This study demonstrates that the presence of distal HV on initial FLAIR imaging is associated with smaller ischemic lesion volume on MRI and milder clinical severity as measured by the NIHSS. While all patients with proximal MCA occlusion had similar perfusion lesion volumes and some degree of diffusion–perfusion mismatch on initial MRI, patients with prominent distal HV had smaller initial ischemic lesion volumes, larger diffusion–perfusion mismatch, relatively smaller lesion growth, and smaller subacute ischemic lesion volumes than did patients without it. The mechanism and causality cannot be definitively established in this study, but it is reasonable to speculate that prominent distal HV may be reflective of good collateral blood flow distal to the site of arterial occlusion and less ischemic injury to tissue supplied by occluded artery.
We categorized the HV in MCA occlusion as occurring proximally and distally. Contrary to proximal HV, which frequently appears as a single, linear structure with limited curvature and with proximity to the M1–M2 segments of the MCA, distal HV appears as a varying number of serpentine vessel-like structures distal to the M2 segment and covers an area variable in size. Therefore, we implemented a grading system for distal HV based on the size of the area involved. Distal HV is frequently observed at the MCA M3 branch level, originating from an MCA M2 segment coursing anterior to posterior in the Sylvian fissure. The M3 branches in this area are still of relatively large vessel caliber and track predominantly in the plane of the axial FLAIR MRI slice, allowing for easy detection. More distal MCA branches are smaller and have an inferior–superior orientation that appear as bright dots in the transverse imaging and are therefore more difficult to detect.
Proximal HV, which is frequently observed proximal to or within the Sylvian fissure, may have different implications in comparison to distal HV. In contrast to distal HV, 92% of patients with proximal MCA occlusion had proximal HV, regardless of the initial ischemic lesion volume, lesion volume progression, and clinical severity. Proximal HV was not a useful prognostic indicator in this study. Proximal HV may be used as a marker for arterial occlusion, presumably the result of the thrombus inside the arterial lumen.4,7
Distal HV is more likely related to either slow, anterograde flow at the site of the occlusion or retrograde collateral flow from arteries unaffected by occlusion, both having a relative delay in transit time with the latter owing to a more circuitous route of delivery. In patients with similar perfusion lesion volumes, prominent distal HV may provide a mechanism for discriminating tissue kept viable for extended periods by way of a well-developed collateral network from tissue rapidly evolving as the result of marginalized flow distal to the site of the occlusion.
We did not find any association between distal HV and successful recanalization at 2 and 24 hours after IV thrombolysis. A previous study using cerebral angiography suggested that both good collateral flow and complete recanalization were independently related to good clinical outcome and small infarction volume.15
However, we could not find a significant difference in infarction volume and 5-day NIHSS score based on the 2-hour recanalization status. We speculated that the small sample size of our study and different outcome evaluation methods (discharge modified Rankin Scale vs 5-day NIHSS) explain these apparently discrepant findings. Subgroup analysis using the patient with prominent distal HV showed that successful recanalization at 2 hours showed trend of smaller subacute ischemic lesion volumes on FLAIR than patients with poor recanalization. This may suggest that successful recanalization, independent of collateral blood flow, remains an important prognostic factor in rt-PA–treated patients.
Multivariate regression analysis demonstrated that only initial NIHSS score was a significant predictor of 5-day NIHSS score. We speculated that the clinical significance of HV to predict good clinical outcome was already reflected to low initial NIHSS score as shown in . Therefore, HV grading showed no significance in predicting 5-day NIHSS score.
Good collateral blood flow in acute ischemic stroke is known to influence prognosis and infarct volume.15–17
The pial collaterals assessed by cerebral angiography have been reported to have prognostic significance, including an association with smaller infarct volumes and good clinical outcomes in acute ischemic stroke.15
Collateral flow can prolong tissue viability and maximize the volume of salvageable tissue. Thus the information of collateral blood flow has potential clinical applications for making treatment decisions and predicting outcome after acute ischemic stroke. Cerebral angiography is the gold standard used to evaluate collateral blood flow, but has the limitation of invasiveness, relatively long acquisition and procedural times, and low accessibility for general use in acute ischemic stroke.18,19
Other imaging modalities like MRI, CT, and transcranial Doppler can be used to evaluate collateral blood flow.20–22
Based on our findings and reported cases,1,12
we suggest that distal HV in patients with MCA occlusion results from collateral blood flow originating in neighboring arterial territories, especially via pial collaterals.
A limitation of this study is the inability to establish a direct association between distal HV on FLAIR imaging and an independent measure of collateral blood flow. We hope that direct comparison of HV on FLAIR and collateral blood flow on conventional angiography may help to define the mechanism of HV in future studies. In addition, we could not establish the relationship between presence of HV and outcome, although there was a trend of lower 5-day NIHSS score in patients with prominent distal HV than without. A larger number of patients and another outcome measurement, such as 90-day modified Rankin Scale score, are needed to prove the clinical significance of HV.
In our cohort, patients with prominent distal HV presented with small acute ischemic lesions and subacute infarct volumes despite proximal MCA occlusion and large perfusion lesions. If prominent distal HV on acute evaluation is predictive of prolonged tissue viability, it can be used to identify patients who will benefit from treatment beyond the current 3-hour thrombolysis time window. Further study is needed to confirm our findings and prove this hypothesis.