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(Stroke. 1995;26:434-438.)
© 1995 American Heart Association, Inc.

Articles

Distinguishing Carotid Artery Pseudo-Occlusion With Color-Flow Doppler

Presented at the Society of Vascular Technology 17th Annual Conference, August 3-7, 1994, Orlando, Fla.

Scott S. Berman, MD, RVT; Jenifer J. Devine, RN, RVT; Luke S. Erdoes, MD Glenn C. Hunter, MD

From the Section of Vascular Surgery, University of Arizona Health Sciences Center, Tucson, Ariz.

Correspondence to Scott S. Berman, MD, RVT, Assistant Professor of Clinical Surgery, Department of Surgery, University of Arizona Health Sciences Center, 1501 N Campbell Ave, Suite 5406, Tucson, AZ 85724.

	Abstract

Top Abstract Introduction Materials and Methods Results Discussion References

 
Background and Purpose This study was undertaken to determine the impact of color-flow Doppler on the accuracy of noninvasive carotid imaging for distinguishing an internal carotid artery pseudo-occlusion (string sign) from a complete occlusion.

Methods From January 1985 to January 1994, review of noninvasive vascular studies, arteriograms, and operative reports of 26 consecutive patients undergoing 27 carotid endarterectomies for carotid pseudo-occlusion was performed. Further review was conducted of all patients identified with carotid occlusion by noninvasive testing who underwent confirmatory arteriography during the same interval.

Results Conventional gray-scale duplex scanning (January 1985 to December 1989) correctly identified 3 of 11 (27%) pseudo-occluded internal carotid arteries compared with 15 of 16 (94%) internal carotid artery pseudo-occlusions correctly identified by color-flow Doppler (January 1990 to June 1994) (P<.01). Similarly, carotid occlusion was more accurately identified by color-flow Doppler (33 of 33, 100%) compared with gray-scale duplex scanning (19 of 27, 90%) (P<.01).

Conclusions The addition of color-flow Doppler to the duplex evaluation of the extracranial carotid circulation improves the accuracy of distinguishing carotid pseudo-occlusion from the occluded internal carotid artery and may obviate the need for arteriography to identify patients with this critical level of carotid stenosis.

Key Words: carotid artery diseases • ultrasonics

	Introduction

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Performance of carotid endarterectomy (CEA) without preoperative arteriography is gaining acceptance as literature supporting this approach accumulates.^{1 2} The widening application of this changing trend hinges on the accuracy achievable with noninvasive duplex imaging of the extracranial carotid system.^{3 4} Moreover, the favorable results of the randomized trials supporting CEA for symptomatic patients with greater than 70% stenosis have kindled enthusiasm for this management regimen.^{5 6} Despite the growing popularity of CEA without arteriography, distinguishing carotid artery pseudo-occlusion from occlusion by noninvasive imaging, particularly in patients with hemispheric symptoms, is considered a limitation of Doppler-based technologies and usually mandates confirmatory arteriography.^{7 8 9 10} Carotid pseudo-occlusion has numerous pseudonyms including preocclusive stenosis, the carotid slim sign, and the carotid string sign, all of which attempt to describe the appearance of the vessel based on contrast arteriography. This study reports our experience comparing duplex imaging with and without color- flow Doppler in distinguishing carotid artery pseudo-occlusion from occlusion.

	Materials and Methods

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The operative reports, noninvasive vascular lab records, and arteriography results of consecutive patients undergoing CEA from January 1985 through June 1994 were reviewed. Patients who underwent CEA for carotid pseudo-occlusion formed the basis of this review. These patients were further subdivided into two time periods, depending on the availability and use of color-flow Doppler in the noninvasive examination of the extracranial carotid system. The gray-scale group comprised patients studied from January 1985 until December 1989, while the color-flow group consisted of patients evaluated from January 1990 through June 1994. Review of noninvasive vascular lab data for both time periods was performed to further determine the number of nonoperative patients in whom the diagnosis of carotid occlusion was established by noninvasive imaging and confirmed by contrast arteriography.

In the gray-scale group, examination of the bilateral extracranial carotid system was performed using an Ultrasonics 750 SD duplex imager (Ultrasonics Inc). With a 7.5-MHz linear array transducer imaging in the longitudinal plane, B-mode and Doppler data were acquired simultaneously. The examination commenced with the common carotid artery and traversed cephalad into the carotid bifurcation. B-mode images, spectral waveforms, and peak systolic frequency data were obtained from the common, external, proximal, and distal internal carotid arteries. The examination was completed by obtaining B-mode images of the carotid vessels and the bifurcation in the transverse plane. Inability to obtain a satisfactory pulsatile spectral waveform from the bifurcation or internal carotid artery or findings consistent with carotid artery occlusion were verified by insonating the vessels with a continuous-wave transducer (5 MHz). Carotid occlusion was diagnosed by applying standard duplex criteria.¹¹ Briefly, carotid artery occlusion was suspected when (1) absence of flow was encountered in the internal carotid artery and plaque or thrombus filled the lumen by B-mode imaging, (2) an audible or visible "thump" was obtained from the thrombus-filled internal carotid artery, (3) a dampened high-resistance waveform was obtained from the ispsilateral common carotid artery, (4) the wavefrom obtained from the ipsilateral external carotid artery was "internalized" in appearance, and/or (5) the frequency obtained from the contralateral common carotid artery was significantly greater than that obtained from the ipsilateral common carotid artery. The pseudo-occlusion classification was applied to the duplex results when a continuous harsh audible Doppler signal was obtained from the bifurcation and internal carotid artery in the absence of pulsatile flow.

Carotid evaluation in the color-flow group was performed with either the ATL Ultramark 9 or the ATL Ultramark 9HDI (Advanced Technology Labs) imager using a similar imaging protocol. As with the gray-scale group, traditional duplex criteria were applied to diagnose carotid occlusion. However, if carotid occlusion was suspected after complete examination of the extracranial system using standard settings (peak repetition frequency [PRF], 5000 Hz; wall filter [WF], 100 Hz) and the high-flow settings (PRF, variable; WF, 100 Hz), the examination was repeated with settings sensitive to low flow. The PRF remained at 5000 Hz, and the WF was reduced to 50 Hz. Specific attention was directed to the proximal and distal internal carotid artery, where low flow may be detected either audibly or by the presence of a wisp of color. Either finding suggested the presence of a patent, preocclusive vessel. Once located by the presence of color, obtaining a spectral waveform was possible with either a linear array or continuous-wave transducer. The availability of color-flow Doppler permitted the detection of flow by the presence of color, therefore obviating the need for blind placement of the sample volume in the patent portion of the vessel.

Digital subtraction arteriography was performed by neuroradiologists using a Toshiba DFP 50A prototype system with a 14-in. image intensifier mounted on a universal C-arm; the system was developed at our institution.¹² When carotid pseudo-occlusion or symptomatic occlusion was suspected on the basis of the noninvasive examination, adjunctive techniques were applied during arteriography including prolonged filming sequences and trickle flow to optimize visualization of a patent vessel if present. Correlation between noninvasive and arteriography findings was determined using the statistic described by Cohen¹³ as well as the standard descriptive parameters of sensitivity, specificity, positive predictive value, and negative predictive value. Comparison of these results between the precolor and color groups were made using the Mantel-Hanzel ² analysis.¹⁴

	Results

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During the period of this review, 26 patients underwent 27 CEAs for carotid pseudo-occlusion. This group represents 10% of the 257 consecutive CEAs performed at the University of Arizona Health Sciences Center during the same time interval. The indications for the 11 CEAs performed in the gray-scale group comprised transient ischemic attacks (TIAs) in 6 patients, acute stroke (<6 weeks) in 2 patients, asymptomatic stenosis in 2 patients, and prior stroke in 1 patient. In the color-flow group, the 16 CEAs were done for TIAs in 9 patients, acute strokes in 3 patients, and prior strokes and asymptomatic disease in 2 patients, respectively. One CEA in the color-flow group was performed for a symptomatic recurrence 5 years after endarterectomy performed at another institution. Operative findings confirmed the patency of the internal carotid artery in all 26 cases.

Correlation of noninvasive examinations and arteriography during our early experience with gray-scale duplex scanning achieved a high level of agreement, with =0.695±0.049. The correlation between our more recent color-flow Doppler scanning results and arteriography achieved =0.670±0.067.

For patients examined with gray-scale duplex scanning alone, carotid pseudo-occlusion was correctly identified in 3 of 11 vessels (27%) by noninvasive imaging (Table 1). Of the remaining 8 patients with pseudo-occlusion, 5 were designated as occlusions by duplex and 3 had technically difficult examinations that limited the certainty of the noninvasive findings. In the same time period, carotid occlusion was correctly diagnosed by gray scale and was confirmed by arteriography in 19 of 206 vessels studied by both imaging techniques (Table 2). Included in this group are two vessels deemed patent by gray scale but found to be occluded by arteriography. Both asymptomatic patients underwent arteriography within 24 hours of the duplex examination; therefore, interval occlusion between the examinations was unlikely.

View this table: [in this window] [in a new window]   Table 1. Diagnosis of Pseudo-Occlusion by Gray-Scale Duplex Scanning

View this table: [in this window] [in a new window]   Table 2. Diagnosis of Occlusion by Gray-Scale Duplex Scanning

In the color-flow Doppler group, carotid pseudo-occlusion was correctly identified by duplex scanning in 15 of 16 vessels (94%) confirmed by arteriography (Table 3). This result was significant when compared with the results for gray-scale duplex scanning as illustrated in Table 4. Furthermore, carotid occlusion was correctly diagnosed in 33 vessels out of 200 studied by both color-flow duplex and arteriography (Table 5). As with carotid pseudo-occlusion, diagnosis of carotid occlusion with color-flow Doppler was more accurate compared with gray-scale duplex (Table 6).

View this table: [in this window] [in a new window]   Table 3. Diagnosis of Carotid Pseudo-Occlusion With Color-Flow Doppler Imaging

View this table: [in this window] [in a new window]   Table 4. Comparison of Color-Flow Doppler Imaging and Gray-Scale Duplex Scanning in Identifying Carotid Pseudo-Occlusion

View this table: [in this window] [in a new window]   Table 5. Diagnosis of Carotid Occlusion by Color-Flow Doppler Imaging

View this table: [in this window] [in a new window]   Table 6. Comparison of Color-Flow Doppler Imaging and Gray-Scale Duplex Scanning in Identifying Carotid Occlusion

	Discussion

Top Abstract Introduction Materials and Methods Results Discussion References

 
Support for the performance of carotid endarterectomy without preoperative contrast arteriography is mounting in the literature, largely due to the accuracy available with noninvasive carotid imaging.^{2 3} However, as Horn et al³ have cautioned, this approach is contingent on the availability of experienced technologists and the verification of the accuracy of the noninvasive laboratory. Despite the growing acceptance of this approach, distinguishing carotid pseudo-occlusion from occlusion by noninvasive testing is considered inadequate and still mandates confirmation by contrast arteriography in most centers. Our results suggest that the addition of color-flow Doppler to the noninvasive carotid evaluation may enhance distinguishing these two entities and obviate further the need for contrast arteriography.

Previous reports of duplex imaging to diagnose carotid pseudo-occlusion are limited and are derived from experience with carotid occlusion. Prior to the availability of color-flow Doppler, carotid pseudo-occlusions comprised the false-positive examinations for carotid occlusion because it was difficult to distinguish these two entities by the available technology. Bornstein et al⁷ reported the results of 124 carotid arteries examined by gray-scale duplex scanning and arteriography. One false-negative and four false-positive occlusions by duplex were included in that series, yielding a sensitivity of 96%, specificity of 95%, positive predictive value of 86%, and negative predictive value of 99%. The authors considered these results inadequate to recommend CEA without arteriography. A similar conclusion was reached by Bridgers⁸ in his review of 58 patients in whom the diagnosis of occlusion was suggested by gray-scale duplex imaging. He further delineated that in patients with symptoms, the diagnosis of occlusion by duplex was not accurate enough to preclude arteriography because seven false-positives occurred in 25 patients in this subgroup. Since the management of patients with symptoms hinges on the presence of a patent vessel, Bridgers encouraged verification with arteriography when the diagnosis of carotid occlusion is suspected based on duplex results.

More recent reports of the utility of noninvasive imaging in diagnosing carotid occlusion have included experience with color-flow Doppler and offer dissenting conclusions.^{15 16} In a large review of their noninvasive experience, Kiell et al¹⁵ compared gray-scale and color-flow Doppler techniques for diagnosing carotid occlusion. Although no statistical comparison of the two techniques was provided, the overall accuracy (91% versus 86%) and specificity (97% versus 89%) of color-flow Doppler exceeded that of gray-scale in detecting carotid occlusion. In a similar review of experience with both gray-scale and color-flow imaging, Kirsch et al¹⁶ failed to establish an improvement in positive predictive value attributable to color-flow Doppler alone in detecting carotid occlusion. However, positive predictive value was significantly greater for diagnosing occlusion in the later 2 years of this study, when more modern color-flow equipment was available and experience with the technology had accumulated.

Our data confirm the findings of previous studies that gray-scale duplex is not adequate for diagnosing carotid occlusions. Moreover, the improvement in diagnosing carotid occlusion using color-flow Doppler suggested by Kiell et al¹⁵ and by Kirsch et al¹⁶ is further supported by the results of this study. It is likely that limited experience with color-flow Doppler in the early time period reviewed in the study of Kirsch et al accounts for the lack of statistical significance that evolves when the later data reported in their study are considered separately.

Noninvasive diagnosis of pseudo-occlusion using color-flow Doppler imaging has been addressed in one previous report. Comeaux and Harkrider¹⁷ detail the diagnosis and outcome of 2 patients found to have symptomatic, near total occlusion of the internal carotid artery by color-flow Doppler imaging. Patency of the vessel was confirmed in one case, but digital subtraction arteriography demonstrated occlusion of the carotid bifurcation in the second case. Repeat noninvasive examination supported the original finding of a patent vessel, and a successful CEA was performed and confirmed the color-flow Doppler impression. A similar course ensued in the single case of carotid pseudo-occlusion diagnosed with gray-scale duplex scanning reported by Sullivan and Patterson.¹⁸ These reports underscore the inadequacy of arteriography alone as the "gold standard" in cases of suspected pseudo-occlusion.

Our study is unique in that the specific phenomenon of carotid pseudo-occlusion was examined. This diagnosis is traditionally arrived at by the appearance of the vessel on contrast arteriography. Typically, there is a high-grade stenosis of the proximal internal carotid artery that results in slow flow and collapse of the distal internal carotid artery, giving the appearance of a hypoplastic distal vessel. There may even be an arteriographic segmental occlusion of the proximal internal carotid artery with reconstitution of the distal vessel. To date, there are no noninvasive criteria to designate this pathology, since the diagnosis is historically established with arteriography and confirmed at operation. It must be emphasized that this terminology is descriptive and probably has no bearing on outcome other than to signify a high-grade stenosis.¹⁹

Color-flow Doppler offers the ability to detect low flow in difficult imaging situations, since flow can be detected without the accurate placement of a sample volume. When occlusion is suspected based on the usual findings with gray-scale B-mode imaging and spectral analysis, color-flow Doppler permits further evaluation of the proximal and distal internal carotid artery. With the addition of color-flow Doppler to the examination and by setting the instrument sensitivity for high flow, a turbulent jet may be visualized and further interrogated for Doppler spectra (Fig 1). Alternatively, the noninvasive color-flow instrument is set to detect very low flow by lowering the WF threshold. In our experience, a pseudo-occlusion will demonstrate a trickle of flow in the distal internal carotid artery identified by a wisp of color (Fig 2). Once localized, Doppler spectral analysis can be performed, often demonstrating a low peak frequency. Using this technique, we have correctly identified 15 of 16 (94%) carotid pseudo-occlusions.

View larger version (198K): [in this window] [in a new window]   Figure 1. Color-flow Doppler image obtained with high-flow sensitivities (peak repetition frequency, variable; wall filter, 100 Hz) permits identification of flow by presence of color (A) and placement of Doppler gate to acquire frequency data to distinguish the carotid string sign displayed on arteriography (B).

View larger version (226K): [in this window] [in a new window]   Figure 2. Color-flow Doppler imaging with instrument sensitivities adjusted for low flow (peak repetition frequency, 5000 Hz; wall filter, 50 Hz) identifies flow by the presence of color (A) in what appears to be an occluded carotid artery by traditional duplex criteria but by arteriography (B) and at surgery is a carotid artery pseudo-occusion.

Our results are further supported by the recent report from Görtler et al,²⁰ who prospectively evaluated similar technical adjustments in color-flow imaging in order to identify subtotal stenoses. Of the descriptive color-flow Doppler criteria they analyzed, "distal colour filling" was most useful in distinguishing subtotal stenoses from occlusions. This terminology was applied when color signal was detected beyond a stenosis with low-flow color-flow Doppler settings and parallels the techniques described in the present report.

An important caveat that must be mentioned in this discussion revolves around the level of experience of the noninvasive laboratory. In our own case, our three technologists have over 20 years of experience with noninvasive imaging, and our laboratory has maintained a quality assurance program to verify our results with arteriography. More importantly, a weekly multidisciplinary conference with the vascular lab staff, neurologists, neuroradiologists, and vascular surgeons reviews cerebrovascular cases, including all imaging studies, and brings into perspective the diagnostic imaging results. Certainly the improved accuracy of identifying carotid pseudo-occlusion in the color-flow era may reflect a plateau of our learning curve; however, by the end of the gray-scale period, our three technologists each had acquired 6 years of experience with carotid testing, and the accuracy of identifying carotid pseudo-occlusion was perceived to be unchanged over the course of this interval. Our numbers are too small to accurately compare results within the gray-scale time period. It is also impossible to determine whether our technologists are more diligent in looking for pseudo-occlusion now as compared with 10 years ago. Moreover, we have not appreciably changed laboratory staff over the course of this review, yet we continue to document carotid pseudo-occlusion with the same frequency whether by duplex scan or arteriography. One further point that deserves emphasis is the confidence level of the noninvasive examination itself. If the technologist believes that the examination was technically difficult, further imaging with arteriography is warranted, particularly for symptomatic patients. Given these constraints, this study confirms that noninvasive imaging using color-flow Doppler technology is adequate for diagnosing carotid artery occlusion and pseudo-occlusion and ultimately that arteriography may be avoided in patients for whom these diagnoses are considered.

Received September 7, 1994; accepted December 21, 1994.

	References

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This Article Abstract Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Request Permissions Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Berman, S. S. Articles by Hunter, G. C. Search for Related Content PubMed PubMed Citation Articles by Berman, S. S. Articles by Hunter, G. C.