
analysis package (CASCADE) [17]. Efficient
workflow and semi-automated image review
help reviewers translate their findings into
precise repeatable quantitative plaque
measurements for clinical trials involving
multiple image readings.
The image review process starts with matching
all contrast weightings by using the carotid
bifurcation as the landmark. Lumen and outer
wall contours are drawn by semi-automated
algorithms [18]. After the lumen is identified on
one contrast weighting, image locations are
accurately registered by an active contour map
method. A morphology-based probabilistic
segmentation algorithm [19] can segment these
registered multi-contrast images into plaque
components. A rendering of the 3D distribution
of plaque components (Figure 3) helps in
comprehensive review and correction of contours.
The radiologist reviews the results and corrects
the contours if necessary. The final plaque
measurements are derived from the radiologist’s
contours. Derived measurements may vary
according to the study design. For example, a
carotid risk score may be derived for each patient
in a patient risk stratification study.
 Contrast-enhanced
MRI improves plaque/
tissue contrast and adds
valuable information.
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
Figure 3. 3D distribution of carotid
atherosclerotic plaque components
segmented from axial multi-contrast
high-resolution MRI at 3T.
Two 3D views (A, B) show the
complex structure of plaque as
visualized by MRI. The plane (green)
on (B) corresponds to the level of
the axial slices shown (C, D).
Contours drawn on the axial images
are shown in (C) with the
corresponding post-contrast image (D).
3

Figure 4. Example of histological
validation of MRI at four consecutive
locations spanning the bifurcation.
Multiple histological sections (at 0.5
to 1.0 mm separation) generally
correspond to each 2 mm thick MR
image. Contours have been drawn for:
 lumen (red)
 outer wall (cyan)
 LR/NC (yellow)
 calcification (black)
 loose matrix (pink/white)
 hemorrhage (orange).
4
H&E indicates hematoxylin-eosin.
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
Figure 5. Multi-contrast weighted
high-resolution 3T MR shows the
presence of a lipid-rich necrotic core
(arrow) at the left carotid bifurcation.
The core produces iso-intense signals
on TOF, T1W, and a slightly
hyper-intense signal on T2W.
However, the CE T1W image has a
clear demarcation of the core
boundary due to the absence of
neovasculature or loose matrix into
the necrotic core.
5
Dynamic contrast information requires
separate processing algorithms. DCE requires
accurate registration of the dynamic series for
obtaining contrast enhancement curves. A
targeted registration algorithm (KFRS) has
been implemented for this purpose [20]. By
modeling the exchange kinetics between the
blood and tissue compartments, Kerwin et al.
obtained a quantitative index of fractional
plasma volume (Vp) and transfer constant (Ktrans)
of contrast into the extracellular space, from the
contrast enhancement curves. Vp correlates well
with plaque neovasculature [17] while Ktrans is
indicative of plaque inflammation [21].
Plaque characterization by MRI
Drawing on a decade of experience obtained
from reviewing hundreds of subjects, Yuan et al.
developed an MRI classification of carotid
atherosclerotic plaque [3]. This classification
has been validated against histology (Figure 4)
and is being further refined with new
technological advances. The currently accepted
signal characteristics of plaque morphology and
components are discussed below.
Vessel morphology
Vessel wall boundaries are used to measure the
volume and extent of atherosclerotic plaque
burden. Black-blood imaging is important for
the identification of the lumen boundary.
Outer wall boundaries are best visualized on
T1W and PDW images and are dependent on
adequate fat suppression and the signal-to-noise
ratio (SNR). Wall thickness measurements can
be calculated once the lumen and outer wall
boundaries are identified, and have been shown
to correlate well with ultrasound intima media
thickness measurements [18].
The change in plaque burden is often used as
the endpoint in clinical trials. Accurate and
reproducible measurement of vessel wall
boundaries are therefore crucial. Use of
semi-automated tools for plaque burden assessment
has not only reduced the effort required by the
radiologist but also improved the reproducibility
of measurement.
 Semi-automated tools
for plaque burden
assessment reduce
effort and improve
reproducibility.
Detection of lipid/necrotic core
The lipid pools of early plaques change with
increased hemorrhage and inflammation into a
necrotic core filled with blood and necrotic debris.
Consequently the appearance of the necrotic
core on MRI is often variable. A pure lipid core
with no hemorrhage is generally hyper-intense on
T1W and PDW and iso-intense on T2W and TOF.
In the presence of hemorrhage the signal
characteristics of hemorrhage (hyper-intense on
TOF) predominate.
The margins of the lipid core are best
appreciated by comparing the pre- and post-CE
images, because the lipid core and hemorrhage
are slow to enhance in post-contrast. Since lipid
cores tend to be large, MRI can measure them
with reasonable precision. Thus they are good
candidate parameters in clinical studies since
they are the direct targets of lipid-lowering drugs
used in attempts to stabilize the plaque.
A representative case is shown in Figure 5.
MEDICAMUNDI 52/1 2008/07
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
Figure 6. Multi-contrast weighted
high-resolution 3T MR shows the
presence of intraplaque hemorrhage
in the common carotid artery.
Intraplaque hemorrhage at 3T is
characterized by a slight hyper-intense
signal on 3D TOF; hyper-intensity
on T1W and PDW; and hypointensity on T2W, depending on the
age of the hemorrhage. However
MPRAGE gives a striking hyperintense signal that corresponds well
with areas of hemorrhage on the
matching histology.
6

Figure 7. Multi-contrast weighted
high-resolution MR readily shows
the presence of a large ulceration in
the atherosclerotic plaque of the
right internal carotid (long arrow).
The lower signal inside the ulcer on
TOF, when compared to the signal
in the parent internal and external
carotid arteries, indicates turbulent
flow. The turbulence is also visualized
as a thin irregular line in the four black
blood images (short arrows).
The oblique black blood MRA (OB
BB MRA) confirms the presence of
the large ulceration.
7
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Detection of hemorrhage
Detection of rupture
Hemorrhage can be identified by using
multiple contrast weightings. Methemoglobin
content varies depending on the age of
hemorrhage, thereby altering signal intensities.
Type-I (fresh) hemorrhages are bright on TOF
and T1W but iso-intense or hypo-intense on
PDW and T2W images. Type-II (recent)
hemorrhages are bright on all pre-contrast
weightings [6]. Recently, direct thrombus
imaging (MP-RAGE) has been shown to be
sensitive for hemorrhage/thrombus detection
[22]. A representative case is shown in Figure 6.
Rupture of the fibrous cap can be detected on
MRI [23] and is often associated with
symptomatic status [24]. The thickness of the
cap can be measured using post-contrast images
[5]. Ulceration after rupture can be identified
on TOF as a bright indentation into the lumen
surface indicative of blood flow into the ulcer.
A representative case is shown in Figure 7.
Detection of inflammation
Unlike other plaque components, inflammation
is an active biological process. DCE can be used

Figure 8. Contrast enhanced T1W
(CE T1W) (left) shows a large plaque
with a non-enhancing lipid rich
necrotic core (arrow).
A corresponding parametric image
(right) obtained from contrast
enhancement curves shows the blood
pool fraction in red, and the transfer
constant for the diffusion of contrast
into the extracellular space in green.
Note the enhancement of the luminal
and adventitial surfaces due to
contrast diffusing directly through
the luminal surface and vasa vasorum,
respectively. This use of contrast
agents is for research purposes only
and not for the purposes of diagnoses.
8
9

Figure 9. Due to the high resolution
of 3T a small area of speckled
calcification is readily visible as a
hypo-intense signal (arrows) in all
contrast weightings. Matched
histology is outlined to show the
boundary of the calcification.
to measure the permeability of tissues by
visualizing the diffusion of contrast out of
vascular spaces and into the surrounding tissues
(Figure 8). Ktrans measured from kinetic modeling
of DCE images correlates well with plaque
inflammation [21]. In addition, ultrasmall
superparamagnetic iron oxide particles (USPIOs)
have been shown to produce hypo-intense signals
in areas of macrophage density [25]. The use of
contrast agents is for research purposes only and
not for the purposes of diagnoses.
Detection of calcification
Calcification appears hypo-intense on all image
weightings (Figure 9). Highly calcified plaques
have historically been thought to be more stable
than non-calcific plaques. However, calcified
plaques containing calcium nodules protruding
into the lumen can trigger coagulative pathways
leading to thrombosis and/or embolism [26].
State of the art
An optimized high-resolution carotid imaging
protocol implemented on the Philips Achieva
3T platform is currently being used in several
research studies. The protocol, based on the latest
advances in black-blood imaging, is described
below:
• A standard three-plane survey is followed by a
2D MRA to locate the A/P coordinates of the
carotid bifurcation.
• An oblique MSDE black-blood Turbo spin-echo
(TSE) sequence is used to find the exact S/I
coordinates of the bifurcation.
• An axial geometry centered on the bifurcation
and covering both arteries is then determined.
• PDW MDIR TSE, T2W MDIR TSE, T1W
QIR TSE, 3D TOF (3D T1-Fast Field Echo
(FFE) MRA), 3D MP-RAGE (3D T1-FFE
with IR preparation and ProSet) are acquired.
MEDICAMUNDI 52/1 2008/07
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• A dynamic T1-FFE with 12 slices, 20 phases
per slice is acquired within 4.5 min immediately
after a single-dose gadolinium-based contrast
agent injection (2 phases pre-contrast).
• A post-contrast T1W QIR TSE is also obtained
with the same parameters as pre-contrast.
The total scan time for this comprehensive
carotid imaging protocol with 0.63 mm in-plane
acquired resolution (0.25 mm interpolated),
2 mm slice thickness and 20 slices is less than
35 minutes for bilateral arteries on a Philips
Achieva 3T scanner. All axial images are obtained
with the same geometry so that they can be used
for multi-contrast analysis. Carotid plaque
measurements are not influenced by cardiac
gating [27]. Thus, gating is generally not
required for carotid plaque imaging. An example
of using this protocol can be found in Figure 5.
 Early identification and
treatment of vulnerable
plaque could reduce
morbidity and mortality.
Quantitative plaque measurements derived from
these images using custom-built software
implementing the segmentation and registration
algorithms described earlier, are currently being
used in pharmaceutical trials and natural history
studies. A carotid artery risk score describing the
vulnerable plaque components derived from
plaque analysis is being assessed for its efficacy
to identify high-risk subjects. The custom-built
software is not an FDA approved device, and is
used for research and investigational purposes
only.
Future of plaque imaging
Reduction of plaque burden, as detected by
MRI, has been used as the primary endpoint in
clinical trials involving lipid-lowering drugs
[28]. Reduction in plaque burden as well as
lipid content [29] of atherosclerotic plaque has
been reported in clinical trials. Large-scale
multi-center clinical trials using carotid MRI
are feasible based on current technology. The
move towards this goal can be seen by the
concerted efforts to standardize imaging
protocols in trials involving multiple imaging
centers and the increased participation by
equipment vendors in coil and sequence
development for carotid MRI.
If vulnerable plaques can be identified and
treated appropriately before they become
symptomatic, morbidity and mortality
associated with stroke could be significantly
reduced. Selection of patients for treatment
based on plaque vulnerability has the potential
to lower health care costs by reducing
unnecessary interventions or the subsequent
devastating cost of stroke. Identifying new
imaging markers for the vulnerable
atherosclerotic plaque is an area of active research
and carotid MRI is quickly establishing itself as
the best non-invasive imaging modality used to
identify vulnerable carotid plaque.
Acknowledgements
The authors would like to thank Marina
Ferguson, MT, Vasily Yarnykh, PhD, and
Zach Miller, MFA, for their assistance with
this manuscript 
References
[1] Stary HC et al. 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. Circulation 1995;
92(5): 1355-1374.
[2] Cai JM, Ferguson MS, Polissar N, Hatsukami TS, Yuan C.
Classification of Human Carotid Atherosclerotic Lesions using In Vivo
Multi-Contrast MR Imaging. Circulation 2002; 106: 1368-1373.
[3] Virmani R, Ladich ER, Burke AP, Kolodgie FD. Histopathology of
the Carotid Atherosclerotic Plaque. Neurosurgery 2006 Nov; 59(5
Supple 3): S219-27; discussion S3-13.
64
MEDICAMUNDI 52/1 2008/07
[4] Lusby RJ, Ferrell LD, Ehrenfeld WK et al. Carotid Plaque
Hemorrhage. Its Role in Production of Cerebral Ischemia. Arch Surg
1982; 117: 1479-1488.
[5] Cai J, Hatsukami TS, Ferguson MS, Kerwin WS, Saam T, Chu B
et al. In Vivo Quantitative Measurement of Intact Fibrous Cap and
Lipid Rich Necrotic Core in Atherosclerotic Carotid Plaque: A
Comparison of High Resolution Contrast Enhanced MRI and
Histology. Circulation 2005; 112: 3437-3444.
[6] Takaya N, Yuan C, Chu BC, Saam TS, Polissar NL, Jarvik G et al.
Presence of Intraplaque Hemorrhage Stimulates Progression of Carotid
Atherosclerotic Plaques: A High-Resolution MRI Study. Circulation
2005; 111: 2768-2775.
[7] Chu BC, Ferguson MS, Underhill H, Takaya N, Cai J, Kliot M et
al. Detection of Carotid Atherosclerotic Plaque Ulceration,
Calcification, and Thrombosis by Multi-Contrast Weighted MRI.
Circulation 2005; 112(1): e3-4.
[19] Liu F, Xu D, Ferguson MS, Chu B, Saam T, Takaya N, Hatsukami
TS et al. Automated In Vivo Segmentation of Carotid Plaque MRI
with Morphology-Enhanced Probability Maps. Magnetic Resonance
in Medicine 2006; 55(3): 659-668.
[8] Kampschulte A, Ferguson MS, Kerwin WS, Polissar NL, Chu B,
Saam T et al. Differentiation of Intraplaque Versus Juxtaluminal
Hemorrhage/Thrombus in Advanced Human Carotid Atherosclerotic
Lesions by In Vivo Magnetic Resonance Imaging. Circulation. 2004;
110: 3239-3244.
[20] Kerwin WS, Cai J, Yuan C. Noise and Motion Correction in Dynamic
Contrast-Enhanced MRI for Analysis of Atherosclerotic Lesions.
Magnetic Resonance in Medicine 2002; 47(6): 1211-1217.
[9] Saam T, Ferguson MS, Yarnykh VL, Takaya N, Xu D, Polissar NL
et al. Quantitative Evaluation of Carotid Plaque Composition by In
Vivo MRI. Arteriosclerosis, Thrombosis, and Vascular Biology
2005; 25: 234-239.
[10] erguson MS, Yuan C. The Vulnerable, or High-Risk, Atherosclerotic
Plaque: Noninvasive MR Imaging for Characterization and Assessment.
Radiology 2007; 244(1): 64-77.
[11] Hayes CE, Mathis CM, Yuan C. Surface Coil Phased Arrays for
High-Resolution Imaging of the Carotid Arteries. Journal of Magnetic
Resonance Imaging 1996; 6(1): 109-112.
[12] Yarnykh VL, Yuan C. Multislice Double Inversion-Recovery BlackBlood Imaging with Simultaneous Slice Reinversion. Journal of
Magnetic Resonance Imaging 2003; 17(4): 478-483.
[13] Yarnykh VL, Yuan C. T-1-Insensitive Flow Suppression using
Quadruple Inversion-Recovery. Magnetic Resonance in Medicine
2002; 48(5): 899-905.
[14] Koktzoglou I, Chung YC, Carroll TJ, Morasch MD, Simonetti
OP, Li D. Three-Dimensional Black-Blood MR Imaging of Carotid
Arteries with Segmented Steady-State Free Precession: Initial
Experience. Radiology 2007; 243(1): 220-228.
[15] Wang J, Yarnykh VL, Hatsukami T, Chu B, Balu N, Yuan C.
Improved Suppression of Plaque-Mimicking Artifacts in Black-Blood
Carotid Atherosclerosis Imaging using a Multislice Motion-Sensitized
Driven-Equilibrium (MSDE) Turbo Spin-Echo (TSE) Sequence.
Magn Reson Med 2007; 58(5): 973-981.
[16] Kerwin W, Ferguson M, O’Brien K, Hatsukam Ti, Yuan C.
Quantitative Detection of Infl ammation in Carotid Atherosclerosis by
Dynamic Contrast Enhanced Magnetic Resonance Imaging. Journal
of the American College of Cardiology 2004; 43(5): 534a-534a.
[17] Kerwin W, Hooker A, Spilker M, Vicini P, Ferguson M, Hatsukami
T et al. Quantitative Magnetic Resonance Imaging Analysis of
Neovasculature Volume in Carotid Atherosclerotic Plaque. Circulation
2003; 107(6): 851-856.
[18] Underhill H, Kerwin WS, Hatsukami TS, Yuan C. Automated
Measurement of Mean Wall Thickness in the Common Carotid Artery
by MRI: A Comparison to Intima-Media Thickness by B-Mode
Ultrasound. Journal of Magnetic Resonance Imaging 2006; 24(2):
379-387.
[21] Kerwin WS, O’Brien KD, Ferguson MS, Polissar N, Hatsukami T
S, Yuan C. Infl ammation in Carotid Atherosclerotic Plaque: A
Dynamic Contrast-Enhanced MR Imaging Study. Radiology 2006;
241(2): 459-468.
[22] Moody AR, Murphy RE, Morgan PS, Martel AL, Delay GS,
Allder S et al. Characterization of Complicated Carotid Plaque with
Magnetic Resonance Direct Thrombus Imaging in Patients with
Cerebral Ischemia. Circulation 2003; 107(24): 3047-3052.
[23] Hatsukami TS, Ross R, Polissar NL, Yuan C. Visualization of
Fibrous Cap Thickness and Rupture in Human Atherosclerotic Carotid
Plaque In Vivo with High-Resolution Magnetic Resonance Imaging.
Circulation 2000; 102(9): 959-964.
[24] Saam T, Cai JM, Ma L, Cai YQ, Ferguson MS, Polissar NL et al.
Comparison of Symptomatic and Asymptomatic Atherosclerotic
Carotid Plaque Features with In Vivo MR Imaging. Radiology 2006;
240(2): 464-472.
[25] Trivedi RA, U-King-Im JM, Graves MJ, Cross JJ, Horsley J,
Goddard MJ. In Vivo Detection of Macrophages in Human Carotid
Atheroma - Temporal Dependence of Ultrasmall Superparamagnetic
Particles of Iron Oxide-Enhanced MRI. Stroke 2004; 35(7):
1631-1635.
[26] Kolodgie FD, Virmani R, Burke AP, Farb A, Weber DK, Kutys R
et al. Pathologic Assessment of the Vulnerable Human Coronary
Plaque. Heart 2004; 90(12): 1385-1391.
[27] Mani V, Itskovich VV, Aguiar SH, Mizsei G, Aguinaldo JG,
Samber DD et al. Comparison of Gated and Nongated Fast Multislice
Black-Blood Carotid Imaging using Rapid Extended Coverage and
Inflow/Outflow Saturation Techniques. Journal of Magnetic
Resonance Imaging 2005; 22(5): 628-633.
[28] Corti R, Fuster V, Fayad ZA, Worthley SG, Helft G, Smith D et
al. Lipid Lowering by Simvastatin Induces Regression of Human
Atherosclerotic Lesions - Two Years’ Follow-Up by High-Resolution
Noninvasive Magnetic Resonance Imaging. Circulation 2002;
106(23): 2884-2887.
[29] Zhao XQ, Yuan C, Hatsukami TS, Frechette EH, Kang XJ,
Maravilla KR et al. Effects of Prolonged Intensive Lipid-Lowering
Therapy on the Characteristics of Carotid Atherosclerotic Plaques In
Vivo, by MRI: A Case-Control Study. Atherosclerosis, Thrombosis,
and Vascular Biology 2001; 21: 1623-1629.
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