(Circulation. 1999;99:1054-1061.)
© 1999 American Heart Association, Inc.
Basic Science Reports |
High-Resolution Intravascular Magnetic Resonance Imaging
Monitoring of Plaque Formation in Heritable Hyperlipidemic Rabbits
From the Departments of Radiology (G.G.Z.-P., H.H.Q., G.K.v.S., J.F.D.) and Pathology (P.V.), University Hospital Zürich (Switzerland), and Hoffmann La Roche Ltd, Preclinical Cardiovascular Research Division (D.K.), Basel, Switzerland.
Correspondence to Dr Jörg F. Debatin, Institute of Diagnostic Radiology, University Hospital Zürich, Rämistr 100. CH-8091 Zürich, Switzerland.
 |
Abstract |
|---|
 Top Abstract IntroductionMethodsResultsDiscussionReferences |
|---|
Background—The individual makeup of atherosclerotic plaque has been identified as a dominant prognostic factor. With the use of an intravascular magnetic resonance (MR) catheter coil, we evaluated the effectiveness of high-resolution MR in the study of the development of atherosclerotic lesions in heritable hyperlipidemic rabbits.
Methods and Results—Sixteen hyperlipidemic rabbits were investigated at the ages of 6, 12, 24, and 36 months. The aorta was studied with digital subtraction angiography and high-resolution MR with the use of a surface coil and an intravascular coil that consisted of a single-loop copper wire integrated in a 5F balloon catheter. Images were correlated with histological sections regarding wall thickness, plaque area, and plaque components. Digital subtraction angiography revealed no abnormalities in the 6- and 12-month-old rabbits and only mild stenoses in the 24- and 36-month-old rabbits. High-resolution imaging with surface coils resulted in an in-plane resolution of 234x468 µm. Delineation of the vessel wall was not possible in younger rabbits and correlated only poorly with microscopic measurements in the 36-month-old rabbits. Intravascular images achieved an in-plane resolution of 117x156 µm. Increasing thickness of the aortic wall and plaque area was observed with increasing age. In the 24- and 36-month-old animals, calcification could be differentiated from fibrous and fatty tissue on the basis of the T2-fast spin echo images, as confirmed by histological correlation.
Conclusions—Atherosclerotic evolution of hyperlipidemic rabbits can be monitored with high-resolution intravascular MR imaging. Image quality is sufficient to determine wall thickness and plaque area and to differentiate plaque components.
Key Words: atherosclerosis • magnetic resonance imaging • balloon • catheters • imaging
|
Introduction |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
Atherosclerosis represents a chronic inflammatory response to injury ending in an acute event induced by plaque rupture.1 2 Originating from fatty streaks, the typical advanced lesion consists of a fibrous cap overlying a central necrotic core that contains cellular debris, abundant extracellular lipid, and foam cells.2 3 This particular plaque configuration carries a high risk of fissure and ensuing thrombosis independent of the degree of associated luminal narrowing.4 Thus, rather than the degree of stenosis, the risk for thrombosis appears to be determined by plaque structure.5 Hence the assessment of atherosclerosis must extend beyond mere angiographic depiction of the arterial lumen.
Driven by continuous improvements in magnetic resonance (MR) hardware and software designs, high-resolution MR imaging (MRI) has been increasingly considered for assessing the vascular walls. With the use of specialized coils that permitted scanning of only ex vivo specimens, high-resolution MR images were found to be superior to intravascular ultrasound with regard to plaque characterization, reflecting the unsurpassed soft tissue contrast inherent to the MR experiment.6 Initial in vivo work was based on external surface coils. Limited signal and depth penetration allowed wall imaging only of peripheral vessels such as the carotid,7 femoral, or popliteal arteries. To overcome these limitations, various intravascular imaging coils have been designed.8 9 10 11 Recently, a design based on a single-loop receiver coil mounted on an inflatable balloon catheter has been introduced.12 The device was shown to render sufficiently high and homogeneous signal to resolve ex vivo plaque13 while suppressing flow artifacts under in vivo conditions.
The purpose of this study was to monitor the age-dependent development of atherosclerotic lesions in heritable hyperlipidemic rabbits by use of a high-resolution intravascular imaging catheter and compare its performance with that of x-ray angiography and high-resolution MR with an external surface coil, with histological analysis used as the standard of reference.
|
Methods |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
Study Design
Experiments were conducted on 16 female heritable hyperlipidemic (HHL) rabbits (Froxfield Farms Ltd, Hampshire, UK). These Froxfield HHL rabbits are a modified strain of Watanabe heritable hyperlipidemic (WHHL) rabbits that have been generated by crossing male WHHL rabbits into a colored commercial colony with strong breeding characteristics.14 15 The females used in our experiments were taken to be homozygous for the LDL receptor defect because of cholesterol values >14 mmol/L at weaning.15 These animals develop extensive aortic atherosclerosis within 16 weeks. Their advantage over Watanabe rabbits is their lower susceptibility to parasitic and bacterial infections.
Animals of 4 different age groups (6, 12, 24, and 36 months) were investigated. Each age group contained 4 animals. The abdominal aorta of each animal was studied with digital subtraction angiography (DSA) and high-resolution MRI with the use of an external surface coil and an intravascular coil. Histological analysis of the aortic specimens served as the standard of reference. The suprarenal aorta was chosen for imaging because it resembles the diameter of the human renal and femoral arteries.
The animal experiments were performed in accordance with state regulations under full anesthesia. After premedication with ketamine (0.6 mL/kg body wt, Dr E. Gräub AG) and xylazine (0.2 mL/kg body wt 2%, Bayer), the animals were tracheotomized with a 3.0-mm tracheal tube (Portex Ltd). Halothane narcosis was subsequently performed under spontaneous breathing conditions with 1.5% halothane and a 60%/40% O2/N2O mixture. For DSA, a 4F introducer was placed from the right carotid artery into the aortic arch. For placement of the intravascular MRI catheter, the right femoral artery was surgically prepared and sectioned. After the animals were killed by injection with pentobarbitol (Veterinaria AG), histological sections of the abdominal aorta were obtained.
Digital Subtraction Angiography
DSA images of the abdominal aorta were acquired with a frame
rate of 2 per second after administration of 5 mL of Topromid (Schering
AG) with the use of standard angiographic equipment (Multiskop
Siemens). Separate series of the suprarenal and infrarenal abdominal
aorta were obtained with a 1024x1024 matrix.
Magnetic Resonance Imaging
All MRI was performed on a 1.5-T system (Signa Echospeed, GEMS).
The rabbit was placed in a quadrature extremity coil centered on the
abdomen of the animal. With the use of a series of fast gradient echo
localizing sequences, a 40-mm region of the suprarenal aorta was
defined for high-resolution MRI with both the external and
intravascular coil approaches. To permit direct comparison, 4-mm
sections were obtained with both techniques in the axial plane.
For noninvasive high-resolution imaging, the extremity surface coil was used for both signal transmission and reception. T1-weighted spin-echo images (TR/TE=500/12 ms, 4NEX) were acquired in 8.36 minutes. A fast spin-echo sequence (TR/TE=2000/85 ms, Etl=8, 8NEX) rendered T2-weighted images also in 8.36 minutes. To reduce flow-related artifacts, both superior and inferior spatial presaturation pulses were used. With each sequence, 10 contiguous 4-mm sections were collected with a field-of-view of 120x120 mm and a 512x256 matrix.
For intravascular MRI, the balloon-mounted intravascular coil was used
for signal reception. The design of the intravascular catheters
(Schneider International) was based on a standard 5F balloon catheter
with an inflatable balloon (4-mm diameters) of 40 mm in length. A
single-loop coil, 40 mm in length and made of copper wire, was
mounted onto the surface of the balloon (Figure 1
).
|
To isolate the nonbiocompatible copper from the vessel, the wire was
covered by a second balloon. A coaxial cable was used to conduct the MR
signal over the length of the catheter (120 cm) and to connect the coil
to remote tuning and matching capacitors Ct
and Cm positioned at the base of the
catheter. An actively switched diode D detunes the catheter
receiving coil during transmission with the body coil (Figure 1
). A sensitivity profile of the intravascular coil, acquired in
a phantom, demonstrated a rather circular signal homogeneity and
penetration depth (Figure 2).
|
20% of the maximal signal at a distance of
3 mm from the balloon surface.The intravascular imaging catheter was placed at the predefined 40-mm-long region of the suprarenal aorta. T1-weighted spin-echo images (TR/TE=400/20 ms, 6NEX) were acquired over 3.54 minutes; T2-weighted fast spin-echo images (TR/TE=2000/85 ms, Etl=8, 8NEX) were collected in 3.16 minutes. With both sequences, 10 contiguous 4-mm sections were collected with a rectangular field-of-view of 30x15 mm and a matrix of 256x96.
Histopathological Evaluation
To ensure identification of the predefined supra-aortic region
of interest, the intravascular catheter remained inside the aorta after
the animals were killed. The aortic segment containing the
balloon-mounted coil was carefully excised from the cadaver. To
facilitate the matching process between MR images and
histological specimen, the aorta was marked with color
(Viomedex, Hausmann Hospital Supply Ltd) at the distal and proximal
ends of the inflated balloon as well as along the anterior vessel wall.
After excision, the specimens were immediately fixed in 10% buffered
formalin for at least 24 hours. For cutting, the specimens were
oriented in the anterior-posterior plane and embedded in paraffin.
Three sections, 4 µm in thickness, corresponding to the center
of the 3 central MR images, were mounted on slides. For subsequent
histopathological evaluation, the slides were stained with
hematoxylin-eosin and elastic van Gieson and analyzed for
fibrous and fat components. To confirm the presence of calcification or
chondroid metaplasia, Kossa stain and AB PAS stain were obtained,
respectively.
Data Analysis
Analysis of the MR images and the
histological specimens was performed by separate
observers blinded to the other findings. Maximum wall thickness and
plaque area were measured in each of the 3 histological
sections as well as the corresponding MR images. In cases of concentric
wall thickening, the average of 3 measurements in 1 section was
calculated. Plaque thickness and area were measured on MR images by
tracing plaque contours manually with a magnification factor of 3.
Histomorphometric measurements of wall thickness and plaque area were
performed on a planimeter (MOP-OM3, Kontron). Because the internal
elastic membrane of older rabbits showed fragmentation with focal media
degeneration, the plaque area was histologically
defined as the area between the lumen of the vessel and the external
elastic membrane. On MR images, the plaque area corresponded to the
region bordered by vascular lumen and adventitia.
Histopathological plaque analysis was provided by an experienced pathologist viewing the histological cross sections along the site of maximal wall thickness. Each analyzed pixel location was characterized as corresponding to 1 of the following plaque components: calcification, chondroid metaplasia, fibrous tissues, and fatty tissues. Rather than focal areas of homogeneous fat, atherosclerotic plaque in HHL rabbits contain varying amounts of crystallized cholesterol and foam cells mixed with fibrous tissue.16 Plaque contained within each section was characterized in accordance with the American Heart Association classification (type 1 to 6).17
Analysis of the plaque structure on MR-images was accomplished
by plotting the signal intensities along a straight line traversing the
plaque at its maximum size. To ensure homogeneous
measurements, the intravascular coil had been positioned to encompass
the wall measurement site within the 60 degree sector of the
sensitivity field of the coil (Figure 2). To compensate for
concentric plaque formation, the line plot traversed the plaque in a
sagittal plane. By use of an analogous line, the signal intensities
(SI) along the plaque seen on the MR images were recorded for every
other pixel. The different pixel SI values could thus be directly
attributed to the various plaque components seen at
histological analysis. Mean SI values and
standard deviations were determined for the various plaque components.
The Fisher's test was used to assess for statistical differences
between the SI values associated with the different plaque components.
Furthermore, MR findings were grossly classified in 3 grades by the
following criteria: MR grade I: wall thickening without evidence of fat
or calcium; MR grade II: wall thickening with lipid deposits without
calcium; MR grade III: wall thickening with evidence of fat and
calcium
The MR gradings were correlated with the histological AHA classification.17 For this purpose, the AHA classification was simplified by lumping together types I and II, types III and IV, and types V and VI lesions.
|
Results |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
In rabbits aged 6 (n=4) and 12 months (n=4) and in 2 animals aged 24 months, DSA failed to demonstrate any vascular abnormalities in the abdominal aorta (Figure 3A
). The
remaining 6 animals (two 24 months old and four 36 months old) revealed
contour irregularities with some degree of stenosis in the
suprarenal and infrarenal parts of the abdominal aorta (Figure 3B).
|
High-resolution imaging with surface coils resulted in an in-plane
resolution of 234x468 µm. This resolution was not sufficient to
permit definitive delineation of vessel wall from vessel lumen and
surrounding structures in the animals aged 6, 12, and 24 months.
Thickening of the vascular wall was identified in the four 36-month-old
rabbits (Figure 4). Correlation of wall
thickness and plaque area based on these 4 animals was poor, as
reflected by correlation coefficients of r=0.71 and
r=0.66 for thickness and area, respectively. The large pixel
size did not permit characterization of plaque components in any age
group on either T1- or T2-weighted images.
|
With intravascular high-resolution images, an in-plane resolution of
117x156 µm was achieved. The vascular wall was easily
delineated in all 16 animals of all age groups (Figure 5). Wall thickness and plaque area
correlated well with the morphometric measurements of the
histological specimens, as evidenced by the high
correlation coefficients of r=0.96 and r=0.98 for
thickness and area, respectively (Figure 6). There was, however, some systematic
overestimation by MRI relative to the true values.
|
|
On the basis of analysis of the intravascular images, the
progression of atherosclerotic changes over time was clearly visible
(Figure 5). With increasing age of the animals, the aortic wall
thickened from 0.56±0.07 mm for the 6-month-old rabbits to
2.41±0.35 mm for the 36-month-old rabbits. Similarly, plaque area
increased from 6.75±0.95 to 23.75±3.86 mm2
in corresponding age groups (Table 1).
Differences in plaque area between 6 and 12 months failed to be
statistically significant (P>0.05). All other wall
thickness and plaque area comparisons between the 4 different age
groups fulfilled the criteria for statistical significance
(P<0.05).
|
Table 2 summarizes the
histological plaque characterization according to the
AHA classification; Table 3 depicts the
grading on the basis of the MR classification. Table 4 reveals good correlation between the
AHA and MR classifications, with an overall agreement of 87.5%.
|
|
|
Reflecting limited soft tissue contrast, T1-weighted images did not
permit differentiation of plaque components in any of the animals
regardless of age. T2-weighted fast spin echo images, on the
other hand, did allow definitive differentiation of calcified plaque
characterized on the basis of SI values. Calcification (129.3±29.9)
could be differentiated from fatty tissue (595.2±146.8) and fibrous
tissue (932.4±127.7). Differences between the 3 components were
statistically significant (P<0.01) (Table 5) (Figure 7). The MRI appearance of chondroid
metaplasia with SI values of 137.5±31.4 was indistinguishable from
that of calcified plaque.
|
|
|
Discussion |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
This study illustrates that intravascular MRI is feasible for detecting early atherosclerosis and characterizing more advanced plaque formations. In contrast to the externally placed surface coil, the intravascular imaging device provided sufficient spatial resolution to accurately quantitate wall thickness as well as plaque area and differentiate various plaque components on the basis of their inherent SIs (Figure 5
). The presented data also
underscore the limitations inherent to luminal angiographic imaging.
DSA failed to identify plaque formation in younger animals altogether
and grossly underestimated the true extent of disease in the older
animals (Figure 3). Similar observations have been reported by
Hong et al18 : Intravascular ultrasound had identified
circumferential wall thickening in 6-month-old heterozygous HHL
rabbits, whereas angiography failed to detect any changes.
MR-based visualization of the vascular wall requires adequate
spatial resolution coupled with sufficient signal strength and
homogeneity. By providing direct contact between the imaging coil and
the vessel wall, the evaluated balloon-mounted coil design ensures
maximal spatial resolution. Positioning the coil next to the vascular
wall allows the latter to fall within the area of maximal coil
sensitivity. Hence, sufficient signal is received to provide an
in-plane resolution of 117x156 µm, with a penetration depth of
up to 10 mm. Wall thickness and atherosclerotic plaque area could
thus be accurately quantified, as evidenced by the high correlation
coefficients (Figure 6). Systematic overestimation of wall
thickness as well as plaque area compared with histology likely
reflects some degree of specimen shrinkage associated with the
preparation for histological
analysis.19
The balloon-mounted coil has been shown to be safe. Heating experiments under worst-case conditions failed to reveal any significant temperature rise.20 The balloon-mounted intravascular imaging coil suppresses flow and pulsatility artifacts, which can render images uninterpretable.8 21 22 The inflatable balloon immobilizes the coil against the vessel wall; flow artifacts are thus eliminated, and coil motion relative to the arterial wall is minimized. Although an occlusion time of 3.16 minutes may be acceptable in the analysis of peripheral arteries,23 it precludes assessment of critical vessels such as the carotid or coronary arteries. Possible solutions include shortening of imaging times with the use of ultrafast echoplanar data acquisition strategies24 or the use of tunneled balloon designs.25 With such a continuous perfusion catheter, dilation times for PTCA could be significantly increased.25
MRI of vascular walls can also be accomplished with external surface coils.26 The relatively poor results obtained in this study primarily reflect differences in the animal model: Whereas Skinner et al26 used a deendotheliazation model resulting in well-developed atherosclerotic plaque, this study included rabbits with very early-stage disease. On the basis of an in-plane resolution of 234x468 µm, a mean wall thickness of 2.4 mm was required to permit definitive delineation of the aortic wall.
Several characteristics supported the choice of the HHL rabbit as a model for this study. The documented similarity between rabbit and human atherosclerotic plaque formation was featured most prominently.15 16 In addition, the quick development of the disease over months, coupled with a robustness of the animals ensuring survival over a period of 3 years,16 allowed the study of disease progression over time.
On the basis of its excellent soft tissue contrast, MRI even provides a
means for characterizing plaque structure.7 13 27 28
Despite the greater heterogeneity characterizing plaque
in the animal model that was used, T2-weighted images permitted
differentiation of fibrous tissue from lipid deposits (Table 5
and Figures 5 through 7). The lower SI of the fatty material
reflects the shorter T2 relaxation times of fat compared with fibrous
material.7 The ability to differentiate the various plaque
components reflects on the excellent soft tissue contrast inherent to
the MR experiment. Intravascular MR images even permitted
classification of plaque. The outlined MR grading scheme correlates
well with a simplified AHA classification (Tables 2, 3, and 4). There was some underestimation of disease extent in 2 of
the 12-month-old rabbits. This appears to reflect difficulties in
visualizing lipid deposits in the preatheromatous stage
on MR images. The overall good correlation points to a considerable
potential of intravascular MRI regarding the characterization of
plaque.29 The wide standard deviation of SIs associated
with the various plaque components does point to limitations of the
intravascular imaging concept as proposed: There is a considerable
signal dropoff from the center of the coil. These difficulties can be
overcome by implementing rather complex correction algorithms, as
proposed by Atalar et al.29 With these algorithms, the
correlation can be expected to be even greater.
The concept of intravascular MRI must be viewed as part of a larger effort exploring the potential of using MRI for guiding and monitoring intravascular interventions. Driven by profound hardware and software innovations, including the development of open-configuration MR scanners that provide direct access to the patient during imaging30 and ultrafast 3-dimensional MRI permitting a detailed display of entire vascular territories,31 32 much progress has been made in this regard. With the use of different active tracking algorithms, intravascular guide wires and catheters can be visualized relative to surrounding structures in real time simultaneously in multiple planes.33 34 The first MR-guided vascular interventions were recently performed under in vivo conditions.35 By accurately quantitating plaque extent and characterizing plaque structure, intravascular MRI will be an important addition to the concept of interventional MR angiography. It promises to provide a prognostic data link regarding the outcome of the most common intravascular procedure: percutaneous transluminal angioplasty.
|
Acknowledgments |
|---|
This work was supported by grants from the German Research Foundation, Bonn, Germany (ZI 551/1-2, Dr Paul), and KTI-3227.1, Switzerland.
Received June 1, 1998; revision received October 6, 1998; accepted October 22, 1998.
|
References |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
-
Berliner JA, Navab M, Fogelman AM, Frank JS, Demer
LL, Edwards PA, Watson AD, Lusis AJ. Atherosclerosis:
basic mechanisms: oxidation, inflammation, and genetics.
Circulation. 1995;91:2488–2496.
[Abstract/Free Full Text]
-
Ross R. The pathogenesis of
atherosclerosis: a perspective for the 1990s.
Nature. 1993;362:801–809.[Medline]
[Order article via Infotrieve]
-
Small DM. Progression and regression of
atherosclerotic lesions.
Arteriosclerosis. 1988;8:103–129.
[Abstract/Free Full Text]
-
Fuster V, Badimon L, Badimon JJ, Chesebro JH. The
pathogenesis of coronary artery disease and the acute
coronary syndromes. N Engl J Med. 1992;326:310–318.[Medline]
[Order article via Infotrieve]
-
Brown BG, Zhao XQ, Sacco DE, Albers JJ. Lipid-lowering
and plaque regression: new insights into prevention of plaque
disruption and clinical events in coronary disease.
Circulation. 1993;87:1781–1791.
[Abstract/Free Full Text]
-
Martin AJ, Ryan LK, Gotlieb AI, Henkelman RM, Foster
FS. Arterial imaging: comparison of high-resolution US and
MR imaging with histologic correlation.
Radiographics. 1997;17:189–202.[Abstract]
-
Toussaint JF, LaMuraglia GM, Southern JF, Fuster V,
Kantor HL. Magnetic resonance images lipid, fibrous, calcified,
hemorrhagic, and thrombotic components of human
atherosclerosis in vivo. Circulation. 1996;94:932–938.
[Abstract/Free Full Text]
-
Hurst GC, Hua J, Duerk JL, Cohen AM. Intravascular
(catheter) NMR receiver probe: preliminary design analysis and
application to canine iliofemoral imaging. Magn Reson Med. 1992;24:343–357.[Medline]
[Order article via Infotrieve]
-
Martin AJ, Plewes DB, Henkelmann RM. MR imaging of
blood vessels with an intravascular coil. J Magn Reson
Imaging. 1992;2:421–429.[Medline]
[Order article via Infotrieve]
-
Kandarpa K, Jakob P, Patz S, Schoen FJ, Jolesz FA.
Prototype miniature endoluminal MR imaging catheter. J Vasc
Interv Radiol. 1993;4:419–427.[Medline]
[Order article via Infotrieve]
-
Atalar E, Bottomley PA, Ocali O, Correia LC, Kelemen
MD, Lima JA, Zerhouni EA. High resolution intravascular MRI and MRS by
using a catheter receiver coil. Magn Reson Med. 1996;36:596–605.[Medline]
[Order article via Infotrieve]
-
Erhart P, Ladd ME, Zimmermann GG, Debatin JF, v
Schulthess GK. Balloon mounted intravascular receiver coil for
MR imaging of vessel walls. MAGMA. 1996;94:129.
Abstract.
-
Zimmermann GG, Erhart P, Schneider J, Schmidt M, v
Schulthess GK, Debatin JF. Intravascular MR imaging of atherosclerotic
plaque: ex vivo analysis of human femoral arteries with
histologic correlation. Radiology. 1997;204:769–774.
[Abstract/Free Full Text]
-
Watanabe Y. Serial inbreeding of rabbits with
hereditary hyperlipidemia (WHHL-rabbit): incidence and
development of atherosclerosis and xanthoma.
Atherosclerosis. 1980;36:261–268.[Medline]
[Order article via Infotrieve]
-
Gallagher PJ, Nanjee MN, Richards T, Roche WR, Miller
NE. Biochemical and pathological features of a modified strain of
Watanabe heritable hyperlipidemic rabbits.
Atherosclerosis. 1988;41:173–183.
-
Esper E, Chan EK, Buchwald H. Natural history of
atherosclerosis and hyperlipidemia in
heterozygous WHHL (WHHL-Hh) rabbits, I: the effects of aging and gender
on plasma lipids and lipoproteins. J Lab Clin Med. 1993;121:97–102.[Medline]
[Order article via Infotrieve]
-
Stary HC, Bleakley C, Dinsmore RE, Fuster V, Glagov S,
Insull W, Rosenfeld ME, Schwartz CJ, Wagner WD, Wissler RW. 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;92:1355–1374.
[Abstract/Free Full Text]
-
Hong MK, Vossoughi J, Mintz GS, Kauffman RD, Hoyt RF
Jr, Cornhill JF, Herderick EE, Leon MB, Hoeg JM. Altered compliance and
residual strain precede angiographically detectable early
atherosclerosis in low-density lipoprotein receptor
deficiency. Arterioscler Thromb Vasc Biol. 1997;17:2209–2217.
[Abstract/Free Full Text]
-
Di Mario C, The SHK, Madretsma S. Detection and
characterization of vascular lesions by intravascular ultrasound: an in
vitro study correlated with histology. J Am Soc
Echocardiogr. 1992;5:135–146.[Medline]
[Order article via Infotrieve]
-
Quick HH, Ladd ME, v Schulthess GK, Debatin JF. Heating
effects of an intravascular imaging catheter. In: Proceedings of
European Society of Magnetic Resonance in Medicine and Biology,
14th Annual Meeting. 1997:563.
-
Martin AJ, Henkelmann RM. Intravascular MR imaging in a
porcine animal model. Magn Reson Med. 1994;32:224–229.[Medline]
[Order article via Infotrieve]
-
Ocali O, Atalar E. Intravascular magnetic resonance
imaging using a loopless catheter antenna. Magn Reson Med. 1997;37:112–118.[Medline]
[Order article via Infotrieve]
-
Eltchaninoff H, Cribier A, Koning R, Chan C. Effects of
prolonged sequential balloon inflations on results of coronary
angioplasty. AJR. 1996;77:1062–1066.
-
Wetter DR, McKinnon GC, Debatin JF, von Schulthess GK.
Cardiac echo-planar MR imaging: comparison of single- and multiple-shot
techniques. Radiology. 1995;194:765–770.
[Abstract/Free Full Text]
-
Erbel R, Clas W, Busch U, von Seelen W, Brennecke R,
Blomer H, Meyer J. New balloon catheter for prolonged
percutaneous transluminal coronary angioplasty
and bypass flow in occluded vessels. Cathet Cardiovasc
Diagn. 1986;12:116–123.[Medline]
[Order article via Infotrieve]
-
Skinner MP, Yuan C, Mitsumori L, Hayes CE, Raines EW,
Nelson JA, Ross R. Serial magnetic resonance imaging of experimental
atherosclerosis detects lesion fine structure,
progression and complications in vivo. Nat Med. 1995;1:69–73.[Medline]
[Order article via Infotrieve]
-
Martin AJ, Gotlieb AI, Henkelman RM. High resolution MR
imaging of human arteries. J Magn Reson Imaging. 1995;5:93–100.[Medline]
[Order article via Infotrieve]
-
Toussaint JF, Southern JF, Fuster V, Kantor HL.
T2-weighted contrast for NMR characterization of human
atherosclerosis. Arterioscler Thromb Vasc
Biol. 1995;15:1533–1542.
-
Atalar Z, Bottomley PA, Ocali O, Correia LC, Kelemen
MD, Lima JA, Zerhouni EA. High resolution intravascular MRI and
MRS by using a catheter receiver coil. Magn Reson Med. 1996;36:596–605.
-
Schenck JF, Jolesz FA, Roemer PB, Cline HE, Lorensen
WE, Vosburgh KE. Superconducting open-configuration MR imaging system
for image-guided therapy. Radiology. 1995;195:805–814.
[Abstract/Free Full Text]
-
Rubin GD, Herfkens RJ, Pelc NJ, Foo TK, Napel S,
Shimakawa A, Steiner RM, Bergin CJ. Single breath-hold
pulmonary magnetic resonance angiography: optimization and
comparison of three imaging techniques. Invest Radiol. 1994;29:766–792.[Medline]
[Order article via Infotrieve]
-
Leung DA, McKinnon G, Davis CP, Pfammatter T, Debatin
JF. Breath-hold, contrast-enhanced, 3-dimensional MR angiography.
Radiology. 1996;201:569–571.
[Abstract/Free Full Text]
-
Dumoulin CL, Souza SP, Darrow RD. Real-time position
monitoring of invasive devices using magnetic resonance. Magn
Reson Med. 1993;299:411–415.
-
Ladd ME, Zimmermann GG, Quick HH, Debatin JF, Boesiger
P, von Schulthess GK, McKinnon GC. Active MR visualization of a
vascular guidewire in vivo. Journal of Magnetic Resonance
Imaging. 1998;8:220–226.[Medline]
[Order article via Infotrieve]
-
Wildermuth S, Debatin JF, Leung DA, Hofmann E, Dumoulin
CL, Darrow RD, Thyregod J, v Schulthess GK. MR guided intravascular
procedures: initial demonstration in a pig model. Radiology. 1997;202:578–583.
[Abstract/Free Full Text]
This article has been cited by other articles:
 |
|
 |
|
  Y. Honda and P. J. Fitzgerald Frontiers in Intravascular Imaging Technologies Circulation, April 15, 2008; 117(15): 2024 - 2037. [Full Text] [PDF]
|
|
|
|
|
|
S. Waxman, F. Ishibashi, and J. E. Muller Detection and Treatment of Vulnerable Plaques and Vulnerable Patients: Novel Approaches to Prevention of Coronary Events Circulation, November 28, 2006; 114(22): 2390 - 2411. [Full Text] [PDF]
|
|
|
|
 |
|
 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]
|
|
|
|
|
|
J. Barkhausen, W. Ebert, C. Heyer, J. F. Debatin, and H.-J. Weinmann Detection of Atherosclerotic Plaque With Gadofluorine-Enhanced Magnetic Resonance Imaging Circulation, August 5, 2003; 108(5): 605 - 609. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 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]
|
|
|
|
 |
|
 I.-K. Jang, B. E. Bouma, D.-H. Kang, S.-J. Park, S.-W. Park, K.-B. Seung, K.-B. Choi, M. Shishkov, K. Schlendorf, E. Pomerantsev, et al. Visualization of coronary atherosclerotic plaques in patients using optical coherence tomography: comparison with intravascular ultrasound J. Am. Coll. Cardiol., February 20, 2002; 39(4): 604 - 609. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. Yuan, S.-x. Zhang, N. L. Polissar, D. Echelard, G. Ortiz, J. W. Davis, E. Ellington, M. S. Ferguson, and T. S. Hatsukami Identification of Fibrous Cap Rupture With Magnetic Resonance Imaging Is Highly Associated With Recent Transient Ischemic Attack or Stroke Circulation, January 15, 2002; 105(2): 181 - 185. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. J. Kern and B. Meier Evaluation of the Culprit Plaque and the Physiological Significance of Coronary Atherosclerotic Narrowings Circulation, June 26, 2001; 103(25): 3142 - 3149. [Full Text] [PDF]
|
|
|
|
|
|
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]
|
|
|
|
|
|
J.-M. Serfaty, E. Atalar, J. Declerck, P. Karmakar, H. H. Quick, K. A. Shunk, A. W. Heldman, and X. Yang Real-time Projection MR Angiography: Feasibility Study Radiology, October 1, 2000; 217(1): 290 - 295. [Abstract] [Full Text]
|
|
|
|
|
|
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]
|
|
|
|
 |
|
 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]
|
|
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||