Moyamoya disease is a progressive, steno-occlusive disease of the cerebral vasculature with particular involvement of the circles of Willis. Time-of-flight (TOF)-MR angiography (MRA) is the most common approach for intracranial MRA, but frequently fails to visualize distal arteries to the steno-occlusive lesion because of the slow or retrograde flow in this disease. Especially, leptomeningeal anastomosis (LMA) collaterals from posterior circulation, which play a critical role in maintaining cerebral perfusion pressure ¹, are poorly visualized with TOF-MRA.

Recently, a gradient design for selective labeling of arteries was proposed where the effective gradient form is such that the first moment (m1) is zero^2,3. This gradient wave form results in rephasing of the signal of spins moving from constant velocity. The signal from spins that are subject to accelaration will be dephased. As the pulsatile arterial flow has a major acceleration component, whereas venous flow is mostly constant, only arterial blood spins will be visualized. This approach is called acceleration-selective arterial spin labeling (AccASL)^2,3. Previously we demonstrated that AccASL-MRA enabled better efficiency for visualizing cerebral arteries compared to the TOF-MRA, while suppressing cortical vein signal⁴. In this study, we evaluated the utility of acceleration-selective arterial spin labeling (AccASL)-MRA in depiction of distal arteries in moyamoya disease.

[Patients] Fifteen patients with Moyamoya disease (age 26.1 ± 23.9 year-old; 6 males, 9 females) were examined. All patients underwent both MRA and digital subtraction angiography (DSA).

[MRI] Both TOF- and AccASL-MRA were performed on a 3T MR scanner (Ingenia3.0T, Philips). The AccASL-MRA consists of control (T2-preparation without motion-sensitized gradient: MSG) and label (with MSG) parts followed by 3D T1-weighted gradient-echo sequence (Figure 1)⁴. In the label part, MSG employs a motion compensation design to selectively detect spins with acceleration component in arteries. The AccASL acquisition parameters were: sequence T1-TFE; TR/TE, 7.5/3.5 ms; flip angle, 11°; turbo factor, 60; shot interval (sequence TR), 1500 ms; 3D slab thickness, 120 mm; voxel size, 0.39×077×1.0 mm (120 partitions); sensitivity encoding factor, 2.0; and total acquisition time for the label and control pair of 6 m 9s. The TOF-MRA was obtained in the identical imaging resolution, geometry and acquisition time as AccASL-MRA.

[Image Analysis] In both MRAs, the number of distal middle cerebral artery (MCA) branches (#vessel) was counted by a line profile analysis and the contrast-to-noise ratio (CNR) was measured in peripheral branches in each hemisphere on an image of maximum intensity projection with 90 mm thickness (Figure 2). Based on the DSA findings, the degree of steno-occlusion of internal carotid artery (ICA) or the development of leptomeningeal anastomosis (LMA) was classified into two grades (early/late ICA stage, mildly/well-developed LMA).

[Statistical Analysis] The #vessel and CNR were compared between the two MR methods by paired t-test. Increment in #vessel between the two MR methods (#vesselAccASL-#vesselTOF) was evaluated based on the DSA findings by Mann-Whitney U test. P<0.05 is considered statistically significant.

The average #vessel obtained with AccASL-MRA (16.9±4.9, P<0.0001) was significantly larger than that with TOF-MRA (7.2±4.5, Figure 3A). The average CNR of M4 branches with AccASL-MRA (20.4±8.0, P<0.0001) was significantly higher than that with TOF-MRA (9.2±9.2, Figure 3B). The increment in #vessel was higher in hemispheres with late ICA stage (11.0±4.0, P<0.01) than those with early ICA stage (6.8±2.4, Figure 4A). The increment in #vessel was higher in hemispheres with well-developed LMA (11.4±3.9, P<0.01) than those with mildly-developed LMA (6.8±2.2, Figure 4B). Figure 5 shows a representative case of Moyamoya disease where the visualization of distal cerebral arteries including LMA was greatly improved with AccASL-MRA compared with TOF-MRA.

In the present study, we found that AccASL-MRA improved the depiction of distal arteries in Moyamoya disease in comparison with TOF-MRA, and this improvement was associated with the severity of ICA steno-occlusion and the development of LMA collateral vessels. AccASL-MRA does not depend on inflow effect, but does directly labels blood spins by using MSG senstive to acceleration. Thus, this method was able to visualize slow flow or non feet-head direction flow in distal cerebral arteries in Moyamoya disease that is the typical limitation of TOF-MRA. In addition, AccASL-MRA is free from the dependency of transit time that is the inherent limitation of spatial selective ASL (PASL or pCASL)-based MRA⁵. The AccASL-MRA is useful in assessing development of collaterals and thus may help in assess and monitor hemodynamic status in Moyamoya disease.The AccASL-MRA significantly improved the depiction of distal arteries in Moyamoya disease compared with TOF-MRA. The AccASL-MRA reflects the development of collaterals and may help assess and monitor hemodynamic status in Moyamoya disease.