Duplex sonography of the carotid arteries

Duplex Sonography of the Carotid Arteries

By Michael L. Robinson

T HE ETIOLOGY of stroke is multifactoral and incompletely understood. Atheroscle-

rotic stenosis of the extracranial carotid artery has been shown to be one of these factors.’ The presence of a hemodynamically significant stenosis of the carotid bifurcation is generally ac- cepted as an indication for surgical intervention in symptomatic patients as well as in selected asymptomatic patients.‘.” The goal of noninvasive testing is to screen patients at high risk for the presence of carotid occlusive disease. The screened population generally falls into the following groups: (1) patients with hemispheric symptoms such a transient ischemic attack or stroke; (2) symptomatic patients with nonlater- alizing symptoms; (3) patients suspected of having vertebrobasilar symptoms; (4) patients with a carotid bruit; (5) patients with evidence of significant vascular disease elsewhere (ie, heart, legs); (6) patients who are being restud- ied for progression of disease; and (7) as a follow up in patients who have had a previous carotid endarterectomy.” The clinical use of duplex sonography as a screening tool is a result of its ability to detect significant stenosis with a high degree of sensitivity, coupled with a high specificity in excluding disease which may obvi- ate the need for invasive testing. For these reasons, duplex sonography has almost com- pletely supplanted all other noninvasive modali- ties for examining the extracranial carotid arteries. In this article, the technique of performance of the examination, diagnostic criteria for interpretation, and pitfalls that may lead to errone- ous interpretation will be discussed.

of the common carotid artery (CCA), carotid bifurcation, and the internal carotid artery (ICA) in longitudinal and transverse planes. This “survey” of the vessel allows for a qualitative determination of amount and distribution of plaque as well as preparing the sonographer to deal with problem areas of the vessel such as kinks, heavily calcified areas, and unusual anatomic variants.

While imaging the vessel in the longitudinal plane, the range gated Doppler sample volume is placed in the lumen of the CCA and slowly advanced to the carotid bifurcation. A small sample size of around 2 mm is suggested to minimize the effects of nonlaminar flow near the vessel wall. An angle of between 30” and 60” is maintained by steering the Doppler beam or by changing transducer position and adjusting the angle of the cursor to be parallel to the flow lumen of the vessel. Doppler angles outside this range may give spurious results.’ A consistent Doppler angle is necessary for reproducibility, since it has been shown in studies using cali- brated phantoms that velocity measurements may vary significantly at different levels of angle correctionh Representative images are then recorded showing the Doppler spectrum with the position of the cursor in the vessel and the angle of insonation of the vessel included. The Doppler waveforms should be displayed in the form of velocities instead of frequency shifts. This compensates for inconsistencies in angle of insonation and for differences in transducer frequency. The use of velocity-based parame-

TECHNIQUE ABBREVIATIONS

In my laboratory, carotid studies are performed on four duplex machines manufactured by the same vendor. Two of these are color Doppler and two are conventional black and white units. The technique used is essentially the same whether using color or not, with some minor modifications as described below.

CCA, common carotid artery; ECA, external carotid artery; ICA, internal carotid artery; ROC, receiver operating characteristic

A 5 or 7 MHz linear array transducer is used to scan the carotid artery from the clavicle to the angle of the mandible in real time with hard copy documentation of representative segments

From the Depavtment of Radiology, The Reading Hospital and Medical Center, West Reading, PA.

Address reprint requests to Michael L. Robinson, MD, Department of Radiology, The Reading Hospital and Medical Center, Sixth and Spruce Sts, West Reading, PA 19603.

Copyright 8 1992 by W.B. Saunders Company 0037-198X192/2701-0003$5.00/0

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Seminarsin Roenfgenology, Vol XXVII, No 1 (January), 1992: pp 17-27 17

18 MICHAEL L. ROBINSON

ters also allows for better comparison of results in follow-up studies.’ This procedure is then extended from the CCA through the carotid bulb and ICA as far as possible, and repeated for the origin and proximal few centimeters of the external carotid artery (ECA). Great care should be taken to ensure that all segments of the artery are insonated because velocities and waveform may normalize within a short distance downstream from a stenosis.‘Therefore, a small gap of coverage could potentially fail to detect a significant lesion. Any high-velocity jet must be thoroughly investigated to assure recording of the peak velocity. The vertebral arteries are then identified, and representative images are obtained with the Doppler waveform document- ing the presence of and direction of flow. Because of the location of these arteries within the foramen transversarium of the vertebra, only short segments of the arteries can be imaged and stenosis cannot be reliably diag- nosed. Lack of flow or the presence of retro- grade flow have been shown to be very accurate indicators of vertebral artery occlusion and subclavian steal, respectively.’

A worksheet is helpful for recording peak velocities, location and severity of plaque, and any unusual features such as kinks or tortu- ousity of the vessel or areas that cannot be adequately studied secondary to calcified plaque, overlying scar, or body habitus. It is also very useful for comparing serial studies in the same

patient. In my practice, an ultrasonography technolo-

gist performs the examination as described above, fills out the worksheet during the examination, and obtains the hardcopy images. A physician then reviews the data and images and checks each patient by briefly rescanning the vessels to determine the appropriateness of the data. If the physician disagrees with the findings, new images and velocities are recorded. Results are immediately reported to the refer- ring physician in cases where a critical stenosis is detected. Not all practices will have the luxury of physician participation during the examination. In these cases, the study should be video- taped for review by the physician during interpretation. Physicians should not hesitate to call

a patient back for further examination if the study is inconclusive.

If color Doppler is available, there are some minor modifications of the above protocol. Fol- lowing the real-time imaging survey, a color Doppler survey is made. It is important that the color scale be set to the appropriate sensitivity to avoid missing lesions. This can be accom- plished by adjusting the scale until some area of the CCA shows color conversion during systole. For the duplex units in our lab, this is usually at approximately 0.46 m/s. Similar to black and white imaging, the angle of insonation of the vessel is important and it is necessary to image the vessel at an angle of 60” or less. This may require frequent changes in transducer position or angulation of the beam in tortuous vessels. The spectral analysis is performed with color superimposed on the real-time image, and any area of color abnormality is carefully interro- gated for spectral abnormalities. Color imaging can be very helpful because it improves visualization of the flow lumen and consequently allows for more accurate placement of the cursor and correction of Doppler angle. It greatly simplifies studying a tortuous vessel, where incorrect Dop- pler angle correction can lead to spurious results. In vessels with calcified plaque, which may frustrate attempts to obtain a spectral tracing, color imaging will rapidly show the best window for imaging. Additionally, the high-velocity jet can be seen in eccentric stenoses, allowing for precise placement of the sample volume and angle correction. Although color Doppler is not necessarily essential, its use does shorten examination time and increase diagnostic confidence in difficult cases.

Polak et al.“’ advocate using color imaging to map the vessel, obtaining spectral analysis only from those areas shown by color to contain the highest mean velocities. Although this method seems very attractive because of the simplicity and time savings, there are potential pitfalls. It assumes that the highest mean velocity as represented by color intensity change is the site of peak systolic velocity, which may or may not be true. With traditional spectral analysis, a Dop- pler sample volume is “walked” through the vessel with constant attention to the Doppler angle, whereas the color image is made with the entire vessel imaged at one angle, possibly

CAROTID DUPLEX SONOGRAPHY

introducing significant error in the calculated mean velocities if the vessel curves with respect to the transducer. Also, an area of extremely high velocity might cause aliasing with misassign- ment of colors which might be interpreted as nothing more than turbulence.” Although aliasing is obvious when performing spectral analysis, it is difficult to detect at times in a color image unless the scale is adjusted to a lower sensitivity than is advocated. For these reasons I advocate the traditional method of performing spectral analysis from the entire vessel until further studies confirm Polak’s method.

NORMAL EXAMINATION

Interpretation of the Doppler spectrum de- pends on a knowledge of the appearance of the normal waveform. This wave consists of the distribution of velocities within the sample volume plotted as a function of time. In the ICA, there is a rapid increase in velocity during systole, with a slightly rounded peak represent-

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ing the peak systolic velocity and a narrow distribution of velocities secondary to laminar flow. This results in a “window” or clear area beneath the systolic peak, indicating that most of the blood is flowing at the same velocity. Because the ICA supplies the brain, which is a low-resistance system, there is continuous antegrade flow during diastole (Fig 1A). The ECA, on the other hand, supplies a high-resistance muscular bed. Its systolic upstroke is brisk, its peak sharper, and its downstroke more abrupt. There is often a brief period of flow reversal just after systole, and the amount of diastolic flow is less than that seen in the ICA. Indeed flow may cease entirely at end diastole (Fig 1B). The CCA waveform is a blending of these two patterns, with about 70% to 80% contribution from the ICA (Fig 1C). The carotid bulb is a focally dilated area at the origin of the ICA, and this dilatation produces complicated flow patterns. Because of the hemodynamics at the bulb and carotid bifurcation, flow in portions of the

Fig 1. Normal Doppler waveforms of the carotid artery. (A) Typical ICA waveform showing antegrade flow throughout the cardiac cycle. The clear “window” under the curve indicates laminar flow. (B) The waveform in the ECA shows early diastolic flow reversal and low end diastolic velocities. (C) The CCA waveform is a blend of that seen in the ICA and CCA. (D) Flow in the carotid bulb is typically low amplitude and turbulent as represented by flow both above and below the baseline.


bulb is not laminar but may be turbulent and even reversed in direction (Fig 1D). This transient reversed flow is referred to as boundary layer separation, and is not pathological, rather the loss of this flow separation may be taken as a sign of disease of the bulb with loss of the normal bulb dilatation.

Norma1 velocities in the carotid arteries are usually between 60 and 100 cm/s, however, they can range from less than 40 to 120 cm/s. There is normally no significant increase in velocity as one progresses from CCA into ICA and ECA, but there may be a slight decrease in peak systolic velocity. Usually the velocities are fairly symmetric from side to side.

ABNORMAL EXAMINATION

Increasing degrees of stenosis produce pro- gressive changes in the Doppler waveform. At low levels of stenosis there are typically no flow abnormalities. As the degree of stenosis in-

creases, mild turbulence in the form of spectra1 broadening can be detected probably caused by irregular plaque surfaces and eddy currents just distal to the plaque. When the severity of stenosis increases beyond a certain point, the velocity of blood through the stenosis must increase to maintain flow volume. This produces a jet of higher velocity blood flow through the stenosis and a variable amount of turbulence at or just distal to the stenosis. This jet of higher velocity is detected on color imaging as a change in color intensity, whereas the turbulence is represented by multiple hues of color and often bidirectional flow (simultaneous red and blue) (Fig 2). When a stenosis produces these changes, it is hemodynamically significant. This has been shown to occur at about 50% diameter or 75% cross-sectional area reduction” (Fig 3). Velocities are not only increased in systole but in diastole as well. Because of these increased velocities at the stenosis, the

CAROTID DUPLEX SONOGRAPHY 21

defines a critical stenosis that corresponds to about 70% diameter or 90% cross-sectional area reduction.” As the degree of stenosis approaches the point of occlusion, there may be a precipitous drop in flow volumes and a con- comitant decrease in velocities to such a point that velocities may even be lower than normal

Fig 3. Peak systolic velocity measurement of 170 cm/s and a turbulent flow pattern with filling in of systolic “window” indicates a greater than 50% stenosis (A). This is confirmed at selective arteriography (B).

ratio of velocities between the stenotic ICA and the CCA increase. The turbulent flow caused by the stenosis produces a wide distribution of velocities at and distal to the stenosis. This wide range of velocities causes “filling in” of the normally clear window under the wave in systole. Further increases in stenosis result in progressively higher velocities and increasing turbulence, until a point is reached beyond which flow begins to diminish (Fig 4). This point

Fig 4. Doppler waveform from the origin of the ICA show-

ing a peak systolic velocity of 315 cm/s (A). A selective arteriogram (6) confirms the presence of a 90% stenosis of the ICA.


or undetectable and indistinguishable from total occlusion.

With total occlusion of the ICA, no flow can be detected by either spectral analysis or color imaging in the occluded segment. The CCA velocity and waveform resembles the ECA and is dependent on the degree of collateralization through the ECA. Generally speaking, flow is damped to some degree with a high-resistance pattern and Iow velocities (Fig 5). But if there is

collateralization from the ECA to the intracranial vessels, the CCA waveform may be normal. Indeed, the ECA waveform may become “internalized” with a low-resistance flow pattern mimicking the ICA due to flow to the brain through extensive ECA collaterals.

DIAGNOSTIC CRITERIA

There are many published diagnostic criteria for categorizing degrees of stenosis in the ca-

Fig 5. There is a low-amplitude, high-resistance flow pattern in the CCA (A) with no detectable flow in the ICA (6) in this case of complete occlusion of the ICA confirmed at arteriography (C). Arrow shows stump of ICA.

CAROTID DUPLEX SONOGRAPHY

rotid arteries.‘3-‘7 Various parameters have been used including peak systolic velocity in the ICA, systolic velocity ratios ICA/CCA, end diastolic velocity in the ICA, peak diastolic velocity in the ICA, diastolic velocity ratios ICA/CCA, spectral broadening (turbulence), and real time or color measurements of the degree of stenosis. The diagnostic criteria used at my institution are shown in Table 1. These criteria were derived by comparing duplex sonograms with carotid arteriograms in 100 patients with varying degrees of disease, and using receiver operating characteristic (ROC) curves to select criteria with the highest combination of sensitivity and specificity.‘” The categories and criteria are similar to those derived by others,‘“,‘h.‘7 with the slight differences explainable by differences in duplex equipment and the degree of sensitivity and specificity desired. We found that all of the criteria were good indicators of disease at each level of stenosis, but the results for peak systolic velocity were best. One would assume that combining multiple diagnostic criteria (in other words peak systolic velocity and velocity ratios or other combinations) would increase diagnostic accuracy, but this was not shown to be true.‘” This is not meant to imply that all data other than peak systolic velocities should be ignored. I use velocity ratios, diastolic velocity, and turbulence in two ways. First, in cases where the velocity measurements suggest a stenosis that is

Table 1. Diagnostic Criteria in Assessing Carotid Artery

Stenosis

Category

Peak Systolic Systolic Velocity Velocity Diastolic

ICA Ratio, Velocity (cm/s) ICAiCCA (cm/s) Turbulence

~50% diameter stenosis

(75% cross-sectional area

reduction) <150 <2 <50 0

> 50% diameter stenosis


reduction) >I50 >2 >50 +

> 70% diameter stenosis


reduction) >225 >3 >75 ++

Occlusion 0 NA 0 NA

NOTE. Turbulence was graded as 0, absent; +, filling in of the

“window” in the waveform; or ++. grow distortion of the

waveform.

Abbreviations: ICA, internal carotid artery; CCA, common

carotid artery; NA, not applicable.

Reprinted with permission.‘”

Fig 6. No high velocities were seen in this case of severe stenosis. Whereas the peak systolic velocity was only 56 cm/s, a severe stenosis was suspected because of the grossly distorted ICA waveform (A). An aortic arch arteriogram (B) confirms a “pinpoint” stenosis of the ICA.

borderline between two categories, I use the other parameters to guide me in choosing the appropriate stenosis category. Second, the presence of marked turbulence with grossly de- formed waveforms helps detect those infre- quent cases where the degree of stenosis is so severe that peak systolic velocities have fallen back to normal levels (Fig 6). Any time there is a


significant discrepancy between the degree of stenosis predicted by the peak systolic velocity and the other parameters, the study must be carefully scrutinized or repeated with an at- tempt to explain the discrepancy.

You will note that I make no effort to differentiate between levels of stenosis that are less than hemodynamically significant. Most classifications group nonhemodynamically significant lesions (less than 50% diameter stenosis) into two or more categories differentiated by real-time measurement or the presence of mild levels of turbulence without velocity abnormalities.” Whereas these methods may accurately estimate minor levels of stenosis, this information is not clinically useful in the asymptomatic patient. One possible use for this information has been in the triage to angiography of symptomatic patients with minor stenosis at duplex examination in the hope of discovering a surgi- cally correctable source of emboli. However, a recent study by Zierler et al.‘” has shown that a duplex scan that shows a normal or minimally diseased vessel on the side of the symptoms obviates the need for angiography because it has no impact on the patient’s treatment or outcome. Patients with stenosis levels of 16% to 40% were not considered in their study since only one patient fell into this group, but the same may be true for these patients.

Some authors advocate a more extensive real-time study for the determination of plaque morphology, to search for ulcerations, and for the measurement of degree of stenosis including residual lumen area measurement.” I do not feel that this is worthwhile. Spectral analysis is more accurate in the detection and classifica- tion of hemodynamically significant stenoses than the real-time image measurement.‘3’s Al- though it is interesting to speculate on the potential usefulness of plaque morphology, there are no longitudinal studies that show that the sonographic appearance of a plaque can be used to predict its future behavior.4 The detection of ulceration by sonographic imaging has been shown to be unreliable.4’3’9

What criteria should you use in your practice? It would be ideal if every ultrasound laboratory could develop their own diagnostic criteria such as I described above, since this

would negate the problems introduced by varia- tions in duplex equipment and patient popula- tions. This is obviously not practical in most situations. I recommend adopting criteria derived from studies using equipment manufactured by the vendor of your duplex scanner. There may be considerable variation between measurements obtained using equipment from different manufacturers, and this will minimize these differences.h

PITFALLS

There are several common situations that can lead to an incorrect interpretation. Most of these can be detected or at least suspected by meticulous documentation of the procedure and careful scrutiny of the hard copy or video tape record. Probably, the most common error is introduced by selecting an inaccurate Dop- pler angle correction. This is readily apparent by noting the Doppler angle recorded on the image from which the velocity data is taken. Angles greater than 60” or less than 30” can introduce significant errors. If the cursor is not placed parallel to the direction of flow, the same errors may be introduced. With a black-and- white unit, one should place the cursor parallel to the vessel walls, which is the expected direction of flow. Unfortunately, there are several situations where flow is not laminar and parallel to the long axis of the vessel, such as through an eccentric stenosis or even more commonly around the bends and kinks of a tortuous vessel. In these situations, color imaging is the best way to approximate the direction of flow and obtain the most accurate measurements. I am reluc- tant to diagnose a significant stenosis from velocity measurements obtained in a very tortuous segment unless there are multiple criteria present for stenosis. I rely heavily on serial studies showing worsening findings in these situations. The argument has been proposed that one can never know the true vector of blood flow in a vessel and consequently all velocity measurements are inherently inaccurate. This argument has been used to propose the use of frequency measurements as opposed to velocity measurements2” Although there may be some inherent inaccuracy in velocity measurements, this would not appear to be clinically


Fig 7. Only one vessel was seen (A) and was incorrectly identified by the technologist as the ICA because of the waveform. Temporal artery compression correctly identifies this vessel as the ECA when reflected waves are seen superimposed on the waveform (B).

significant since numerous articles have shown excellent correlation between velocity measurements and degrees of stenosis.

Areas of dense calcification may obscure segments of a vessel that could contain a stenosis. Because the calcifications are often eccentric and discontinuous, altering the transducer position and angle will often allow visualization of these segments. Color imaging may facilitate the search for the optimal transducer position. If these maneuvers still result in an incomplete study, one must note this in the interpretation and rely on secondary criteria such as high- resistance flow in the vessel proximal to the calcification or turbulence and a damped low- amplitude flow pattern distally to suggest the possibility of an occult stenosis more proximally.

In some cases, whether caused by disease or anatomic variation, it may be difficult to differentiate between the ICA and ECA. With mild to moderate plaque, there may be enough

turbulence in the ECA to mask its characteristic waveform. One simple method is to look for branches with the aid of color imaging. The ICA has no branches. If you are in doubt, a simple technique for identifying the ECA is to perform temporal artery compression. While obtaining a spectral tracing from the ECA, alternately com-

Fig 8. No flow could be detected beyond the origin of the ICA (A). Selective atteriogram (B) shows a pinpoint stenosis with very slow flow in a patent ICA (arrow) which was subsequently confirmed at surgical endarterectomy.

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press and release the temporal artery just ante- rior to the ear. This produces a reflected wave that is seen superimposed on the ECA spectral waveform. This can also be useful when there is occlusion of one of the vessels. The ECA waveform may become internalized, but these techniques will allow for its recognition (Fig 7).

Not all stenoses or occlusions occur within the portion of the carotid artery that is amena- ble to sonographic evaluation. Stenoses at the CCA origin, the innominate artery, or in the intracranial ICA are not uncommon. Distal occlusions or high-grade stenoses often cause a high-resistance flow pattern with little or no diastolic flow with very low velocities throughout the ICA. Proximal stenoses may cause damped flow in the CCA recognized by very low amplitude waves. Of course, these phenomena are only produced by very high-grade occlusive disease.21

Apparent occlusion of an ICA is not infre- quently detected at duplex examination during the investigation of symptomatic patients. It is extremely important to differentiate between occlusion and very high-grade stenosis with slow flow distal to the stenosis, because the latter patients are candidates for surgical endarterec-

MICHAEL L. ROBINSON

tomy. The entire ICA must be carefully interro- gated using the highest sensitivity settings for any evidence of flow. I have seen several cases in which no flow could be detected at duplex examination that were subsequently shown at angiography to be “pinpoint” stenosis with extremely slow flow through a patent ICA (Fig 8). Special “low flow” detection features available on many of the newer color duplex machines may help prevent these errors in the future. The best rule is to interpret occlusions cautiously in symptomatic patients, including a caveat in your report that it is not always possible to exclude a very high-grade stenosis.

SUMMARY

Duplex sonography is the best noninvasive modality for investigation of possible carotid artery stenosis. By using the above described techniques, almost all significant stenoses can be detected and categorized correctly. Knowl- edge of common pitfalls in the performance and interpretation of the examination is essential to avoid misdiagnosis. Color imaging is a helpful addition to conventional duplex imaging, but is not essential to the performance of high-quality examinations.

REFERENCES

1. Brown PB, Zwiebel WJ, Call GK: Degree of cervical

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and long-term results of carotid endarterectomy. Stroke 20: 1138-l 142,1989

3. Moneta GL, Taylor DC, Nicholls SC, et al: Operative

versus nonoperative management of asymptomatic high- grade internal carotid artery stenosis: Improved results with endarterectomy. Stroke 18:1005-1010, 1987

4. Strandness DE: Extracranial arterial disease, in Strand- ness DE (ed): Duplex Scanning in Vascular Disorders. New York, NY, Raven, 1990, pp 92-120

5. Zwiebel WJ: Color duplex imaging and Doppler spectrum analysis: Principle, capabilities, and limitations. Semin Ultrasound, CT, MR 11:84-96, 1990

6. Kimme-Smith C, Hussalin R, Duerinckx A, et al: Assurance of consistent peak-velocity measurements with a variety of duplex Doppler instruments. Radiology 177:265- 272,199O

7. Zwiebel WL: Spectrum analysis in carotid sonography. Ultrasound Med Biol 13:625-636, 1987

8. Evans DH, Macpherson DS, Asher MJ, et al: Changes in Doppler ultrasound sonograms at varying distances from stenoses. Cardiovasc Res 16:631-636. 1982

9. Bluth EI, Merritt CRB, Sullivan MA, et al: Usefulness

of duplex ultrasound in evaluating vertebral arteries. J Ultrasound Med 8:229-235, 1989

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11. Strandness DE: Color, in Strandness DE (ed): Du- plex Scanning of Vascular Disorders. New York, NY, Raven, 1990, pp 185-195

12. Jacobs MJ, Grant EG, Schellinger D, et al: Duplex carotid sonography: Criteria for stenosis, accuracy, and pitfalls. Radiology 154:385-391, 1985

13. Robinson ML, Sacks D, Perlmutter GS, et al: Diag- nostic criteria for carotid duplex sonography. AJR 151:1045- 1049,1988

14. Bluth EI, Stavros AT, Marich KW, et al: Carotid duplex sonography: A multi-center recommendation for standardized imaging and Doppler criteria. RadioGraphics

8:487-506, 1988 15. Taylor DG, Strandness DE: Carotid artery duplex

scanning. J Clin Ultrasound 15:635-644, 1987

16. Zwiebel WJ, Knighton R: Duplex examination of the carotid arteries. Semin Ultrasound, CT, MR 11:97-135, 1990


17. Garth KE, Carroll BA, Sommer FG, et al: Duplex bifurcation disease: Prediction of ulceration with B-Mode ultrasound scanning of the carotid arteries with velocity US. Radiology 162523-525, 1987 spectrum analysis. Radiology 147:823-827, 1983 20. Phillips DJ, Beach KW, Primozich J, et al: Should _.

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Correlation with arteriography and clinical outcome. J Vast Surg 12:447-455, 1990

19. O’Leary DH, Holen J, Ricotta JJ, et al: Carotid

results of ultrasound Doppler studies be reported in units of

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Duplex sonography of the carotid arteries

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