Relationship between haemodynamic impairment and collateral blood flow in carotid artery disease

Abstract

Collateral blood flow plays a pivotal role in steno-occlusive internal carotid artery (ICA) disease to prevent irreversible ischaemic damage. Our aim was to investigate the effect of carotid artery disease upon cerebral perfusion and cerebrovascular reactivity and whether haemodynamic impairment is influenced at brain tissue level by the existence of primary and/or secondary collateral. Eighty-eight patients with steno-occlusive ICA disease and 29 healthy controls underwent MR examination. The presence of collaterals was determined with time-of-flight, two-dimensional phase contrast MRA and territorial arterial spin labeling (ASL) imaging. Cerebral blood flow and cerebrovascular reactivity were assessed with ASL before and after acetazolamide. Cerebral haemodynamics were normal in asymptomatic ICA stenosis patients, as opposed to patients with ICA occlusion, in whom the haemodynamics in both hemispheres were compromised. Haemodynamic impairment in the affected brain region was always present in symptomatic patients. The degree of collateral blood flow was inversely correlated with haemodynamic impairment. Recruitment of secondary collaterals only occurred in symptomatic ICA occlusion patients. In conclusion, both CBF and cerebrovascular reactivity were found to be reduced in symptomatic patients with steno-occlusive ICA disease. The presence of collateral flow is associated with further haemodynamic impairment. Recruitment of secondary collaterals is associated with severe haemodynamic impairment.

Keywords: MRI; MRI angiography; Stroke; carotid artery; cerebral hemodynamics; perfusion-weighted MRI.

Figure 1.

Transverse flow territory maps projected onto a standard brain template and visual demonstration of how the ROI’s were constructed. Colors correspond to the colorbar, which indicates the percentage of patients who demonstrated perfusion in that region of the brain. Panel A and B show how the ACA territory was delineated. The median border was defined by superimposing all the ICA’s without collateral blood flow, in which the ACA is supplied by its ipsilateral ICA (a). The border between the ACA and MCA was determined by superimposing all the contralateral ICAs from patients with anterior collateral blood, in which the ACA is supplied by the contralateral ICA (b). Panel C and D show how the MCA territory was delineated. The border between the ACA and MCA was determined by superimposing all the ipsilateral ICAs from patients with anterior collateral blood flow, where the ACA territory was fed by the contralateral ICA (c). The border between the MCA and PCA was determined by superimposing all the BAs from patients without collateral blood flow involving the posterior circulation on that side, in which the PCA is supplied by the BA (d). Panel E and F show how the PCA territory was delineated. The border between both PCA’s (Figure 1(e)), and the PCA and vertebrobasilar supply of the cerebellum was determined by superimposing all the ICA’s from patients with anterior-to-posterior collateral flow, in which the contralateral PCA is supplied by the ICA and the entire cerebellum is still supplied by the vertebrobasilar artery. To ensure that the tissue within the ACA, MCA and PCA was only fed by that specific artery, ROI were determined conservatively as only that tissue that was fed in all patients (Figure 1(g)). ACA: anterior cerebral artery; ICA: internal carotid artery; MCA: middle cerebral artery; PCA: posterior cerebral artery; ROI: region of interest.

Figure 2.

Case example of a 64-year-old female asymptomatic patient with right-sided ICA stenosis >70%. Time-of-flight MR angiogram images (a) of the circle of Willis show the presence of all vessels. 2D phase contrast images (b,c) show blood flowing from right-to-left in white and left-to-right in black (b), and flowing from anterior-to-posterior in white and posterior-to-anterior in black (c). FLAIR images (d) from cranial (top) to caudal (bottom) correspond with ASL perfusion images before (e) and after (f) acetazolamide, CVR images (g), and territorial ASL maps (h) of the right (red), left (green) carotid arteries and the basilar artery (blue). There is no evidence of reduced cerebral perfusion (e, f), and the cerebrovascular reactivity (g) is unimpaired. The perfusion territories (h) are symmetrical according to the morphology of the circle of Willis.

Figure 3.

Case example of a 68-year-old female asymptomatic patient with a left-sided ICA occlusion. There is anterior collateral flow from right to left via the AcomA and retrograde flow in the left A1 segment (a-c, arrow) towards the left MCA territory from the contralateral ICA. FLAIR images (d) correspond with ASL perfusion images before (e) and after (f) acetazolamide, CVR images (g), and territorial ASL maps (h). Reduced CBF at baseline (e), after a vasodilatory challenge (f) and impaired CVR (g) is present in both hemispheres. CVR (g) is most notable impaired in the left MCA territory (g, star). Territorial ASL images show anterior collateral flow from the contralateral ICA (h, red) towards the left MCA territory (h, star).

Figure 4.

Case example 47-year-old male patient with left-sided ICA occlusion. There is absence of flow in the left ICA (a, arrow) with distinct primary anterior collateral flow towards the contralateral MCA (b and c, arrow). FLAIR images (d) correspond with ASL perfusion images before (e) and after (f) acetazolamide, CVR images (g), and territorial ASL maps (h). An overlap region in the territorial ASL images (h, star) can be seen where blood from secondary collaterals (purple) fed by the basilar artery (blue) mix with blood from the primary collaterals (red) to supply part of the MCA territory. There is an infarct visible in the left hemisphere (d, arrow) where primary and secondary collaterals mix. Reduced baseline CBF (e, star) can be appreciated against the left hemisphere, without increase after the vasodilatory challenge (f, star). CVR (g) is severely impaired in the left MCA territory (g, star).