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1
Department of Radiology, The Cleveland Clinic Foundation, Desk Hb6, 9500
Euclid Ave., Cleveland, OH 44195.
2
Department of Diagnostic Radiology, Allegheny General Hospital, 320 E. North
Ave., Pittsburgh, PA 15212-9986.
Received March 25, 1999;
accepted after revision July 15, 1999.
Address correspondence to A. Dagirmanjian.
Abstract
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SUBJECTS AND METHODS. Seven patients undergoing carotid angiography were evaluated with transcranial Doppler sonography. Patients were also screened for ICA occlusions using carotid duplex sonography. In the seven patients, we saw five right ICA occlusions and two left ICA occlusions. Real-time visual and auditory confirmations of emboli were obtained by recognizing their specific spectral signatures and harmonic qualities. Routes of collateral flow were determined from angiography. Specific phases of the examination were correlated with embolic occurrences.
RESULTS. Overall, emboli were seen during all phases of arteriography. In the individual patients, emboli were identified in one to four of the eight angiographic phases we defined. Most emboli occurred during catheter flushing and contrast injection rather than during wire and catheter manipulation. The emboli were detected in the middle cerebral artery distribution ipsilateral to the occluded ICA in all seven patients. Collateral flow patterns included, in four patients, external carotid artery—to-ICA collateral flow; in all seven patients, patent anterior communicating arteries; and in three patients, patent posterior communicating arteries.
CONCLUSION. Emboli seen in middle cerebral arteries ipsilateral to occluded ICAs during cerebral angiography strongly indicate that emboli can occur distal to an occlusion. Our findings support the thought that emboli arising from sources proximal to an occluded ICA may reach the hemisphere distal to the occlusion, resulting in parenchymal ischemia or infarction.
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We reported previously on the transcranial Doppler detection of clinically silent intracranial emboli during carotid catheter angiography in 15 patients [8]. In retrospect, three patients emerged from this group in whom emboli were detected in the middle cerebral artery ipsilateral to an occluded ICA. We prospectively obtained transcranial Doppler sonograms of the middle cerebral artery during intraarterial digital subtraction angiography of the aortic arch and carotid arteries in four additional patients to further determine the routes of intracranial embolization in patients with occluded ICAs.
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Digital subtraction angiography was performed by neuroradiologists with the assistance of neuroradiology fellows and residents. The catheter was introduced into the common femoral artery. A 0.038-inch (1-mm) flexible polytetrafluoroethylene-coated guidewire was used. Arch arteriography was performed with pigtail catheters (Cook, Bloomington, IN), and selective carotid catheterization was performed with 5-French Simmons 2.0 catheters (Meditech, Watertown, MA). Plastic syringes were used for flushing the catheter with heparinized saline (1 ml/500 ml) and for test injections of contrast material. Injector syringes and stopcocks were plastic. Digital subtraction angiography of the aortic arch was performed after 10-15 ml of ioversol (Optiray 240; Mallinckrodt Medical, St. Louis, MO) or meglumine diatrizoate (Hypaque Meglumine 60%; Nycomed, New York, NY) was injected for a total of 20-30 ml. Digital subtraction angiography of the carotid bifurcation was performed after 3-4 ml of contrast material was injected into each artery for a total of 4-6 ml. A closed reservoir system was used for refilling syringes with saline and contrast material and for expelling waste material [9]. Injections were given with a Mark IV power injector (Medrad, Pittsburgh, PA).
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On angiography, only patient 4 showed mild irregularity of the aortic arch consistent with atherosclerotic disease. Patients 1, 3, 4, and 7 had a 50-60% stenosis of the contralateral internal arteries and mild irregularity of the common carotid arteries without significant stenosis. Patients 2, 5, and 6 had widely patent contralateral internal and common carotid arteries without evidence of atherosclerotic change on angiography. Patients 1, 2, 4, and 6 had residual ICA stumps.
All potential collateral pathways were not evaluated in every patient. Vertebral arteries are not routinely injected during evaluation of the carotid bifurcations. The patterns of collateral flow are shown in Table 2. Patients 1, 2, 3, and 5 did not have vertebral artery injections so the status of the posterior communicating artery is not known in these patients. In addition, we were not able to insonate the middle cerebral artery during injection of the vertebral arteries in patient 4 because the probe obstructed our view.
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Each patient was tested for gross motor, sensory, cranial nerve, and verbal responses after each injection and at termination of the procedure. Nursing personnel monitored vital signs and oxygen saturation. No gross transient or permanent neurologic sequelae occurred during this study. Subtle neurologic changes related to the emboli may not have been detected.
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Georgiadis et al. [7] were able to physically document embolization by showing that emboli exist in anterior cerebral arteries ipsilateral to ICA occlusions in patients with contralateral carotid stenosis. These researchers showed flow reversal in the ipsilateral anterior cerebral artery, thus documenting that the vessel was serving as a collateral flow. They hypothesized that contralateral carotid endarterectomy may eliminate this source of embolization.
Moody et al. [10] have provided pathologic evidence of emboli. These researchers observed focal dilatations of small capillaries and arterioles in the brains of patients who had undergone cardiopulmonary bypass. They speculated that these dilatations represented gas bubbles of fat emboli. They also observed smaller numbers of these dilatations in the brains of patients who had not undergone cardiopulmonary bypass but had undergone proximal angiography. This finding suggests that these emboli may be liberated during arteriography proximal to the brain.
The embolic events that we observed during carotid angiography with transcranial Doppler sonography of the middle cerebral arteries may represent the precursors of these dilatations. Moody et al. [10] observed dilatations 10-50 µm in diameter in terminal arterioles and capillaries. However, in larger arterioles, the dilatations were frequently as large as 40 µm. These measurements would be within the range of detection for transcranial Doppler sonography, which has been shown to detect gaseous microemboli as small as 30 µm [11, 12]. Transcranial Doppler sonography has a high degree of sensitivity and specificity for the detection of embolic occurrences [13]. Emboli have a signal intensity of 3 dB or more greater than the background Doppler signal and a characteristic harmonic quality [14, 15]. The sound produced can be described as chirps and whistles, depending on the size and composition of the emboli. The size or composition of an embolus cannot currently be determined by its transcranial Doppler signal [16]; however, transcranial Doppler sonography continues to be routinely used for emboli detection during cardiopulmonary bypass surgery and carotid endarterectomy, and in patients with prosthetic valves [14, 17, 18].
Previously, we reported our results of transcranial Doppler monitoring of a group of patients with carotid bifurcation atherosclerotic disease during catheter angiography [8]. We detected microemboli distal to occluded ICAs in a subgroup of these patients. Microemboli were detected in the ipsilateral middle cerebral artery during selective common carotid artery angiography of an occluded ICA in two of the three patients. Both patients had collateralization via the ophthalmic artery to the ipsilateral ICA. Emboli were also detected in the ipsilateral left middle cerebral artery in the third patient. However, only nonselective injections of the left common artery were performed because of the inability to select the left common carotid artery. External carotid artery—to—internal artery collaterals could not be seen, but a left vertebral artery injection showed filling of the left middle cerebral artery via a posterior communicating artery that may have represented the route for emboli we detected in the left middle cerebral artery. We decided that these findings were objective evidence that proximal sources of emboli can embolize distal to ICA occlusions via collateral flow pathways.
The four patients we prospectively evaluated again showed emboli during catheter angiography distal to ICA occlusions caused by a proximal source of clinically silent embolization [8]. Patients 2 and 4 are straightforward. External carotid artery—to-ICA collateral flow via the ophthalmic artery provided the pathway for embolization. In patient 4, emboli were insonated during both aortic and common carotid angiography. In this patient, the potential routes for embolization during arch angiography included the anterior communicating artery, the posterior communicating artery, and the ophthalmic artery. During common carotid angiography, the ophthalmic artery provided the route for embolization in patient 4. In patients 1 and 3, the anterior communicating artery may have represented the route for embolization during aortic arch angiography. The status of the posterior communicating arteries was not known in either patient. Emboli were also detected in patients 1 and 3 during selective common carotid artery angiography; however, no clear collateral flow to the carotid siphon could be shown radiographically in these patients. External carotid artery—ICA collaterals may have existed but may not have been evident as a result of the digital subtraction technique, low frame rates, or low total contrast injection volumes. Alternatively, emboli may have traveled via the ipsilateral posterior communicating artery. Both injections were right common carotid artery injections and contrast material may have refluxed into the posterior circulation via the subclavian artery.
We previously reported the association of emboli with catheter angiography [8]. The importance of this article is not the actual number of the embolic phenomena, but their presence distally in an occluded carotid system. The presence of emboli in middle cerebral arteries ipsilateral to occluded ICA during cerebral angiography strongly suggests that emboli can occur distal to an occlusion from a proximal source. This supports the previous work in the literature [1, 2, 3, 4, 5, 6, 7]. In conclusion, our findings indicate that emboli arising from sources proximal to ICA occlusions may reach the hemisphere distal to an occlusion and result in parenchymal ischemia or infarction.
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