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Ultrasonography |
1 From the Depts of Angiology (S.S., M.S., W.M., A.W., M.H., T.N., R.A., E.M.), Emergency Medicine (M.M.), and Clinical Neurology (W.L.), Vienna General Hosp, Medical School, Waehringer Guertel 18–20, A-1090 Vienna, Austria. Received May 20, 2003; revision requested Aug 4; final revision received Nov 24; accepted Jan 5, 2004. Address correspondence to M.S. (e-mail: martin.schillinger@akh-wien.ac.at).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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MATERIALS AND METHODS: The authors studied 1,006 carotid arteries in 503 patients at duplex US and angiography. The degree of stenosis was determined by using duplex flow US velocities and applying 13 previously published sets of criteria and the criteria used at the authors’ institution. Two independent observers evaluated the angiograms according to North American Symptomatic Carotid Endarterectomy Trial (NASCET) criteria. 
statistics, sensitivities, specificities, positive predictive values (PPVs), negative predictive values (NPVs), and generalized linear mixed regression models were used to assess agreement between duplex US and angiographic findings.
RESULTS: Stenoses of 0%–29%, 30%–49%, 50%–69%, 70%–99%, and 100% could be differentiated with 73% overall agreement between duplex US and angiographic findings according to flow velocity criteria ( = 0.57; 95% confidence interval [CI]: 0.54, 0.60); however, with duplex US, the angiographic degree of stenosis tended to be overestimated. In the differentiation of stenoses of less than 70%, only 45% agreement ( = 0.26; 95% CI: 0.23, 0.29) was observed, whereas in the differentiation of high-grade (
70%) stenoses, 96% agreement was observed ( = 0.85; 95% CI: 0.83, 0.87). The PPV and NPV for the identification of 70%–99% angiographic stenosis were 69% and 98%, respectively, with use of the most sensitive duplex US criteria.
CONCLUSION: Duplex US is an excellent examination to screen for high-grade carotid artery stenosis; however, it tends to lead to an overestimation of the degree of stenosis. Exclusion of 70%–99% angiographic stenosis can be achieved with a sensitivity of up to 98%.
© RSNA, 2004
Index terms: Carotid arteries, angiography, 172.1245, 172.1247, 904.122 • Carotid arteries, stenosis or obstruction, 172.721, 904.721 • Carotid arteries, US, 172.12983, 172.12984, 172.12985, 904.12983, 904.12984, 904.12985 • Ultrasound (US), Doppler studies, 172.12983, 172.12984, 172.12985, 904.12983, 904.12984, 904.12985
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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Several criteria for quantifying degrees of stenosis have been introduced with variable intentions (1–13): Differentiating high-grade (70% diameter narrowing) from low-grade stenoses may help in identifying candidates for elective surgical or endovascular repair (7,9–12). Other investigators have proposed that differentiation as precise as that of 10% stenosis increments can be achieved with good agreement with the results of angiography (1,2,5), the reference standard examination. Angiography can be performed for serial follow-up investigations to sensitively quantify the progression of disease over time.
In general, methods based on the measurement of blood flow velocities in the common carotid artery (CCA) and ICA are thought to be more reliable than planimetric duplex US grading by means of direct imaging with gray-scale or color Doppler US (1). Nevertheless, accepted standard criteria to correlate blood flow velocity with stenosis are still lacking, and the question of which combination of blood flow parameters should be considered is the subject of ongoing debate. However, the criteria used to determine degrees of stenosis did not evolve from complex mathematic models; rather, they were derived by exploratively applying multiple cutoff values and adjusting the best-fitting correlations to a single data set. Thus, a comparative analysis and validation of published reports might help in developing a consensus on the quantification of carotid artery stenosis with duplex US.
The aim of the present study was to compare 13 previously published sets of duplex US criteria with the duplex US criteria used at our institution in terms of agreement with carotid artery angiographic findings.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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Patient Examinations
At presentation, the patients’ medical histories were obtained and physical examinations were performed after they completed a standard questionnaire. Demographic data, atherothrombotic risk factors, and cardiovascular comorbidities were recorded (by S.S., T.N., and W.M.). Before the patients underwent angiography, a complete neurologic examination, including determination of the National Institutes of Health Stroke Scale status (15), was routinely performed by one neurologist (W.L.).
Duplex US Evaluation
Duplex US grading of the carotid arteries was performed in accordance with both the principles established at a previous consensus meeting to address the quantification of extracranial carotid artery stenosis (16) and the proposals of Nicolaides et al (1). One day before angiography, US scanning was performed bilaterally with an Acuson XP 10 system or an Acuson Sequoia system (Acuson, Mountain View, Calif) by using a 5-MHz linear probe in 387 patients and with a Vingmed System 5 (Vingmed Sound AIS [now GE Medical Systems], Horton, Norway) by using a 10-MHz linear probe in 116 patients. A maximum angle of 60° to the blood flow was applied in all US examinations. These two duplex US systems have comparable technical equipment and precision and are color Doppler units with pulsed angle–adjusted Doppler technology for spectral analysis.
Seven medical technical assistants performed the duplex US examinations with the supervision of either of two authors (A.W., M.H.). All of the investigators had at least 3 years of experience performing duplex US. The duplex US examinations included gray-scale and color Doppler imaging in the transverse and sagittal planes. The examinations included imaging of the CCA, beginning immediately suprasternally and continuously advancing to the distal extracranial part of the ICA. A 15–20-cm segment was imaged, depending on the patient’s anatomy.
Pulsed-wave spectral Doppler US data were acquired bilaterally in the CCAs and ICAs. Maximum blood flow velocities were measured in only the sagittal planes. Doppler US data in the CCA were measured 3 cm below the bifurcation and were used to calculate carotid artery ratios. The peak systolic velocities (PSVs) and end-diastolic velocities (EDVs) in these vessels were measured. When a stenosis was present, the maximal velocities within the narrowed area of the segment were recorded. The lesion was localized according to its distance from the bifurcation as measured at B-mode duplex US.
Doppler US velocities in ICAs were measured in the narrowest segment of the vessel, as indicated at B-mode duplex US and with electronic calipers. Two independent observers (M.S., T.N.) other than the duplex US investigator determined the degree of ICA stenosis by using the given blood flow velocities and carotid artery ratios. All calculations were performed by both observers, each of whom had at least 1 year of experience in performing these types of calculations. These investigators were blinded with respect to patient data and angiographic findings. In cases of disagreement regarding the measured degree of stenosis, the vessel data were reevaluated by both observers in consensus.
Thirteen previously published sets of criteria, as well as the criteria that have been routinely used at our institution since 1997 (Table 1), were applied to quantify the degree of stenosis. Our stenosis-grading criteria were internally validated; we have been performing such validation systematically since 1995. After the Nicolaides et al (1) study was published in 1996, we adapted our carotid artery ratio and PSV criteria according to these investigators’ recommendations; however, we simplified the criteria in terms of the number of criterion subgroups.
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statistics for multiple outcomes) were used to validate the results were considered for further analysis. Redundant criteria were included only once. The specific duplex US criteria used in the eligible previously published studies are listed in Figure 1.
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Angiographic Evaluation
Angiographic examinations were performed by one investigator (R.A.). Angiography was begun by gaining transfemoral access after inducing local anesthesia in the patient. Each patient received 5,000 IU of heparin intraarterially after placement of the sheath. An overview angiogram was obtained at digital subtraction angiography of the supraaortic arteries from the aortic arch by using a 5-F pigtail catheter. Selective angiograms were then obtained in at least two planes of both carotid arteries and their intracranial branches by using a 5-F sidewinder catheter.
The degree of stenosis was calculated according to North American Symptomatic Carotid Endarterectomy Trial (NASCET) criteria (17) by two independent observers (S.S., W.M.) other than the interventionist. These observers were blinded with respect to patient data and duplex US findings. All measurements were performed by both observers, each of whom had at least 1 year of experience in performing these types of calculations. All measurements were averaged. Measurements were made on the angiographic view that showed the most severe vessel narrowing. The stenosis diameter used to calculate the NASCET angiographic degree of stenosis was measured in the area of the most severe narrowing by using manual calipers.
Statistical Analyses
Continuous data are cited as means ± standard deviations. Actual values and percentages are presented for discrete variables. Chance-corrected statistics, including 95% confidence intervals, were used to analyze agreement between the duplex US and angiographic findings. For these calculations, the NASCET angiographic degrees of stenosis were grouped into the same ranges as the corresponding duplex US stenosis degree ranges; thus, two categorical variables (ie, duplex US and angiography) that consisted of the same stenosis degree ranges were compared. Although there are no absolute definitions of values, in this study a value of less than 0.20 indicated poor; a value of 0.21–0.40, fair; a value of 0.41–0.60, moderate; a value of 0.61–0.80, good; and a value of 0.81–1.00, very good agreement (18).
Furthermore, the sensitivity, specificity, PPV, and NPV, as well as the corresponding 95% confidence intervals, of each set of duplex US criteria for the prediction of a 70%–99% NASCET angiographic stenosis were calculated. For these calculations, data were dichotomized into a concordant data group—in cases of agreement between angiographic and duplex US findings for the given stenosis degree ranges—or a discordant data group—in cases of disagreement. Spearman rank correlation coefficients were calculated to correlate the duplex US and angiographic data; the resulting r2 value was a measure of the variability of one blood flow parameter defined by the other.
Generalized linear mixed regression models were applied to assess the association between duplex US grade of stenosis and NASCET angiographic degree of stenosis. The objective of the generalized linear mixed regression model was to estimate the angiographic degree of stenosis from the US findings while adjusting for clustering of the side (ie, right vs left carotid artery) of the stenosis. Bilateral analysis of the agreement between duplex US and angiographic findings made this adjusted analysis necessary; otherwise, the analysis of arteries instead of patients might have introduced a systematic error. The generalized linear mixed regression model accounted for this possibility and yielded an estimate of the angiographic degree of stenosis that was expected to correspond with the given duplex US degree of stenosis.
The generalized linear mixed regression model was calculated for only our criteria (ie, those routinely used at our institution). With this model, one takes into account that the variables observed in such a setting are not necessarily independent: Each side is "nested" within a patient, and each patient is "nested" in a particular duplex US investigator (n = 7) and duplex US system (n = 2).
The angiographic degrees of stenosis for the generalized linear mixed regression model were applied as continuous data; all degrees ranged from 0% to 100%, with normal errors. The angiographic degree of stenosis was the dependent variable, and the duplex US degree of stenosis was the primary predictor variable. Our duplex US criteria were entered as the midpoint score of the corresponding interval. We calculated robust standard errors. Furthermore, data were analyzed for sex-dependent differences by using stratification. The regression coefficient is a measure of the increase in NASCET angiographic degree of stenosis that corresponds to an increase in each given duplex US degree of stenosis. Two authors (M.M., M.S.) performed the statistical calculations by using computer software programs (Stata, release 7, Stata, College Station, Tex; or SPSS, version 10.0 or Windows, SPSS, Chicago, Ill).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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The mean NASCET angiographic degree of ICA stenosis was 56% ± 26 on the right side and 50% ± 30 on the left side. The correlation between duplex US degree of stenosis (in five ranges of stenosis degrees for the criteria applied at our institution) and NASCET angiographic degree of stenosis (Spearman r2 = 0.66, P < .001) is illustrated in Figure 2. The presented data suggest that duplex US findings accounted for approximately 66% of the variability in the NASCET angiographic degree of stenosis.
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analysis ( = 0.57; 95% confidence interval: 0.54, 0.60). When we stratified the lesions into low-grade and high-grade stenosis categories, we observed only 45% agreement between duplex US and angiography in the differentiation of stenoses of less than 70%; this level of agreement was rated as fair at analysis ( = 0.26; 95% confidence interval: 0.23, 0.29). We observed excellent agreement, 96%, between the two modalities in the differentiation of high-grade (ie, 70%) stenoses, with a rating of very good ( = 0.85; 95% confidence interval: 0.83, 0.87). However, duplex US tended to lead to an overestimation of the angiographic degree of stenosis. The data in Figure 2 show that the mean NASCET angiographic degree of stenosis was lower than the mean degree of stenosis estimated by using duplex US. To account for the hierarchical structure of the data (clustering of side [right vs left carotid artery] and duplex US investigator [n = 7]), generalized linear mixed regression analysis was performed to calculate the NASCET angiographic degree of stenosis that corresponded to each set of duplex US criteria. The NASCET angiographic degrees of stenosis predicted on the basis of each given range of duplex US stenosis grades are listed in Table 2. These data support the view that duplex US tended to lead to an overestimation of the NASCET degree of stenosis overall: The NASCET degrees of stenosis were lower than or in the lower range of the duplex US degrees of stenosis. We did not further stratify data on the basis of the carotid artery side investigated, the duplex US investigator, or the duplex US machine (Acuson or Vingmed) used because our models revealed that the intracluster correlation coefficient was zero, which indicated that the agreement between duplex US and angiographic findings was independent of each of these variables. No sex-based differences were observed.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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The degree of carotid artery stenosis is a critical parameter in considering the risk-to-benefit ratio for carotid endarterectomy. Patients with severe stenosis (ie, 70%) of the ICA are expected to benefit from surgical repair (17,19–22). Subgroups of patients with 60%–70% stenosis, particularly if they are symptomatic, may also expect a small benefit from revascularization therapy. Patients with higher degrees of stenosis will gain a greater benefit from surgery, however, so precise estimation of the stenosis grade is important.
Depending on whether a patient is symptomatic or asymptomatic, different degrees of stenosis will be clinically relevant and thus will need to be correctly identified. This point emphasizes the importance of ensuring that the given evaluation method has not only good sensitivity but also adequate specificity. Although intraarterial digital subtraction angiography is considered the reference method for determining the ICA stenosis grade, the risk of complications, which ranges from 1% to 4%, makes this examination inadequate for patient screening (23–25).
Duplex US has the advantages of being noninvasive and not being associated with complications. When we addressed the controversy of whether carotid endarterectomy can be performed without angiography (26–32), our findings and previous observations (3) suggested that duplex US tends to lead to an overestimation of the degree of stenosis, which in turn leads to the establishing of inadequate indications for surgical repair in up to 20% of cases (30,31); these data correspond to the maximum PPV of 79% for the most specific duplex US criteria used in the current data set (4). Magnetic resonance angiography or computed tomography may be used to clarify unclear duplex US findings (3,28,33).
Carotid artery angiography is still the reference method for quantifying the degree of stenosis. However, several inaccuracies of carotid angiography have to be acknowledged: (a) Some degree of interobserver variation in measurement is inherent to this technique (34), (b) two competing measuring systems—those of the NASCET and the European Carotid Surgery Trial, or ECST—can complicate interpretations, and (c) even with use of multiple imaging planes, the maximum degree of stenosis may be missed. It has been reported that duplex US findings can be even more precise than angiographic findings (35). However, the experiences from the NASCET and the Committee for the Asymptomatic Carotid Atherostenosis, which provide the rationale for performing carotid artery surgery, evolved from stenosis diameter measurements on angiograms. Thus, the diameter of a stenosis measured at angiography remains the reference standard.
The accuracies of different duplex US criteria observed in the present study might seem relatively low compared with those in the previous studies (1–13). When interpreting these controversial results, one has to acknowledge that the number of carotid arteries investigated in the present study was up to 10 times larger than that investigated in the previous studies. Furthermore, in the present study we validated predefined criteria rather than fit the best criteria to preexisting data in a post hoc manner. However, the value (for agreement) decreases with increasing number of stenosis degree ranges within each classification, particularly for the duplex US classifications that include more ranges of stenosis degrees. Nevertheless, in the present study the accuracy of duplex US was excellent in the identification of high-grade stenoses (70%) but only moderate in the identification of stenoses of less than 70%. These results seem to be pathophysiologically reasonable since the duplex US grading methods used were based on the quantification of blood flow parameters.
Lesions with 50%–70% stenosis, which are hemodynamically less relevant, can be quantified less accurately by measuring alterations in blood flow velocities. Nevertheless, given the embolic potential of stenoses, even those of lower degrees of narrowing, at least a crude quantification of midgrade lesions with duplex US seems desirable. Lesions of less than 50% stenosis cannot be differentiated with duplex US and have no clinical relevance; therefore, the strata of stenoses of less than 50% should be omitted.
When we compared the different duplex US criteria in terms of agreement between US and angiographic findings, the best agreement was observed when the criteria were used to discriminate between low grades of stenosis (<70%), high grades of stenosis, and occlusions (7,9–12,36). The lowest agreement was observed when we differentiated stenoses in up to 10% degree increments. When we analyzed the duplex US criteria that included more than four parameter categories, it seems that the criteria based on the quantification of PSVs (eg, those of Nederkoorn et al [3], AbuRahma et al [4], and our group) were more accurate than were the more complex criteria that are also based on EDVs and carotid artery ratios (ie, those of Nicolaides et al [1], Zwiebel [2], and Filis et al [5]).
The clinical decision of whether or not to initiate carotid artery revascularization is based on the detection of a 70%–99% stenosis. Therefore, we calculated the sensitivity, specificity, PPV, and NPV of each of the 14 duplex US criteria (including our institution criteria) for the correct identification of a 70%–99% stenosis, irrespective of the number of corresponding stenosis degree ranges. These calculations revealed a considerably different impression of the usefulness of the different criteria, as indicated by the overall agreement values illustrated in Figure 3. The criteria of Nicolaides et al (1), Hwang et al (8), Filis et al (5), and Robinson et al (6) enabled the most sensitive detection of a 70%–99% stenosis, whereas the criteria of AbuRahma et al (4) had the highest specificity.
Because different investigators have applied different blood flow parameters, alone or in combination, to estimate degrees of stenosis, we intended to determine the sensitivities and specificities for the correct identification of a 70%–99% stenosis by using our (institution) criteria. We did not, however, separately evaluate the effect that criteria involving a single duplex US parameter had on sensitivities and specificities. Therefore, it was virtually impossible to assess the influence of high or low thresholds of PSV, EDV, or carotid artery ratio on sensitivities and specificities in the current analyses because combinations of these parameters were used to determine degrees of stenosis.
Some limitations of the present study have to be acknowledged. Owing to the specific preselection of patients scheduled for angiography, our analysis was focused mainly on the identification of high-grade stenoses. It has to be mentioned that the use of the means of the angiographic measurements obtained by two observers may have limited the conclusions that could be drawn in the study. Furthermore, the accuracy of duplex US measurements in very-high-grade stenotic lesions may have been limited owing to the occurrence of slow turbulent flow. Nicolaides et al (1) referred to this phenomenon as "trickle flow" rather than high-flow velocity. However, to use a consistent approach when applying the 13 previously published sets of criteria (some authors considered this phenomenon, while others ignored it), we ignored this phenomenon when we performed our calculations. Nevertheless, to use duplex US routinely, the investigator has to be aware of the possibility of misleading duplex US velocity measurements in very-high-grade stenotic lesions.
In conclusion, duplex US is an excellent examination to screen for high-grade carotid artery stenoses; however, it tends to lead to an overestimation of the stenosis grade. Duplex US can enable the differentiation of clinically relevant stenoses of greater than 50%, and even better, of stenosis of greater than 70%, with excellent agreement with angiographic findings. Duplex US can enable the identification of a 70%–99% NASCET angiographic stenosis with a sensitivity of up to 98%; however, it cannot enable the differentiation of lower grades of stenosis (ie, <50%). The differentiation of stenoses in 10% degree increments in particular seems inadequate.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Author contributions: Guarantors of integrity of entire study, S.S., M.S., A.W., M.H.; study concepts, M.S., S.S., M.H.; study design, A.W., R.A., W.L.; literature research, S.S., M.S.; clinical studies, M.H., A.W., S.S., M.S.; data acquisition, S.S., T.N., W.M.; data analysis/interpretation, M.S., M.M., M.H., E.M.; statistical analysis, M.S., M.M.; manuscript preparation, S.S., M.S., W.M.; manuscript definition of intellectual content and final version approval, all authors; manuscript editing, S.S., M.S.; manuscript revision/review, S.S., M.S., A.W., M.H., E.M.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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, listed in 
). With increasing specificity of duplex US owing to increasing numbers of stenosis degree ranges, agreement between US and angiographic findings decreased.