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(Stroke. 1996;27:1965-1969.)
© 1996 American Heart Association, Inc.

Articles

Carotid Doppler Ultrasound Criteria for Internal Carotid Artery Stenosis Based on Residual Lumen Diameter Calculated From En Bloc Carotid Endarterectomy Specimens

Nijasri Suwanwela, MD; Ufuk Can, MD; Karen L. Furie, MD; James F. Southern, MD, PhD; Nancy R. Macdonald, RN; Christopher S. Ogilvy, MD; Calvin J. Hansen, MD; Ferdinando S. Buonanno, MD; William M. Abbott, MD; Walter J. Koroshetz, MD J. Philip Kistler, MD

the Stroke Service, Neurology Service (N.S., U.C., K.L.F., C.J.H., F.S.B., W.J.K., J.P.K.), Neurosurgery Service (C.S.O), Vascular Laboratory (N.R.M.), Vascular Surgery Service (W.M.A.), and Pathology Service (J.F.S.), Massachusetts General Hospital, Boston, Mass.

Correspondence to J. Philip Kistler, MD, Stroke Service/Cerebrovascular Section, Vascular Laboratory, Massachusetts General Hospital, Fruit St, Boston, MA 02114. E-mail Furie@helix.mgh.harvard.edu.

	Abstract

Top Abstract Introduction Subjects and Methods Results Discussion References

 
Background and Purpose Carotid duplex ultrasound is widely used to screen patients for carotid endarterectomy and if combined with MR angiography and transcranial Doppler may be an alternative to conventional angiography in the preoperative assessment. We have examined the correlation between Doppler velocities and the residual lumen diameters of internal carotid arteries from surgical pathological specimens to establish Doppler criteria for residual lumen diameter independent of percent stenosis.

Methods Ninety-one patients who underwent 99 carotid endarterectomies for internal carotid artery stenosis within 6 months of their carotid duplex ultrasound evaluation were studied. The endarterectomy specimens were removed en bloc, and the minimal residual lumen diameter was calculated by computer analysis. The sensitivity and specificity of the Doppler criteria for determining high-grade stenosis were calculated and receiver-operator curves generated.

Results Peak systolic velocity (PSV), end-diastolic velocity (EDV), and carotid index (peak internal carotid artery velocity/common carotid artery velocity) correlated with the residual lumen diameter. PSV >440 cm/s, EDV >155 cm/s, or carotid index >10 indicated a residual lumen diameter of 1.5 mm (specificity of 100% and sensitivity of 58%, 63%, and 30%, respectively). When these criteria were combined, the sensitivity increased to 72%. A PSV >200 cm/s combined with either an EDV >140 cm/s or a carotid index >4.5 has a sensitivity of 96% and a specificity of 61%.

Conclusions Doppler criteria can be both specific and sensitive for detecting a significant stenosis, defined as a 1.5 mm residual lumen diameter. By adjustment of the velocity criteria, it can be 100% specific or a highly sensitive test (96%).

Key Words: carotid endarterectomy • Doppler • pathology

	Introduction

Top Abstract Introduction Subjects and Methods Results Discussion References

 
Since Fisher's original observation in 1951, atherosclerotic stenosis at the origin of the ICA has been known as an important cause of cerebral infarction.^{1 2} In the last 10 years, several randomized controlled trials have evaluated the efficacy and safety of CEA. The results suggest that it effectively prevents ischemic strokes in symptomatic patients with 70% to 99% stenosis if it is performed with an acceptable surgical morbidity.^{3 4 5} Although recent evidence suggests that CEA may benefit selected asymptomatic patients with 60% to 99% carotid stenosis, the issue is still controversial.^{6 7 8} Unfortunately, cerebral angiography, the diagnostic technique these trials used to identify surgical candidates, carries its own risk and expense.^{9 10} Moreover, the endarterectomy trials have used different methods to measure the percentage of stenosis, and the measurements are subject to error. An imprecise determination of arterial borders may distort the true lumen diameter, and the severity of radiographic stenosis may inaccurately reflect the true stenosis as a result of effects of the limited planes of view used in angiographic imaging.

CDUS has become a standard noninvasive test for evaluating extracranial carotid disease.^{7 11 12 13 14 15 16 17 18 19 20 21 22} The advent of transcranial Doppler assessment of intracranial arterial flow and MRA combined with the known inherent risk of angiography has motivated us to evaluate patients preoperatively with the focused use of CDUS, transcranial Doppler, and MRA.²³ Thus, in many patients we have avoided conventional angiography before CEA. With this approach, the marker of severity becomes residual lumen diameter rather than percent stenosis. To date, however, Doppler criteria for establishing the severity of stenosis at the origin of the ICA have been mainly based on angiographic measurement of percent stenosis.^{24 25 26 27 28 29 30 31 32}

We believe that the residual lumen diameter of the carefully dissected ICA endarterectomy specimen removed en bloc at CEA is the most accurate measure of the degree of stenosis. If CEA is to be recommended on the basis of CDUS information, then it is imperative to establish precise Doppler criteria based on the correlation of Doppler signal with residual lumen diameter measured from intact CEA specimens.

We present the correlation between Doppler velocity measurements and the residual lumen diameters obtained from pathological examination of intact CEA specimens. The correlation between residual lumen diameter of a stenotic lesion at the origin of the ICA and quantitative spectral analysis of the carotid bruit and continuous-wave Doppler velocities is well established,^{33 34} but these tests have largely been replaced by range-gated pulsed Doppler ultrasonography combined with B-mode imaging (CDUS) of the origin of the ICA. Our study seeks to correlate PSV, EDV, and ratio of ICA to CCA velocity (carotid index) with the minimal residual lumen diameter of the stenotic lesion at the origin of the ICA.

	Subjects and Methods

Top Abstract Introduction Subjects and Methods Results Discussion References

 
We studied 91 consecutive patients who underwent CEA within 180 days (median, 10 days) after CDUS evaluation at the Massachusetts General Hospital between 1993 and 1995. Eight patients had severe bilateral carotid artery disease and underwent bilateral CEA, resulting in a total of 99 pathological specimens. Patients with severe tandem lesions in the distal ICA determined by MRA and CDUS were excluded. Patients with symptomatic cardiac valvular disease that was severe enough to affect flow at the bifurcation of the CCA were excluded from CEA. The atherosclerotic plaques were removed intact without disturbing the lumen.³⁵ En bloc specimens were sectioned at 0.2-cm intervals orthogonal to the luminal axis and then scanned into a computer for analysis. Sixty-nine patients (77%) did not have angiographic examination but underwent CEA on the basis of CDUS and MRA alone.

CDUS Examination
CDUS evaluation was performed by means of an ATL Ultramark 9 HDI scanner with 4-to-7– or 5-to-10–MHz linear transducers in the Vascular Laboratory at Massachusetts General Hospital. The hand-held probe was positioned first over the CCA in the lower part of the neck. By moving the probe distally and scanning in various planes, the examiner identified the carotid bifurcation, ICAs, and external carotid arteries. The vessels were scanned in both transverse and longitudinal planes to assess the severity of the stenosis and the relationship of the plaque to the vessel wall. Using color-flow B-mode real-time imaging as a map, the examiner placed the pulsed Doppler sample volume parallel to the stream of flow in the center of the vessels and set the Doppler angle of insonation at approximately 60 degrees. At the level of maximal stenosis of the ICA, the PSV and EDV were recorded. In addition, flow velocity in the CCA was recorded, and the ICA-CCA PSV ratio was calculated.

Pathological Specimens
Endarterectomy specimens were removed en bloc, promptly placed in formalin, and decalcified in nitric acid and EDTA. It had been shown in previous reports that fixation does not change the residual diameter of the specimens appreciably.^{14 34} The length, width, and thickness of each specimen were measured in centimeters with a ruler, and a photographic image (Kodachrome, Kodak) was taken. The specimens were then sectioned manually with a razor blade and laid in series. Each section was 0.2 cm thick. Another photographic image for each specimen was taken. Site and shape of the residual lumen, as well as plaque characteristics such as intramural hemorrhage, ulceration, and intraluminal thrombosis, were recorded. The sections with the smallest residual lumens were scanned by a slide scanner, and the images were stored on floppy diskettes. For each specimen, the area of maximal stenosis was measured and the minimal residual luminal diameter was calculated digitally with the use of an Aldus Photostyler computer program. Residual lumen diameter measurements were rounded to the nearest 0.1 mm such that 0.14 mm was recorded as 0.1 mm and 0.15 mm recorded as 0.2 mm.

	Results

Top Abstract Introduction Subjects and Methods Results Discussion References

 
In 34 patients (37 surgical specimens), ipsilateral ischemic symptoms were not found. Patients with symptomatic carotid disease manifested with either stroke (22%) or transient ischemic attack (29%). Transient monocular blindness occurred in 9% (Table 1). The residual lumen diameter ranged from 0.21 to 2.72 mm (mean, 1.08 mm). Residual lumen correlated well with PSV, EDV, and carotid index (Fig 1). Stenotic lesions with residual lumen diameters 1.5 mm were found in 76 carotid specimens (77%). Receiver-operator characteristic curves were generated to predict a residual lumen diameter 1.5 mm. These curves describe the sensitivity and specificity of each of the ultrasound criteria (Fig 2).

View this table: [in this window] [in a new window]   Table 1. Clinical Findings of the Studied Patients

View larger version (49K): [in this window] [in a new window]   Figure 1. Correlation between Doppler criteria (PSV, EDV, and carotid index) and residual lumen diameter.

View larger version (17K): [in this window] [in a new window]   Figure 2. Receiver-operator curves (ROC) of PSV, EDV, and carotid index for residual lumen diameter 1.5 mm.

PSVs >440 cm/s, EDVs >155 cm/s, or a carotid index >10 always indicated a residual lumen diameter 1.5 mm (specificity of 100% and sensitivity of 58%, 63%, and 30%, respectively). CDUS of ICA origins with residual lumen diameters 1.5 mm almost always demonstrated a PSV >220 mm/s and an ICA-CCA ratio >3.5 (sensitivity of 99% and specificity of 26% and 35%, respectively). The sensitivity approached 100% if one patient who had very low velocities but very tight carotid stenosis demonstrated by B-mode ultrasound was excluded. Pathologically, this patient had a residual lumen diameter <0.5 mm. The low systolic flow velocity and low carotid index in this patient were likely secondary to the reduction of flow in the critically narrowed ICA. The sensitivity, specificity, positive predictive value, negative predictive value, and accuracy of various Doppler criteria are shown in Table 2. Fourteen patients had an occluded or hemodynamically significant stenotic lesion of the contralateral ICA origin. None of these patients had an ipsilateral carotid stenosis with a calculated residual lumen diameter >1.5 mm and a PSV >440 cm/s.

View this table: [in this window] [in a new window]   Table 2. Various Doppler Criteria to Determine Residual Lumen 1.5 mm and Their Sensitivities, Positive Predictive Value, Negative Predictive Value, and Accuracies

If each of the three criteria—PSV >440 cm/s, EDV >155 cm/s, or carotid index >10—was present, the 100% specificity was preserved for a residual lumen diameter 1.5 mm but the sensitivity increased to 72%. Since ultrasound provides a noninvasive screening test, establishing highly sensitive criteria is paramount. Our data indicate that combining a PSV >200 cm/s with either an EDV >140 or a carotid index >4.5 produced 96% sensitive and 61% specific criteria for detecting a lumen 1.5 mm.

	Discussion

Top Abstract Introduction Subjects and Methods Results Discussion References

 
These data define the sensitivity and specificity of CDUS in our laboratory to detect a stenotic lesion at the origin of the ICA with a minimal residual lumen diameter 1.5 mm. Our data demonstrate that each of the following three velocity criteria have 100% specificity for detecting a minimal residual lumen 1.5 mm: PSV >440 cm/s, EDV >l55 cm/s, or carotid index >10. However, the sensitivity of the combination of these criteria is only 72%. The highly specific criteria clearly signify a residual lumen diameter 1.5 mm. Because a contralateral hemodynamically significant stenosis results in an ipsilateral increase in volume of flow and PSV, we reviewed the data for false-positive PSVs in patients with these hemodynamically significant contralateral lesions. None of the 14 patients with contralateral carotid occlusion or hemodynamically significant stenosis had false-positive elevations in their ipsilateral PSV. One patient with a contralateral ICA origin occlusion had an ipsilateral PSV of 561 cm/s and a residual lumen of 1.54 mm, which when rounded to the nearest 0.1 mm was recorded as 1.5 mm. Theoretically, contralateral carotid occlusion could result in false-positive PSVs (>440 cm/s), but this did not occur in this series. By contrast, our data also outline highly sensitive (96%) but only moderately specific CDUS criteria to detect the same minimal lumen diameter. These highly sensitive criteria combine a PSV >200 cm/s with either an EDV >140 cm/s or a carotid index >4.5 mm. The sensitivity of these criteria improved to 100% when B-mode information of a very tight stenosis was added. Our highly sensitive criteria allow the detection of all patients with a lumen diameter 1.5 mm but also identify some patients who do not have a high degree of stenosis. When the suspicion of a significant stenosis is raised by very sensitive criteria, ancillary tests examining the hemodynamic significance of the lesion or noninvasive imaging studies, eg, transcranial Doppler, MRA, or CT angiography, may help to improve the specificity. They are therefore under investigation in our laboratory. In addition, the use of new ultrasound techniques such as power Doppler may provide additional information regarding the vascular wall and may be useful as a noninvasive method of measuring the residual lumen.^{36 37 38} But short of conventional angiography, the preocclusive lesion with a trickle of flow through it cannot reliably be distinguished from an occlusion by Doppler or MRA.

Our CDUS criteria for high-grade stenosis defined as 1.5 mm residual lumen are consistent with CDUS data reported in the literature.^{27 31} In addition, our data correlating the minimal lumen diameter of the intact endarterectomy specimen to PSV, EDV, and carotid index obtained from CDUS are compatible with the data of our previous study correlating the minimal residual lumen diameter of the intact endarterectomy specimen with continuous-wave Doppler peak frequency shifts and carotid index.³³

There are two compelling reasons to correlate Doppler data with the actual residual lumen diameter obtained from a pathological specimen removed en bloc at CEA. First, the minimal residual lumen diameter assessed by examination of the intact endarterectomy specimen may be the most accurate method for quantifying the severity of a stenotic lesion at the origin of the ICA. Natural history studies and randomized endarterectomy trials of symptomatic carotid stenosis showed an increased ischemic event rate in the more severely stenotic lesions.^{3 4 5 39 40 41} When a 1.5-mm residual lumen diameter target is used, it corresponds to a 60% to 75% stenosis by NASCET criteria, which use a 4- to 6-mm distal ICA lumen diameter. According to our transcranial Doppler data, hemodynamic change secondary to a carotid stenosis usually occurs when the residual lumen diameter is <1.5 mm (U. Can, K. Furie, N. Suwanwela, J. Southern, N. Macdonald, C. Ogilvy, F. Buonanno, W. Koroshetz, J.P. Kistler, unpublished data, 1996). Therefore, we used a residual lumen diameter of 1.5 mm as a cutoff point for significant stenosis and developed Doppler criteria for it. However, ischemic symptoms, especially transient ones, do occur in patients with carotid stenosis that have residual lumen diameter >1.5 mm. Of the 62 patients with symptomatic carotid disease, 12 had carotids with a minimal lumen diameter >1.5 mm. Only 3 of the 12 had stroke in the >1.5 mm group compared with 21 of the 50 patients in the 1.5 mm residual lumen group.

The second and most compelling reason for correlating the actual residual lumen diameter with CDUS criteria is that conventional angiography is less likely to be used in the future to estimate percent stenosis in symptomatic or asymptomatic patients. Angiography has approximately a 0.5% to 1% risk of stroke or death.^{3 4 5 6 7 8 9 10} This has clear effects on the decision to perform CEA in asymptomatic patients in whom the risk reduction is modest and may be offset by the increased complication rate. Although traditionally held as the gold standard, angiographic measurements may be inaccurate and poorly reproducible. In addition, the various methods the randomized trials used to measure the percent stenosis confuse the selection of patients for surgery. The distal ICA lumen was the standard denominator in the NASCET and the Asymptomatic Carotid Atherosclerosis Study,^{3 7} while the estimated carotid bulb diameter was used in the Medical Research Council European Carotid Surgery Trial.⁴ For these reasons we and others have been proceeding to CEA based on CDUS and transcranial Doppler results complemented by MRA or CT angiography.^{23 42 43 44} Unlike angiography, none of these noninvasive methods directly measures percent stenosis. Establishing ultrasound criteria to define the minimal residual lumen diameter measured in our study provides us with a standard that obviates the need for angiographic criteria (percent stenosis) to select CEA patients. In the future, we hope to correlate transcranial Doppler and MRA findings with minimal residual lumen diameter to establish noninvasive testing modalities as adjuncts to our CDUS criteria. We anticipate that these noninvasive tests will not only increase the specificity of our highly sensitive CDUS criteria but also identify intracranial arterial lesions that may influence the outcome of CEA.

	Selected Abbreviations and Acronyms

 

CCA = common carotid artery CDUS = carotid duplex ultrasound CEA = carotid endarterectomy EDV = end-diastolic flow velocity ICA = internal carotid artery MRA = magnetic resonance angiography NASCET = North American Symptomatic Carotid Endarterectomy Trial PSV = peak systolic flow velocity

	Acknowledgments

 
This study was supported in part by the Eliot B. Shoolman Fund, the Merrill Lynch Fund for cerebrovascular disease, the Paul O'Neill Fund, the Vera and J.W. Gilliland Fund, and by generous gifts from Robert P. Gwinn and Max Rohlich. Drs Suwanwela and Can are John Conway Fellows in cerebrovascular disease. We acknowledge with appreciation the contribution of the Vascular Laboratory technicians: C. Oliver, RN, RVT; S. Croteau, RN, RVT; V. McCallum, RN, RVT; D. Henry, RVT; C.X. He, RVT; D. Moller, RDMS; and N.R. Macdonald, RN, RVT.

Received May 30, 1996; revision received August 16, 1996; accepted August 16, 1996.

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