Planning-free cerebral blood flow territory mapping in patients with intracranial arterial stenosis

Abstract

A noninvasive method for quantifying cerebral blood flow and simultaneously visualizing cerebral blood flow territories is vessel-encoded pseudocontinuous arterial spin labeling MRI. However, obstacles to acquiring such information include limited access to the methodology in clinical centers and limited work on how clinically acquired vessel-encoded pseudocontinuous arterial spin labeling data correlate with gold-standard methods. The purpose of this work is to develop and validate a semiautomated pipeline for the online quantification of cerebral blood flow maps and cerebral blood flow territories from planning-free vessel-encoded pseudocontinuous arterial spin labeling MRI with gold-standard digital subtraction angiography. Healthy controls (n = 10) and intracranial atherosclerotic disease patients (n = 34) underwent 3.0 T MRI imaging including vascular (MR angiography) and hemodynamic (cerebral blood flow-weighted arterial spin labeling) MRI. Patients additionally underwent catheter and/or CT angiography. Variations in cross-territorial filling were grouped according to diameters of circle of Willis vessels in controls. In patients, Cohen's k-statistics were computed to quantify agreement in perfusion patterns between vessel-encoded pseudocontinuous arterial spin labeling and angiography. Cross-territorial filling patterns were consistent with circle of Willis anatomy. The intraobserver Cohen's k-statistics for cerebral blood flow territory and digital subtraction angiography perfusion agreement were 0.730 (95% CI = 0.593-0.867; reader one) and 0.708 (95% CI = 0.561-0.855; reader two). These results support the feasibility of a semiautomated pipeline for evaluating major neurovascular cerebral blood flow territories in patients with intracranial atherosclerotic disease.

Keywords: Angiography; MR angiography; MRI; arterial spin labeling; atherosclerosis; cerebral blood flow territory; cerebrovascular disease; circle of Willis; collaterals; imaging; neuroradiology; vessel-encoded arterial spin labeling.

Figure 1.

Example of how the cross-territorial index is calculated in a healthy control with aplastic right A1 and aplastic right P1 vessels. (a) Left: When considering the right hemisphere, LICA voxels overlapping with RICA voxels in the standard CBF territory map are shown in red, and RICA voxels overlapping with VBA voxels are shown in purple. Right: The standard CBF territory map in this subject’s native space. As a result of the coregistration process, small differences exist between the two maps with regards to the total number of voxels shown. (b) To optimize the k-means analysis, spatial weighting parameters were evaluated in the same control by quantifying the extent of cross-territorial filling. The goal of this analysis was to identify the highest possible spatial weighting factor that also accurately reflected the anatomy, in order to produce robust results in patients. (c) Qualitative cross-territorial filling analysis, which corresponds with the quantitative analysis above, shown across three slices in the brain for multiple spatial weighting factors.

Figure 2.

Qualitative comparison between MRA and CBF territory maps in healthy controls. (a) A complete circle of Willis is seen on MRA. The CBF territories closely resemble the standard CBF territory map. (b) An absent right A1 segment of the ACA (red arrow) and absent right P1 segment of the PCA (yellow arrow, only the superior cerebellar artery can be seen) is visualized on MRA. The CBF territory map shows that the right ACA territory is collateralized by the left ICA (red arrows) and that the right PCA territory is perfused from the right ICA (yellow arrows). (c) Hypoplastic right A1 segment of the ACA (yellow arrow) is seen on MRA. The corresponding CBF territories demonstrate left ICA perfusion supplying the right ACA territory (yellow arrows).

Figure 3.

(a) When sizes of the A1 segment of the ACA are grouped into three categories (present, hypoplastic, and absent), there is an observable difference between the corresponding mean cross-territorial indices for ICA–ICA overlap across hemispheres. (b–c) Similarly, when sizes of the P1 segment of the PCA and PCOM are grouped, there is an observable difference between the corresponding mean cross-territorial indices for ipsilateral ICA–VBA overlap. Note: the scale of the y-axis is different between graphs.

Figure 4.

Qualitative comparison between DSA and CBF territory maps in patients with intracranial stenosis and occlusion. Subtitles above DSA images are formatted as View (AP or lateral): Injection site. (a) 68 y/o M: DSA demonstrates complete occlusion of the right ICA near the skull base (blue arrow, top DSA image) with collateral supply from the LICA distribution (red arrow, middle DSA image). The corresponding CBF territory map demonstrates filling of the entire anterior circulation by the left ICA. Posterior circulation is normal (bottom DSA image). (b) 62 y/o F: DSA showing severe multifocal stenosis of the left ICA (blue arrow, top DSA image) with near complete occlusion of the intracranial ICA both proximal and distal to the patent ophthalmic artery origin (orange arrow, top DSA image) with collaterals to the left ACA distribution from the RICA territory (red arrow, middle DSA image) and collaterals to the left MCA distribution from the VBA (green arrow, bottom DSA image). CBF territory maps reflect this perfusion pattern (red arrows and green arrows correspond to RICA and VBA collateralization, respectively). (c) 51 y/o M: DSA reveals occlusion/absence of the left proximal A1 segment (blue arrow, top DSA image) with collateral filling of the left A1 region from the RICA (red arrow, middle DSA image). The corresponding CBF territory map is in agreement with the DSA findings (red arrows correspond to RICA cross-filling of LICA territory). Flow from the VBA does not extend into the ICA territories (bottom DSA image).

Figure 5.

Qualitative comparison between DSA and mixing CBF territory maps in three representative ICAD patients. Subtitles above DSA images are formatted as View (AP or lateral): Injection site. (a) 51 y/o M: DSA reveals that the RICA cross-fills the left A1 segment territory (blue arrows, top DSA image), and that the LICA fills the left A1 segment normally (red arrow, bottom DSA image). This region of mixed perfusion in the left A1 territory can be seen on the mixing CBF territory maps (bright green clusters). (b) 64 y/o F: DSA shows that the LICA cross-fills the right A1 segment territory (blue arrow, top DSA image), and that the RICA fills the right A1 segment normally with no cross-filling on the left (red arrow, bottom DSA image). The region of mixed flow is seen on the mixing CBF territory maps (bright green clusters). Mixing between the ICAs and VBA is also seen. (c) 51 y/o M: DSA shows the basilar artery cross-filling the LICA territory (red arrow, top DSA image). The corresponding CBF territory map demonstrates mixing between the LICA and VBA territories (purple cluster). DSA (bottom two images) also shows cross-filling of the LICA territory by the RICA (blue arrow, middle DSA image), with the LICA territory also being perfused normally by the LICA (green arrow, bottom DSA image). The region of mixed flow is seen on the CBF territory maps (bright green clusters).

Figure 6.

Qualitative comparison showing good correlation between CTA/MRA and CBF territory maps in patients with intracranial artery occlusion. (a) 75 y/o F: CTA demonstrates occlusion of the right P2 segment of the PCA (green arrow). CBF territory maps do not have ASL signal in this corresponding region (yellow arrows), signifying infarct. (b) 57 y/o M: CTA demonstrates a right aplastic/occluded A1 segment of the ACA (top image, green arrow). MRA also shows a large ACOM (bottom image, red arrow). CBF territories demonstrate perfusion of the right A1 segment by the left ICA territory region (yellow arrows), presumably through the ACOM. (c) 53 y/o F: MRA shows a right aplastic/occluded P1 segment of the PCA (top image, green arrow; of note, there is a vein underlying the same area). MRA also shows a patent right PCOM (bottom image, red arrow). CBF territory maps show a clear demarcation between the right and left hemisphere in the VBA territory, with flow supplied to the right VBA territory (yellow arrows) by the right ICA territory, presumably through the PCOM. (d) 72 y/o M: CTA shows a small left P1 segment of the PCA (green arrow) with a large left fetal-type PCOM (red arrow, top and bottom image). CBF territory maps shows perfusion of the left side of the VBA territory by the left ICA territory (yellow arrows), presumably through the left PCOM. (e) Sagittal CTA image shows abrupt cutoff of the left ICA (top image, green arrow). Axial MRA image does not reveal an ACOM (bottom image, red arrow). CBF territory maps show perfusion of the entire left hemisphere by the VBA territory alone (yellow arrows); the right ICA territory does not supply the left A1 region if no ACOM exists. (f) MRA demonstrates an aplastic/occluded A1 segment of the right ACA (green arrow). CBF territory maps reveal that only the posterior right A1 region receives supply from the left ICA territory (yellow arrows), although collaterals from the left ICA territory to the anterior right A1 region (red arrows) would also be expected. (g) CTA shows bilateral fetal-type PCOMs (yellow arrows) and small P1 segments (green arrows). The CBF territory map shows a complete Circle of Willis configuration, although minimal perfusion from the posterior circulation above the cerebellum would be expected.