Discussion
The number of carotid arteries supplying the cerebral circulation (carotid score) in the setting of IAT for large (M1 or T-top) artery occlusion seems to be an independent predictor of good clinical outcome after 3 months. However, we observed no relation between completeness of the circle of Willis and clinical outcome after IAT.
Incompleteness of the circle of Willis may result in worse cerebral perfusion and hence more damage in case of acute cerebral ischaemia.10–12 Previous studies have shown that completeness of the circle of Willis, particularly the posterior circle of Willis, is a hallmark of deteriorated cerebral perfusion.24 25 In addition, patients with ipsilateral carotid occlusion before IAT in whom ACoA or PCoA or both were absent were shown to have less favourable clinical outcomes at 90 days.26 We could not confirm such a detrimental effect in our patients who had a stroke with an incomplete circle of Willis treated with IAT. A possible explanation for this might be that in our study, only three patients (2%) suffered from an ipsilateral carotid occlusion. We did find a negative influence of impaired carotid contribution by means of our carotid score. Hence, one could hypothesise that the sum of both the carotid occlusion and the incompleteness of the circle of Willis results in less favourable outcome in the aforementioned study. A larger, more recent study combined patients from the DEFUSE2 and CRISP Studies and studied completeness of the circle of Willis in relation to functional outcome after IAT. In line with our results, no association was found between incomplete circle of Willis and functional outcome.27
Contralateral carotid occlusion is well known to increase risk of stroke or death in patients treated with carotid endarterectomy because of symptomatic carotid stenosis.28 In addition, contralateral carotid artery stenosis has been shown to be an independent predictor of poor clinical outcome in patients who had a stroke with acute tandem occlusion treated with IAT.29 These studies are in line with our results, showing that that loss of carotid arteries supplying the cerebral circulation reduces the likelihood of good clinical outcome. Conversely, another study showed that there was no strong effect of a coexisting ICA stenosis in acute MCA stroke on tissue status or perfusion parameters on MRI.30 Moreover, cerebral blood volume was found to be elevated in patients who had a stroke with coexisting ICA stenosis, possibly reflecting improved peripheral collateral circulation. However, patients with carotid occlusions were excluded in this study, only ipsilateral carotid stenosis was studied.
Our study has several limitations. First, our study focused on the collateral circulation by the circle of Willis and carotid arteries. Previous studies have shown that the leptomeningeal collaterals play a key role in chances of successful recovery after IAT.3 13–15 31 32 We, therefore, included a score for leptomeningeal collaterals (CFG)19 and corrected the RR for good clinical outcome for this score (see online supplemental table). After this adjustment, however, the RRs remained essentially the same. Second, we did not measure the flow in the ophthalmic artery. When flow is reversed in the ophthalmic artery, it also functions as collateral for the cerebral circulation. Nevertheless, this reversed flow is merely considered an indicator of diminished cerebral perfusion24 and as such not a rescue pathway for cerebral circulation in case of an acute cerebral arterial occlusion. Third, extracranial carotid disease and basilar artery disease were not included in the study. One could hypothesise that any atherosclerotic disease on these locations also influences the cerebral collateral circulation. In addition, we did not register the presence of fetal-type posterior cerebral artery. The presence of such artery might substitute loss of blood flow in case of an occluded ipsilateral carotid artery and hence influence extent of infarction and functional outcome. However, given the rather low number of patients included in our study, we assume that these effects are limited. Fourth, patients included in our cohort were treated with IAT in the era before IAT was standard of care. We realise that our series is relatively old; however, we think we still retrieve valuable information from it about the pathophysiology of reperfusion and outcome. Although the applied IAT techniques were probably less sophisticated as they are nowadays, we do not expect that this had a substantial impact on our results because our study aimed at finding causal relation between completeness of the circle of Willis and clinical outcome after IAT and hence studied cause of disease.
A possible explanation for the lack of a positive relation between completeness of the circle of Willis and clinical outcome might be that we studied the primary circulation in the acute setting. Previous studies showed that collateralisation may take months to develop and animal models show that restoration of blood flow through collateral vessels after MCA occlusion takes a month.33 34 Most of these studies focused on the role of the collateral circulation by the circle of Willis in patients with atherosclerotic carotid artery disease. We did not select our cohort based on the presence of carotid artery disease. However, we did study the effect of the number of carotid arteries supplying cerebral circulation and found a relation between this carotid score and clinical outcome.
In patients with acute ischaemic stroke treated with IAT, chances of good clinical outcome improve with the number of carotid arteries supplying the cerebral circulation. Completeness of the circle of Willis does not seem to relate to clinical outcome after IAT. Further studies are needed to confirm our findings in a larger cohort.