| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
(Stroke. 1997;28:2201-2207.)
© 1997 American Heart Association, Inc.
Articles |
Reproducibility of Ultrasound Assessment of Carotid Plaque Occurrence, Thickness, and Morphology
The Tromsø Study
From the Institute of Community Medicine, University of Tromsø (Norway).
Correspondence to Oddmund Joakimsen, Institute of Community Medicine, University of Tromsø, N-9037, Norway. E-mail oddmund.joakimsen{at}ism.uit.no
 |
Abstract |
|---|
 Top Abstract IntroductionSubjects and MethodsResultsDiscussionReferences |
|---|
Background and Purpose Ultrasonography is increasingly used in vascular research, but there is limited information about the reproducibility of the ultrasound method for screening purposes. In this study the reproducibility of ultrasound assessment of carotid plaque occurrence, thickness, and morphology was examined within the setting of a population health survey.
Methods In 1994/1995, 6720 participants in the Tromsø Study, Norway, underwent B-mode ultrasound scanning of the right carotid artery. The between- and within-sonographer reproducibility of ultrasound assessment of plaque occurrence and thickness was estimated by repeated scanning of a random sample of 107 participants. The between- and within-sonographer reproducibility of plaque morphology classification (echogenicity, four categories and heterogeneity, two categories) was determined by repeated reading of videotaped images of 119 randomly selected arteries with plaques.
Results Between- and within-sonographer agreement on plaque
occurrence was substantial with 
values (95% CI) of 0.72 (0.60 to
0.84) and 0.76 (0.63 to 0.89), respectively. Reproducibility of plaque
thickness measurements was moderate, with mean absolute differences
ranging between 0.25 and 0.55 mm (coefficients of variation
between 13.8% and 22.4%). Agreement on plaque morphology
classification was high, with values ranging between 0.54 and
0.73.
Conclusions Population screening using B-mode ultrasound provides a valuable means for the detection and morphological evaluation of carotid plaques, whereas measurements of plaque thickness are subject to considerable measurement error.
Key Words: atherosclerosis • carotid arteries • ultrasonography
|
Introduction |
|---|
|
TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
|---|
Ultrasound-assessed carotid atherosclerosis correlates with atherosclerosis in other arterial territories and is associated with clinical cardiovascular disease.1 2 Both uniformly increased intima-media thickness and protruding plaques appear to be ultrasound markers of general atherosclerosis, the latter being an expression of more advanced disease and a potential precursor of clinical events. Not only the extent of atherosclerosis but also morphological characteristics of plaques may be evaluated with ultrasound. Lipid-rich plaques, which may be particularly prone to rupture and cause a cardiovascular event, only poorly reflect emitted ultrasound and appear echolucent (dark) and heterogeneous on ultrasound images.3 4 5 6 Studies on selected groups of patients indicate that ultrasound morphology of stenotic carotid plaques is an independent risk factor of stroke,5 7 8 and plaque composition might therefore affect decision making in reference to carotid endarterectomy in asymptomatic patients. Since recent studies indicate that cardiovascular risk factors correlate with histological plaque characteristics,5 9 the sonographic appearance of plaques might also be used for in vivo studies of the determinants of atherosclerosis within populations.
The reproducibility of ultrasound carotid intima-media thickness measurements has been examined extensively. Surprisingly, studies on variability among sonographers on carotid plaque detection have not been published, and to our knowledge only two reproducibility studies of ultrasound plaque morphology are reported.10 11 We therefore examined the reproducibility of ultrasound assessment of carotid plaque occurrence, thickness, and morphology within the setting of a population health screening in Tromsø, Norway.
|
Subjects and Methods |
|---|
|
TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
|---|
Subjects
The Tromsø Study was started in 1974 and is a single-center prospective follow-up study of inhabitants in the municipality of Tromsø, Norway. The primary objective is to investigate determinants of chronic diseases by means of epidemiological, clinical, and basic research to assess etiologic significance and to identify potentially modifiable determinants that may be developed into preventive or therapeutic strategies. The main focus is on cardiovascular diseases. The study design includes repeated population health surveys to which total birth cohorts and random samples are invited.
The fourth survey of the Tromsø population study started in September
1994 and was completed in October 1995. The survey was conducted by the
University of Tromsø in cooperation with the National Health Screening
Service and comprised two screening visits 4 to 12 weeks apart. All
inhabitants older than 24 years were invited to the first visit, and
27 161 subjects, 78% of the eligible population, participated. A
protocol similar to the previous surveys in this population was
followed.12 The examination included standardized
measurements of height, weight, blood pressure, nonfasting serum
lipids, serum calcium, 
-glutamyltransferase, hemoglobin and blood
cell counts, and a 20-second
electrocardiography of lead I. Two
questionnaires covered previous and present diseases and symptoms,
use of drugs, lifestyle (physical activity, smoking, alcohol intake),
dietary habits, and socioeconomic status.
All subjects aged 55 to 74 years and random 5% to 10% samples in the other age groups were invited to the second visit. A total of 6891 subjects, 98% of those who participated in the first visit and were eligible for the second visit, attended. The second visit comprised ultrasonographic examination of the right carotid artery and the abdominal aorta, echocardiography, a 12-lead resting electrocardiogram, a 90-second rhythm electrocardiogram during standardized deep breathing, measurements of bone density, body fat composition, waist and hip circumference, sitting and standing blood pressures, and urine and blood sampling. The study was approved by the regional ethical committee.
Reproducibility of Plaque Occurrence and Plaque Thickness
The reproducibility study was designed to study
between-sonographer (different sonographers on the same occasion) and
within-sonographer (same sonographers on two separate occasions)
agreement on the presence of carotid atherosclerotic plaque in the
beginning (first reproducibility study) and the end (second
reproducibility study) of the survey period. The subjects were examined
by the three same sonographers with an interval of 1 week in the first
(weeks 10 and 11) and 3 weeks in the second (weeks 37 and 40)
reproducibility study.
The sonographers were blinded to each other's results and to medical information about the participants. One of the sonographers was a neurologist with 10 years of experience in ultrasound examination of the carotid artery, the second was a physician, and the third was a specially trained technician. A 2-month training protocol was completed before the survey started. In addition, the first 200 survey examinations conducted by the physician and the technician were supervised by the neurologist. At the start of the first reproducibility study the physician and the technician had performed approximately 300 and 600 examinations, respectively, on their own.
A total of 111 subjects were invited to the two reproducibility studies. All of them attended, but some of them met on only one occasion, and in a few instances some participants were not examined by all three sonographers. For the between-sonographer study we chose the weeks from the first and second reproducibility studies with the largest number of paired observations. The neurologist did not examine participants in week 40, and data on within-sonographer variability for the neurologist are therefore available only from the first reproducibility study. A total of 107 subjects were included in the analysis. Among these there were 77 subjects who attended the first and 30 subjects who attended the second reproducibility study.
High-resolution B-mode ultrasonography of the right carotid artery was performed with an ultrasound scanner (Acuson Xp10 128 ART [upgraded]) equipped with a linear array 5- to 7-MHz transducer. The subjects were examined in the supine position with the head turned slightly to the left. The common, internal, and external carotid arteries were identified by combining B-mode and color Doppler/pulsed-wave Doppler ultrasound. We attempted to identify and record atherosclerotic plaques from six segments of the carotid artery: the near and far walls of the right internal carotid artery as far upstream from the bifurcation as technically possible, the right carotid bulb of the common carotid artery (the bifurcation segment), and the right common carotid artery from the bifurcation and downstream to the supraclavicular region. Frozen ultrasound images were stored on sVHS videotapes; a 1-minute live recording of the carotid artery from different transducer positions and angles was also stored to obtain a representative recording of plaque thickness and morphology.
Instrument imaging adjustments (preprocession and postprocession, persistence, transmit zones, log compression, image depth, transmit power) were set at fixed values. The gain setting (including the depth gain compensation curve), however, was adjusted according to interindividual differences such as neck thickness, subcutaneous fat, and echogenicity of the near artery wall structures to obtain optimal visualization of arterial wall morphology. The gain setting was also continuously changed during the scanning procedure on the same individual to enhance plaque detection and characterization. The gain should not be set so high that structure details of the high-echogenic far wall media-adventitia interface are concealed.
A plaque was defined as a localized protrusion of the vessel wall into the lumen. The maximum plaque thickness was measured on-line on frozen B-mode images marked with electronic calipers with measurement readout in tenths of a millimeter. The results were recorded on videotapes and on written forms by the sonographers. In the far wall the plaque thickness was defined as the distance between the lumen-plaque interface and the media-adventitia boundary. Plaques in the near wall were measured from the far edge of periadventitia-adventitia interface to the far edge of the intima-lumen interface.13 According to the protocol, plaques should be visualized in the full diameter of the vessel; ie, both the proximal and the distal parts of the plaque should be "attached" to the typical double-lined intima-media structure, and the double lines should also be visible on the opposite side of the vessel lumen. The sonographers attempted by gain adjustments and transducer angling to obtain the highest possible echogenicity of the plaques, ie, echo signals as bright as possible without obscuring structural details. Plaque thickness was defined as the single maximum plaque thickness in any of the six measured segments.
Reproducibility of Plaque Morphology Classification
Two of the sonographers performed a separate between-observer
reproducibility study on plaque echogenicity and
heterogeneity on 119 carotid arteries with plaques. The
echogenicity and heterogeneity classification was
performed off-line on plaques from one sVHS videotape from the first
and one from the second part of the survey period. The two sonographers
were blinded for each other's results. To study within-observer
variability a second reading was performed by one of the sonographers 5
weeks after the first reading.
Plaque echogenicity was graded from 1 to 4, where grade 1 denotes low
echogenicity or echolucency (defined as a plaque appearing black or
almost black as flowing blood), and grade 4 denotes strong echogenicity
(defined as a plaque appearing white or almost white, similar to the
far wall media-adventitia interface) (Fig 1
). Plaques that were difficult to
classify because of echo-shadowing from calcifications in near wall
plaques, calcifications just below the surface of a far wall plaque
hiding substantial parts of the rest of the plaque, or unsatisfactory
imaging quality were defined as unclassifiable (n=7).
|
Plaques were also classified according to structural appearance
criteria as either heterogeneous or homogeneous
(Fig 1
). Plaques were characterized as heterogeneous if the
echogenicity of more than 20% of the plaque area differed from the
echogenicity of the rest of the plaque by two or more echogenicity
grades. All other plaques were defined as homogeneous. If
more than one plaque was present in a carotid artery, an overall
echogenicity and heterogeneity score was estimated from
the total plaque area following the aforementioned guidelines.
Statistical Analysis
The between- and within-sonographer variability in the
assessment of plaque occurrence, echogenicity, and
heterogeneity was analyzed by the use of the
kappa statistic (). measures the agreement that occurs above
chance14 and may have values between -1 (complete
disagreement) and +1 (perfect agreement). values from 0 to 0.20 are
categorized as slight agreement, those from 0.21 to 0.40 as fair, those
from 0.41 to 0.60 as moderate, those from 0.61 to 0.80 as substantial,
and those above 0.80 as almost perfect agreement.15 The
95% confidence intervals (CIs) were estimated as estimates ±2 SE
according to Fleiss.14 Mean arithmetic differences (95%
CI) and mean absolute differences were used to estimate the
reproducibility of measurements of plaque thickness. The coefficient of
variation (CV) of differences was calculated according to the
formula
 |
. SD is the
standard deviation of the arithmetic differences between measurements,
and ¯x is the mean value of plaque
thickness.16 The arithmetic differences between paired
examinations were plotted against their average to examine whether the
differences were reasonably constant throughout the range of
measurements.17 If the differences are normally
distributed, 95% of the differences will lie within a range of ±1.96
SDs of the mean arithmetic difference. This range will be referred to
as "the limits of agreement." Means were compared with the use of
Student's t test. Differences between proportions were
analyzed by the 
2 test. Two-sided values
of P<.05 were considered statistically significant. The SAS
software package was used.18 |
Results |
|---|
|
TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
|---|
Table 1
shows that those who took
part in the reproducibility study were representative
of the total study population. The participants in the reproducibility
study were slightly younger than the rest of the study population since
very old persons were not invited to the reproducibility study because
it was strenuous and time-consuming. About 49% of the participants had
one or more atherosclerotic plaques (Table 1).
|
Plaque Occurrence
Overall between-sonographer agreement on the presence of
atherosclerotic plaques showed a value of 0.72 (95% CI, 0.60 to
0.84), indicating substantial agreement (Table 2) There was no significant difference in
the agreement between the first and the second reproducibility study.
Within-sonographer agreement on plaque occurrence was slightly better
than between-sonographer agreement with an overall of 0.76 (95%
CI, 0.63 to 0.89) (Table 2). Reproducibility of plaque detection did
not differ significantly among the three sonographers.
|
Plaque Thickness
Between-sonographer reproducibility of plaque thickness is
summarized in Table 3. The mean
arithmetic differences were generally small, ranging from 3% to 12%
of mean plaque thickness. The physician tended to measure plaques
thinner than the technician and the neurologist. The mean absolute
differences varied between 0.25 and 0.55 mm, and the CVs were
between 17.9% and 22.4%. The limits of agreement were ±1.04, ±1.27,
and ±1.32 mm for comparisons of the technician versus the
physician, the neurologist versus the technician, and the physician
versus the neurologist, respectively. Fig 2 shows that between-sonographer
variability is greater with increasing plaque thickness.
|
|
Within-sonographer reproducibility of plaque thickness is shown in
Table 3. The reproducibility was similar for the three sonographers and
was better than the between-sonographer reproducibility. The
within-sonographer variability was greater with increasing plaque
thickness (Fig 2).
Plaque Morphology
Between- and within-sonographer agreement on plaque echogenicity
classification was substantial (Table 4).
When echogenicity grades 1 and 2 were merged into one low-echogenicity
category and grades 3 and 4 were merged into one high-echogenicity
category, the values for between- and within-sonographer
variability were 0.80 (95% CI, 0.61 to 0.99) and 0.79 (95% CI, 0.61
to 0.97), respectively. Between- and within-sonographer agreement on
plaque heterogeneity classification showed values
of 0.71 (95% CI, 0.52 to 0.90) and 0.54 (95% CI, 0.36 to 0.72),
respectively (Table 4).
|
|
Discussion |
|---|
|
TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
|---|
Ultrasound is increasingly used as a noninvasive method in basic and clinical research. The reproducibility of echographic measurements of carotid artery intima-media thickness is well established,19 20 21 22 23 24 but the reliability of ultrasound plaque detection and morphological classification has been studied less well. The present results show that ultrasound can be used both to identify and to classify carotid plaques with an acceptable degree of between- and within-sonographer reliability. Measurements of plaque thickness, however, are subject to considerable measurement error. To enhance the generalizibility of the results we examined a random sample of participants in a population health survey, and we did not exclude subjects on the basis of ultrasonographic, demographic, or medical characteristics.
The dependence of B-mode image quality on interrogation angle and fine adjustment of instrument controls makes the role of the sonographer crucial to the measurement process. Previous reproducibility studies on plaque detection were based on multiple off-line readings of single vessel-wall images recorded on videotape,20 25 thus bypassing the influence of the sonographer on measurement variability. Although the present study demonstrates a substantial overall agreement on the presence of plaques, a number of plaques could not be identified on repeated examinations. What are the characteristics of such plaques?
We identified two factors influencing agreement, plaque localization,
and plaque size. Agreement on the occurrence of near wall plaques was
significantly lower than of far wall plaques: complete agreement among
all three sonographers on the presence of a plaque was found in 61% of
those near wall plaques that were identified by any of the
sonographers, whereas complete agreement was found in 82% of the far
wall plaques
(2df=1=4.46;
P=.035). Higher variability of detection was also observed
for smaller plaques: the mean (SEM) thickness of plaques detected by
only one or two of the three sonographers was 1.58 (0.07) mm,
whereas the mean thickness of those plaques detected by all
sonographers was 2.42 (0.09) mm (P<.001). Our study
was conducted within the setting of a population health survey, and
each scanning was scheduled to be completed within approximately 20
minutes. It is possible that the available time was not sufficient for
scrutinizing near wall structures, which apparently are more difficult
to identify than far wall structures. Furthermore, it may often be
difficult to decide whether a minor wall irregularity
represents a plaque or only "wall roughness." We defined
a plaque as a "localized protrusion of the vessel wall into the
lumen." The results might have improved by specifying in the
protocol that the qualifying lesion was a distinct area with an
intima-media thickness more than 50% thicker than neighboring sites
judged visually.26 However, this definition might have
excluded a significant proportion of early lesions from being
identified. There were no notable differences between the results
obtained in the first and the second reproducibility studies,
indicating that presurvey training of sonographers and standardization
of the procedures were sufficient.
The present study indicates that plaque thickness can be measured
without systematic differences (bias) among sonographers. There is,
however, much room for improvement regarding the precision of such
measurements: the limits of agreement (Table 3) indicate that even a
60% change in an individual's plaque thickness may be attributable to
measurement error if the measurements are performed by different
sonographers. The corresponding percentage for repeated measurements by
a single sonographer is 40%, illustrating that within-sonographer
variability was considerably lower than between-sonographer
variability. Clinical studies on selected groups of patients have found
mean absolute differences between sonographers ranging between 0.31 and
0.36 mm (reader variability not included),19 21 which
are similar to our findings, whereas a greater difference (0.63
mm) was reported from a population-based study.24 These
results indicate that ultrasound may not be used for monitoring the
progression/regression of plaque thickness on an individual level. Our
data suggest that sample size requirements for clinical trials will
vary considerably depending on whether the ultrasound measurements are
conducted by a single or by several sonographers: a single sonographer
may detect a 10% difference (0.20 mm) in plaque thickness at
P=.05 with a power of 0.90 with a total study size of 150
subjects (for a two-sample comparison), whereas approximately 400
subjects are required if the measurements are done by several
sonographers. The reproducibility of the thickness measurements might
improve by having a fixed and known angle of interrogation and by using
the average of values obtained on separate occasions.
The usefulness of plaque thickness measurements in epidemiological studies may be limited because plaques available for quantitative measurements are present in only a proportion of the population. Reproducible measurements of intima-media thickness in the carotid artery are achievable in most subjects,27 but a thick intima-media may not always reflect early atherosclerosis.28 29 One of the outstanding issues to be resolved in atherogenesis is which mechanisms and risk factors are associated with the evolution of a uniform wall thickening into an atherosclerotic plaque.30 This requires prospective studies with baseline and follow-up data on both intima-media thickness and plaque occurrence.
High-resolution ultrasound allows morphological characterization of the
carotid artery plaque that matches reasonably well with
histological features of specimens from
endarterectomies4 5 31 or from autopsy.4 32
Plaques that only poorly reflect emitted ultrasound (echolucent) have a
high content of lipid and/or hemorrhage, whereas plaques that
strongly reflect ultrasound (echogenic) have a higher content of dense
fibrous tissue and calcified material. Carotid plaque composition
analyzed by ultrasound correlates with
cardiovascular risk factor levels,10 and
some reports,5 6 7 8 33 34 but not all,35 36 have
found an association between the morphology of stenotic plaques
and the risk of stroke. There is, however, no consensus on
ultrasonographic criteria for morphological characterization of carotid
plaques. It is important to standardize echogenicity classification
against defined and well-recognized reference structures located
adjacent to the plaque. Because such classifications are based on
subjective judgment, it has been suggested to use densitometric
evaluation or radiofreqency-based tissue
characterization.3 37 Such methods provide more objective
and quantitative measures on plaque morphology, but they are
time-consuming and not practical for use in epidemiological studies. In
the present study the two ultrasound reference structures used as
extremes on a gray scale were the almost nonreflecting flowing blood
(echolucent, grade 1) on the one side and the bright, high-echogenic
far wall media-adventitia interface (echo-rich, grade 4) on the other
side (Fig 1). It has been suggested that the mastoid muscle and the
cervical vertebra may be used as reference structures.38
The usefulness of those structures is not documented, to our knowledge,
and it may be suggested that reference structures that are
located close to the plaque should be preferred compared with more
remote structures. The deeply localized vertebrae may not always give
rise to high-reflecting echoes, possibly because of scarce remaining
ultrasound energy after passage of the high-frequency ultrasound
signals through the tissues in the neck. Lack of adequate reference
structures is probably a major source of error in studies evaluating
ultrasound morphology. In the present study we obtained an
acceptable agreement on the classification of carotid plaques in terms
of echogenicity and heterogeneity. Grønholdt et
al10 and Geroulakos et al11 have previously
reported similar values (0.61 and 0.79, respectively) for
interobserver agreement on echogenicity classification on
stenotic carotid plaques. No reference structures were used in
those studies.
Although the agreement on plaque morphology was acceptable in the
present study, several plaques were differently classified on
repeated examinations. There was no association between disagreement of
echogenicity scoring and plaque size or plaque localization (data not
shown). Disagreement on heterogeneity classification
was, however, associated with lower plaque echogenicity (grades 1 and
2)
(2df=1=10.1;
P=.002) but was not associated with plaque localization or
size. The reason may be that some echogenic plaques containing
echo-poor areas caused by shadows from calcium deposits were scored as
heterogeneous instead of either homogeneous or
unclassifiable.
Lipid-rich atherosclerotic plaques in the coronary arteries are particularly vulnerable for rupture and are associated with higher risk of myocardial infarction and death than fibrocalcified plaques.39 There are, however, currently no sensitive and practical means of detecting vulnerable coronary plaques in vivo. If carotid and coronary artery plaques share common morphological characteristics within individuals, then ultrasound of the carotid artery may be a simple, noninvasive test to screen asymptomatic subjects at high risk of cardiovascular events.
In conclusion, reproducible ultrasound measurements of carotid plaque occurrence and plaque morphology may be achieved within the setting of a population health survey. Variability of plaque thickness measurements is considerably greater between than within sonographers and is also dependent on plaque thickness. Further studies are needed to clarify whether ultrasound plaque morphology reflects different stages in atherogenesis or different influences on the development of atherosclerosis and whether carotid and coronary plaques share common histological characteristics within individuals. We are currently conducting a population-based prospective follow-up study to assess whether ultrasound plaque morphology predicts the risk of cerebrovascular and cardiovascular morbidity and mortality.
|
Acknowledgments |
|---|
This study was supported by grants from the Norwegian Research Council and in collaboration with the National Health Screening Service. We thank our ultrasound technician Jon T. Moe Joakimsen for skillful contribution to the data collection and analysis of plaque morphology.
Received June 19, 1997; accepted July 30, 1997.
|
References |
|---|
|
TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
|---|
-
Wofford J, Kahl F, Howard G, McKinney W, Toole J,
Crouse J. Relation of extent of extracranial carotid artery
atherosclerosis as measured by B-mode ultrasound to the
extent of coronary atherosclerosis.
Arterioscler Thromb. 1991;11:1786-1794.
[Abstract/Free Full Text] -
Wendelhag I, Wiklund O, Wikstrand J.
Atherosclerotic changes in the femoral and carotid arteries in familial
hypercholesterolemia: ultrasonographic
assessment of intima-media thickness and plaque occurrence.
Arterioscler Thromb. 1993;13:1404-1411.
[Abstract/Free Full Text] -
Urbani M, Picano E, Parenti G, Mazzarisi A, Fiori L,
Paterni M, Pelosi A, Landini L. In vivo radiofrequency-based
ultrasonic tissue characterization of the atherosclerotic
plaque. Stroke. 1993;24:1507-1512.
[Abstract/Free Full Text] - Wolverson M, Bashiti H, Peterson G. Ultrasonic tissue characterization of atheromatous plaques using a high resolution real time scanner. Ultrasound Med Biol. 1983;9:599-609.[Medline] [Order article via Infotrieve]
- European Carotid Plaque Study Group. Carotid artery plaque composition: relationship to clinical presentation and ultrasound B-mode imaging. Eur J Vasc Endovasc Surg. 1995;10:23-30.[Medline] [Order article via Infotrieve]
- Sterpetti A, Shultz R, Feldhaus R, Davenport K, Richardson M, Farina C, Hunter W. Ultrasonographic features of carotid plaque and the risk of subsequent neurologic deficits. Surg. 1988;104:652-660.
- Geroulakos G, Domjan J. Ultrasonic carotid artery plaque structure and the risk of cerebral infarction on computed tomography. J Vasc Surg. 1994;20:263-266.[Medline] [Order article via Infotrieve]
- Langsfeld M, Gray-Weale A, Lusby R. The role of plaque morphology and diameter reduction in the development of new symptoms in asymptomatic carotid arteries. J Vasc Surg. 1989;9:548-557.[Medline] [Order article via Infotrieve]
- Spagnoli L, Mauriello A, Palmieri G, Santeusanio G, Amante A, Taurino M. Relationships between risk factors and morphological patterns of human carotid atherosclerotic plaques: a multivariate discriminant analysis. Atherosclerosis. 1994;108:39-60.[Medline] [Order article via Infotrieve]
-
Grønholdt M, Nordestgaard B, Nielsen T, Sillesen
H. Echolucent carotid artery plaques are associated with
elevated levels of fasting and postprandial
triglyceride-rich lipoproteins. Stroke. 1996;27:2166-2172.
[Abstract/Free Full Text] - Geroulakos G, Ramaswami G, Nicolaides A, James K, Labropoulos N, Belcaro G, Holloway M. Characterization of symptomatic and asymptomatic carotid plaques using high-resolution real-time ultrasonography. Br J Surg. 1993;80:1274-1277.[Medline] [Order article via Infotrieve]
- Thelle D, Førde O, Try K, Lehmann E. The Tromsø Heart Study: methods and main results of the cross-sectional study. Acta Med Scand. 1976;200:107-118.[Medline] [Order article via Infotrieve]
- Wendelhag I, Gustavsson T, Suurküla M, Berglund G, Wikstrand J. Ultrasound measurement of wall thickness in the carotid artery: fundamental principles and description of a computerized analysing system. Clin Phys. 1991;11:565-577.
- Fleiss J. Statistical Methods for Rates and Proportions. 2nd ed. New York, NY: John Wiley & Sons, Inc; 1981:212-236.
- Landis J, Koch G. The measurement of observer agreement for categorical data. Biometrics. 1977;33:159-174.[Medline] [Order article via Infotrieve]
- Bots M, Mulder P, Hofman A, Van Es G, Grobbee D. Reproducibility of carotid vessel wall thickness measurements: the Rotterdam Study. J Clin Epidemiol. 1994;47:921-930.[Medline] [Order article via Infotrieve]
- Bland J, Altman D. Statistical methods for assessing agreement between two methods of clinical measurement. Lancet. 1986;307-310.
- SAS Institute Inc. SAS/STAT Guide for Personal Computers. Cary, NC: SAS Institute Inc; 1987.
- Mercuri M, Bond M, Nichols F, Carr A, Flack J, Byington R, Raines J. Baseline reproducibility of B-mode ultrasound imaging measurements of carotid intima media thickness: the Multicenter Isradipine Diuretic Atherosclerosis Study (MIDAS). J Cardiovasc Diag Proc.. 1993;11:241-255.
-
O'Leary D, Bryan F, Goodison M, Rifkin M, Gramiak R,
Bond M, Dunn R, Goldberg B, Toole J, Wheeler H, Gustafson N, Ekholm S,
Raines J. Measurement variability of carotid
atherosclerosis: real-time (B-mode) ultrasonography and
angiography. Stroke. 1987;18:1011-1017.
[Abstract/Free Full Text] -
Riley W, Barnes R, Applegate W, Dempsey R, Hartwell T,
Davis V, Bond M, Furberg C. Reproducibility of noninvasive
ultrasonic measurement of carotid atherosclerosis: the
Asymptomatic Carotid Artery Plaque Study.
Stroke. 1992;23:1062-1068.
[Abstract/Free Full Text] -
Crouse J, Harpold G, Kahl F, Toole J, McKinney
W. Evaluation of a scoring system for extracranial carotid
atherosclerosis extent with B-mode ultrasound.
Stroke. 1986;17:270-275.
[Abstract/Free Full Text] -
Persson J, Stavenow L, Wikstrand J, Israelsson B,
Formgren J, Berglund G. Noninvasive quantification of
atherosclerotic lesions. Reproducibility of ultrasonographic
measurement of arterial wall thickness and plaque
size. Arterioscler Thromb. 1992;12:261-266.
[Abstract/Free Full Text] -
O'Leary D, Polak J, Wolfson S, Bond M, Bommer W, Sheth
S, Psaty B, Sharrett A, Manolio T. Use of sonography to evaluate
carotid atherosclerosis in the elderly: the
Cardiovascular Health Study (CHS).
Stroke. 1991;22:1155-1163.
[Abstract/Free Full Text] -
Wen-Harn P, Chyi-Huey B, Jiunn-Rong C, Hou-Chang
C. Associations between carotid atherosclerosis
and high factor VIII activity, dyslipidemia, and
hypertension. Stroke. 1997;28:88-94.
[Abstract/Free Full Text] -
Salonen R, Seppänen K, Rauramaa R, Salonen
J. Prevalence of carotid atherosclerosis and
serum cholesterol in Eastern Finland.
Arteriosclerosis. 1988;8:788-792.
[Abstract/Free Full Text] - Stensland-Bugge E, Bønaa K, Joakimsen O. Reproducibility of ultrasonographically determined intima-media thickness is dependent on the arterial wall thickness: the Tromsø Study. Stroke. 1997;In press.
- Glagov S, Zarins C. Is intimal hyperplasia an adaptive response or a pathologic process? Observations on the nature of nonatherosclerotic intimal thickening. J Vasc Surg. 1989;10:571-573.
- Stary H. Evolution and progression of atherosclerotic lesions in coronary arteries of children and young adults. Arteriosclerosis. 1989;9(suppl I):I-19-I-32.
-
Margitic S, Bond M, Crouse J, Furberg C,
Probstfield J. Progression and regression of carotid
atherosclerosis in clinical trials.
Arterioscler Thromb. 1991;11:443-451.
[Free Full Text] - Gray-Weale A, Graham J, Burnett J, Byrne K, Lusby R. Carotid artery atheroma: comparison of preoperative B-mode ultrasound appearance with carotid endarterectomy specimen pathology. J Cardiovasc Surg. 1988;29:676-681.[Medline] [Order article via Infotrieve]
- Goes E, Janssens W, Maillet B, Freson M, Steyaert L, Osteaux M. Tissue characterization of atheromatous plaques: correlation between ultrasound image and histological findings. J Clin Ultrasound. 1990;18:611-617.[Medline] [Order article via Infotrieve]
- Steffen M, Gray-Weale A, Byrne K, Lusby R. Carotid artery atheroma: ultrasound appearance in symptomatic and asymptomatic vessels. Aust N Z J Surg. 1989;59:529-534.[Medline] [Order article via Infotrieve]
-
Iannuzzi A, Wilcosky T, Mercuri M, Rubba P, Bond
M. Ultrasonographic correlates of carotid
atherosclerosis in transient ischemic attack
and stroke. Stroke. 1995;26:614-619.
[Abstract/Free Full Text] - Bassiouny H, Davis H, Massawa N, Gewertz B, Glagov S, Zarins C. Critical carotid stenoses: morphologic and chemical similarity between symptomatic and asymptomatic plaques. J Vasc Surg. 1989;9:202-212.[Medline] [Order article via Infotrieve]
-
Hatsukami T, Ferguson M, Beach K, Gordon D, Detmer P,
Burns D, Alpers C, Strandness Jr D. Carotid plaque morphology
and clinical events. Stroke. 1997;28:95-100.
[Abstract/Free Full Text] -
Beletsky V, Kelley R, Fowler M, Phifer T.
Ultrasound densitometric analysis of carotid plaque
composition. Stroke. 1996;27:2173-2177.
[Abstract/Free Full Text] - De Bray J, Baud J, Dauzat M. Consensus concerning the morphology and the risk of carotid plaques. In: Program and abstracts of the Concensus Conference; December 13-14, 1996; Paris, France. Abstract.
-
Burke A, Farb A, Malcolm G, Liang Y, Smialek J, Virmani
R. Coronary risk factors and plaque morphology in men
with coronary disease who died suddenly. N
Engl J Med. 1997;336:1276-1282.
[Abstract/Free Full Text]
This article has been cited by other articles:
 |
|
 |
|
  S. H. Johnsen, E. B. Mathiesen, O. Joakimsen, E. Stensland, T. Wilsgaard, M.-L. Lochen, I. Njolstad, and E. Arnesen Carotid Atherosclerosis Is a Stronger Predictor of Myocardial Infarction in Women Than in Men: A 6-Year Follow-Up Study of 6226 Persons: The Tromso Study Stroke, November 1, 2007; 38(11): 2873 - 2880. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 I. J. Kullo and A. R. Malik Arterial Ultrasonography and Tonometry as Adjuncts to Cardiovascular Risk Stratification J. Am. Coll. Cardiol., April 3, 2007; 49(13): 1413 - 1426. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 L. Jorgensen, T. Jenssen, S. H. Johnsen, E. B. Mathiesen, I. Heuch, O. Joakimsen, E. Fosse, and B. K. Jacobsen Albuminuria as risk factor for initiation and progression of carotid atherosclerosis in non-diabetic persons: the Tromso Study Eur. Heart J., February 1, 2007; 28(3): 363 - 369. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Zureik, S. Czernichow, D. Courbon, J. Blacher, P. Ducimetiere, S. Hercberg, M. E. Safar, and P. Galan Parental Longevity, Carotid Atherosclerosis, and Aortic Arterial Stiffness in Adult Offspring Stroke, November 1, 2006; 37(11): 2702 - 2707. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 E Seyahi, S Ugurlu, R Cumali, H Balci, N Seyahi, S Yurdakul, and H Yazici Atherosclerosis in Takayasu arteritis Ann Rheum Dis, September 1, 2006; 65(9): 1202 - 1207. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. J Roman, T. Z Naqvi, J. M Gardin, M. Gerhard-Herman, M. Jaff, and E. Mohler American Society of Echocardiography Report: Clinical application of noninvasive vascular ultrasound in cardiovascular risk stratification: a report from the American Society of Echocardiography and the Society for Vascular Medicine and Biology Vascular Medicine, August 1, 2006; 11(3): 201 - 211. [PDF]
|
|
|
|
 |
|
 M. J. Roman, E. Moeller, A. Davis, S. A. Paget, M. K. Crow, M. D. Lockshin, L. Sammaritano, R. B. Devereux, J. E. Schwartz, D. M. Levine, et al. Preclinical carotid atherosclerosis in patients with rheumatoid arthritis. Ann Intern Med, February 21, 2006; 144(4): 249 - 256. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
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]
|
|
|
|
|
|
S. H. Johnsen, E. Fosse, O. Joakimsen, E. B. Mathiesen, E. Stensland-Bugge, I. Njolstad, and E. Arnesen Monocyte Count Is a Predictor of Novel Plaque Formation: A 7-Year Follow-up Study of 2610 Persons Without Carotid Plaque at Baseline The Tromso Study Stroke, April 1, 2005; 36(4): 715 - 719. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 L. Jorgensen, O. Joakimsen, G. K. Rosvold Berntsen, I. Heuch, and B. K. Jacobsen Low Bone Mineral Density Is Related to Echogenic Carotid Artery Plaques: A Population-based Study Am. J. Epidemiol., September 15, 2004; 160(6): 549 - 556. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. Zureik, P. Galan, S. Bertrais, L. Mennen, S. Czernichow, J. Blacher, P. Ducimetiere, and S. Hercberg Effects of Long-Term Daily Low-Dose Supplementation With Antioxidant Vitamins and Minerals on Structure and Function of Large Arteries Arterioscler. Thromb. Vasc. Biol., August 1, 2004; 24(8): 1485 - 1491. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 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]
|
|
|
|
|
|
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]
|
|
|
|
|
|
A. Cremonesi, R. Manetti, F. Setacci, C. Setacci, and F. Castriota Protected Carotid Stenting: Clinical Advantages and Complications of Embolic Protection Devices in 442 Consecutive Patients Stroke, August 1, 2003; 34(8): 1936 - 1941. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. Denzel, K. Balzer, K.-M. Muller, F. Fellner, C. Fellner, and W. Lang Relative Value of Normalized Sonographic In Vitro Analysis of Arteriosclerotic Plaques of Internal Carotid Artery Stroke, August 1, 2003; 34(8): 1901 - 1906. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 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]
|
|
|
|
 |
|
 J Isaksen, A Egge, K Waterloo, B Romner, and T Ingebrigtsen Risk factors for aneurysmal subarachnoid haemorrhage: the Tromso study J. Neurol. Neurosurg. Psychiatry, August 1, 2002; 73(2): 185 - 187. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 T. J. Tegos, K. J. Kalomiris, M. M. Sabetai, E. Kalodiki, and A. N. Nicolaides Significance of Sonographic Tissue and Surface Characteristics of Carotid Plaques AJNR Am. J. Neuroradiol., September 1, 2001; 22(8): 1605 - 1612. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
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]
|
|
|
|
 |
|
 M. Zureik, F. Kauffmann, P.-J. Touboul, D. Courbon, and P. Ducimetiere Association Between Peak Expiratory Flow and the Development of Carotid Atherosclerotic Plaques Arch Intern Med, July 9, 2001; 161(13): 1669 - 1676. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
E. B. Mathiesen, K. H. Bonaa, and O. Joakimsen Echolucent Plaques Are Associated With High Risk of Ischemic Cerebrovascular Events in Carotid Steno |