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Original Research |
1 Department of Radiology, University of Southern California Keck School of
Medicine, University Hospital, 1500 San Pablo St., Los Angeles, CA
90033.
2 Department of Radiology, West Los Angeles VA Medical Center, Los Angeles,
CA.
3 University of Miami Medical School, Miami, FL.
4 Department of Vascular Surgery, West Los Angeles VA Medical Center, Los
Angeles, CA.
5 University of Wisconsin School of Medicine, Madison, WI.
Received June 25, 2004;
accepted after revision January 24, 2005.
Address correspondence to E. G. Grant.
Abstract
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MATERIALS AND METHODS. A review of all cerebrovascular sonograms at our institutions was undertaken to identify patients with complete or partial flow reversal in the right vertebral artery and reversal or midsystolic deceleration of flow in any one of the three major segments of the right carotid system (common, internal, or external carotid artery). The distribution and appearance of these abnormalities was evaluated, and the presence or absence of tardus-parvus waveforms was noted in any segment of the right carotid artery. Additionally, a left to right common carotid peak systolic velocity ratio (LCCA/RCCA) was calculated and compared to published normal values. All patients had correlative contrast or MR angiography. Correlation was made between the severity of stenosis as determined by angiographic images and waveform aberrations as well as the more objective LCCA/RCCA ratios.
RESULTS. Twelve patients were identified as having the abnormalities described above in the right vertebral and carotid arteries. Doppler waveforms from the right vertebral artery revealed that eight of the 12 patients had complete reversal of flow at rest. Bidirectional flow was found in the remaining four as manifested by the presence of marked midsystolic deceleration. In the carotid arteries, one patient had complete reversal of flow in all segments of the right carotid system. Waveforms with midsystolic deceleration were identified in at least one of the carotid arteries of the remaining 11 patients: common carotid artery (8/11 = 73%), internal carotid artery (10/11 = 91%), external carotid artery (3/11 = 27%). The average LCCA/RCCA was 3.1 with a range of 1.7 to 5.7 (normal = 0.7-1.3). All patients had severe innominate artery disease (from 70% to occlusion) by contrast angiography or MR angiography. There was no correlation between the angiographically determined degree of stenosis and the Doppler findings.
CONCLUSION. A distinctive pattern of hemodynamic alterations occurs in the right vertebral and carotid arteries of patients with severe innominate artery disease. Findings include reversed or bidirectional flow in the right vertebral artery, the presence of midsystolic deceleration in any of the branches of the right carotid system, and elevated LCCA/RCCA ratio.
Keywords: angiography • cardiovascular disease • Doppler sonography • innominate artery • subclavian steal syndrome
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The invasive and noninvasive findings of innominate artery stenosis and occlusion have been reported in the remote past, but a detailed evaluation emphasizing the color and duplex Doppler findings observed at sonography performed with current technology has not been undertaken to our knowledge. Because sonography is currently the initial examination for most patients undergoing evaluation for cerebrovascular disease, physicians need to be aware of the features of possible innominate artery compromise. The purpose of this article, therefore, is to describe the sonographic features of a series of patients with innominate artery stenosis or occlusion and correlate those features with findings on contrast-enhanced or MR angiography [7-9].
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One experienced neuroradiologist and one sonologist independently reviewed all angiograms and color duplex sonography examinations thus located. On the sonography examinations, the vertebral arteries, CCA, ICA, and ECA were evaluated bilaterally for flow direction and waveform configuration as displayed by color and spectral analyses. In addition to noting the possible finding of complete flow reversal in any of the arteries mentioned, evaluation included examination for presence and severity of midsystolic deceleration. Because we were dealing with potential poststenotic flow, the presence or absence of tardus-parvus waveforms was also evaluated. The tardus-parvus phenomenon has been described in several other arteries distal to a vessel with significant narrowing and is typified by a delayed systolic upstroke and loss of the early systolic peak [11, 12]. Comparisons were also made between peak velocity in the right CCA (RCCA) and left mid CCA (LCCA) in each patient and a ratio (RCCA/LCCA) was calculated. The waveforms obtained after provocative maneuvers (blood pressure cuff-induced arm ischemia) were recorded when a maneuver was performed. In an effort to further our understanding of possible collateral pathways in these patients, resistivity was calculated in the ECAs bilaterally.
Correlation was made between the severity of stenosis as determined by angiographic images and waveform aberrations and the more objective LCCA/RCCA ratios. Angiographic measurements of innominate artery stenoses were obtained directly from the conventional angiographic images and from the source images of MR angiograms. Measurements were performed at the narrowest segment and compared with the nearest distal segment of normal-appearing lumen to calculate the percentage of reduction in the luminal diameter.
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Eleven of the 12 patients had histories typical of severe atherosclerotic vascular disease (coronary artery disease, lower extremity disease, claudication, and so on), and one had Takayasu's arteritis. Four patients were clinically asymptomatic: three were referred for sonography on the basis of neck bruits, and one underwent sonography as part of an evaluation before coronary artery bypass surgery.
Of the eight symptomatic patients, two had a history of amaurosis fugax involving the right side, three had syncope (one of these had symptomatic subclavian steal syndrome manifested as dizziness with exercise of the right arm), and three had a history of stroke. Among the latter group, two had previous right hemispheric strokes with infarctions proven by CT and presented with recurrent transient ischemic attacks, and the third patient had cerebellar infarcts on MRI. Two of the 12 patients underwent surgical correction of the innominate lesion with bypass grafting. In one case, the innominate artery occlusion was bypassed using a Y graft from the aorta to the CCA and right subclavian artery, whereas in the other patient an axillary-to-axillary graft was constructed. In both patients, there was symptomatic improvement. One additional patient refused surgery and was lost to follow-up. The remaining nine were treated conservatively.
Evaluation of the Doppler waveforms from the right vertebral artery revealed that eight of the 12 patients had complete reversal of flow. In five of these eight cases, there was a low-resistance spectral waveform at rest with retrograde (caudad) flow throughout the entire cardiac cycle (Fig. 2A). In the other three patients, flow was retrograde during systole and absent throughout diastole (Fig. 2B). In the remaining four patients, a partial steal was manifest as marked midsystolic deceleration. Three of these patients underwent a provocative maneuver that induced hyperemia of the right arm (3-min occlusive inflation of a blood pressure cuff on the right arm with subsequent release), and their bidirectional flow converted to complete flow reversal (Figs. 3A and 3B). Of note, there was minimal change in the waveforms of the carotid arteries, as opposed to the waveforms of the vertebral artery, in response to the ischemic maneuver.
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In evaluating the carotid arteries, we found that one patient had complete reversal of flow in all segments of the right carotid system—that is, the ECA, CCA, and ICA. This patient had Takayasu's arteritis (Figs. 4A, 4B, 4C, and 4D). MR angiography showed innominate artery occlusion (Fig. 4E). Waveforms with varying degrees of midsystolic deceleration were identified in at least one of the carotid arteries of the remaining 11 patients (Figs. 5A, 5B, 5C, and 5D). These distinctive waveforms were not found in all arterial segments of the right carotid system in every patient. They were most common in the CCA (8/11 [73%]) and ICA (10/11 [91%]) and were found in the ECA in a minority of patients (3/11 [27%]). Tardus-parvus waveforms were never found in the right CCA or ICA of any patient and were questionably present in one ECA segment.
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All patients who had sonography findings suggestive of innominate artery disease had a confirmatory correlative imaging examination that depicted stenosis or occlusion. In all cases, stenosis or occlusion was confirmed. The degree of stenosis measured at conventional angiography or MR angiography ranged from 70% to occlusion (100%), with an average percentage of narrowing of 84.6%.
As we mentioned, we detected no correlation between CCA ratios and the severity of stenosis. With regard to the qualitative waveform analysis, although the patient with the most pronounced qualitative Doppler waveform changes (complete flow reversal in all portions of the CCA and vertebral arteries) did, indeed, have a complete occlusion of the innominate artery, a second patient with innominate artery occlusion had waveform features that were indistinguishable from those of other patients with lesser degrees of stenosis.
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The degree to which the carotid circulation was affected was more varied. Doppler findings ranged from subtle midsystolic deceleration to complete reversal of flow, the so-called "innominate steal phenomenon" [14, 15]. This latter finding was present in one of our 12 patients and has rarely been reported. Reversal of carotid flow was described in only one of six patients in the series of Verlato et al. [16] and in two of 20 patients reported by Brunhölzl and von Reutern [5]. Killen and Gobbel [17], in fact, termed preservation of antegrade flow in the right carotid system at the expense of the vertebral artery as "carotid recovery." Although the physiologic basis for this phenomenon has not been thoroughly explained, it is likely that flow is more readily diverted across the vertebrobasilar junction than across the circle of Willis.
Midsystolic deceleration in the vertebral artery has been described previously as part of a spectrum of increasingly severe flow disturbances produced by progressive compromise of flow in the more proximal subclavian artery. Waveform abnormalities range from a mild to moderate decrease in forward flow velocity immediately after peak systole to prolonged periods of flow reversal with restoration of forward flow in diastole and, ultimately, to complete reversal of flow throughout the cardiac cycle. Similar physiology is undoubtedly also responsible for this distinctive finding occurring in the right carotid arteries of patients with severe innominate artery disease.
Several theories have been proposed to explain the cause of midsystolic deceleration in the vertebral artery seen in patients with subclavian stenosis and can likely be extended to the right carotid system in patients with innominate artery disease. Kotval et al. [18] proposed that the rapid deceleration after peak systole results from the pressure gradient that occurs beyond the subclavian stenosis relative to that of the systemic circulation. As systole progresses and systemic pressure exceeds that in the arm, blood flow slows dramatically or reverses in the vertebral artery. As systemic pressure falls in late systole and diastole, the pressure in the poststenotic segment eventually exceeds systemic pressure and antegrade flow is restored in the vertebral artery, accounting for the forward flow seen in diastole at sonography. As the proximal stenosis worsens, midsystolic deceleration and eventually flow below baseline (flow reversal) occupy an increasing portion of each cardiac cycle.
Although the explanation is generally accepted for the classic subclavian steal physiology, midsystolic deceleration in the carotid system is more difficult to explain. Flow direction is likely determined by both pressure and peripheral resistance. The midsystolic deceleration in the carotid artery may be the result of a pressure differential between two connected circuits (the left and right carotid arterial systems) communicating through the circle of Willis. Antegrade flow in late systole and diastole in the low-pressure system could reflect a lesser pressure differential between the two systems, both flowing into the equally low-resistance intracranial cerebral circuit.
Considering the central location and large caliber of the innominate artery and the presumed gradual development of stenosis or occlusion in most patients, the potential for recruiting collateral arterial flow is considerable and extends beyond the vertebrobasilar system. The right vertebral artery may steal blood flow from the left vertebral artery, the ipsilateral occipital branch of the ECA, or the circle of Willis via the posterior communicating arteries. Potential sources of collateral flow for the ICA include the circle of Willis, ipsilateral ECA-to-ICA collaterals, and leptomeningeal artery-to-artery collaterals.
The right ECA shows midsystolic deceleration or flow reversal less frequently than the CCA, ICA, or vertebral artery. The rich collateral bed between the right and left ECA may well be the reason for this observation because it provides a good source of antegrade flow. The potential for numerous and varied collateral circulatory pathways explains the observation that midsystolic deceleration does not affect all vessels in the right carotid and vertebral systems equally. It also likely explains the poor correlation between the severity of angiographically measured stenosis and the severity of the Doppler waveform abnormalities. Furthermore, it is likely that the sonographic abnormalities associated with innominate artery disease are not static and change as new collaterals are recruited.
The dominant collateral circulatory routes and the ability to estimate the degree of innominate artery stenosis are further complicated by the fact that many patients with lesions of the innominate artery have stenoses elsewhere in the cerebrovascular system that can also change over time. Although Brunhölzl and von Reutern [5] proposed a classification system of innominate artery stenosis based on various subjective Doppler criteria from both the extracranial and intracranial vessels, our experience is more in keeping with that of Schwend et al. [10] who thought that the variability in Doppler findings was more reflective of collateral circulatory patterns than of the severity of innominate artery stenosis.
Although patients with typical subclavian steal physiology are symptomatic only rarely, patients with innominate artery lesions have a fairly high incidence of clinical manifestations of their disease. In our series, eight of 12 patients presented with a wide variety of symptoms referable to both the posterior circulation (syncope and cerebellar infarcts) and the anterior circulation (right-sided amaurosis fugax or stroke). Earlier reports described similar patterns, with a preponderance of posterior circulation ischemic symptoms. In the largest series to date, Brunhölzl and von Reutern [5] found that 10 of their 20 patients had symptoms referable to the posterior circulation; seven were asymptomatic; and three had hemispheric symptoms, such as transient ischemic attack or stroke. In that series, most patients with hemispheric symptoms also had concurrent ipsilateral ICA disease. This was not the case in our series. In both of our patients with right hemispheric strokes, the right ICAs were normal.
Severe compromise of the innominate artery is an unusual phenomenon. Because of the small numbers of patients in our series and the lack of large numbers of comparative arch aortograms in all of the participating institutions, it is impossible to determine the sensitivity of sonography in the diagnosis of innominate artery disease. Likewise, the degree of stenosis necessary to produce alterations in the carotid circulation and vertebral circulation cannot be precisely determined from existing data; however, among our patients, it should be noted that all had severe stenosis, ranging from 70% to occlusion. Given this degree of stenosis, it seems likely that the noninvasive findings described in this and other series become manifest only when there is marked compromise of innominate artery flow. This is difficult to confirm on review of the literature because the degree of stenosis by angiography was frequently not given.
The use of the LCCA/RCCA ratio might allow lesser degrees of stenosis to be detected by Doppler examination. This objective parameter has not been used in the diagnosis of innominate artery disease in previous studies, to our knowledge. Patients in our series had LCCA/RCCA ratios ranging from 1.7 to 5.7, which are well above the normal values of 0.7-1.3 established by Vaisman and Wojciechowski [19]. Although sensitivity of Doppler sonography in the diagnosis of innominate artery disease remains in question, reversal of flow in the right vertebral artery in connection with midsystolic decelerations in the right carotid artery appears to be specific. All 12 patients with these findings on sonography were confirmed to have innominate artery disease by angiography.
In conclusion, a distinctive pattern of hemodynamic alterations occurs in the right vertebral and carotid arteries of patients with severe innominate artery disease that is readily recognized on sonography. Findings include reversed or bidirectional flow in the right vertebral artery, the presence of midsystolic deceleration in any of the branches of the right carotid artery system, and an elevated LCCA/RCCA ratio. Given that sonography is frequently the initial or only imaging examination that patients suspected of having cerebrovascular disease undergo, it is essential to recognize these findings because innominate artery lesions are associated with neurologic symptoms in a high percentage of patients.
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