Although many articles have been published on the diagnosis and imaging of carotid stenosis, very few articles have been dedicated to a common-sense evaluation of patients with carotid vascular disease. This article will review the current literature and present a common-sense evaluation of patients with carotid vascular disease. An algorithm also is provided as a useful guide to the proper work-up of patients with carotid stenosis (figure 5).

The three most useful imaging modalities for carotid vascular disease, carotid duplex ultrasound, magnetic resonance angiography (MRA), and angiography, will be discussed, including their strengths, weaknesses, and accuracy. Each modality's most common pitfalls will be outlined as well as how to avoid them. A brief discussion of computed tomography (CT) angiography also is included.

Data from the multicenter study of the surgical and medical treatment for carotid stenosis (North American Symptomatic Carotid Endarterectomy Trial [NASCET]) demonstrated a definite benefit of carotid endarterectomy for symptomatic patients with a 70% to 99% stenosis of the internal carotid artery.1-3,19 The NASCET studied symptomatic patients with ipsilateral carotid stenosis of 70% to 99%. The 30-day postoperative risk for stroke or death was 5.8%. The cumulative risk of ipsilateral stroke at two years was 9% in the surgical group and 26% in the medical group. In the 70% to 99% stenotic group, the benefit from surgery was in direct proportion to the severity of the stenosis. The difference in stroke-free survival at two years was 26% for patients with 90% to 99% stenosis, 18% for those with 80% to 89% stenosis, and 12% for those with 70% to 90% stenosis.1,3

According to the National Institute for Neurological Disorders and Stroke, patients with asymptomatic 60% to 99% carotid stenosis who underwent carotid endarterectomy had a 55% decrease in the incidence of stroke or death within five years, compared to medically treated patients. This was the case only at medical centers that had perioperative morbidity and mortality rates of less than 3%.1

Duplex sonography

Carotid duplex sonography is an excellent screening study for carotid stenosis. It is inexpensive, noninvasive, and fairly accurate, and it can be performed at the patient's bedside. Carotid duplex ultrasound combines high-resolution real-time grey-scale imaging with Doppler, providing information on physiologic blood flow and luminal stenosis.

Ultrasound is more accurate than angiography and MRA in evaluating the atherosclerotic plaque morphology, regardless of whether the plaque is soft or hard, has intraplaque hemorrhage, or is ulcerated. Furst et al demonstrated that Doppler sonography is accurate in demonstrating ulcerated plaques in patients with high-grade or critical stenosis, with a specificity of 95.3% and an accuracy of 94%.1,4

Edwards et al concluded that conventional angiography identified only 60% of the ulcers demonstrated at surgery.5 An ulcerated plaque also can be a source of distal embolism in patients who do not have a critical stenosis.9

Ultrasound pitfalls

There are many drawbacks to the use of carotid ultrasound; some of the more common ones are discussed below.6,12,24,38

1. The most common pitfall of carotid ultrasound is that it is very technologist-dependent. Only highly qualified, experienced sonologists should be performing the procedure (figure 2).
2. There is more (inter- and intraobserver) variability with ultrasound than with MRA or angiography in the measurement of carotid stenosis.1,35
3. Because of the technical difficulty with Doppler ultrasound, only dedicated high-quality color-flow equipment should be used.

4.  

5. A vessel may be absent or of anomalous origin. The internal carotid usually arises posterolaterally to the external, but there can be at least a 5% variability in the normal anatomic relationship. Thus, one actually may be visualizing the external carotid artery, confusing it with the internal carotid or vice versa. The two vessels have different wave forms. However, if there is a stenosis or tandem lesion, this can change the normal wave-form pattern and make it difficult to differentiate the internal carotid from the external carotid.
6. As an ultrasound pulse encounters dense material, such as calcification or bone, most of the energy is reflected back towards the transducer with shadowing distal to the dense material; this obscures the normal anatomy or stenosis, which may cause under- or overestimation of the degree of stenosis.

7.  

8. At times, ultrasound is unable to determine accurately whether there are tandem lesions. Tandem lesions are additional stenotic lesions that are either proximal or distal to the original stenosis. Tandem lesions occur in 2% of patients who have significant stenosis of the cervical portion of the internal carotid artery.1,2 Tandem lesions occur most commonly in the region of the cavernous segment of the internal carotid artery (ICA) or the horizontal segment of the middle cerebral artery or in the common carotid artery.34 The effect of the distal stenosis depends on the degree of its severity. The effect of a second stenosis is additive if each of the two lesions is capable of reducing flow. If one lesion is a critical stenosis, then that single vessel will govern the degree of the flow.1,2,7 There is debate in the literature about the significance of tandem lesions.

9. In a study by Schuler et al, there were no strokes and one death in patients with stenosis limited to the bifurcation. In patients with distal tandem lesions, 11.4% had intraoperative or perioperative strokes and four operative deaths.1,10 At times, a tandem lesion can be suggested by ultrasound if there is a proximal lesion because the velocity measurements may not correspond to the measured stenosis, as the proximal lesion alters the velocity measurements. Obviously, MRA and conventional angiography can detect tandem lesions within the common carotid, cavernous segment of the carotid, or large intracranial branch vessels.

10. The internal and external carotid vessels often are very tortuous; when this occurs, it is difficult to obtain good axial orientation of the vessel. The tortuosity of the vessel will change the velocity measurements just as a sharp angulation in a high-pressure pipe will change the velocity across the area of angulation (figure 3).

11.  

12. A soft plaque can mimic flowing blood; this can be minimized by performing good color-flow measurements and obtaining good visualization of the vessel.

13.  

14. Velocity measurements can increase in hypertensive patients. Patients with decreased cardiac output can have lower velocity measurements. Cardiac arrhythmias, aortic valvular lesions, and cardiomyopathies all can effect velocity measurements.1,2 Velocity measurements can increase in the contralateral vessel by shunting of blood through the involved vessel.1,2
15. The vertebral arteries can be difficult to visualize with ultrasound because of their small size and deep location. The vertebral may have decreased flow or be occluded, which may be responsible for the patient's symptoms.

16.  

17. MRA is more accurate than ultrasound in the diagnosis of carotid stenosis.1,2,17,21 In a study by Anderson and colleagues, ultrasound misdiagnosed 20% of cases, which altered surgical management, compared to only 5% misdiagnosed with MRA.21 In some studies, MRA also is superior to ultrasound in diagnosing an occlusion.14

In certain situations, ultrasound can be more accurate than angiography in diagnosing stenosis. The atherosclerotic plaque is associated with arterial wall expansion.9 Angiography measures only the patent lumen and cannot evaluate the vessel wall; ultrasound, however, can evaluate the vessel wall. If the plaque is concentric, it may be difficult to evaluate the degree of stenosis accurately, especially if there is some normal luminal dilation of the vessel. This same pitfall also is encountered when comparing coronary angiography with intraarterial ultrasound.

Magnetic resonance angiography

Magnetic resonance angiography is an excellent screening and diagnostic examination for carotid vascular disease, stenosis, or occlusion.13,15,29,32 Magnetic resonance angiography has gained acceptance rapidly, with stronger, more uniform magnets, improved surface coils and software, and with experience.

MRA has certain advantages over ultrasound and angiography. However, MRA also has certain pitfalls, which will be discussed. Because the physics of MRA is complicated, there will be only a brief discussion.

In MRA, a magnetic field is applied to flowing blood. A radiofrequency pulse is then applied, which changes the alignment of the protons of the flowing blood within the selected slice. When the protons begin to realign with the magnetic field, they emit a radiofrequency pulse that is used to generate an image. The signal from flowing blood is dependent on the MRA technique used and can vary with different MRA parameters, including repetition time (TR), echo delay time (TE), and other MRA parameters.

There are two main MRA techniques: time-of-flight (TOF) and phase-contrast imaging.11,29 In time-of-flight imaging, the protons of flowing blood have full magnetization on the entering slice. TOF imaging can be two-dimensional (2D) or three-dimensional (3D). In 3D TOF imaging, an extra phase-encoding gradient is added, and volumetric measurement can be performed. In 2D imaging, selected slices are obtained and stacked together like a roll of coins to generate an image (figures 1 to 4).

Phase-contrast MRA measures changes in the phase spin magnetization along the magnetic field gradient. 2D TOF has greater intrinsic contrast than 3D, is less sensitive to motion, and has greater sensitivity for differentiating occlusion or slow flow (figure 4). 3D TOF imaging tends to have higher intrinsic resolution because it obtains volumetric measurements rather than thin-section images with 2D imaging. 3D also is less susceptible to areas of turbulent flow that occur at the carotid bulb and areas of stenosis.

Because phase-contrast MRA is more sensitive to slow flow than TOF imaging, it can be used to help differentiate severe stenosis from occlusion and to evaluate tortuous vessels; however, it has less resolution than TOF. One disadvantage of phase-contrast MRA versus TOF imaging is that areas of slow- or high-velocity flow can cause signal dropout. Thus, one may overestimate the degree of stenosis.

Most recent studies evaluating MRA report sensitivities and specificities approaching those of angiography in the diagnosis of carotid stenosis. A new MRA technique, multiple overlapping thin-section angiography (MOTSA), found sensitivity and specificity of 90% to 95% for stenosis of equal to or greater than 70%.1,16

Recent studies using multiplanar reconstruction technique, which requires selection of the angle that best delineates the stenosis, have an almost 100% correlation with the degree of pathologic stenosis. Studies by De Marco et al and others found no significant error in the measurement of stenosis when MRA was compared to conventional angiography using this technique.20 Multiple papers claim 100% accuracy in the diagnosis of carotid occlusion with MRA.21,26-28

The biggest pitfall of MRA is that it overestimates stenosis. This may occur in greater than 10% of patients and it varies, depending on different articles. However, it often does not change patient management. Increased experience, review of source data, 2D axial techniques sensitive for flow, and the new MRA techniques previously described can help prevent overestimation of stenosis.1,2,20,21,40 Using phase-contrast MRA in combination with time-of-flight imaging can help reduce the overestimation of stenosis. Also, the computer can rotate the image in 360° and can help determine whether the visualized degree of stenosis is a projectional finding or a real stenosis. This is one advantage over angiography.

If duplex ultrasound and MRA are performed together and the patient has severe carotid stenosis and both studies agree, then 100% accuracy can be achieved.2,17,22,23 This is remarkable, as most imaging studies can never hope to approach 100% accuracy.

Many centers now perform MRA alone in patients who are evaluated for surgery without any false-positive results.33 As described previously, MRA is superior to ultrasound in delineating carotid stenosis. Other advantages already described are the ability to detect tandem lesions and the easier visualization of the vertebral arteries and the intracranial vasculature. MRA also is excellent for the evaluation of carotid dissection.

Another rare pitfall of MRA is the possibility of diagnosing a complete occlusion when, in fact, there is an extremely high-grade stenosis with very slow flow through the area of stenosis.17,21,30 Again, this pitfall can be avoided by evaluating source data and axial images and performing phase-contrast imaging (figure 2). Also, correlation with ultrasound and the patient's symptoms could help avoid this pitfall.

MRA and ultrasound are complementary modalities, as duplex ultrasound has certain advantages over MRA. Thus, the two modalities should be used in conjunction with each other, and the pitfalls of each modality should be known, evaluated, and applied to each individual patient and circumstance.

Angiography

Angiography often has been described as the gold standard for evaluating carotid stenosis or occlusion. But what is a gold standard? Oftentimes in imaging, certain studies are called the gold standard. Thus, if the gold standard indicates one finding, it often is accepted as fact.

However, this often is not the case. Ninety percent correlation of angiography with MRA does not mean that angiography is 10% more accurate than MRA or ultrasound. In the series of 94 carotid arteries studied by Litt et al, interobserver agreement for grading conventional carotid angiograms was only 72%.1,8 In the study by Chikos et al, the intraobserver agreement was only 82%, and the interobserver agreement was only 74%.1,18

Angiography is an invasive procedure, and complications include hemorrhage, infection, arteriovenous fistula, pseudoaneurysm, dissection, embolic stroke, and death, with a potential total complication rate of up to 4%.25,31 There also is the risk of an allergic reaction to the contrast, and the patient may not be able to cooperate with the study after the procedure has begun.

Angiography results also vary depending on whether digital angiography or film screen angiography is performed. The Asymptomatic Carotid Study Group reported at least a 1.2% incidence of carotid-associated infarction (National Institute of Health Clinical Advisory, September 28, 1994). The incidence of catheter-related infarction or complication rates from angiography often are reported from institutions where dedicated fellowship training invasive radiologists are performing multiple daily examinations. Obviously, the complication rate will be higher in the community hospital setting. Angiography complication rates almost double in patients with ischemic disease, compared to those studied for other indications. Also, the risk will vary depending on the age of the patient and other risk factors.

Angiography has other pitfalls. The degree of stenosis may vary depending on the orientation and projection performed. Thus, stenosis may be under- or overestimated, based on the projection. The increased number of projections can help avoid this pitfall, but the longer the catheter is in place (either in the patient's groin or in the carotid artery), the greater the complication rate. Angiography also may be difficult if there are very tortuous overlapping vessels. Also, as previously described, angiography only measures the actual patent lumen. The vessel wall itself cannot be evaluated. Thus, stenosis may be under- or overestimated.

As described previously, angiography is less sensitive than MRA or ultrasound in evaluating ulcerated or hemorrhagic plaques. In some patients, angiography is more accurate than ultrasound or MRA in evaluating the degree of stenosis because of the previously described pitfalls of MRA and ultrasound.

Computed tomography angiography

Computed tomography angiography requires the combination of a helical scanner and intravenous contrast enhancement. Multiple studies claim a sensitivity and specificity approaching MRA results. Marks recently reviewed several papers that demonstrated a sensitivity of 82% to 100% and a specificity of 94% to 100% for the detection of surgically treatable stenosis.41

CT angiography has certain advantages over MRA. It is not as susceptible to flow artifact and patient motion. Also, claustrophobic patients and patients with pacemakers can be imaged. However, CT angiography does require contrast injection, and it is limited in patients with severe concentric calcifications. Because its results parallel those of MRA, it may be able to replace MRA in the provided algorithm (figure 5).

Conclusion

What is the most practical approach for the evaluation and diagnosis of carotid vascular disease? There is controversy in the literature. However, if one can obtain almost 100% accuracy with the combination of MRA and ultrasound, why proceed with angiography and its risk of complications (figure 5)? De Marco et al recently suggested that noninvasive studies can replace conventional angiography.42 (Please see the algorithm that has been provided, which can help make a more accurate assessment of patients with carotid vascular disease.)

There is no one test that has 100% accuracy. Angiography, duplex ultrasound, and MRA all have certain advantages and disadvantages. The important thing is to recognize the advantages, disadvantages, and pitfalls and how to avoid and overcome them.

As with any procedure in medicine, one has to assess the risk-benefit ratio. Ultrasound is an excellent screening study; it is accurate, inexpensive, and quick, and it can be performed at the bedside. Ultrasound should be the screening study of choice. Its advantages include its ability to evaluate the plaque morphology and correlate this with the patient's symptoms. If the ultrasound is normal or demonstrates mild disease, then why proceed with MRA or angiography? There are few false-negative cases (figure 5).

If there are technical problems with ultrasound or a discrepancy between the velocity measurements and the measured stenosis and if there is moderate to severe disease, then proceed with MRA (figure 5).19

At certain institutions, surgery is performed on the basis of ultrasound findings only. If there is a technically good study and the degree of the visualized stenosis corresponds with the velocity measurements, then ultrasound is fairly accurate. This depends on the institution and the degree to which the surgeons feel comfortable with the procedure.36,37,39

If there is a discrepancy between the ultrasound and the MRA, it may be better to repeat one of the two studies, depending on which type of pitfall was encountered. The visualization of the MRA 2D axial images, 3D rotating images, phase-contrast MRA, or even the IV injection of gadolinium can be performed to overcome these pitfalls rather than proceeding to angiography. Angiography should be reserved for cases in which the MRA and ultrasound still disagree on repeat imaging (figure 5).

Conventional angiography or CT angiography can be performed in patients in whom MRA cannot be performed due to pacemakers or metallic implants. Conventional angiography or CT angiography also can be indicated in cases in which subtotal occlusion is suspected but not demonstrable on ultrasound and MRA.

Duplex ultrasound, MRA, CT angiography, and conventional angiography should be used in conjunction with each other, and the pitfalls of each should be known, evaluated, and applied to each individual case. AR

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