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(Stroke. 1995;26:1743-1746.)
© 1995 American Heart Association, Inc.

Articles

Skepticism Toward Carotid Ultrasonography

A Virtue, an Attitude, or Fanaticism?

E.B. Ringelstein, MD

From the Klinik und Poliklinik für Neurologische, Westfalische Wilhelms-Universität Münster (Germany).

Correspondence to Prof E.B. Ringelstein, MD, Klinik und Poliklinik für Neurologische, Westfalische Wilhelms-Universität Münster, Albert Schweitzer Str 33, Münster, Germany.

Key Words: carotid arteries • ultrasonics • carotid endarterectomy • diagnostic imaging

	Introduction

Top Introduction References

 
Routine ultrasonography of the brain-supplying arteries is not a well-defined procedure. It may range from simple periorbital directional flow assessment to highly sophisticated imaging of the carotid arteries, or even thorough workup of all sonographically accessible extracranial and intracranial brain arteries.¹ Continuous-wave Doppler sonography with or without frequency analysis is still widely used, but today color-coded B-mode imaging in conjunction with transcranial Doppler sonography is the state-of-the-art technique.^{2 3 4 5} The latter was not used during the North American Symptomatic Carotid Endarterectomy Trial (NASCET).⁶

The detection of carotid artery occlusive disease by means of ultrasound has its own nearly 40-year history.⁷ Broad acceptance of ultrasound investigations in neurovascular patients was first achieved in the late 1970s after introduction of the direct continuous-wave Doppler technique continuously tracking the cervical portions of the carotid arteries.^{8 9} Further considerable diagnostic improvement became reality by the introduction of B-mode scanning of the carotid bulb in conjunction with Doppler ultrasound.^{10 11} This duplex scanning permitted detection of not only moderate or high-grade stenoses and occlusions but also nonstenosing plaques and low-grade stenoses and allowed for the correct diagnosis of acute internal carotid artery thrombosis despite an echolucent arterial lumen.¹² Finally, color-coded B-mode imaging in conjunction with frequency analysis made the distinction between internal carotid artery occlusion and pseudo-occlusion (ie, "near occlusion") highly reliable.¹³ The oncoming ultrasound contrast media¹⁴ and new ultrasound techniques like power Doppler¹⁵ will additionally contribute to future improvement and will help to close (or at least reduce) the remaining diagnostic gaps. The quantification of carotid artery stenoses, however, remains a challenging issue, since it has regained actuality and striking clinical importance through recently published trials on carotid endarterectomy.^{6 16}

Although ultrasound tools were rapidly adopted for neuroangiologic diagnosis by neurologists and vascular surgeons in Japan, France, Germany, Austria, Scandinavia, Italy, Switzerland, and the Netherlands, the Anglo-Saxon countries were more hesitant, due to either a presumed lack of therapeutic consequences of ultrasound findings or a generally presumed higher reliability of "black-on-white" imaging. In fact, precise and reliable ultrasonographic diagnoses concerning occlusive disease of the brain arteries still require considerable expertise in the technique used, are difficult to document as long as they rely on a multimodal synopsis of a variety of ultrasound information, and are additionally improved by the clinical experience of the examiner. With this background in mind, it is understandable that NASCET⁶ researchers, not being experts in ultrasonography themselves, have severely questioned the validity and reliability of Doppler ultrasound findings in the assessment of carotid stenoses during the NASCET trial.¹⁷

Low-risk carotid endarterectomy is the most efficacious, presently available prevention of carotid-borne stroke and should be performed as soon as moderate or high-grade internal carotid artery stenoses have become symptomatic by transient ischemic attacks or minor strokes.^{6 16} Of a series of potentially relevant patient characteristics, the degree of carotid stenosis, a seemingly simple item, has turned out to be of decisive impact for the patient's prognosis and therapeutic decision making. Faced with the striking clinical implications of these findings from NASCET as well as from the European Carotid Surgery Trial (ECST),¹⁶ noninvasive methods to detect and quantify carotid artery stenosis need a thorough reappraisal¹⁸ to avoid the worldwide misuse, overuse, or even neglect of a potentially valuable, if not ideal, tool. In the article by Eliasziw et al,¹⁷ the accuracy and prognostic consequences of ultrasonography in identifying moderate and severe carotid artery disease were compared with cerebral angiography and found to be substantially poor as long as the ultrasonographic information consisted of peak-systolic velocities and peak frequency changes from both the internal and common carotid arteries. The sensitivity and specificity of the ultrasound findings compared with angiographic stenoses calculated according to NASCET ranged from .65 to .71. The specific finding by Eliasziw et al (not surprising, however, for experts in the field of ultrasonography) was the lack of decline in the risk of future stroke as the degree of ultrasonographically defined stenoses declined. By contrast, such a pattern of decline was clearly seen on the basis of the angiographic data. The authors' conclusion was to recommend carotid ultrasonography merely as a screening tool and only to exclude patients with no carotid artery disease from further testing, but they postulated to apply conventional angiography as the key investigation, and in the first range, before assigning the individual risk of stroke and allocating the patient to medical or surgical treatment.

These findings are intriguing at first glance but not finally convincing. In the article by Eliasziw et al, the complex multimodal flux of acoustic and visual information, with its additional characteristic modulations within the time frame of cardiac cycles during duplex ultrasonography, has been reduced to a single one-dimensional number like peak-systolic frequency (or the corresponding peak-systolic flow velocity). This naive, simplistic approach was termed "ultrasonography," an unspecific expression inadequately miscrediting even highly sophisticated and precise, modern ultrasound methodology with the accusation of unreliability. Under these circumstances, one would hardly expect a strong statistical correlation between ultrasound, anatomy of the stenosis, and clinical events. Albert Einstein's warning, "Make things as simple as possible, but not simpler," has not been kept in mind.

The angiography-based NASCET method underestimates carotid stenoses compared with the ECST approach.¹⁸ This leads to the unsatisfying situation that some patients with less than 70% stenosis by NASCET will be allocated to medical treatment, whereas the same patients will undergo operation if evaluated by the ECST technique. It remains undefined which of the diagnostic techniques presently available to assess carotid disease best reflects biological reality.

While the angiographic findings in themselves are consistent, the Doppler findings are not, and it becomes evident that the ultrasound technique used in the NASCET trial is inadequate. Too much ultrasound information is lost, or at least neglected, for a more precise evaluation of the carotid lesion, such as vessel wall covibrations⁹ ; increase in low-frequency noise during systole, diastole, or both,⁹ or right-to-left comparison of common carotid artery flow velocity^{19 20} ; retrograde, lacking, or pendulum-like flow in the periorbital branches of the ophthalmic artery;²⁰ length and severity of "disturbed flow" downstream to the stenotic lesion and residual poststenotic flow velocities;²¹ visualization of the stenotic plaque in high-resolution B-mode scanning,^{21 22} with additional color-coded imaging of blood flow showing intrastenotic or poststenotic jets and poststenotic turbulences; and transverse and longitudinal vessel-wall motion, including prestenotic and poststenotic pulsatility indices.^{21 22} All these potential diagnostic aids, though already known, have not been used in the ultrasound evaluation of NASCET patients.

Eliasziw et al¹⁷ suspected a bias due to the sequence of diagnostic techniques applied to carotid arteries during the screening and selection of patients for carotid endarterectomy. Ultrasound checks are usually performed first, and only the "positive" patients are subsequently subjected to arteriography. Specifically, sensitivities and specificities of ultrasonographic findings reported in the literature may be "inflated" and would explain the "previous optimistic reports of high levels of accuracy." I wonder whether this principal skepticism toward ultrasonography constitutes another bias in the sense of self-fulfilling prophecy (see below). The more experienced and competent an ultrasonographer is the more cautious he will be with generalizing dogmatic statements, but also the more demanding he will become in terms of quality control and training and, in the end, the more self-confident he will be about his final diagnoses. With respect to the specific "ultrasonography" chosen by the NASCET trialists for their purposes, I wonder whether the study of Eliasziw et al pinpoints a local rather than a global problem.

The authors' idea to accuse Doppler ultrasonography of the neck arteries of definite (though slight) invasiveness and potential harm is amazing. With millions of patients having been tested by ultrasound techniques for occlusive disease in the neck arteries, many of these tests in close temporal relation to preceding transient ischemic attacks, or the patients simultaneously suffering from concomitant coronary heart disease, the low frequency of strokes (n=4) and heart attacks (n=2) occurring arbitrarily during carotid testing speaks for itself and demonstrates that ultrasound is completely noninvasive unless carotid compression maneuvers are performed. One would have expected a rather higher incidence of adverse events. Thus, the low number of these coincidental accidents again underlines the noninvasiveness of ultrasound studies and reflects their relaxing effect on the patient's anxiety and fears. By contrast, with intra-arterial cerebral angiography, the burden of severe complications is considerably higher than claimed by Eliasziw and coworkers, accounting for approximately 1% of major strokes and death in candidates for carotid endarterectomy^{23 24} even if a modern technique of arteriography is used. The authors also addressed the detection of ulcerated lesions and intraluminal thrombi. Although color-coded duplex scanning is far from perfect in predicting plaque ulceration or intraluminal thrombus, it is at least equivalent or even superior to arteriography^{11 18 22 25 26} and still being improved.

Stenoses of 70% diameter reduction as measured by NASCET have an 82% diameter reduction as measured by ECST but have only minimal residual lumens of 10% or less by area luminal reduction. There is no doubt that the linear measurements used in the above carotid endarterectomy trials label various degrees of stenoses with equivocal numbers discrepant to values reflecting the cross-sectional lumens. Consequently, these linear parameters are discrepant to the real anatomic situation as well. Recent findings by Alexandrov and coworkers¹⁸ on quantification of carotid stenoses by 7.5-MHz color-coded duplex sonography indicated a nearly perfect ultrasound evaluation when the luminal area reduction during ultrasound was compared with planimetric evaluation of the surgically removed plaques. They could not, however, find a satisfying consistency of the linear ECST parameters with true anatomy, and the linear NASCET parameters were even worse. Alexandrov and coworkers concluded that "when area stenosis is used, ultrasound continues to be consistent" and that "Duplex is more, not less, accurate than either of the NASCET and ECST methods."

The fundamental shortcoming of the methodology in the article by Eliasziw et al¹⁷ is their choice of an inadequate ultrasonographic technique. This is convincingly documented in their Fig 1, top. About 40% of the carotid lesions contained in this graph have a degree of stenosis of 85% or more according to NASCET criteria but reveal an extreme scattering of peak systolic velocities ranging from nearly 0 to 650 cm/s. Flow velocities measured within such lesions are subject to a phenomenon intensively investigated and first described by Spencer and Reid in a milestone 1979 article in Stroke.²⁷ They demonstrated that in high-grade lesions, peak frequencies decrease again despite an increasing degree of stenosis (bell-shaped curve), with the individual peak frequency being modified by a variety of concomitant but unpredictable physiological parameters. The study by Spencer and Reid proved the peak systolic frequency a parameter inadequate to quantify very high-grade stenoses. The selection by Eliasziw et al of the systolic peak frequency (or its derivates) as the ultrasonographic parameter of choice reflects a mechanism of (presumably unwanted and unnoticed) self-fulfilling prophecy in that this approach could not lead to a positive result. Another detail from their Fig 1, top, is also striking: How did NASCET ultrasonographers find peak frequencies of >8 kHz (corresponding to flow velocities of 250 cm/s or more) in stenoses of no more than 50% lumen reduction (according to NASCET criteria)? Two explanations are probable: Either high-grade external carotid artery stenoses were erroneously identified as internal carotid artery lesions or (more probably) the estimation of the degree of stenosis by angiography was incorrect. The latter would again emphasize that biplane angiography does not deserve the status of a gold standard.

In the end, the article by Eliasziw et al is of considerable historical interest since it reflects different attitudes and feelings in the old as opposed to the new world. It also deserves the merit of finally supporting ultrasound techniques as the preferable diagnostic tool in carotid disease. Their paper will have a "therapeutic" impact on the scientific community of vascular ultrasonographers comparable to the "paradoxical intention" used in psychotherapy. The arousal effect of this article should not be underestimated. Efforts will be made to dig out the profound technical and physiological knowledge already available and to demonstrate again not only the reliability of ultrasound techniques for the detection and quantification of carotid disease but also their superiority over other procedures in terms of precision, cost-to-benefit ratio, and noninvasiveness. Obviously, the awareness of such knowledge is prone to become the victim of neglect or forgetfulness. Ultrasound techniques are strongly operator and interpreter dependent and hard to document in a reproducible way. The consequence should be (1) to validate both angiography and ultrasound techniques by true, independent, and reliable gold standards based on anatomic reality; (2) to standardize equipment, training procedures, and sonographic criteria for the diagnosis and quantification of lesions, and to do this worldwide; and (3) to respect and acknowledge the diagnostic efficacy and fruitfulness of "today's ultrasonography," no longer comparable to historical approaches. The best available ultrasound technique is just good enough for trials of the NASCET format. The "widespread availability of both color-flow Doppler and MR angiography"¹⁷ has already become a reality, and together with Eliasziw and coworkers we, in fact, "await the final perfection." Ultrasonographers should be self-confident enough not to rely on questionable, inconsistent, and even discrepant angiographic findings, since angiography is only a surrogate of a gold standard sensu stricto. But they should keep in mind that angiographic fundamentalism is as inadequate as ultrasonographic conceitedness.

	Acknowledgments

 
The author appreciates the helpful comments by Dr Bernhard Widder of Ulm, Germany, during the preparation of the manuscript.

	Footnotes

 
The opinions expressed in this editorial are not necessarily those of the editors or of the American Heart Association, Inc.

Stroke. 1995;26;1743-1746.

	References

Top Introduction References

 

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