(Stroke. 2000;31:2426.)
© 2000 American Heart Association, Inc.
Original Contributions |
Carotid Artery Intima-Media Thickness Measured by Ultrasonography in Normal Clinical Practice Correlates Well With Atherosclerosis Risk Factors
From the E. Grossi Paoletti Center, Institute of Pharmacological Sciences, University of Milan (Italy).
Correspondence to Professor E. Tremoli, Institute of Pharmacological Sciences, Via Balzaretti 9, 20129 Milan, Italy. E-mail damiano.baldassarre{at}unimi.it
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Abstract |
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Background and Purpose—The intima-media thickness (IMT) of extracranial carotid arteries determined by B-mode ultrasound is a measurable index of the presence of atherosclerosis. The ultrasonographic scan protocol and the scan reading techniques used until now to measure IMT are, however, time consuming and require the participation of specialized research centers. In this study we present a cross-sectional study of 963 patients attending the Enrica Grossi Paoletti Center in Milan, Italy, with the aim of assessing whether ultrasonographic measurements of carotid artery in routine clinical practice can yield the same results as those obtained with quantitative methods used until now in clinical trials.
Methods—Maximum and mean maximum IMT of carotid arteries were assessed by B-mode ultrasound with the use of the electronic caliper of the machine in real time.
Results—The intraobserver and interobserver variability of IMT of carotid arteries performed with the electronic caliper in real time was similar to that of quantitative processing of frozen images (coefficients of variation of intraobserver and interobserver mean maximum IMT measurements were 4.2% and 7.3%, respectively). Carotid artery IMT thus measured correlated with most of the known atherosclerosis risk factors and discriminated between patients with and without previous history of cardiovascular events. IMT was linearly related to the total number of vascular risk factors both in the whole group and after stratification of patients into 3 age classes.
Conclusions—–These observations establish a strong correlation between B-mode imaging of carotid atherosclerosis evaluated in normal clinical practice and data provided by clinical trials and validate this simple reading technique as a means of identifying IMT as another possible risk factor in patients at high risk of vascular disease.
Key Words: intima-media thickness • risk factors • ultrasonics
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Introduction |
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The intima-media thickness (IMT) of extracranial carotid arteries provides an index of atherosclerosis in other vascular regions1 2 3 4 5 and has been shown to be associated with most risk factors for atherosclerosis.6 7 8 Recently, an increased thickness of carotid IMT determined by B-mode ultrasound has been shown to be directly associated with an increased risk of myocardial infarction and stroke in older adults without a previous history of cardiovascular disease.9 Thus, carotid artery IMT has been proposed as a risk factor that may be included in the algorithms for cardiovascular risk assessment.9 However, the ultrasonographic scan protocol and the scan reading techniques used until now are time consuming and require the participation of highly specialized research centers. Large-scale epidemiological studies testing the connection between conventional or unconventional risk factors and carotid atherosclerosis would become more feasible if simpler methods were available to measure carotid IMT, possibly during normal clinical practice. Some authors, to shorten the time for image processing, have limited the number of carotid segments to a single sector, eg, the first centimeter of the common carotid. This approach, however, may result in a loss of information and patient misclassification.
We have investigated whether carotid IMT, measured with an electronic caliper, a method feasible in routine clinical practice, provides suitable information to associate carotid IMT with a patient’s risk profile.
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Subjects and Methods |
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Nine hundred sixty-three consecutive patients (487 men and 476 women) attending for the first time the Ultrasound Laboratory of the E. Grossi Paoletti Center for metabolic studies (Niguarda Hospital, Milan, Italy) were analyzed by carotid B-mode ultrasound imaging. The carotid IMT10 was determined manually in real time. Clinical and laboratory parameters were simultaneously assessed. Oral informed consent was obtained from all patients; the study was approved by the Institutional Review Board.
Patients were on a low-fat diet (26% lipids, 22% proteins, 52% carbohydrates; polyunsaturated/saturated fat ratio 0.43) for at least 3 months. Six hundred sixty-eight patients were hyperlipidemic (443 type IIa, 164 type IIb, 2 type III, 55 type IV, and 4 type V) according to World Health Organization criteria11 ; 245 were borderline hyperlipidemic (plasma LDL cholesterol, 4.14 to 4.92 mmol/L; triglycerides, 1.70 to 2.05 mmol/L), and 50 had normal lipid levels. Three hundred three patients (31.5%) were hypertensive (systolic or diastolic blood pressure >160 mm Hg and >90 mm Hg, respectively, or under treatment with hypotensive drugs). Fifty-eight patients (6%) were diabetic and on oral hypoglycemic therapy. One hundred thirty-nine patients (14.4%) had a previous history of coronary heart disease (CHD), 93 (9.7%) of cerebrovascular disease (CVD), and 150 (15.6%) of peripheral arterial disease (PAD). Eighty-two patients had xanthomas, 48 xanthelasmas, and 146 a corneal arcus. Most of the patients had a family history of ischemic vascular disease: 43.6% for CHD, 27.6% for CVD, and 6.4% for PAD. More than a third of the patients were being treated with hypolipidemic drugs (statins, resins, probucol, or fibrates); 25% with hypotensive drugs (ß-blockers, calcium antagonists, angiotensin-converting enzyme inhibitors, or diuretics); 20% with antiplatelet drugs; 5.7% with oral anticoagulants; 6% with hypoglycemic drugs (insulin or metformin); and <2% with uricosuric drugs or with hormonal replacement therapy. Two hundred seventeen patients were current smokers (186 hypercholesterolemic, 31 normocholesterolemic), and 274 were previous smokers (at least 1 year after smoking cessation).
To investigate the relationship between the number of vascular risk factors and carotid atherosclerosis, we classified each patient according to the presence of single or multiple vascular risk factors, arbitrarily assigning to each risk factor an equal weight. Patients were considered to be exposed to a risk factor when 1 of the following criteria was satisfied: male sex or at least 5 years after menopause for women; age >55 years; LDL cholesterol >4.14 mmol/L; triglycerides >2.28 mmol/L; HDL cholesterol <0.91 or <1.04 mmol/L in men and women, respectively; hypertension; diabetes; smoking habit; or family history of cardiovascular disease. In addition, patients with diabetes (cases; n=58) were compared with 116 patients (controls) matched for age, sex, and total cholesterol levels. The same case-control protocol was applied to patients with hypertension, CHD (angina, myocardial infarction), CVD (stroke, transient ischemic attack), or PAD.
Lipids
Blood samples were collected from the antecubital vein after
overnight fasting. Total and HDL cholesterol and
triglyceride levels were determined in fresh serum by
enzymatic methods12 13 ; HDL levels were obtained by
selective precipitation with
dextran-MgCl2.14 Serum LDL
cholesterol levels were calculated by Friedewald’s
formula.15
Ultrasound Protocol
Ultrasound examination was performed with the use of an 8-MHz
annular array ultrasound imaging system (2000 II s.a., Biosound)
by a single trained sonographer. With this technique, 2 parallel
echogenic lines separated by an anechoic space can be visualized at
levels of the artery wall. It was previously shown that these lines
were generated by the blood-intima and media-adventitia
interfaces.10 The distance between the 2 lines gives a
reliable index of the thickness of the intimal-medial
complex.10 Subjects were examined in the supine position.
Ultrasound scans of the right and left last distal centimeter of common
carotid arteries and bifurcation and of the first proximal centimeter
of internal carotid arteries in 3 different projections (anterior,
lateral, and posterior) were performed. All measurements were made at
the time of scanning on unfrozen images of longitudinal scans by using
the machine’s electronic caliper. Six carotid segments for each
projection (near and far walls of bulb and internal and common
carotid arteries) were examined. The maximal IMT value of each segment
was measured. The complete procedure is generally performed in
approximately 30 to 35 minutes. IMT values for the 3 different
projections and for right and left carotid arteries were averaged
to obtain the mean maximum IMT (MM-IMT). A total of 11 566 carotid
segments were imaged, and there were 544 instances of missing data
(4.7%). The analysis presented in this report provides
substantially identical results when patients with missing data are
either considered or excluded. In addition, a pilot study was performed
in a random sample of 100 patients of the overall study group. The mean
MM-IMT of these subjects did not significantly differ from that
calculated after a random deletion of the 5% of observations. Thus, in
the MM-IMT assessment, values are presented that include
patients with missing data. The highest IMT value found among the 36
segments was defined as the maximal IMT (Max-IMT). For the assessment
of interobserver and intraobserver variability of carotid measurements,
20 patients of the study group underwent 2 carotid ultrasound
investigations 2 weeks apart. Ultrasound investigation was performed
twice at each visit by 2 trained sonographers.
Statistical Analysis
Mean±SD values were used as descriptive measures of normally
distributed variables. Because of the highly skewed distribution of
triglycerides, these values were log transformed, which
yielded an almost gaussian distribution. Groups were compared by
ANCOVA. Differences in categorical variables were analyzed
by the 
2 test. Correlation was
analyzed by the nonparametric Spearman method.
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Results |
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Table 1
shows the intraobserver and
interobserver variability of IMT of carotid arteries performed with the
electronic caliper in real time. The reproducibility was similar to
that of quantitative processing of frozen images.16 In
particular, coefficients of variation of intraobserver and
interobserver MM-IMT measurements were 4.2% and 7.3%,
respectively.
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Table 2 shows the characteristics of the
population studied. Men in the group were younger than women, had the
greatest body mass index (BMI), and presented the greatest
percentage of smokers. They had, however, lower values of total, LDL,
and HDL cholesterol and higher values of
triglycerides and blood glucose than the women. MM-IMT and
Max-IMT values were greater in men than in women. Carotid IMT values
correlated highly with age in the total population (r=0.43
and r=0.46 for Max-IMT and MM-IMT, respectively;
P<0.0001).
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The relationship of carotid IMT to the different variables was then
evaluated after adjustment for age. Carotid IMT significantly and
positively correlated with systolic blood pressure, total
cholesterol, LDL cholesterol,
triglycerides, and blood glucose and negatively with HDL
cholesterol (Table 3).
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The Figure shows that
MM-IMT and Max-IMT values increased with the number of risk factors,
with the greatest IMT occurring in patients with >4 risk factors
(P<0.003 and P<0.015 for MM-IMT and Max-IMT,
respectively). The relationship between carotid IMT and the number of
risk factors was also observed after stratification of patients into 3
age groups (data not shown).
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Case-control analysis (Table 4) showed that hypertensive
patients had greater IMT. They also differed from the corresponding
controls in BMI, triglycerides, and blood glucose. In
diabetic patients, by contrast, no significant difference in carotid
parameters was found, despite the presence of higher BMI,
higher serum triglycerides, and lower levels of HDL
cholesterol.
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Table 5 shows that patients with
CHD and patients with PAD had greater values of MM-IMT and Max-IMT than
corresponding controls, whereas no difference in MM-IMT and Max-IMT was
found between patients with CVD and controls.
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Discussion |
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These data demonstrate that IMT measured by a simple method for image processing, which can be performed directly during scanning of the carotid arteries, can provide a reliable index of carotid atherosclerosis. In a population of 963 patients attending a lipid clinic, IMT values of carotid arteries determined in real time with the electronic caliper (1) correlated with most atherosclerosis risk factors, (2) were associated with the number of atherosclerosis risk factors, and (3) discriminated between patients with and without previous history of cardiovascular events. The precision of the method (approximately 0.1 mm) is lower than that of more sophisticated quantitative methods (0.02 to 0.06 mm),16 but our data suggest that this does not represent a real limitation when an adequate patient sample is used.
In agreement with previous reports, we found statistically significant differences between men and women in carotid IMT.4 8 17 The correlation coefficients between Max-IMT or MM-IMT and age (r=0.43 and r=0.46, respectively) were similar to the mean value of correlation coefficients reported by 5 studies (r=0.48).18 19 20 21 22
Direct and significant correlations between carotid IMT and systolic blood pressure, total cholesterol (age-adjusted Max-IMT only), LDL cholesterol, triglycerides, blood glucose (age-adjusted Max-IMT only), and HDL cholesterol (inversely) were found, all in accordance with previously reported findings.20 23 24 Again in accordance with previous findings,20 24 25 26 IMT was greater in hypertensive patients. On the contrary, no difference was found between diabetic and nondiabetic patients; the high prevalence of these patients with hypercholesterolemia may have masked the effect of diabetes on carotid IMT.27 28
Results of the British Regional Heart Study6 suggest that the presence of plaque, but not IMT, is associated with high risk of disease. In our study Max-IMT but also MM-IMT allowed us to identify groups of patients with previous cardiovascular events, ie, CHD or PAD. We suggest that MM-IMT and/or Max-IMT may represent comprehensive indices of atherosclerosis and that, when a normogram in different types of patients has been defined, they will help clinicians to identify groups of patients likely to benefit from aggressive preventive measures.
Carotid IMT increased with the number of concurrent risk factors, even after stratification of patients for age, a further indication that MM-IMT and Max-IMT may represent comprehensive indices of carotid and even more widespread atherosclerosis.
The data discussed in this report strongly suggest that measurement of IMT with the electronic caliper is a method feasible in routine clinical practice and provides suitable information to associate carotid IMT with the risk profile of different groups of patients. By the use of this simple methodology, as a result of the reduction in time and costs, it is possible to extend the analysis of arterial wall thickness to the whole carotid tree, instead of selecting a single segment. However, to perform such studies properly, the following aspects should be carefully taken into account. First, the training of sonographers/readers for each study should be considered, and changes over time in sonographer/reader behavior should also be taken into account. Moreover, in studies involving different sonographers, interobserver variability should be carefully determined. Finally, in longitudinal and/or pharmacological studies, the use of this technique should not be allowed until appropriate validation is performed.
In conclusion, we have shown that measurement of the IMT of carotid arteries with an electronic caliper is a rapid, low-cost method that provides information similar to that obtained by more precise methods. This approach should prove useful in large clinical and/or epidemiological trials in which the evaluation of arterial wall morphological targets using more sophisticated methods for IMT measurement is not practical because of cost and time constraints.
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Footnotes |
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Reprint requests to Dr Damiano Baldassarre, E. Grossi Paoletti Center (Padiglione Vergani), Ospedale Niguarda "Ca’ Granda," Piazza Ospedale Maggiore 3, 20162 Milan, Italy.
Received January 27, 2000; revision received June 22, 2000; accepted June 23, 2000.
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