Collateral circulation in symptomatic intracranial atherosclerosis

Abstract

Collateral circulation in intracranial atherosclerosis has never been systematically characterized. We investigated collaterals in a multicenter trial of symptomatic intracranial atherosclerotic disease. Baseline angiography was reviewed for information on collaterals in stenoses of the internal carotid, middle cerebral, vertebral, and basilar arteries. A battery of angiographic scales was utilized to evaluate lesion site, arterial patency, antegrade flow, downstream territorial perfusion, and collateral circulation, blinded to all other data. Collateral circulation was adequately available for analysis in 287/569 (50%) subjects with proximal arterial stenoses ranging from 50% to 99%. Extent of collaterals was absent or none in 69%, slow or minimal in 10%, more rapid, yet incomplete perfusion of territory in 7%, complete but delayed perfusion in 11%, and rapid, complete collateral perfusion in 4%. Extent of collateral flow correlated with percentage of stenosis (P<0.0001), with more severe stenoses exhibiting greater compensation via collaterals. Overall, collateral grade increased with diminished antegrade flow across the lesion (thrombolysis in myocardial ischemia) and resultant downstream perfusion (thrombolysis in cerebral infarction) (both P<0.001). Our findings provide the initial detailed description of collaterals across a variety of stenoses, suggesting that collateral perfusion is a pivotal component in pathophysiology of intracranial atherosclerosis and implicating the need for further evaluation in ongoing studies.

Figure 1

Severe atherosclerotic stenosis of the proximal left middle cerebral artery (MCA) (A) with associated rapid and complete perfusion via leptomeningeal collaterals (B).

Figure 2

Specific patterns of collateral circulation associated with anatomical sites of intracranial stenosis. Leptomeningeal collaterals provide blood flow to the right middle cerebral artery (MCA) territory from the contralateral hemisphere in the setting of severe right internal carotid artery (ICA) stenosis and limited Willisian supply (A). A combination of antegrade and retrograde collateral perfusion feeds downstream tissue beyond an MCA stenosis (B). Cerebellar anastomoses between posterior inferior and superior cerebellar arteries distribute blood to offset midbasilar atherosclerosis (C).

Figure 3

Antegrade flow is largely preserved in an elongated stenosis of the left middle cerebral artery (MCA) despite considerable luminal irregularity and vessel tortuosity.

Figure 4

Posterior communicating artery flow maintains poststenotic regions of the basilar distribution (A). In another case, posterior cerebral artery anastomoses supply distal reaches of the anterior and middle cerebral arteries in an internal carotid artery (ICA) stenosis (B).