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(Stroke. 1997;28:1981-1987.)
© 1997 American Heart Association, Inc.


Articles

Power Doppler Imaging of Carotid Artery Stenosis

Comparison With Color Doppler Flow Imaging and Angiography

W. Steinke, MD; S. Ries, MD; N. Artemis, MD; A. Schwartz, MD; M. Hennerici, MD

From the Department of Neurology, Klinikum Mannheim, University of Heidelberg (Germany). Dr Artemis was a visiting fellow from the Department of Neurology, AHEPA Hospital, Thessaloniki, Greece.

Correspondence to PD Dr W. Steinke, Department of Neurology, Marien-Hospital Düsseldorf, Rochusstr 2, 40479 Düsseldorf, Germany.


*    Abstract
up arrowTop
*Abstract
down arrowIntroduction
down arrowSubjects and Methods
down arrowResults
down arrowDiscussion
down arrowReferences
 
Background and Purpose Power Doppler imaging (PDI) is a new sonographic technique that has recently been introduced for vascular application. Since the technical principles of PDI may provide increased sensitivity to visualize the continuity of blood flow in arterial stenoses, we investigated the diagnostic significance of PDI and the intermethod relationship for the measurement and classification of internal carotid artery (ICA) stenosis in comparison with both color Doppler flow imaging (CDFI) and angiography.

Methods One hundred patients with a total of 128 ICA stenoses (50% to 69%, n=37; 70% to 79%, n=27; 80% to 99%, n=64) and 12 ICA occlusions were consecutively investigated by means of PDI, CDFI, and intra-arterial angiography (n=48). Reduction of the intrastenotic lumen was measured on longitudinal and transverse views of PDI and CDFI for the calculation of the degree of diameter and area stenosis, respectively. Angiographic stenosis was determined with the use of the North American Symptomatic Carotid Endarterectomy Trial (NASCET), European Carotid Surgery Trial (ECST), and common carotid (CC) methods.

Results PDI provided significantly more excellent or good (92% versus 79%; P<.01) displays of the intrastenotic lumen than CDFI, particularly in complicated high-grade stenosis. While linear regression analysis demonstrated a high overall correlation between PDI and CDFI for diameter (r=.88; P<.001) and area stenosis (r=.79; P<.001), categorization of ICA stenosis revealed best agreement for 80% to 99% area stenoses. Since angiography frequently either underclassified (NASCET method) or overclassified (ECST, CC methods) the degree of ICA stenosis in comparison to both PDI and CDFI, the sonographic-angiographic correlation was only moderate (regression coefficients ranged from .62 to .70; P<.001).

Conclusions PDI further improves the assessment of ICA stenosis by providing better visualization of the stenotic vascular lumen than CDFI. Sonographic imaging of the stenotic plaque on both PDI and CDFI provided a direct measurement of the local degree of stenosis, while the angiographic grade of stenosis essentially depended on the method used for evaluation.


Key Words: angiography • carotid artery diseases • ultrasonics


*    Introduction
up arrowTop
up arrowAbstract
*Introduction
down arrowSubjects and Methods
down arrowResults
down arrowDiscussion
down arrowReferences
 
Since the publication of the North American and European carotid endarterectomy trials, which demonstrated a significant benefit of surgery for patients with symptomatic carotid artery stenosis greater than 70%,1 2 an ongoing discussion about the different angiographic methods of measuring carotid stenosis has emerged.3 4 5 6 7 In this context, another method using the diameter of the CC artery as the denominator for the calculation of ICA stenosis was introduced more recently.8 9 10 However, because these methods provide discrepant results, the patient's management essentially depends on the method used for evaluation of the angiogram. Furthermore, it was recently confirmed in the Asymptomatic Carotid Atherosclerosis Study and a large prospective Australian study11 12 that angiography was associated with a relevant risk of stroke and systemic complications. Therefore, the need for an accurate and safe noninvasive assessment of carotid artery disease is evident.

For more than a decade, Doppler sonography and conventional duplex scanning using distinct parameters of the Doppler frequency spectrum have been well accepted as reliable diagnostic tools for the detection and classification of ICA stenosis.13 14 15 16 17 18 19 20 21 More recently, CDFI, which provides a color-coded visualization of the velocity and flow direction of moving blood cells superimposed on a gray-scale image of vascular structures, has become the leading routine method in most neurovascular departments because CDFI improves the diagnostic accuracy and reproducibility of sonographic assessment of carotid stenosis.6 22 23 24 25 26 27 28 29 However, plaque calcification remained a significant limitation for the visualization of the intrastenotic diameter and area reduction.25 29 In contrast to CDFI, PDI, the most recently introduced sonographic technique, generates intravascular color signals based on the reflected echo amplitude, which essentially depends on the amount of red blood cells within the sample volume. Thus, the color display on PDI is independent from the angle of insonation and, more importantly, from the velocity and direction of moving blood cells. In addition, because of the different technique of image generation, an increased sensitivity to display the continuity of the stenotic lumen and improved definition of the intravascular surface are claimed for PDI. Since experience in the assessment of carotid stenosis by PDI is limited to date,30 31 this study was performed to systematically evaluate the display quality of PDI in comparison to CDFI in patients with symptomatic and asymptomatic ICA stenoses. The second objective was to correlate measurements of ICA stenosis on PDI and CDFI with the three different angiographic techniques to investigate the clinically important intermethod relationship.


*    Subjects and Methods
up arrowTop
up arrowAbstract
up arrowIntroduction
*Subjects and Methods
down arrowResults
down arrowDiscussion
down arrowReferences
 
One hundred patients (70 men, 30 women; mean age, 67 years; range, 35 to 81 years) were consecutively included in the study if they had at least a 50% ICA stenosis according to conventional CW Doppler criteria,16 17 19 while ICA occlusion was not an inclusion criterion. A total of 128 ICA stenoses (50% to 69%, n=37; 70% to 79%, n=27; 80% to 99%, n=64) and 12 complete ICA occlusions were diagnosed. Fifty-one patients presented with acute cerebrovascular events (related to the ICA stenosis in 45 cases), 41 outpatients were seen for follow-up studies of asymptomatic carotid artery disease, and in 8 patients with significant risk factors the ICA stenosis was revealed by Doppler sonography as a screening test.

PDI and CDFI examinations were performed by three experienced examiners (W.S., S.R., N.A.) using an Acuson 128 XP ultrasound device with a 7.0-MHz linear array transducer. PDI and CDFI were performed without knowledge of the degree and side of ICA stenosis and of the presence of ICA occlusion on CW Doppler sonography. The technical principles of CDFI have been reported elsewhere.32 33 The crucial difference between PDI and CDFI is that PDI uses the amplitude of the echo signal reflected from red blood cells and does not process information of frequency or phase shift for the generation of intravascular color signals. Thus, the visualization of blood flow essentially does not depend on the velocity and direction of moving blood cells and is free from color aliasing phenomenon. In addition, special filter systems further improve the blood-tissue discrimination, resulting in a relatively homogeneous angiography-like visualization of the vascular lumen surface superimposed on a conventional B-mode display of tissue and vessel structures.34

Sequential parallel longitudinal views and perpendicular cross sections were displayed on PDI and CDFI. On-line measurements of the vessel wall and the minimal residual lumen of the ICA stenosis contrasted by color signals of either method on longitudinal and transverse displays were used to calculate the degree of stenosis as percentage of the diameter and area reduction, respectively (Fig 1Down). Measurement of the diameter reduction on longitudinal views was consistently performed at the narrowest site of the stenosis perpendicularly to the long axis of the vessel regardless of the angle to the intrastenotic flow direction. Measurements were performed at exactly the same site of stenosis by directly switching from CDFI to PDI display. Pulsed-wave Doppler spectra were not recorded with the integrated Doppler system to avoid bias for the measurement of ICA stenosis. The display quality of both sonographic techniques was classified as excellent, good, poor, and not visualized depending on the continuity and intensity of intravascular color signals in the prestenotic, intrastenotic, and poststenotic vessel segments and on the delineation of the plaque surface and the residual stenotic lumen by color contrast.



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Figure 1. Measurement of ICA diameter stenosis (A, B) and area stenosis (C, D) on CDFI (A, C) and PDI (B, D). The minimal residual intrastenotic lumen and the normal width of the vessel at the same site in longitudinal (white divided line, perpendicular to the long axis of the vessel) and transverse (broken white line delineates the vessel wall) views are used to calculate the degree of stenosis.

Intra-arterial selective biplane digital subtraction angiography was conducted according to clinical indications in 43 symptomatic patients (48 ICA stenoses). In all cases angiography followed the sonographic examinations (mean interval, 4.8 days; range, 1 to 17 days). The neuroradiologist who evaluated the angiograms was unaware of the measurement of carotid stenosis on PDI and CDFI. Calculation of the degree of diameter stenosis was performed with the use of the NASCET and ECST criteria, as well as the CC method.1 2 10 For statistical evaluation of the correlation between measurements of stenosis by different sonographic and angiographic methods, simple regression analysis was used. Frequencies were analyzed with the use of the {chi}2 test.


*    Results
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up arrowAbstract
up arrowIntroduction
up arrowSubjects and Methods
*Results
down arrowDiscussion
down arrowReferences
 
Display Quality
PDI provided excellent or good visualization of the plaque configuration and intrastenotic lumen of 128 ICA stenoses more frequently (92%) than CDFI (79%), in particular in complicated high-grade stenosis (Fig 2Down). Accordingly, CDFI failed to visualize the stenosis or provided poor displays of the vascular lumen surface more frequently than PDI (21% versus 8%, {chi}2 [df=1]=9.13, P<.01) (Fig 3Down). Plaque calcification was the predominant cause of inadequate visualization of the stenotic vessel segment. Measurement of the diameter stenosis was feasible in 97% of the ICA stenoses on PDI and in 93% on CDFI, and area stenosis could be reliably measured in more PDI studies (94%) than CDFI studies (88%). However, the difference was not statistically significant ({chi}2 [df=1]=2.33).



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Figure 2. Sonographic display quality. Visualization of plaque surface and stenotic lumen is more frequently excellent on PDI than on CDFI (**P<.01).



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Figure 3. High-grade ICA stenosis. a, Poor display on CDFI without visualization of the residual stenotic lumen due to a calcified plaque at the anterior vessel wall with a dense echo shadow. b, Color signals of PDI contrast the stenotic vascular lumen and the plaque surface. c, Angiogram corresponds to PDI.

Measurement of ICA Stenosis
PDI Versus CDFI
Linear regression analysis demonstrated a high correlation between PDI and CDFI for the measurement of both diameter stenosis (r=.88, P<.001) and area stenosis (r=.79, P<.001). After classification of the ICA stenoses into distinct categories according to the degree of stenosis, overall agreement between both methods was better for area stenosis (75.0%) than for diameter stenosis (67.5%) (Table 1Down). While the rate of stenoses classified into a higher category by PDI compared with CDFI did not differ between diameter (9.4%) and area stenoses (9.8%), underclassification by PDI occurred more frequently in diameter (23.1%) (Fig 1Up) than in area stenoses (15.2%). This was particularly evident in diameter measurements of high-grade stenoses: 44.1% of the 80% to 99% ICA stenoses according to CDFI were classified into the 70% to 79% category by PDI (Table 1Down).


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Table 1. Classification of ICA Diameter and Area Stenosis by PDI and CDFI

PDI and CDFI Versus CW Doppler
Correlation of CW Doppler with the measurement of diameter and area reduction on PDI and CDFI was significant for both imaging methods (P<.001). On CDFI, measurement of ICA stenosis on longitudinal views correlated slightly better (r=.74) than measurement on transverse views (r=.70), while correlation with CW Doppler sonography was not different for diameter and area stenosis on PDI (r=.75) (Fig 4Down). Further evaluation demonstrated that both PDI and CDFI had a relevant tendency to underestimate the degree of stenosis in comparison to CW Doppler.



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Figure 4. Linear regression analysis of the correlation between ICA stenosis assessed by CW Doppler sonography and diameter stenosis on PDI (A) and CDFI (B).

PDI and CDFI Versus Angiography
Measurement of carotid stenosis between both sonographic techniques and the three angiographic methods correlated significantly (P<.001). Coefficients of correlation demonstrated only minor differences between PDI and CDFI (Fig 5Down). They were highest for PDI versus ECST (r=.70) and CC (r=.69) results, while correlation of PDI versus NASCET (r=.63) and of CDFI versus NASCET (r=.64), ECST (r=.64), and CC (r=.62) results was slightly worse.



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Figure 5. Linear regression analysis of the correlations of measurement of ICA diameter stenosis between PDI (A, C), CDFI (B, D), and angiography evaluated according to NASCET (A, B) and ECST (C, D) methods. All correlations are statistically significant (P<.001). Coefficients of correlation are higher for PDI vs ECST (r=.70) than for PDI vs NASCET (r=.63), and for CDFI vs NASCET (r=.64) and ECST (r=.64).

Classification of ICA diameter stenosis by PDI, CDFI, and angiography revealed only a moderate overall agreement between sonographic and angiographic methods (Tables 2 through 4DownDownDown). Mismatch was essentially due to a significant rate of overclassification of ICA stenosis measured according to the ECST and CC methods in comparison to both PDI (30.9% and 33.3%) and CDFI (28.9% and 42.1%) (Tables 3Down and 4Down). In contrast, evaluation of angiography with the NASCET method resulted in a significant underclassification of stenosis compared with PDI (38.1%) and CDFI (39.6%), respectively (Table 2Down). However, if all the 70% to 79% stenoses and 80% to 99% stenoses were grouped together into one category, the overall agreement increased significantly and was highest for PDI versus CC (95.2%). Angiography performed in 7 of 12 patients with the sonographic diagnosis of ICA occlusion confirmed the results of PDI and CDFI in all cases. Furthermore, none of the ICA stenoses assessed by sonography were occluded on the angiograms.


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Table 2. Classification of Diameter ICA Stenosis by Angiography According to the NASCET Method Correlated With PDI and CDFI


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Table 3. Classification of Diameter ICA Stenosis by Angiography According to the ECST Method Correlated With PDI and CDFI


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Table 4. Classification of Diameter ICA Stenosis by Angiography According to the CC Method Correlated With PDI and CDFI

The comparative analysis of measurement of the individual ICA stenosis by PDI and angiography revealed that application of the NASCET method resulted in a lower degree of stenosis than the ECST method in 95% of the angiograms (Fig 6Down). In those cases in which NASCET significantly underestimated the ICA stenosis compared with PDI, ECST was regularly closer to the sonographic results. Conversely, when the angiographic degree of stenosis was higher than the PDI measurement, NASCET results correlated slightly better with PDI than ECST (Fig 6Down). However, angiographic overestimation of stenosis was commonly less significant.



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Figure 6. Comparative analysis of measurement of the individual ICA stenosis by PDI and angiography (ECST and NASCET methods).


*    Discussion
up arrowTop
up arrowAbstract
up arrowIntroduction
up arrowSubjects and Methods
up arrowResults
*Discussion
down arrowReferences
 
PDI is a new sonographic method that is based on different technical principles than CDFI for the generation of intravascular color signals.34 The intensity of color signals on PDI essentially depends on the reflected echo amplitude from red blood cells, thus indicating the density of blood cells within the sample volume. Addition of positive and negative frequency shifts from moving blood cells and the use of special filter systems for blood/tissue discrimination further increases the signal-to-noise ratio, resulting in a higher sensitivity to visualize blood flow and improved edge definition of intravascular surfaces. Accordingly, the present study demonstrated a significant increase of the number of sonographic examinations with adequate display quality using PDI. This result confirms the findings of two recent studies that also reported superior visualization of the stenotic vessel segment on PDI compared with CDFI.30 31

Different from CDFI, PDI provides relatively homogeneous color signals even in high-grade stenosis and generates an angiography-like visualization of the vascular lumen surface (Figs 1Up and 3Up). Since PDI thus facilitates the visual perception of the configuration of the ICA stenosis, angiograms will be less frequently required before carotid endarterectomy. In this respect, the greater acceptance of modern sonographic techniques instead of angiography for the preoperative assessment and visualization of ICA stenosis is particularly important because of the well-known risks of intra-arterial angiography.11 12 However, although we included a considerable number of very high-grade ICA stenoses and contralateral occlusions, the diagnostic significance of PDI for the assessment of near occlusion in comparison to CDFI and angiography could not be determined sufficiently from the present data.

Independence from the angle of insonation and absence of aliasing phenomena are other advantages of PDI compared with CDFI.30 31 However, since the color signals of PDI do not provide any information about the velocity and direction of moving blood cells, the site of maximal stenotic flow velocity is not indicated, and areas of abnormal hemodynamics cannot be identified directly. Therefore, PDI and CDFI are complimentary sonographic methods and should be used together for optimal diagnostic results.

In the present study measurement of the diameter stenosis correlated significantly between PDI and CDFI when we used linear regression analysis. However, classification of ICA stenosis into distinct categories of severity revealed highest agreement for area reduction in high-grade (80% to 99%) ICA stenosis. This high concordance of both sonographic imaging techniques further supports the view of a recent study of PDI and CDFI in ICA stenosis that measurements of lumen reduction on transverse views comes probably closest to the "true anatomic degree of stenosis." Accordingly, Alexandrov et al6 reported that color-assisted duplex sonography correlated significantly with planimetric measurements of cross sections of surgical specimens from endarterectomy of carotid stenosis. A corresponding conclusion was consequently drawn in an international consensus meeting on the quantification of ICA stenosis that suggested measurement of the area ratio on transverse views of CDFI as a valid criterion for the assessment of the degree of stenosis.4

Measurement of diameter stenosis performed on PDI and CDFI correlated only moderately with angiography in this study regardless of the method used for evaluation of the angiograms. However, among all sonographic-angiographic correlations, agreement was best between PDI and ECST and CC methods, respectively. Griewing et al31 also found a higher correlation of PDI and angiography evaluated according to the ECST method in comparison to the correlation between CDFI and angiography. However, the significantly better performance of PDI in the study by Griewing et al was at least partially due to unusual discrepancies between measurements on CDFI and angiography.31

The cause of only moderate accordance between sonographic imaging and angiographic methods in our study became more evident after classification of the ICA stenoses into distinct categories of diameter reduction. Both ECST and CC methods frequently overestimated the stenoses, whereas the NASCET method led to significant underestimation compared with both PDI and CDFI. Corresponding findings were reported by Rothwell et al,10 who demonstrated that ECST and CC methods classified twice as many stenoses as severe (70% to 99%) than did the NASCET method in a comparison of the three angiographic methods for the measurement of carotid stenosis on 1001 angiograms. Conversely, more than 60% of the 30% to 69% stenoses according to the ECST and CC methods were assigned to the 0% to 29% category by the NASCET method.10 With regard to these findings, which confirmed previous analyses,5 6 9 and the results of the present study, it may be postulated that modern sonographic techniques such as PDI and CDFI provide the best approximation of the degree of carotid stenosis because of the capability to visualize directly the intrastenotic residual lumen diameter and the distance between vessel walls at the same site. In contrast, calculation of the angiographic degree of ICA stenosis uses denominators that frequently are either too small (NASCET), too wide (CC), or roughly estimated (ECST). Unfortunately, CDFI and PDI were not available when the large endarterectomy trials started. Retrospective analysis of duplex scanning with Doppler spectrum analysis in selected NASCET and ECST patients did not provide adequate information to judge the state of the art of sonographic imaging.35 36

However, there are still some limitations of sonographic measurement of carotid stenosis. Although the display of the intrastenotic continuity of blood flow is improved by PDI, severe plaque calcification remains a major obstacle for adequate sonographic visualization of carotid stenosis in a few cases. It may also be difficult to exactly outline the vessel wall on transverse views at the narrowest site of the stenosis, potentially resulting in some error of measurement of area stenosis. In addition, difficulties in determining the long axis of the vessel at the site of stenosis, which is important for perpendicular measurement of diameter reduction, may represent a source of underestimation of the degree of stenosis depending on the geometry of the carotid bifurcation and the configuration of the stenotic plaque.

In conclusion, although the present study revealed superiority of PDI over CDFI in providing color contrast of the stenotic vascular lumen, in particular in high-grade calcified ICA stenosis, agreement with angiography was only slightly better for PDI when correlated with the ECST and CC methods. In comparison to both PDI and CDFI, which directly visualize the local diameter and area lumen reduction, angiographic classification either underestimated (NASCET method) or overestimated (ECST and CC methods) the degree of ICA stenosis, thus indicating that sonographic imaging probably provides the best approximation of the actual grade of stenosis. However, since the present study did not investigate the benefit of carotid endarterectomy with regard to the sonographic degree of stenosis, the potential role of PDI and CDFI in this respect needs further confirmation.


*    Selected Abbreviations and Acronyms
 
CC = common carotid
CDFI = color Doppler flow imaging
CW = continuous wave
ECST = European Carotid Surgery Trial
ICA = internal carotid artery
NASCET = North American Symptomatic Carotid Endarterectomy Trial
PDI = power Doppler imaging


*    Footnotes
 
Presented in part at the 48th Annual Meeting of the American Academy of Neurology, San Francisco, Calif, March 23-30, 1996.

Received February 21, 1997; revision received May 12, 1997; accepted June 5, 1997.


*    References
up arrowTop
up arrowAbstract
up arrowIntroduction
up arrowSubjects and Methods
up arrowResults
up arrowDiscussion
*References
 

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