Revascularization improves vascular hemodynamics - a study assessing cerebrovascular reserve and transit time in Moyamoya patients using MRI

Abstract

Cerebrovascular reserve (CVR) reflects the capacity of cerebral blood flow (CBF) to change. Decreased CVR implies poor hemodynamics and is linked to a higher risk for stroke. Revascularization has been shown to improve CBF in patients with vasculopathy such as Moyamoya disease. Dynamic susceptibility contrast (DSC) can measure transit time to evaluate patients suspected of stroke. Arterial spin labeling (ASL) is a non-invasive technique for CBF, CVR, and arterial transit time (ATT) measurements. Here, we investigate the change in hemodynamics 4-12 months after extracranial-to-intracranial direct bypass in 52 Moyamoya patients using ASL with single and multiple post-labeling delays (PLD). Images were collected using ASL and DSC with acetazolamide. CVR, CBF, ATT, and time-to-maximum (Tmax) were measured in different flow territories. Results showed that hemodynamics improved significantly in regions affected by arterial occlusions after revascularization. CVR increased by 16 ± 11% (p < 0.01) and 25 ± 13% (p < 0.01) for single- and multi-PLD ASL, respectively. Transit time measured by multi-PLD ASL and post-vasodilation DSC reduced by 13 ± 7% (p < 0.01) and 9 ± 5% (p < 0.01), respectively. For all regions, ATT correlated significantly with Tmax (R² = 0.59, p < 0.01). Thus, revascularization improved CVR and decreased transit times. Multi-PLD ASL can serve as an effective and non-invasive modality to examine vascular hemodynamics in Moyamoya patients.

Keywords: Arterial spin labeling; Moyamoya disease; arterial transit time; cerebral blood flow; cerebrovascular reserve.

Figure 1.

Experimental design for characterizing the hemodynamics of Moyamoya patients before and after revascularization. MRA was acquired to determine the location and condition of vasculopathy. Single-PLD and Multi-PLD ASL were acquired to measure CVR, CBF, and ATT. T1-weighted images were collected to facilitate image registration and group analysis. DSC images were acquired to compute Tmax. ASL data were acquired before and 15 minutes after the administration of the vasodilator (acetazolamide, ACZ). Other MRI sequences (not shown in this figure) included GRE and DWI acquired before vasodilation and post-contrast T1.

Figure 2.

MRA, CBF, and CVR maps of a 42-year-old female Moyamoya patient. In the pre-surgery images, the unilateral (left-sided) occlusion of the MCA and ACA affected perfusion and vasodilation, causing vascular steal (negative ΔCBF and CVR, red arrows). After the surgery, the perfusion and CVR of these regions were restored to normal levels. CBF and CVR maps measured by multi-PLD PCASL were higher than those measured by single-PLD PCASL in all conditions. (a) MRA before and after the surgery. (b and c) CBF, ΔCBF, and CVR measured by single- and multi-PLD PCASL before the surgery. (d and e) CBF, ΔCBF, and CVR measured by single- and multi-PLD PCASL after the surgery.

Figure 3.

MRA, CBF, and CVR maps of a 42 year-old female Moyamoya patient (same patient as in Figure 2). In the pre-bypass images, the occlusion of the left MCA and ACA (subplot a) caused delayed transit time (both ATT and Tmax, red arrows in subplots b and c). ATT increased slightly after vasodilation in the same regions where vascular steal was seen on CBF maps. After the surgery, both ATT and Tmax decreased, and ATT declined after vasodilation.

Figure 4.

CVR, ΔCBF, and pre- and post-vasodilation CBF in regions affected by vasculopathy. (a and b) CVR and ΔCBF in the affected regions increased significantly after bypass surgery. The effect size of multi-PLD PCASL was higher than that of single-PLD PCASL and (c) CBF within the affected regions increased significantly in both pre- and post-vasodilation conditions after bypass surgeries. The effect size of the post-vasodilation CBF change was larger than the pre-vasodilation condition. CBF measured by multi-PLD PCASL were higher than the values measured by single-PLD PCASL in all conditions (p < 0.05 in all cases). Each box plot indicates, from top to bottom, the maximum, 75th, 50th, 25th percentiles, and minimum not considering outliers, and the outliers represented by diamonds.

Figure 5.

Regions of significant CVR differences (paired t-test; corrected p-value <0.05) before and after surgery. Overall, the CVR difference between before and after surgery was between 2.3% and 27% in these regions.

Figure 6.

(a and b) ATT and Tmax change in regions with vasculopathy after bypass surgeries. Both ATT and Tmax decreased significantly after bypass surgeries pre- and post-vasodilation and (c and d) correlation between mean ATT (measured by multi-PLD PCASL) and Tmax (measured by DSC) before and after bypass surgeries in regions with vasculopathy. The correlation reduced slightly after bypass surgeries in both pre- and post-vasodilation conditions. The correlation was higher post-vasodilation. Each box plot indicates, from top to bottom, the maximum, 75th, 50th, 25th percentiles, and minimum without considering outliers, and the outliers represented by diamonds. The shaded area represents the 95% confidence interval.