(Circulation. 2001;103:2171.)
© 2001 American Heart Association, Inc.
Clinical Investigation and Reports |
Echolucent Plaques Are Associated With High Risk of Ischemic Cerebrovascular Events in Carotid Stenosis
The Tromsø Study
From the Institute of Community Medicine, University of Tromsø, Norway.
Correspondence to Ellisiv B. Mathiesen, Institute of Community Medicine, University of Tromsø, N-9037 Tromsø, Norway. E-mail ellisiv.mathiesen{at}ism.uit.no
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Abstract |
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Background—The purpose of the study was to assess in a prospective design whether plaque morphology is associated with risk of ischemic stroke and other cerebrovascular events in subjects with carotid stenosis.
Methods and Results—A
total of 223 subjects with carotid stenosis (123 with 35% to
49% degree of stenosis, 100 with 50% to 99%
stenosis) and 215 control subjects matched by age and sex who
participated in a population health survey at baseline were followed up
for 3 years. Plaque echogenicity was assessed by ultrasound at baseline
and scored as echolucent, predominantly echolucent, predominantly
echogenic, or echogenic. Forty-four subjects experienced 
1
ischemic cerebrovascular events in the follow-up period. Plaque
echogenicity, degree of stenosis, and white blood cell count
were independent predictors of cerebrovascular events. The unadjusted
relative risk for cerebrovascular events was 13.0 (95% CI 4.5 to 37.4)
in subjects with echolucent plaques and 3.7 (95% CI 0.7 to 18.2) in
subjects with echogenic plaques when subjects without stenosis
were used as the reference. The adjusted relative risk for
cerebrovascular events in subjects with echolucent plaques was 4.6
(95% CI 1.1 to 18.9), and there was a significant linear trend
(P=0.015) for higher risk with
increasing plaque echolucency. The adjusted relative risk for a 10%
increase in the degree of stenosis was 1.2 (95% CI 1.04 to
1.4).
Conclusions—Subjects with echolucent atherosclerotic plaques have increased risk of ischemic cerebrovascular events independent of degree of stenosis and cardiovascular risk factors. Subjects at high risk for ischemic vascular events may be identified by ultrasound assessment of plaque morphology.
Key Words: plaque • ultrasonics • carotid arteries • stenosis • stroke • follow-up studies
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Introduction |
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Stroke is the second leading cause of death in the world,1 with stenotic atheromatous plaques of the carotid bifurcation as one of the important risk factors. The degree of stenosis is recognized as an important risk factor for stroke. It is well known, however, that many high-grade stenoses remain stable and never cause cerebrovascular events, whereas others rapidly produce serious, potentially life-threatening disease. Thus, there has been a search for additional risk factors that might help identify the individuals with a high risk for stroke.
Plaque echogenicity as assessed by B-mode ultrasound has been found to reliably predict the content of soft tissue and the amount of calcification in carotid plaques.2 Plaques that appear echolucent on B-mode ultrasound are lipid-rich, whereas echogenic plaques have a higher content of fibrous tissue and calcification.3 4 Plaque echogenicity has been reported to be associated with stroke and other cerebrovascular events in univariate analysis in previous studies.5 6 7 8 9 10 11 12 13 14 15 16 Most of these were cross-sectional,6 7 9 12 13 14 15 but an association has also been found in prospective studies.5 8 10 11 16 Only 2 prospective studies have made adjustments for other cerebrovascular risk factors.8 16 In a majority of previous studies, the participants were symptomatic patients referred to ultrasonography and/or carotid endarterectomy, whereas little is known about plaque echogenicity and the risk of stroke in the general population of stenotic subjects.
The purpose of the present study was to assess, in a population-based, prospective design, whether plaque morphology is an independent predictor of stroke and other cerebrovascular events.
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Methods |
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In the fourth survey of the Tromsø Study in 1994 to 1995, a total of 6727 persons, 77% of the eligible population, were examined with ultrasound of the carotid arteries, and among these, 237 subjects were found to have stenosis or occlusion of the carotid artery.17 After 3 years, all subjects with carotid stenosis and 227 control subjects without stenosis, matched by age and sex and recruited from the study population, were invited to a follow-up examination. Ten subjects (2 with stenosis and 8 without) did not want to participate, and 5 subjects (1 with stenosis and 4 without) had moved out of the region and were excluded from the study. Informed consent was obtained from the participants, and the regional ethical committee approved the study.
Details about the ultrasound methods have been published
previously.17 18
Briefly, high-resolution B-mode and color Doppler/pulsed-wave
Doppler ultrasonography of both carotid arteries were performed
with an ultrasound scanner (Acuson Xp10 128 ART) equipped with a
linear-array 5- to 7-MHz transducer. Plaque morphology in terms of
echogenicity, defined as reflectance of the emitted ultrasound signal,
was assessed in a modified version of the classification proposed by
Gray-Weale et
al19 20 and
graded from 1 to 4 as echolucent, predominantly echolucent,
predominantly echogenic, or echogenic. The vessel lumen was used as the
reference structure for defining echolucency, and the bright echo zone
produced by the media-adventitia interface in the far wall was used as
the reference structure for defining echogenicity. We have previously
assessed interobserver reproducibility of plaque morphology in
stenotic arteries, with acceptable results (
=0.56, 95% CI
0.38 to 0.74).18 Subjects
with plaques that could not be classified because of either occlusion
of the carotid artery (n=10) or too much echo shadowing or
unsatisfactory image quality (n=1) were excluded. Plaque morphology was
not recorded in 1 subject. Thus, assessment of plaque morphology
was available in 226 cases at baseline, but because of nonparticipation
in the follow-up study, a total of 223 cases and 215 controls were
included in the analyses.
The degree of stenosis was calculated by the
following equation: (1-PSVr/PSVs)x100%, where PSVr denotes peak
systolic velocity at the point of reference (here, the distal
carotid artery) and PSVs the peak systolic velocity in the
stenosis. One subject had missing data on PSVr and another on
PSVs. In these persons, the degree of stenosis was estimated by
calculating lumen diameter reduction: (plaque thickness/lumen
diameter)x100%. An increase in PSVs with respect to PSVr,
corresponding to 
35% lumen diameter
stenosis,21 or a
narrowing of the lumen diameter in the longitudinal plane by 35% was
used as the cutoff point for stenosis. In 55% of the cases,
the degree of stenosis was <50%, in 26% of the cases the
stenosis was 50% to 69%, and 19% of cases had
stenosis 70%. In the case of bilateral stenosis or
multiple plaques, the carotid artery or plaque with the highest degree
of stenosis was selected for analysis.
At the baseline examination, measurements of height, weight, body mass index, blood pressure, nonfasting serum total cholesterol, HDL cholesterol, triglycerides, fibrinogen, and white blood cell count were done, and information about smoking habits was collected from self-administered questionnaires.17
During the follow-up period, subjects with a
stenosis of 70% and incident ipsilateral transient
ischemic attacks (TIAs) or nondisabling strokes (n=9) were
referred to surgery, according to the North American
Symptomatic Carotid Endarterectomy
Trial (NASCET) guidelines.22
Symptomatic cases with <70% stenosis and
asymptomatic subjects with high-grade stenosis were
given prophylactic antiplatelet treatment unless
contraindicated, usually aspirin 160 mg/d.
Endarterectomy was performed on an
asymptomatic person with a rapidly progressing
stenosis in 1 internal carotid artery (from 40% to 90% in 1
year) and contralateral occlusion and on 2 subjects with
asymptomatic high-grade stenosis before renal
transplantation. All other participants were given the best medical
therapy available to lower cardiovascular risk factor
levels.
At the 3-year follow-up examination, a detailed history of cerebrovascular events was recorded, and clinical neurological and ultrasound examinations were done in all subjects. All interviews and examinations were done by the same neurologist (E.B.M.), who was blinded to previous assessments of plaque echogenicity but not to whether the subject had stenosis or not. TIA was defined as a new-onset focal neurological abnormality lasting <24 hours, with no other apparent cause than cerebrovascular, and stroke likewise, except that the duration had to be >24 hours unless interrupted by death.23 Strokes were considered to be of ischemic origin when cerebral hemorrhage was excluded by CT or MR scans of the brain, which were performed in all subjects with a clinical diagnosis of stroke. Amaurosis fugax was defined as partial or complete uniocular loss of vision of sudden onset lasting <1 hour. Deceased subjects (27 cases and 11 controls) were identified by linkage to the National Population Register. Data on cerebrovascular events and details of all deaths were documented by hospital records (available in all but 2), death certificates (available in all), and autopsy records (available in 11 subjects).
Differences in mean values between groups were compared by
ANOVA. Differences in proportions were tested by
2 test and Fisher’s exact test.
Significance of trends was tested by linear regression or by
2 test for trend. Event rates were
calculated by dividing number of events by observation-years. The
Kaplan-Meier method was used for survival analysis, with
censoring for nonstroke death, carotid
endarterectomy, or at the time of the 3-year
follow-up examination. Few ischemic events occurred in the
echogenic group, and the proportion of survival was similar to the
predominantly echogenic group; thus, the predominantly echogenic and
echogenic groups were pooled in the life-table analysis
(Figure
).
Cox proportional-hazards regression models were used to model the
outcomes stroke and cerebrovascular event as a function of plaque
echogenicity, degree of stenosis, and
cardiovascular risk factors. Predictor variables
were logarithmically transformed to achieve normal distribution when
appropriate, but because this had no significant influence on results,
untransformed values were used. The SAS software
package was used for the statistical analyses (SAS, release
6.12, 1996), except for 2 tests for
trend, which were calculated by the Epi Info software package (Epi
Info, version 6.04, 1997). Two-sided probability values of
P<0.05 were considered
significant.
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Results |
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Selected characteristics of the study population are shown in Table 1
. Persons with echolucent plaques had a
higher degree of stenosis, lower levels of HDL
cholesterol, and higher levels of total
cholesterol, fibrinogen, white blood cell count, and
systolic blood pressure than others. A larger proportion of
subjects with stenosis than subjects without stenosis
were current smokers. There was a male preponderance and slightly lower
age among subjects with echolucent plaques compared with subjects in
the other plaque morphology groups and subjects without
stenosis, but these differences were not significant. There
were no significant differences in diastolic blood pressure
or body mass index between groups.
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Compared with subjects with no stenosis, subjects
with stenosis had an increased risk for stroke (RR 2.72, 95%
CI 1.06 to 7.03) and any cerebrovascular event (6.95, 95% CI 2.94 to
16.45). There were trends toward increasing incidence of both TIA and
stroke with increasing degree of echolucency
(Table 2). For amaurosis fugax, the trend was less clear,
because of lack of events in 3 of the groups. Although the absolute
number of ipsilateral events was low (n=22), there was a significant
linear trend toward higher number of events with increasing echolucency
(P=0.017)
(Table 2). When adjusted for age, sex, and degree of
stenosis, the relative risk of ipsilateral events in the
predominantly echolucent group was 3.52 (95% CI 1.0 to 12.42), and in
the echolucent group, 3.64 (95% CI 0.79 to 16.75). In this model, the
combined group of echogenic and predominantly echogenic plaques was
treated as the reference, because there were no incidents in the
echogenic group.
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There was a significant linear trend toward higher risk for
cerebrovascular events with more echolucent plaques
(Table 3,
Figure
).
The unadjusted relative risk for cerebrovascular events was >12 times
higher in subjects with echolucent plaques than in subjects without
stenosis. When adjustments were made for age, sex, and degree
of stenosis, there was still a significant linear trend toward
higher risk with increasing echolucency
(Table 3). The exclusion of persons with previous
cerebrovascular events did not alter the results (data not shown). The
adjusted relative risk for each 10% increase in degree of
stenosis was 1.19 (95% CI 1.04 to 1.37).
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White blood cell count, fibrinogen, and smoking were significant predictors of events in univariate analysis, whereas there were no significant associations between risk of cerebrovascular events and age, sex, total cholesterol, HDL cholesterol, triglycerides, systolic or diastolic blood pressure, or body mass index (data not shown). In a multivariate Cox regression in which age, sex, degree of stenosis, fibrinogen, white blood cell count, smoking, and plaque echogenicity were included in the model, only white blood cell count (P=0.004), degree of stenosis (P=0.019), and plaque echogenicity (P=0.026) were independent predictors of cerebrovascular events. Inclusion in the multivariate model of other cardiovascular risk factors, such as systolic blood pressure and HDL cholesterol, did not change the results.
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Discussion |
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In the present study, subjects with echolucent stenotic plaques had a much higher risk of stroke and cerebrovascular events than subjects with other plaque types. The increased risk was independent of degree of stenosis, age, sex, and other cardiovascular risk factors. Thus, the present study supports the existence of a higher risk of stroke in subjects with echolucent plaques.
It is known from autopsy studies of coronary heart disease that lipid-rich plaques are unstable and prone to rupture and thrombus formation and are associated with unstable angina, myocardial infarction, and sudden death.24 25 On B-mode ultrasound assessments, lipids, thrombi, and hemorrhage all will appear as echolucent structures. Hemorrhage seldom occupies >2% of total plaque size,26 however; thus, it seems unlikely that hemorrhage contributes substantially to the observed echolucency. The association between plaque morphology in carotid arteries and cerebrovascular disease in the present prospective study may therefore be analogous to the relationship between lipid-rich plaques and coronary events. Because many clinical ischemic events occurred in a vascular territory different from the one supplied by the artery with the echolucent plaque, however, we cannot assume the same causal relationship between plaque morphology and events as seen in studies of coronary heart disease, although it seems clear that plaque echolucency is a marker of higher risk.
Our results are in line with the findings from previous
studies. In the Cardiovascular Health Study
(CHS),16 a cohort of 4886
persons 65 years old were followed up for a mean of 3.3 years. Plaque
echogenicity was characterized as hypoechoic, isoechoic, or
hyperechoic. The relative risk of ipsilateral stroke for hypoechoic
plaques was 2.78 (95% CI 1.36 to 5.69). The hypoechoic group probably
corresponds to our echolucent group and perhaps partly to the
predominantly echolucent group. The older study population probably
explains why the stroke rate was higher in the CHS than in the
present study. Sterpetti et
al8 examined prospectively
214 consecutive patients referred to a vascular laboratory and found
that degree of stenosis 50% and heterogeneous
plaques were independent predictors of new cerebrovascular events. The
term heterogenic in the Sterpetti study referred to plaques with mixed
high-, medium-, and low-level echoes and probably included plaques
containing zones with echolucency, whereas the term homogenic was used
to characterize all plaques that gave uniformly high-level echoes and
probably corresponds to what we have called echogenic.
Known cardiovascular risk factors such as sex, blood pressure, total cholesterol, and HDL cholesterol were not significant predictors of cerebrovascular events in the present study. This is not surprising, because these risk factors are associated with both presence of stenosis and plaque echogenicity, which will attenuate the effect of the cardiovascular risk factors on cerebrovascular events. Also, the effects of age will be difficult to detect in a matched design. Smoking, fibrinogen, and white blood cell count were the only risk factors that were significant predictors of events in univariate analysis. Both fibrinogen and leukocyte count correlate with smoking. Interestingly, in multivariate analysis, only white blood cell count was a significant predictor of cerebrovascular events (along with degree of stenosis and plaque echolucency). This might reflect inflammatory processes related to the atherosclerotic lesion.27
The low number of events in each echogenicity group in our study calls for a cautious interpretation of the results. Although a significant linear trend was found, the confidence intervals were wide. A similar trend was observed for ipsilateral events, but the study did not have enough power to assess the independent effect of plaque morphology on ipsilateral events. Conclusions about whether plaque echolucency plays a causal role in the development of cerebrovascular ischemic events or merely acts as a marker of higher risk cannot be made on the basis of data from an observational study. The fact that the examiner knew whether a participant in the study had stenosis or not may have biased the results toward a greater difference between subjects with and without stenosis when it comes to clinical events, especially events like TIAs and amaurosis fugax, which are more susceptible to the subjective evaluation of the observer than stroke. We do not think, however, that this has led to substantial impact on the results. More importantly, the observer was blinded to plaque morphology, which makes it unlikely that any serious observation errors have biased the results in this respect. It is likely that the present study underestimates the true relationship between plaque morphology and risk of clinical disease because of random misclassification of plaque morphology.
TIA and amaurosis fugax are by definition transient, benign symptoms, which in themselves are no threat to the patient’s health. They do, however, represent "warning signs" and as such are important predictors of stroke. Evaluation of plaque morphology in addition to the grade of stenosis might improve clinical decision-making and differentiate treatment for individual patients. Computer-quantified plaque morphology assessment, which is a more objective method of ultrasonic plaque characterization, may further improve this.28 It has been suggested that plaque echolucency should be used to select patients with asymptomatic stenosis for carotid surgery,6 but it is not known whether surgery is of greater benefit than medical treatment in subjects with echolucent stenotic plaques compared with subjects with echogenic plaques.
We conclude that plaque echolucency and degree of stenosis are independent predictors of stroke and cerebrovascular events. The present population-based study provides support for the concept that echolucent plaques are more likely to produce clinical cerebrovascular events.
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Acknowledgments |
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The study was supported by grants from the research program "Research on the Elderly in Tromsø," which is funded by the Ministry of Health and Social Affairs, and from the Norwegian Research Council.
Received November 17, 2000; revision received January 31, 2001; accepted February 6, 2001.
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S. Sabeti, O. Schlager, M. Exner, W. Mlekusch, J. Amighi, P. Dick, G. Maurer, K. Huber, R. Koppensteiner, O. Wagner, et al. Progression of Carotid Stenosis Detected by Duplex Ultrasonography Predicts Adverse Outcomes in Cardiovascular High-Risk Patients Stroke, November 1, 2007; 38(11): 2887 - 2894. [Abstract] [Full Text] [PDF]
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 J. J. Cao, A. M. Arnold, T. A. Manolio, J. F. Polak, B. M. Psaty, C. H. Hirsch, L. H. Kuller, and M. Cushman Association of Carotid Artery Intima-Media Thickness, Plaques, and C-Reactive Protein With Future Cardiovascular Disease and All-Cause Mortality: The Cardiovascular Health Study Circulation, July 3, 2007; 116(1): 32 - 38. [Abstract] [Full Text] [PDF]
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G. Ostling, B. Hedblad, G. Berglund, and I. Goncalves Increased Echolucency of Carotid Plaques in Patients With Type 2 Diabetes Stroke, July 1, 2007; 38(7): 2074 - 2078. [Abstract] [Full Text] [PDF]
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 K. I. Paraskevas, D. P. Mikhailidis, and C. D. Liapis Internal Carotid Artery Occlusion: Association With Atherosclerotic Disease in Other Arterial Beds and Vascular Risk Factors Angiology, June 1, 2007; 58(3): 329 - 335. [Abstract] [PDF]
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 B. H. Tonnessen and S. R. Money Redgrave JNE, Lovett JK, Gallagher PJ, et al. Histological assessment of 526 symptomatic carotid plaques in relation to the nature and timing of ischemic symptoms: the Oxford Plaque Study. Circulation. 2006; 113:2320-2328 Perspectives in Vascular Surgery and Endovascular Therapy, June 1, 2007; 19(2): 194 - 195. [Abstract] [PDF]
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E. R. Bates, C. J. D. Babb, D. E. Casey, C. U. Cates, G. R. Duckwiler, T. E. Feldman, W. A. Gray, K. Ouriel, E. D. Peterson, K. Rosenfield, et al. ACCF/SCAI/SVMB/SIR/ASITN 2007 Clinical Expert Consensus Document on Carotid Stenting: A Report of the American College of Cardiology Foundation Task Force on Clinical Expert Consensus Documents (ACCF/SCAI/SVMB/SIR/ASITN Clinical Expert Consensus Document Committee on Carotid Stenting) Vascular Medicine, February 1, 2007; 12(1): 35 - 83. [PDF]
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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]
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S. Prabhakaran, T. Rundek, R. Ramas, M. S.V. Elkind, M. C. Paik, B. Boden-Albala, and R. L. Sacco Carotid Plaque Surface Irregularity Predicts Ischemic Stroke: The Northern Manhattan Study Stroke, November 1, 2006; 37(11): 2696 - 2701. [Abstract] [Full Text] [PDF]
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 N. Fiotti, N. Altamura, M. Fisicaro, N. Carraro, L. Uxa, G. Grassi, L. Torelli, R. Gobbato, G. Guarnieri, B. T. Baxter, et al. MMP-9 Microsatellite Polymorphism and Susceptibility to Carotid Arteries Atherosclerosis Arterioscler Thromb Vasc Biol, June 1, 2006; 26(6): 1330 - 1336. [Abstract] [Full Text] [PDF]
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J.N.E. Redgrave, J.K. Lovett, P.J. Gallagher, and P.M. Rothwell Histological Assessment of 526 Symptomatic Carotid Plaques in Relation to the Nature and Timing of Ischemic Symptoms: The Oxford Plaque Study Circulation, May 16, 2006; 113(19): 2320 - 2328. [Abstract] [Full Text] [PDF]
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R. Sztajzel, I. Momjian-Mayor, M. Comelli, and S. Momjian Correlation of Cerebrovascular Symptoms and Microembolic Signals With the Stratified Gray-Scale Median Analysis and Color Mapping of the Carotid Plaque Stroke, March 1, 2006; 37(3): 824 - 829. [Abstract] [Full Text] [PDF]
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N. Takaya, C. Yuan, B. Chu, T. Saam, H. Underhill, J. Cai, N. Tran, N. L. Polissar, C. Isaac, M. S. Ferguson, et al. Association Between Carotid Plaque Characteristics and Subsequent Ischemic Cerebrovascular Events: A Prospective Assessment With MRI--Initial Results Stroke, March 1, 2006; 37(3): 818 - 823. [Abstract] [Full Text] [PDF]
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W. A. Willinek Looking Beyond the Lumen to Predict Cerebrovascular Events: "The Road Less Travelled By" Stroke, March 1, 2006; 37(3): 759 - 760. [Full Text] [PDF]
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N.F. Fanning, T.D. Walters, A.J. Fox, and S.P. Symons Association between Calcification of the Cervical Carotid Artery Bifurcation and White Matter Ischemia. AJNR Am. J. Neuroradiol., February 1, 2006; 27(2): 378 - 383. [Abstract] [Full Text] [PDF]
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 S Soumian, R Gibbs, A Davies, and C Albrecht mRNA expression of genes involved in lipid efflux and matrix degradation in occlusive and ectatic atherosclerotic disease J. Clin. Pathol., December 1, 2005; 58(12): 1255 - 1260. [Abstract] [Full Text] [PDF]
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J. Aoki, A. C. Abizaid, P. W. Serruys, A. T.L. Ong, E. Boersma, J. E. Sousa, and N. Bruining Evaluation of Four-Year Coronary Artery Response After Sirolimus-Eluting Stent Implantation Using Serial Quantitative Intravascular Ultrasound and Computer-Assisted Grayscale Value Analysis for Plaque Composition in Event-Free Patients J. Am. Coll. Cardiol., November 1, 2005; 46(9): 1670 - 1676. [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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S. H. Johnsen, E. B. Mathiesen, E. Fosse, O. Joakimsen, E. Stensland-Bugge, I. Njolstad, and E. Arnesen Elevated High-Density Lipoprotein Cholesterol Levels Are Protective Against Plaque Progression: A Follow-Up Study of 1952 Persons With Carotid Atherosclerosis The Tromso Study Circulation, July 26, 2005; 112(4): 498 - 504. [Abstract] [Full Text] [PDF]
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S Soumian, C Albrecht, A. Davies, and R. Gibbs ABCA1 and atherosclerosis Vascular Medicine, May 1, 2005; 10(2): 109 - 119. [Abstract] [PDF]
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R. Sztajzel, S. Momjian, I. Momjian-Mayor, N. Murith, K. Djebaili, G. Boissard, M. Comelli, and G. Pizolatto Stratified Gray-Scale Median Analysis and Color Mapping of the Carotid Plaque: Correlation With Endarterectomy Specimen Histology of 28 Patients Stroke, April 1, 2005; 36(4): 741 - 745. [Abstract] [Full Text] [PDF]
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 K. R. Nandalur, E. Baskurt, K. D. Hagspiel, C. D. Phillips, and C. M. Kramer Calcified Carotid Atherosclerotic Plaque Is Associated Less with Ischemic Symptoms Than Is Noncalcified Plaque on MDCT Am. J. Roentgenol., January 1, 2005; 184(1): 295 - 298. [Abstract] [Full Text] [PDF]
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I. Goncalves, M. W. Lindholm, L. M. Pedro, N. Dias, J. Fernandes e Fernandes, G. N. Fredrikson, J. Nilsson, J. Moses, and M. P.S. Ares Elastin and Calcium Rather Than Collagen or Lipid Content Are Associated With Echogenicity of Human Carotid Plaques Stroke, December 1, 2004; 35(12): 2795 - 2800. [Abstract] [Full Text] [PDF]
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A. Kitamura, H. Iso, H. Imano, T. Ohira, T. Okada, S. Sato, M. Kiyama, T. Tanigawa, K. Yamagishi, and T. Shimamoto Carotid Intima-Media Thickness and Plaque Characteristics as a Risk Factor for Stroke in Japanese Elderly Men Stroke, December 1, 2004; 35(12): 2788 - 2794. [Abstract] [Full Text] [PDF]
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 L. G. Spagnoli, A. Mauriello, G. Sangiorgi, S. Fratoni, E. Bonanno, R. S. Schwartz, D. G. Piepgras, R. Pistolese, A. Ippoliti, and D. R. Holmes Jr Extracranial Thrombotically Active Carotid Plaque as a Risk Factor for Ischemic Stroke JAMA, October 20, 2004; 292(15): 1845 - 1852. [Abstract] [Full Text] [PDF]
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G. M. Biasi, A. Froio, E. B. Diethrich, G. Deleo, S. Galimberti, P. Mingazzini, A. N. Nicolaides, M. Griffin, D. Raithel, D. B. Reid, et al. Carotid Plaque Echolucency Increases the Risk of Stroke in Carotid Stenting: The Imaging in Carotid Angioplasty and Risk of Stroke (ICAROS) Study Circulation, August 10, 2004; 110(6): 756 - 762. [Abstract] [Full Text] [PDF]
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L. Jorgensen, T. Jenssen, O. Joakimsen, I. Heuch, O. C. Ingebretsen, and B. K. Jacobsen Glycated Hemoglobin Level Is Strongly Related to the Prevalence of Carotid Artery Plaques With High Echogenicity in Nondiabetic Individuals: The Tromso Study Circulation, July 27, 2004; 110(4): 466 - 470. [Abstract] [Full Text] [PDF]
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S. Golemati, T. J. Tegos, A. Sassano, K. S. Nikita, and A. N. Nicolaides Echogenicity of B-mode Sonographic Images of the Carotid Artery: Work in Progress J. Ultrasound Med., May 1, 2004; 23(5): 659 - 669. [Abstract] [Full Text] [PDF]
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R. Kern, K. Szabo, M. Hennerici, and S. Meairs Characterization of Carotid Artery Plaques Using Real-time Compound B-mode Ultrasound Stroke, April 1, 2004; 35(4): 870 - 875. [Abstract] [Full Text] [PDF]
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E. B. Mathiesen, K. Waterloo, O. Joakimsen, S. J. Bakke, E. A. Jacobsen, and K. H. Bonaa Reduced neuropsychological test performance in asymptomatic carotid stenosis: The Tromso Study Neurology, March 9, 2004; 62(5): 695 - 701. [Abstract] [Full Text] [PDF]
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H. Yamagami, K. Kitagawa, Y. Nagai, H. Hougaku, M. Sakaguchi, K. Kuwabara, K. Kondo, T. Masuyama, M. Matsumoto, and M. Hori Higher Levels of Interleukin-6 Are Associated With Lower Echogenicity of Carotid Artery Plaques Stroke, March 1, 2004; 35(3): 677 - 681. [Abstract] [Full Text] [PDF]
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P. Ehlermann, W. Mirau, J. Jahn, A. Remppis, and A. Sheikhzadeh Predictive Value of Inflammatory and Hemostatic Parameters, Atherosclerotic Risk Factors, and Chest X-Ray for Aortic Arch Atheromatosis Stroke, January 1, 2004; 35(1): 34 - 39. [Abstract] [Full Text] [PDF]
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 M. Zureik, J.-M. Bureau, M. Temmar, C. Adamopoulos, D. Courbon, K. Bean, P.-J. Touboul, A. Benetos, and P. Ducimetiere Echogenic Carotid Plaques Are Associated With Aortic Arterial Stiffness in Subjects With Subclinical Carotid Atherosclerosis Hypertension, March 1, 2003; 41(3): 519 - 527. [Abstract] [Full Text] [PDF]
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E. Mohler III Vascular calcification: good, bad or ugly? Vascular Medicine, August 1, 2002; 7(3): 161 - 162. [PDF]
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J. L. Hunt, R. Fairman, M. E. Mitchell, J. P. Carpenter, M. Golden, T. Khalapyan, M. Wolfe, D. Neschis, R. Milner, B. Scoll, et al. Bone Formation in Carotid Plaques: A Clinicopathological Study Stroke, May 1, 2002; 33(5): 1214 - 1219. [Abstract] [Full Text] [PDF]
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K. Sheikh, E. B. Mathiesen, K. H. Bonaa, and O. Joakimsen Cholesterol and Carotid Stenosis Stroke, January 1, 2002; 33(1): 321 - 322. [Full Text] [PDF]
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E. B. Mathiesen, K. H. Bonaa, and O. Joakimsen Low Levels of High-Density Lipoprotein Cholesterol Are Associated With Echolucent Carotid Artery Plaques: The Tromso Study Stroke, September 1, 2001; 32(9): 1960 - 1965. [Abstract] [Full Text] [PDF]
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