MRI-Based Assessment of Risk for Stroke in Moyamoya Angiopathy (MARS-MMA): An MRI-Based Scoring System for the Severity of Moyamoya Angiopathy

Abstract

Before revascularization, moyamoya patients require hemodynamic evaluation. In this study, we evaluated the scoring system Prior Infarcts, Reactivity and Angiography in Moyamoya Disease (PIRAMID). We also devised a new scoring system, MRI-Based Assessment of Risk for Stroke in Moyamoya Angiopathy (MARS-MMA), and compared the scoring systems with respect to the capability to predict impaired [¹⁵O]water PET cerebral perfusion reserve capacity (CPR). We evaluated 69 MRI, 69 DSA and 38 [¹⁵O]water PET data sets. The PIRAMID system was validated by ROC curve analysis with neurological symptomatology as a dependent variable. The components of the MARS-MMA system and their weightings were determined by binary logistic regression analysis. The comparison of PIRAMID and MARS-MMA was performed by ROC curve analysis. The PIRAMID score correlated well with the symptomatology (AUC = 0.784). The MARS-MMA system, including impaired breath-hold-fMRI, the presence of the Ivy sign and arterial wall contrast enhancement, correlated slightly better with CPR impairment than the PIRAMID system (AUC = 0.859 vs. 0.827, Akaike information criterion 140 vs. 146). For simplified clinical use, we determined three MARS-MMA grades without loss of diagnostic performance (AUC = 0.855). The entirely MRI-based MARS-MMA scoring system might be a promising tool to predict the risk of stroke.

Keywords: MRI; [15O]water PET; cerebral perfusion reserve capacity; moyamoya angiopathy; scoring system.

Figure 1

Exemplary MRI and [¹⁵O]water PET data evaluation of one patient. Each territory of the anterior cerebral artery and the middle cerebral artery (MCA) was evaluated with respect to postischemic FLAIR lesions > 4 mm ((a), see arrow), Ivy sign on axial FLAIR images ((b), see arrows), arterial vessel wall contrast enhancement (c) and >50% reduced breath-hold fMRI cerebrovascular reactivity (bh-fMRI CVR) response compared to the cerebellar bh-fMRI CVR response ((d), see the right MCA territory (MCA-r)), as well as at least a severely reduced cerebral perfusion reserve capacity after acetazolamide administration ((e), see right MCA territory).

Figure 2

ROC curves of the PIRAMID components, the PIRAMID score and its grade with regard to the prediction of neurological symptomatology. In the evaluation of the territories of the internal carotid arteries (a), the AUCs of the PIRAMID score (0.749 *) and grade (0.724 *) were higher than the AUCs of all individual parameters (modified Suzuki Score (mSS) (0.692 *), impaired collateralization (0.638 *), prior infarcts (0.708 *), cerebrovascular reactivity (CVR) (0.646 *)). This was also evident in the evaluation of the territories of the anterior and the middle cerebral arteries (b): PIRAMID score (0.784 *), PIRAMID grade (0.745 *), mSS (0.654 *), impaired collateralization (0.654 *), prior infarcts (0.722 *), CVR (0.716 *)). * Confidence intervals not given since multiple territories (2 or 4) per patient were evaluated.

Figure 3

ROC curves of the MARS-MMA score, the MARS-MMA grade, the adapted PIRAMID score and all components of the scores predicting [¹⁵O]water PET cerebral perfusion reserve impairment. The AUC of the MARS-MMA score (0.859 *) was slightly higher than the AUC of the adapted PIRAMID score (0.827 *). The AUC of the MARS-MMA grade was 0.855 *. The AUCs of the components of the scores were lower (cerebrovascular reactivity (CVR) 0.777 *, modified Suzuki Score (mSS) 0.652 *, impaired collateralization 0.640 *, prior infarcts 0.708 *, arterial wall contrast enhancement 0.649 *, Ivy sign 0.699 *). * Confidence intervals not given since multiple territories (4) per patient were evaluated.

Figure 4

Bar graph showing MARS-MMA grade versus cerebral perfusion reserve (CPR) impairment on [¹⁵O]water PET. The negative predictive value impairment of MARS-MMA grade 1 was 97.7% and the positive predictive value of MARS-MMA grade 3 was 78.4%.

Figure 5

Flowchart of MARS-MMA score calculation and recommendations for therapeutic and diagnostic procedures for each of the 3 grades. Note: All suggested clinical decisions must be correlated with the clinical findings for final decision-making in each case.