From the Department of Vascular Surgery, Rigshospitalet, (M.-L.M.G.),
Department of Clinical Biochemistry, Herlev Hospital (B.G.N.), Laboratory of
Neuropathology, Rigshospitalet (B.M.W.), and Department of Vascular Surgery,
Gentofte Hospital (H.S.), University Hospital of Copenhagen, Denmark, and the
Department of Information Technology, Technical University of Denmark
(J.E.W.).
Correspondence to Dr Marie-Louise Moes Grønholdt, Department of Vascular Surgery, RK 3112, Rigshospitalet, Blegdamsvej 9, DK-2100 Copenhagen Ø, Denmark. E-mail: mlg{at}rh.dk
Methods and Results—The study included 137 patients with
neurological symptoms and
Conclusions—Increased plasma levels of
triglyceride-rich lipoproteins predict echo-lucency of
carotid plaques, which is associated with increased plaque lipid
content. Because echo-lucency has been associated with a high incidence
of brain infarcts on CT scans, triglyceride-rich
lipoproteins may predict a plaque type particularly vulnerable to
rupture.
In a recent study, we demonstrated that elevated plasma levels of
triglyceride-rich lipoproteins in the fasting or
postprandial state were associated with echo-lucent carotid artery
plaques as evaluated subjectively by B-mode
ultrasonography.12 Weak reflection of ultrasound
from carotid atherosclerotic plaques, ie, echo-lucency, is also
associated with a higher histological content of
lipids,13 as well as with increased risk of
developing neurological symptoms.14 15 16 17 It is
therefore conceivable that elevated plasma levels of
triglyceride-rich lipoproteins may be associated with
atherosclerotic plaques, with lipid-rich cores particularly prone to
rupture and causing neurological symptoms, and that such plaques can be
diagnosed noninvasively and subjectively as echo-lucent plaques on
B-mode ultrasonography.
Recently, computerized assessment of plaque echogenicity (measured as
gray-scale level) has been introduced as a more quantitative and
objective method of ultrasonographic plaque
characterization.18 19 20 With this improved
method, a high fibrous tissue content was associated with a high
gray-scale value (echo-rich plaque), whereas a high lipid and
hemorrhage content was associated with a low gray scale value
(echo-lucent plaque).20 In addition, plaque
echo-lucency was associated with a higher incidence of brain infarcts
as assessed with CT scans.18 19
In this study, we tested the hypotheses that (1) elevated plasma levels
of triglyceride-rich lipoproteins in the fasting or
postprandial state predict echo-lucency of carotid atherosclerotic
plaques on computerized ultrasound B-mode imaging and (2) echo-lucency
predicts increased relative plaque lipid content.
Ultrasound Examination
At the beginning of each ultrasound examination, the gain setting was
set so that blood visually appeared black. To validate this
standardization approach, an area of blood was also outlined for each
patient on the B-mode ultrasound image, showing an average median
gray-scale value of 38.3±2.1 (mean±SD). The difference in gray-scale
level between the region of the atherosclerotic plaque and blood was
calculated for each patient, and this adjusted gray-scale value for the
atherosclerotic plaque was used to recalculate all the statistics
presented in "Results." Whether unadjusted or adjusted
gray-scale levels were used, the main results and conclusions were the
same. We therefore chose to show results based on unadjusted gray-scale
levels throughout this article. Ultrasound examinations including
generation of outlines were all performed by a single experienced
ultrasonographer (M.-L.M.G.) who was unaware of the fat tolerance test
values and histological examinations.
Fat Tolerance Test
Histological Examination
The total volume of each constituent in the removed plaque was
calculated as the sum of the area of the individual constituent in all
blocks multiplied by the mean distance in millimeters between each
section. The relative volume of each constituent was calculated as the
total volume of that constituent divided by the total volume of all
four constituents. The pathologist was unaware of values from the
ultrasound examination and fat tolerance test.
Reproducibility
Statistical Analysis
Qualitative Plaque Characteristics
When ANCOVA was performed, BMI, fasting IDL cholesterol,
and fasting plasma triglycerides were independent
predictors of gray-scale median values (Table 4
Relative plaque lipid content (39.8±1.7%; mean±SEM) was negatively
associated, and relative plaque fibrous tissue content (58.5±1.7%)
was positively associated with gray-scale median level (Table 5
Histology
Reproducibility
One important new observation in the present study is that elevated
plasma levels of triglyceride-rich lipoproteins in the
fasting or postprandial state predict echo-lucency (measured as a low
gray-scale level) of computerized ultrasound images of carotid
atherosclerotic plaques. This is in accordance with our previous
findings using subjective evaluation of plaque
echogenicity.12 Subjective evaluation of plaque
echogenicity was found in the present study to correlate well with
the objective computer-assisted evaluation, which had an intraobserver
coefficient of variation of 5.5%. Other previous studies found that
elevated plasma levels of triglyceride-rich lipoproteins in
the fasting or postprandial state (IDL, VLDL, chylomicron remnants, and
postprandial triglycerides) were predictors of the
presence, severity, progression, or familial risk of
atherosclerosis24 25 26 27 28 29 30 31 32 33 34 35 ; however,
none of these studies examined qualitative plaque characteristics as in
the present study.
Another important observation in the present study is that
echo-lucency of carotid atherosclerotic plaques was a predictor of
increased relative plaque lipid content within a subgroup of patients
undergoing carotid endarterectomy. This is in
accordance with findings in previous studies using either
subjective13 or objective20
computer-assisted evaluation of plaque echogenicity. A high gray-scale
value was associated with a high relative plaque fibrous tissue content
in the present study and in a previous
study.20
The present and former12 13 14 15 16 17 18 19 studies together
support the hypothesis that elevated plasma levels of
triglyceride-rich lipoproteins in the fasting or
postprandial state promote development of atherosclerotic plaques with
lipid-rich cores and that such plaques are particularly vulnerable to
rupture, thereby causing embolism and subsequent neurological symptoms
like stroke, transient ischemic attack, or amaurosis fugax.
Like LDL, triglyceride-rich lipoproteins can transfer from
plasma into the arterial intima,36 37
where such particles appear to be retained
selectively.37 38 In contrast to LDL, however,
triglyceride-rich lipoproteins without prior modification
can then be taken up directly by macrophages to produce
lipid-rich foam cells,39 a key cell type of the
atherosclerotic plaque.40
In our former study,12 indexes of elevated
VLDL/chylomicron remnant levels were primarily associated with
echo-lucency of carotid atherosclerotic plaques, whereas in this study,
elevated IDL cholesterol levels also were associated with
echo-lucency, ie, with a low gray-scale level. Both VLDL/chylomicron
remnant and IDL particles represent smaller
triglyceride-rich lipoproteins in plasma, and the
cholesterol contents of these two types of particles are
positively associated (data not shown). A likely explanation for the
small discrepancy between the two studies is the greater statistical
power of the present study, the inclusion of more patients (137
versus 85), and the use of a more objective measurement of plaque
echogenicity. In both studies, high BMI values were associated with
echo-lucency or low gray-scale values, and in this study, BMI was the
strongest independent predictor of low gray-scale levels. This
association could potentially also be explained by
triglyceride-rich lipoproteins because BMI is positively
associated with all indexes of triglyceride-rich
lipoproteins; however, the data cannot exclude that BMI, either by
itself or through yet another risk factor like low HDL
cholesterol levels associated with BMI, has an effect on
plaque echogenicity independent of triglyceride-rich
lipoproteins.
Interestingly, we found that triglyceride-rich lipoproteins
predicted the qualitative plaque characteristic of gray-scale level on
ultrasound B-mode images, whereas the most significant lipid predictors
of quantitative plaque characteristics like total plaque volume, total
plaque lipid, and total plaque fibrous tissue were LDL
cholesterol directly and HDL cholesterol
inversely. These associations between LDL and HDL
cholesterol and the extent of
atherosclerosis are well
recognized.1 2 41 The difference in predictors
between qualitative and quantitative plaque characteristics supports
the notion that triglyceride-rich lipoproteins in
particular are involved in the development of plaques with lipid-rich
cores, whereas LDL and HDL levels are important determinants of the
extent and severity of atherosclerosis. A reduction in
LDL cholesterol levels,5 6 7 increases
in HDL cholesterol levels,10 and a
reduction in levels of triglyceride-rich lipoproteins in
plasma9 10 11 all seem to be associated to some
extent with a reduced incidence of cardiovascular
events.
In conclusion, elevated plasma levels of triglyceride-rich
lipoproteins in the fasting or postprandial state appear to predict
echo-lucency of carotid atherosclerotic plaques, which is associated
with increased plaque lipid content and an increased incidence of brain
infarction on CT images. Triglyceride-rich lipoproteins may
therefore predict a plaque type particularly vulnerable to rupture and
thus leading to embolism and neurological symptoms. Computer-assisted
analysis of high-resolution B-mode ultrasound images may
improve the diagnoses of patients with particularly vulnerable plaques
and may in the future play an important role in the selection of
patients for carotid endarterectomy. Furthermore,
the present data might ultimately lead to strategies for
identifying patients who might benefit from specific lipid-lowering
therapies, ie, those with echo-lucent plaques, increasing the
cost-effectiveness of such therapy.
Received April 29, 1997;
revision received July 17, 1997;
accepted July 20, 1997.
© 1998 American Heart Association, Inc.
Clinical Investigation and Reports
Echo-Lucency of Computerized Ultrasound Images of Carotid Atherosclerotic Plaques Are Associated With Increased Levels of Triglyceride-Rich Lipoproteins as Well as Increased Plaque Lipid Content
Abstract
Top
Abstract
Introduction
Methods
Results
Discussion
References
Background—Echo-lucency of carotid
atherosclerotic plaques on computerized ultrasound B-mode images has
been associated with a high incidence of brain infarcts as evaluated on
CT scans. We tested the hypotheses that triglyceride-rich
lipoproteins in the fasting and postprandial state predict carotid
plaque echo-lucency and that echo-lucency predicts a high plaque
lipid content. 
50% stenosis of the relevant
carotid artery. High-resolution B-mode ultrasound images of carotid
plaques were computer processed to yield a measure of echogenicity
(gray-scale level). Lipoproteins were measured before and hourly for 4
hours after a standardized fatty meal. A subgroup of 58 patients
underwent endarterectomy. On linear regression
analysis, echo-lucency (low gray-scale level) was associated
with elevated levels of fasting and postprandial plasma
triglycerides (P=.0002 and
P=.002), IDL cholesterol
(P=.0009 and P=.006), and
VLDL/chylomicron remnant cholesterol
(P=.0003 and P=.0004) and
triglycerides (P=.0003 and
P=.003), the area under the plasma
triglyceride curve 0 to 4 hours after a fatty meal
(P=.001), and body mass index (P=.0001).
On ANCOVA, body mass index, fasting IDL cholesterol, and
fasting plasma triglycerides were independent predictors of
echo-lucency. Echo-lucency was associated with increased relative
plaque lipid content (P=.02).
Key Words: arteriosclerosis • carotid arteries • ultrasonics • lipoproteins • pathology
Introduction
Top
Abstract
Introduction
Methods
Results
Discussion
References
Low density
lipoprotein cholesterol is causally related to the
development of
atherosclerosis,1 2 and a
reduction in LDL levels leads to reduced progression of
atherosclerosis,3 4 reduced
incidence of myocardial infarction5 6 7 and
stroke,5 7 and even reduced total
mortality.5 6 The role of
triglyceride-rich lipoproteins is much less clear.
Nevertheless, elevated plasma triglyceride levels have
repeatedly been associated with an increased incidence of myocardial
infarction,8 and three intervention trials have
provided some evidence that a reduction in
triglyceride-rich lipoproteins is associated with a
reduction in the progression of coronary
atherosclerosis9 and the
incidence of coronary events.9 10 11
Methods
Top
Abstract
Introduction
Methods
Results
Discussion
References
Subjects
Consecutive symptomatic patients (96 men and 41
women; median age, 64 years) were enrolled. Symptoms were stroke (n=77
or 56%), transient ischemic attack (n=45 or 33%), or
amaurosis fugax (n=15 or 11%). Criteria for entry into the study were
a degree of carotid stenosis of 50% on the
symptomatic side, no use of lipid-lowering medications, and
a willingness to perform the fat tolerance test. Fifty-eight of these
patients underwent carotid endarterectomy. Patients
performed the fat tolerance test either 3 months after inclusion or 3
months after carotid endarterectomy. Collection of
basic characteristics has been described
previously.12 The study was approved by the
medical ethics committee for Copenhagen and Frederiksberg counties (No.
KF 01- 062/94), and all patients gave informed consent.
All patients had their carotid artery on the
symptomatic site ultrasound scanned with an Interspec RX
400 with a 5- to 10-MHz linear array transducer. Degree of
stenosis was determined by routine Doppler
criteria.12 Furthermore, high-resolution B-mode
and color Doppler images of the plaque from the anterior, lateral,
and cross-sectional scan plane were evaluated on-line by use of the
criteria of the European Multicenter Study on Plaque Morphology:
echogenicity was evaluated as either echo-rich, intermediate, or
echo-lucent.12 13 In addition,
representative images were captured from a videotape of
the ultrasound examination and digitized with a Targa 2000-E
framegrabber (20 MB PAL, Truevision Inc). The B-mode and corresponding
color Doppler images were processed with the software program
Image-Pro Plus, version 1.2.01 for Windows (Media Cybernetics); the
carotid artery plaque was outlined and the gray-scale value of each
pixel in the region was used to generate a median gray scale value (see
the Figure 1
); in case of acoustic
shadowing from a plaque, the outline did not include this shadow
region. In the histogram in the Figure, the number of pixels with a
given gray-scale value in the outlined region is plotted against the
gray-scale level (0 to 255; 0=black and 255=white).
View larger version (49K):
[in a new window]
Figure 1. Ultrasound B-mode image of a carotid artery plaque. Outline
(excluding the acoustic shadowing) shows the plaque area where
gray-scale levels of all pixels are used to construct the histogram
showing distribution of gray-scale level among pixels. Median of the
gray-scale level is used for further analysis.
After a 12-hour overnight fast, all patients were given a fatty
meal consisting of 1 g dairy cream fat per 1 kg body weight.
Plasma lipids and lipoproteins were measured before and at hourly
intervals for 4 hours after the fatty meal, as described
elsewhere.12 The magnitude of postprandial
triglyceridemia and cholesterolemia was
calculated as the area under the plasma cholesterol
(AUCC, AUCC-C 0h) and
triglyceride (AUCTG,
AUCTG-TG 0h) curves 0 to 4 hours after a fatty
meal.12
In 58 patients, the carotid artery plaques were removed in toto
during endarterectomy. After the external carotid
artery was discarded, the remaining plaque was cut transversely into
3-mm-thick blocks (4 to 14 per patient). Consecutive sections from each
block were stained with hematoxylin and eosin, Van Gieson's, and
Verhoeff's stain, respectively. Plaque constituents (lipid,
hemorrhage, calcification, thrombus, and fibrous tissue) in all
sections were measured morphometrically by a single experienced
pathologist (B.M.W.) using a Leitz Texture Analyzing System (TAS).
The same ultrasonographer (M.-L.M.G.) reexamined 58
consecutively chosen images; new outlines of carotid artery plaques
were created to obtain new gray-scale values, with the ultrasonographer
unaware of the first outlines of the plaques performed 3 to 6 months
earlier. Likewise, the pathologist (B.M.W.) reexamined 10 randomly
chosen plaques morphometrically, without knowledge of the values from
the first examination. The reproducibility of plasma lipid and
lipoprotein measurement during a fat tolerance test seems to be as good
as those for fasting levels.21
Student's t test, ANOVA, 
2
test, univariate linear regression, and ANCOVA (forward
stepwise method) were performed with the Statistica
program.22 Predictors significant
(P
.05) on univariate linear regression
analysis or on the t test entered the ANCOVA. To
approach normal distribution, medians of gray-scale values; plaque
volumes; lipoprotein(a); triglycerides in plasma, IDL, and
VLDL; cholesterol in IDL and VLDL; and
AUCTG and AUCTG-TG 0h were
all transformed logarithmically before statistical tests.
Reproducibility was tested with the method of Bland and
Altman,23 in which the difference between two
repeated measurements was plotted against the mean of the same two
measurements to calculate a mean bias with 95% confidence interval. A
coefficient of variation based on duplicate measurements was also
calculated. A probability value of P.05 on two-sided tests
was considered statistically significant.
Results
Top
Abstract
Introduction
Methods
Results
Discussion
References
There were no major differences in the characteristics of the 137
symptomatic patients with 50% stenosis of the
relevant carotid artery compared with the subgroup of 58 patients who
had their carotid plaque removed by endarterectomy
(Tables 1 and 2). The average degree of
stenosis in the total group of patients and in the
endarerectomy subgroup was 81%±2% and 71%±2% (mean±SEM),
respectively.
View this table:
[in a new window]
Table 1. Characteristics of Patients With Carotid Artery
Plaques
View this table:
[in a new window]
Table 2. Age, BMI, and Biochemical Characteristics of
Patients With Carotid Artery Plaques
Gray-Scale Median
The gray-scale level of carotid atherosclerotic plaques was
negatively associated with fasting and postprandial levels of plasma
triglycerides, IDL cholesterol,
VLDL/chylomicron remnant cholesterol and
triglycerides, the area under the plasma
triglyceride curve 0 to 4 hours after a fatty meal, and
body mass index (BMI) (Table 3). BMI was
positively associated with most characteristics of
triglyceride-rich lipoproteins and negatively associated
with HDL cholesterol (data not shown).
View this table:
[in a new window]
Table 3. Univariate Linear Regression
Analysis of Age, BMI, and Biochemical Characteristics as
Predictors of Ultrasonic Gray-Scale Median, Total Plaque Volume, Total
Plaque Lipid, and Total Plaque Fibrous Tissue of Carotid Artery Plaques ). If
this analysis was based on gray-scale level adjusted for
gray-scale level of blood (see "Methods"), the independent
predictors of plaque gray-scale values were fasting plasma
triglycerides (P=.0004) and fasting IDL
cholesterol (P=.02).
View this table:
[in a new window]
Table 4. Ranking by ANCOVA of Independent Predictors of
Gray-Scale Median, Total Plaque Volume, and Total Plaque Lipid and
Fibrous Tissue of Carotid Artery Plaques ). Relative plaque content of calcification
(1.2±0.2%) or hemorrhage (0.5±0.1%) was not associated with
gray-scale median level (data not shown). Subjective evaluation of
plaque echogenicity (echo-lucent versus intermediate versus echo-rich)
was associated with computer-assisted measurement of gray scale median
values (Table 5); echo-lucency of the plaque was associated with low
gray-scale medians.
View this table:
[in a new window]
Table 5. Comparison of the Objective Computer-Assisted
Measurement of Gray-Scale Median With Relative Lipid and Fibrous Tissue
in Plaques Measured Histomorphometrically as Well as With the
Subjective Evaluation of Plaque Echogenicity
On univariate linear regression analysis,
total plaque volume, total plaque lipid, and total plaque fibrous
tissue were directly related to age, BMI, and fasting and postprandial
LDL cholesterol, whereas they were inversely related to
fasting and postprandial levels of HDL cholesterol (Table 3
). Of the characteristics shown in Table 1, sex alone predicted total
plaque volume (Student's t test, P=.00005) and
total plaque lipid (P=.000003). Sex and diabetes mellitus
both predicted total plaque fibrous tissue (P=.000001 and
P=.01). On ANCOVA, sex, BMI and fibrinogen were independent
predictors of total plaque volume; sex and fasting LDL
cholesterol were independent predictors of total plaque
lipid; and sex, BMI, and fasting LDL cholesterol were
independent predictors of total plaque fibrous tissue (Table 4).
When 58 computerized digital images had carotid plaque outlines
redrawn to recalculate gray-scale median levels, the mean bias between
the two independent determinations of gray-scale median values was
-0.4 (95% confidence interval [CI], -1.5 to 0.1). Likewise, the
mean bias for a repeated measurement (n=10) of relative plaque lipid
and fibrous tissue content was 0.6% (95% CI, -1.5% to 2.6%) and
1.1% (95% CI, -0.8% to +3.1%), respectively. The coefficients of
variation for these three measurements based on the repeated
analysis were 5.5%, 3.5%, and 2.2%, respectively.
Discussion
Top
Abstract
Introduction
Methods
Results
Discussion
References
Echo-lucency on subjective evaluation and a low gray-scale value
(echo-lucency) on objective computer-assisted evaluation of carotid
atherosclerotic plaques have previously been associated with an
increased incidence of neurological
symptoms14 15 16 17 and an increased incidence of
nonsymptomatic brain infarction on CT
scans,18 19 respectively.
Acknowledgments
This study was supported by the Danish Medical and Technical
Research Council. We appreciate the technical assistance of Hanne Damm,
Anne Merete Bengtsen, Ann Meisler, and Birgitte Søe Hansen.
References
Top
Abstract
Introduction
Methods
Results
Discussion
References
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T. J. Tegos, M. Sohail, M. M. Sabetai, P. Robless, N. Akbar, G. Pare, G. Stansby, and A. N. Nicolaides Echomorphologic and Histopathologic Characteristics of Unstable Carotid Plaques AJNR Am. J. Neuroradiol., November 1, 2000; 21(10): 1937 - 1944. [Abstract] [Full Text] [PDF]
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J. J. P. Kastelein, J. W. Jukema, A. H. Zwinderman, S. Clee, A. J. van Boven, H. Jansen, T. J. Rabelink, R. J. G. Peters, K. I. Lie, G. Liu, et al. Lipoprotein Lipase Activity Is Associated With Severity of Angina Pectoris Circulation, October 3, 2000; 102(14): 1629 - 1633. [Abstract] [Full Text] [PDF]
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M.M. Sabetai, T.J. Tegos, A.N. Nicolaides, S. Dhanjil, G.J. Pare, and J.M. Stevens Reproducibility of Computer-Quantified Carotid Plaque Echogenicity : Can We Overcome the Subjectivity? Stroke, September 1, 2000; 31(9): 2189 - 2196. [Abstract] [Full Text] [PDF]
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S. Takiuchi, H. Rakugi, K. Honda, T. Masuyama, N. Hirata, H. Ito, K. Sugimoto, Y. Yanagitani, K. Moriguchi, A. Okamura, et al. Quantitative Ultrasonic Tissue Characterization Can Identify High-Risk Atherosclerotic Alteration in Human Carotid Arteries Circulation, August 15, 2000; 102(7): 766 - 770. [Abstract] [Full Text] [PDF]
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