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(Stroke. 1997;28:665-671.)
© 1997 American Heart Association, Inc.

Articles

Reproducibility of In Vivo Carotid Intima-Media Thickness Measurements

A Review

Suzan D.J.M. Kanters, MD; Ale Algra, MD, PhD; Maarten S. van Leeuwen, MD, PhD; Jan-Dirk Banga, MD, PhD

From the Departments of Internal Medicine (S.D.J.M.K., J.-D.B), Clinical Epidemiology (A.A.), and Radiology (M.S. van L.), University Hospital Utrecht, The Netherlands.

Correspondence to Jan-Dirk Banga, MD, PhD, Department of Internal Medicine, University Hospital Utrecht, Heidelberglaan 100, PB 85500, 3508 GA Utrecht, Netherlands. E-mail a.algra{at}neuro.azu.nl.

	Abstract

Top Abstract Introduction Image Acquisition Image Analysis Reproducibility Data Discussion References

 
Background The early phase of atherosclerosis can be studied by two-dimensional B-mode ultrasonography. Measurements of the combined thickness of the carotid intima and media are currently used as intermediate outcome in clinical trials. Comparison of results between studies is difficult because of the different methods of image acquisition and analysis used. We review these methods and the reported reproducibility of intima-media thickness (IMT) measurements.

Summary of Review Articles were collected using the MEDLINE literature search system and the references in the selected articles. Literature concerning human in vivo IMT measurements published in the English language in the period 1991 through 1995 was reviewed. A description of the methods of measuring IMT to determine intraobserver and/or interobserver variability was a prerequisite for inclusion. Twenty-three studies were included. Best reproducibility was found when measuring the mean IMT in the common carotid artery in more than one direction.

Conclusions We conclude that a consensus concerning the assessment of IMT is urgently needed. Variability of IMT measurements is lowest when determining the mean thickness in the common carotid artery in different directions.

Key Words: carotid arteries • observer variation • ultrasonics

	Introduction

Top Abstract Introduction Image Acquisition Image Analysis Reproducibility Data Discussion References

 
The first clinical manifestations of cardiovascular disease often arise in a stage of well-advanced atherosclerosis. Arterial vessel wall changes occur during a presumably long subclinical lag phase of endothelial damage and gradual diffuse thickening of the intima. The early phase can be studied by two-dimensional B-mode ultrasonography. This technique yields information on atherosclerotic wall changes that cannot be obtained by conventional contrast angiography or MRI.¹ Its noninvasive character and easy applicability make B-mode ultrasonography a powerful tool for measurement of the atherosclerotic burden.

With use of B-mode ultrasonography, several layers of the vessel wall in several locations of the body can be studied. The measurement of the combined thickness of the intima and media, the intima-media complex, is widely applied. The carotid arteries are most suitable for study because of their superficial localization, size, and limited movement.

In a two-dimensional image of the carotid artery, the anterior wall, the lumen, and the posterior wall can be distinguished. Both walls present as an echogenic, an echo-poor, and an echogenic zone. The upper demarcation line of the echogenic zone ("leading edge") corresponds to an anatomic transition zone that gives rise to an echo, and the location of this is not gain dependent.² Conversely, the lower demarcation line of the echogenic zone ("far edge") is defined by the gain setting of the recording system and does not correspond to an anatomic boundary. Therefore, to assess IMT, the use of the upper demarcation lines of echogenic zones is strongly recommended. This is the "leading edge" principle. In the posterior wall, the interface between blood and intima gives rise to the leading edge of the first echogenic zone. The leading edge of the second echogenic zone in this wall very likely corresponds to the media-adventitia interface. For combined IMT measurement in the far wall, there is agreement between histology and sonography.³ On the basis of leading edge measurements, the near wall is underestimated relative to histopathology.³ The adventitia is normally quite echogenic in contrast to the media. Therefore, in the near wall any potential echo from the adventitia-media interface is lost in the echo produced by the lower parts of the adventitia.

Median population values of IMT range between 0.4 and 1.0 mm, while progression rates of 0.01 to 0.3 mm/y have been reported.^{4 5 6 7 8 9} Increased common carotid IMT is associated with several cardiovascular risk factors, including age, male sex, diabetes, total cholesterol, and smoking. There is also an association with the prevalence of angina pectoris, myocardial infarction, aortic aneurysm, and lower extremity arterial disease.¹⁰ Therefore, IMT measurements are currently used as intermediate outcome in clinical trials on atherosclerosis. Comparison of results among studies is difficult because of the different methods of image acquisition and analysis used. A consensus concerning the method of measuring is urgently needed, as was concluded during the First International Symposium devoted to arterial wall thickening that was held in Paris in July 1995.

In this article, we review the reported reproducibility of IMT measurements. The intraobserver and interobserver variability of different measuring methods is described. Articles reviewed in this study were collected using the MEDLINE literature search system. In addition, the references in the selected articles were used. Literature published in the English language concerning human in vivo IMT measurements was reviewed. Because we wanted to evaluate studies applying recent technology only, we restricted our analysis to articles published from 1991 to and including 1995. A description of the methods of measuring IMT to determine intraobserver and/or interobserver variability was a prerequisite for inclusion.

	Image Acquisition

Top Abstract Introduction Image Acquisition Image Analysis Reproducibility Data Discussion References

 
The intraobserver and interobserver variabilities of IMT measurements reported in the 23 studies retrieved from the literature^{11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35} are summarized in Table 1. In addition, a short description is given of the method used to measure IMT.

View this table: [in this window] [in a new window]   Table 1. Survey of Intraobserver and Interobserver Variability of IMT Measurements

Various scanning procedures were used. Most investigators determined the IMT of the far wall only, whereas others combined its measurement with that of the near wall^{16 17 32} or even calculated a mean of both measurements.^{19 25} In the near-wall sonographic measurement, IMT is 80% of the histological thickness.³ A difference of 0.02 mm was found between near- and far-wall measurements when pooled data from three studies (n=1947) were analyzed.⁵ The IMT measured in the near wall is in part dependent on gain setting. When gain settings are standardized, the error is systematic and will not bias associations. Associations of IMT with coronary artery disease were no stronger when information from only the far wall was used, and measurement variability of data from the far wall exceeded that of the near plus far wall.³⁶ No difference was found in rates of progression between both walls.⁵ Moreover, reduced variability of progression has been reported when near-wall measurements are included in the estimation of disease extent.⁵ Thus, combined measurements of near and far wall might enhance precision without loss of validity. When reporting absolute IMT, results from both walls should be shown separately to allow the reader his or her own interpretation.^{8 10}

The CCA was examined in most studies. The ICA and the bulbus were studied less frequently.^{13 16 17 18 19 26 34} The distal end of the CCA was usually defined as the beginning of the dilatation of the carotid bulb, with loss of the parallel configuration of the near and far walls of the CCA (see the Figure). The ICA was defined as the segment beyond the tip of the flow divider. Good-quality scans of the CCA can be achieved in nearly every patient, in contrast with those of the ICA and the carotid bulb.³⁷ The CCA is easier to image because it is relatively close and parallel to the skin surface. The ICA is especially difficult to visualize. When measuring in the ICA and the carotid bulb, there are many missing images, and intraobserver and interobserver variabilities are large. In the Asymptomatic Carotid Artery Progression Study (ACAPS), the walls from the CCA segments were visualized 99% of the time, and those of the bifurcation and ICA segments 88% and 67% of the time, respectively.³⁸ However, atherosclerotic lesions appear later in the CCA than in the ICA or at the bifurcation.³⁹ Inclusion of measurements made in the ICA did not attenuate the clinical relevance of the association between IMT and coronary artery disease.³⁶ The mean IMT for 12 measurement sites (CCA, bifurcation, ICA, near and far walls, and left and right sides) was found to be more strongly associated with coronary atherosclerosis than the IMT from individual segments.³⁶ The ability to accurately predict wall thickness at a site, given the wall thickness at other sites, is modest.⁴⁰ Among the different sites, Howard et al⁴⁰ found the highest associations between the contralateral CCA sites and between the adjacent ipsilateral bifurcation and ICA sites. With increasing IMT at one site, IMT at other sites became less predictable.

View larger version (57K): [in this window] [in a new window]   Figure 1. Schematic representation of the CCA, the bifurcation, the ICA, and the external carotid artery.

Ultrasound scanning was performed in more than one direction (anterolateral/lateral/posterolateral) in 50% of the included studies. Measuring in more directions will give a better impression of reality in case of wall-thickness eccentricity. Variability of IMT values of specific carotid sectors (eg, anterior) were compared with the variability of the mean of all directions. The percentage of intraoperator and interoperator errors rose from 2.5% to 11.6% and 5.9% to 15.0%, respectively, when directions were taken separately.²⁷

Both carotid arteries were examined in 16 studies, the right carotid artery in four studies. In four studies, the side of measurement was not mentioned. No systematic differences in IMT between the left and the right CCA could be found.^{5 10}

Plaque thickness was usually included in the measurement of IMT. However, sometimes plaques were not measured at all³⁰ or were analyzed separately.¹⁸ Touboul et al²⁰ restricted wall recordings to arterial segments where the lumen-intima interface was regular and parallel to the adventitia. If a plaque is located at the site of IMT measurement, the plaque thickness should be included in the IMT value.⁸ There is no clear definition of plaque, so exclusion or separate analysis of plaques will give results that cannot be compared with other studies.

External reference points were used in one study to improve the repeated identification of the CCA sector in subsequent determinations.²⁷ With this method, external references projected on the neck by a slide projector were used to place the probe. In another study, carotid arteries were investigated using either a standard procedure or recorded information from the earlier investigation to direct a comparable ultrasound beam with special computer software.²⁰ Mask construction during the second procedure consisted of recording the anatomic situation of the investigated area, the scanning direction (longitudinal or transverse, lateral or posterior), the position of the head (30° or 60° toward the right or left), and the inclination of the ultrasound bundle in relation to the neck axis. Image and mask archiving was performed separately on an optical disk. During a second investigation, the real-time echographic image and the fixed contours recorded during the first investigation were superimposed on the screen.

	Image Analysis

Top Abstract Introduction Image Acquisition Image Analysis Reproducibility Data Discussion References

 
Measuring procedures differed among the studies. IMT was usually determined by visual assessment of the leading edges by the ultrasonographer. However, some investigators used an automated computerized edge-tracking method.^{23 25 35} After visual determination of an approximate echo boundary, an automated search was made along paths perpendicular to this curve. The computer searched for the points at which the rate of pixel-intensity change was maximal. These points were conditionally labeled as edges until they were converted to true edges or discarded. The third step in the process was to compare the gradient value for each conditional edge with the maximum gradient value of all conditional edges of the boundary. Points with gradient values less than the preselected fraction of the maximum value were eliminated. Variability may be minimized by replacing manual edge tracking by an automated edge-tracking method. Automated IMT measurement eliminates the component of variability associated with manual cursor placement. In addition, the automated edge tracking using subpixel interpolation determines edge boundaries at a resolution greater than monitor line resolution.³⁵ However, at present and with the available software, well-standardized manual measurements by trained technicians are probably as good as automated measurements, although there is a clear prospect for automation and an obvious attraction. During manual tracing of the lumen-intima and the media-adventitia interfaces, values of IMT were sometimes automatically calculated by the software of the ultrasound machine.^{11 13 18 21 22 28 30 32}

Measurements were performed on a video image or on the digitally frozen image. Off-line analysis has the advantage of separating data acquisition from data interpretation, making patient examination more efficient. On-line analysis requires utmost precision and skill, but it has the advantage of optimal imaging without pixel loss and no need for a storage system and a second measurement (interpretation) session. Furthermore, the ultrasonographer is forced to acquire an optimal image because he has to perform the measurements himself. If during the measuring the quality of the scan appears to be not good enough, a new image can be obtained immediately. In most studies, measurements were done on a video image. In this case, a second person, the reader, measured IMT off-line. The variability based on only different sonographers was generally larger than the variability based on only different readers in studies in which both reproducibility of sonographers and readers was presented for the same population.^{13 19}

About 50% of the investigators determined the mean IMT over a length of 1 cm. This mean IMT was calculated from the total intima-media area or was determined by many repeated computer measurements in this section.^{23 25 35} In 14 of 23 studies, maximum IMTs were measured, from which either the maximum or the mean was taken. Veller et al²⁴ took the mean IMT of five randomly selected values, and Baldassarre et al²⁷ took the mean over a maximum length of the CCA.

	Reproducibility Data

Top Abstract Introduction Image Acquisition Image Analysis Reproducibility Data Discussion References

 
In the selected literature, intraobserver and interobserver variability were expressed as mean difference between the measurements, variation coefficient, correlation coefficient, and percent error. Table 2 summarizes the definitions of these statistics. The most direct way to express reproducibility is by computing the mean difference between two measurements and the standard deviation of this mean difference. This can be visualized by making a scatterplot of the difference of two measurements against the mean of those two measurements. Bland and Altman⁴¹ explained that the use of a correlation coefficient is misleading in determining repeatability. The correlation coefficient measures only the strength of a relation between two variables and not the agreement. Data that seem to be in poor agreement can produce high correlations.

View this table: [in this window] [in a new window]   Table 2. Variability Measures

As shown in Table 1, intraobserver variability in the selected studies varied between a mean±SD difference of 0.02±0.02 mm²³ and 0.66±1.13 mm,¹³ a variation coefficient of 2.4%³² and 10.6%,²¹ a correlation coefficient of 0.62²⁰ and 0.97,^{12 15} and an error percentage of 2.5%²⁷ and 15.9%.¹⁸ Reported interobserver variability varied between a mean±SD difference of 0.01±0.04³³ and 0.65±0.69,¹³ a variation coefficient of 3.1%²⁵ and 18.3%,¹⁶ a correlation coefficient of 0.58^{19 20} and 1.00,²⁹ and an error percentage of 5.9%²⁷ and 13.7%.¹⁸ In many studies, the intraobserver and interobserver variations are similar in magnitude. From a theoretical point of view, one would expect a more pronounced difference in favor of intraobserver reproducibility. Reproducibility of IMT measurements was worse in studies including measurements in the ICA and bulb than in studies limited to the CCA. In general, variability was less when measuring mean IMT compared with maximum IMT in studies where both were measured. Measuring in more than one direction seems to provide better reproducibility than measuring in only one direction. The investigators who used the automated edge-tracking method reported good reproducibility.^{23 25 35}

	Discussion

Top Abstract Introduction Image Acquisition Image Analysis Reproducibility Data Discussion References

 
It is desirable to have a consensus on the method of measuring and expressing reproducibility of IMT. Better comparison of study results will then be possible. To decide which measuring method is most suitable, various features have to be considered: the reproducibility, the predictive value for presence of atherosclerosis elsewhere in the body, the assessment of atherosclerosis over time, and the prognostic value for occurrence of cardiovascular disease.

Whether increased carotid IMT reliably reflects the presence of atherosclerosis has been a matter of discussion. Ultrasound imaging cannot discriminate between the intima and the media of the vessel wall, while atherosclerosis predominantly affects the intima.⁴² An association has been found between increased CCA IMT and atherosclerosis of the arteries of the lower extremities as assessed by ankle-arm index measurement.⁴³ Salonen and Salonen³⁴ observed a correlation of 0.42 and 0.34 between mean maximal IMT in the CCA and in the carotid bulb and femoral artery, respectively. They found a correlation of 0.35 and 0.30 between change in IMT over a 12-month period between those arteries, respectively. Different risk-factor profiles have been described for carotid and femoral IMT.^{34 44} A clear relationship has been found between the thickness of the intima-media complex in the CCA and the prevalence of plaque in the carotid and femoral arteries.²² In a cross-sectional study in which carotid IMT was measured on the day of coronary angiography, only a weak correlation was found between coronary artery disease severity and carotid IMT (r=.26, P<.0001).⁴⁵ However, in a prospective study in 1257 men, for each 0.1-mm increase in IMT, the risk of acute myocardial infarction increased by 11% (P<.001).⁴⁶ In another study, carotid IMT was related to clinically manifest cardiovascular disease affecting distant vascular beds, such as the cerebral, peripheral, and coronary arteries.⁴⁷

Some studies have used polychotomous measures of wall status instead of IMT. Salonen and Salonen¹⁵ classified their ultrasonographic findings into four categories: (1) no atherosclerotic lesion, (2) intima-media thickening (>1.0 mm), (3) nonstenotic plaque, and (4) stenotic plaque. They measured IMT in the CCA and scanned both this artery and the carotid bifurcation to look for plaques. The association of any structural change with the risk of acute myocardial infarction was strongest for stenotic plaques, less for nonstenotic plaques, and least for intima-media thickening. Identification of plaque compared with wall thickening may be important because minimal increases in wall thickness may be manifestations of nonatherosclerotic intimal thickening.⁴⁸

The major advantage of using IMT in clinical trials is that every patient randomized will produce an end point, and adequate statistical power can be achieved with much smaller sample sizes and thus with less cost.⁹ However, large studies that use disease events as end points will always be required to eventually establish the clinical benefits. IMTs measured with ultrasound are now useful to indicate early atherosclerosis and give information on the regression and progression of atherosclerotic lesions. They can also provide more insight in the pathophysiology of atherosclerosis. Ultrasonographic assessment of IMT is especially useful in phase II clinical trials when there is no adequate statistical power to analyze clinical end points. The clinical usefulness of this method in the follow-up of individual subjects has yet to be proved. In studies that make comparisons between groups, poor reproducibility can be accepted if group size is large. For clinical management of individual patients, poor reproducibility may lead to inappropriate management. The ratio of random measurement error to the variability among progression rates is large, and only by repeated measures or longer follow-up may the contributions of random error be sufficiently decreased to allow individual diagnoses.³⁸

In ACAPS, nonsystematic error caused 89% of the cross-sectional within-subject variance of measured IMT.³⁸ Eleven percent was attributable to systematic differences among readers. In making sample size estimates for studies, implications of measurement error should be considered. Espeland et al³⁸ showed that the observed correlation between IMT progression and risk factors is probably less than one half of the true correlation. When the measurement error can be diminished, the observed correlation will give a better impression of the true correlation, and a smaller sample size is needed. Reproducibility of IMT measurements may improve by the training of observers and feedback of information on variation. Furthermore, repeat readings, standard films, database checks, standard equipment, blinding of technicians, and contemporaneous readings of baseline and follow-up films for progression studies or clinical trials are important quality-control measures that may reduce variability. Sample size can also be reduced by adopting statistical methods to correct for missing data. This is an important issue when measuring in the ICA.

In conclusion, image acquisition and analysis of IMT and quantification of variability have been reported in a variety of ways. The best expression of reproducibility is the mean difference of repeated measurements. Best reproducibility was found when measuring the mean IMT of the CCA in more than one direction.

	Selected Abbreviations and Acronyms

 

ACAPS = Asymptomatic Carotid Artery Progression Study CCA = common carotid artery ICA = internal carotid artery IMT = intima-media thickness

	Acknowledgments

 
The authors thank Professor Dr D.W. Erkelens, MD, for his critical review of the manuscript.

	Footnotes

 
The opinions expressed in this article are not necessarily those of the editors or of the American Heart Association.

Received September 9, 1996; revision received November 22, 1996; accepted November 26, 1996.

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Top Abstract Introduction Image Acquisition Image Analysis Reproducibility Data Discussion References

 
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