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1 Both authors: Department of Radiology, University of North Carolina at Chapel Hill, CB #7510, 101 Manning Drive, Chapel Hill, NC 27599-7510.
Received July 25, 2006;
accepted after revision August 8, 2007.
Address correspondence to B. Y. Huang
(bhuang{at}unch.unc.edu).
Abstract
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A 50-year-old man presented with neurologic symptoms and upper extremity claudication associated with exercise. Perfusion MRI of the brain showed delayed time-to-peak in the right cerebral hemisphere, and MR angiography (MRA) of the circle of Willis showed decreased flow-related enhancement in the right internal carotid artery and its branches. Neck MRA showed occlusion of the right innominate (brachiocephalic) artery and retrograde flow in the ipsilateral vertebral artery. On the basis of this clinical scenario, we discuss the radiologic evaluation of unilateral decreased brain perfusion, which, in this case, was due to an occlusion of the innominate artery with resultant innominate steal.
Conclusion
In the absence of an explanatory intracranial stenosis, the finding of unilateral decreased cerebral perfusion on MRI or CT mandates evaluation of the aortic arch and cervical arteries to determine a level and cause of occlusion. Severe stenoses may be associated with steal phenomena, which can be diagnosed with MRA or Doppler sonography.
Keywords: angiography • brain perfusion • neuroimaging • subclavian steal syndrome
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Nonatheromatous processes, including arterial dissection, embolus, vasculitis (especially Takayasu's arteritis), fibromuscular dysplasia, and tumor compression could also result in significant carotid stenosis. These entities should be included in the list of potential causes of abnormal unilateral cerebral perfusion, particularly with appropriate clinical history. Options for investigating the arteries of the neck include Doppler sonography, MRA, CT angiography (CTA), and catheter angiography of the aortic arch and the great vessels.
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Although digital subtraction angiography (DSA) has been considered the gold standard for diagnosing and characterizing cerebrovascular steal phenomena, Doppler sonography and MRA have supplanted DSA as first-line imaging techniques. CTA can show stenoses in the innominate artery and the SCA, but will not show vertebral artery flow reversal. Ultimately, the diagnostic study of choice will depend on the preferences of the individual radiologists and their referring clinicians.
In some institutions, MRA has become the preferred technique for investigating subclavian and innominate steal. As stated previously, we routinely use two separate and complementary techniques in our neck MRA protocol: an unenhanced 2D TOF sequence with saturation bands placed immediately above each image slice, and a subtracted 3D gadolinium-enhanced technique. Each of these techniques has its own relative advantages and disadvantages, but each can add useful data not provided by the other. Our subtracted gadolinium-enhanced technique uses a 3D gradient-echo sequence that can be acquired in less than 20 seconds. Unenhanced and enhanced acquisitions are performed using the same parameters. The unenhanced series is then used as a subtraction mask, leaving a subtracted data set that shows only gadolinium enhancement in vessels. At the beginning of the acquisition, we use a bolus technique that is triggered manually by the technologist. Gadolinium-enhanced MRA is rapid and allows coverage of a large field of view (usually from the aortic arch to the skull base). This technique has reasonably good spatial resolution, and there is good correlation between 3D gadolinium-enhanced MRA and DSA for diagnosing significant carotid stenoses [5]. The technique has also been shown to be useful in ruling out significant stenoses at the ostia of the great vessels [6]. Limitations of the technique include nonspecific information about the direction of flow and dependence on accurate bolus timing. A mistimed contrast bolus can result in significant venous contamination.
Unenhanced 2D TOF MRA relies on differences in longitudinal magnetization that arise when unsaturated spins in flowing blood pass through stationary tissue containing saturated spins, a phenomenon known as "flow-related enhancement." Sequential slices are generated, with tissue in each image slice exposed to repeated excitation pulses, which causes partial saturation of spins. Because flowing blood is less saturated than background tissue, it has higher signal intensity. Saturation pulses placed immediately above each imaging slice can be used to reduce the signal created by blood flowing in the caudal direction (venous blood), so that only blood flowing in the cranial direction (arterial blood) is visualized. Advantages of this technique are that it requires no contrast agent, provides information about the direction of flow, and is sensitive to slow flow. Disadvantages are that it has a tendency to overestimate stenoses due to dephasing from turbulent flow, and that in-plane vessels will not show flow-related enhancement. Most TOF sequences take longer than the gadolinium-enhanced technique. As a result, the images are more susceptible to degradation by patient motion, particularly if patients swallow during acquisition. In addition, this technique generally does not provide the amount of coverage that the gadolinium-enhanced technique does.
In cases of subclavian steal, the 2D TOF technique provides valuable information about the direction of flow in the vertebral arteries. Specifically, if enhancement is present in a vertebral artery on gadolinium-enhanced MRA, but no corresponding flow-related enhancement is seen on TOF MRA, then flow in that vessel must be reversed.
We do not routinely use 2D phase contrast MRA for evaluation of the cervical vessels at our institution, but this technique can also provide directional information about flowing blood [7]. Two-dimensional phase contrast MRA relies on phase shifts that occur when flowing blood encounters a change in gradient strength. A velocity- or flow-encoding gradient pulse is applied between the initial excitation and the readout pulses, inducing a phase shift in moving protons, but not in stationary tissue. The velocity-encoding gradient is preselected on the basis of the range of velocities in which one is interested. Two acquisitions with velocity-encoding pulses of opposite polarity are obtained. The acquisitions are then subtracted, nullifying the signal of background tissue. In general, 2D phase contrast MRA provides better background suppression than TOF techniques. It also has the advantage of allowing velocity measurements because signal intensity is proportional to the velocity of flowing blood.
Sonography has been used in the diagnosis of subclavian steal and has the advantage of being a relatively rapid and inexpensive test with no exposure to ionizing radiation. Doppler sonography has the added benefit of being able to show changes in vertebral artery waveforms that are suggestive of early subclavian steal, even in the absence of frank flow reversal [8, 9]. In one small case series, Doppler sonography was highly sensitive and specific for the diagnosis of subclavian steal, and there was excellent correlation between sonographic waveform alterations observed in the vertebral artery and the degree of subclavian or innominate stenosis on angiography [8]. Altered vertebral artery waveforms are typically seen only when the degree of subclavian stenosis is greater than 60%; permanent flow reversal can be seen when a subclavian or innominate stenosis is greater than 75%.
Kliewer et al. [9] described four distinct waveform patterns (types 1–4) that occur in vertebral arteries before the onset of complete flow reversal in subclavian steal [9]. The type 1 waveform shows a transient decline in velocity at mid-systole, resulting in two systolic peaks; the velocity observed at the nadir of the notch created by the deceleration remains antegrade and greater than end-diastolic velocity. The type 2 waveform shows a more pronounced cleft between the two systolic peaks, with its nadir at or below velocity at end-diastole but above the baseline. In the type 3 waveform, the nadir of the mid-systolic cleft reaches the baseline. In type 4 waveforms, the nadir dips well below the baseline. A higher-type waveform generally reflects a more severe stenosis.
The major disadvantage of Doppler sonography is its high degree of user dependence. The sensitivity and specificity of the technique for diagnosing vascular steal depend largely on the skill and experience of the operator. In addition, factors such as patient habitus and anatomy can have a significant effect on one's ability to visualize the vertebral and subclavian arteries.
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Another steal phenomenon that has been described is carotid steal [10]. This entity occurs when there is severe stenosis or occlusion of the CCA or innominate artery and resultant diversion of blood from the contralateral external carotid artery (ECA) into the ipsilateral ECA to supply the ipsilateral ICA. In these cases, there is retrograde flow in the ECA on the side of the stenosis. Flow can also be recruited to the ECA via anastomoses between muscular branches of the vertebral arteries and the ipsilateral occipital artery. The diagnosis of carotid steal can be made on sonography [10] or DSA, but the usefulness of MRA in revealing this entity has yet to be determined.
Almost certainly, in most cases of carotid steal the ECA is not the sole supply of blood to the ICA because a number of additional pathways exist, not the least of which is the circle of Willis, that act to ensure continued perfusion to the affected hemisphere. Furthermore, it is also possible for multiple steals to occur simultaneously. In cases of innominate artery occlusion, for instance, both innominate and carotid steals can be observed, with the ICA being supplied via retrograde flow through both the ipsilateral vertebral artery and the ipsilateral ECA.
Early reports of subclavian steal, which included cases due to both subclavian and innominate stenosis, described a litany of symptoms, including symptoms of upper extremity ischemia (pain, claudication, and paresthesias) and various neurologic symptoms [2, 4, 11]. Diminished or absent upper extremity pulses on the side of the stenosis and asymmetric blood pressures are the most consistent clinical findings in symptomatic patients with subclavian steal [4, 11]. One review reported systolic blood pressure differences between the arms of greater than 20 mm Hg in 64 of 65 patients with subclavian steal [11]. Note that symptoms of upper extremity ischemia alone are observed in a minority of patients with subclavian steal. Most symptomatic patients (> 80%) have some neurologic complaints [4, 11].
The most common neurologic symptoms reported are dizziness, visual impairment, vertigo, and syncope [4, 11]. These symptoms are presumably due to shunting of blood away from the vertebrobasilar system into the affected SCA, resulting in posterior circulation ischemia (mainly affecting the brainstem, cerebellum, and occipital lobes), which manifested as occasional syncope in our patient. Although neurologic symptoms from a subclavian steal are classically exacerbated by exercising the affected extremity, this phenomenon is observed in only 16–52% of patients [4, 11].
Interestingly, many of the early reports of subclavian steal described a fairly large proportion of patients presenting with symptoms of anterior circulation ischemia [2, 4, 11], which is a bit difficult to reconcile with our understanding of normal aortic arch anatomy. It is unclear how an isolated SCA stenosis could cause symptoms of anterior circulation ischemia or a cerebral perfusion abnormality as dramatic as we observed in our patient. A recent retrospective review of cases of angiographically diagnosed subclavian stenosis noted that nearly 90% of patients with subclavian stenosis and unilateral hemispheric symptoms also had stenoses of the anterior circulation, usually involving the ipsilateral ICA [12]. Another review of 168 cases of subclavian steal phenomenon reported finding concomitant extracranial carotid stenoses in more than 80% of cases [13]. These observations, taken in concert with the observation that most instances of physiologic subclavian steal are neurologically asymptomatic [14], suggest that hemispheric symptoms in patients with subclavian steal are actually due to the presence other extracranial stenoses and not to the steal itself.
In our patient, the occlusion was located in the innominate artery, resulting in diminished flow to both the right CCA and the right SCA. This explains the findings on perfusion MRI and the symptoms of right upper extremity claudication. Symptoms of anterior circulation ischemia could easily result from significant hemispheric hypoperfusion due to diminution of flow through the right carotid artery, and in this case manifested as facial weakness.
The indications for treatment of subclavian steal remain controversial. As stated previously, it is now generally believed that subclavian steal is more likely to be a marker for significant atherosclerotic disease elsewhere in the head and neck than a true cause of symptoms. Therefore, treatment of subclavian and innominate stenoses resulting in steal should be reserved for patients with claudication or in whom the steal itself is determined to be the cause of neurologic symptoms. In these patients, surgical or endovascular intervention usually results in complete symptomatic relief. Surgical treatment options include carotid-to-subclavian bypass, subclavian-to-subclavian bypass, aortic-to-subclavian bypass, and carotid–subclavian transposition.
Percutaneous transluminal angioplasty (PTA) is gaining favor as an alternative to surgery for symptomatic subclavian and innominate occlusive disease and has shown promising results [15]. Placement of endovascular stents has also been performed and has been shown to improve short- and mid-term vessel patency over PTA alone, but the long-term benefits of stenting remain to be determined [16].
In summary, the finding of unilateral decreased cerebral perfusion on MRI or CT in the absence of an explanatory intracranial stenosis implies the presence of an upstream arterial stenosis and mandates evaluation of the aortic arch and cervical arteries to determine the level and, in some cases, the cause of obstruction. Severe stenoses may be associated with steal phenomena. MRA and Doppler sonography have largely supplanted DSA as the initial imaging techniques of choice for the evaluation of extracranial cerebrovascular disease and subclavian steal. Although neurologic symptoms are frequently seen in the setting of a subclavian steal, the steal itself is often not the underlying cause of these symptoms, but rather a marker for significant atherosclerotic disease elsewhere in the neck. Therefore, if a subclavian steal is detected on imaging, a thorough search should be performed for additional stenoses in the head and neck.
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