Prior Infarcts, Reactivity, and Angiography in Moyamoya Disease (PIRAMD): a scoring system for moyamoya severity based on multimodal hemodynamic imaging

Abstract

Objective: Quantification of vasculopathy severity and its impact on parenchymal hemodynamics is a necessary prerequisite for informing management decisions and evaluating intervention response in patients with moyamoya disease (MMD). The authors performed digital subtraction angiography and noninvasive structural and hemodynamic MRI, and they outline a new classification system for patients with moyamoya that they have named Prior Infarcts, Reactivity, and Angi- ography in Moyamoya Disease (PIRAMD). Methods: Healthy control volunteers (n = 11; age 46 +/− 12 years [mean +/− SD]) and patients (n = 25; 42 +/− 13.5 years) with angiographically confirmed moyamoya provided informed consent and underwent structural (T1-weighted, T2- weighted, FLAIR, MR angiography) and hemodynamic (T2*- and cerebral blood flow–weighted) 3-T MRI. Cerebrovascular reactivity (CVR) in the internal carotid artery territory was assessed using susceptibility-weighted MRI during a hy- percapnic stimulus. Only hemispheres without prior revascularization were assessed. Each hemisphere was considered symptomatic if localizing signs were present on neurological examination and/or there was a history of transient ischemic attack with symptoms referable to that hemisphere. The PIRAMD factor weighting versus symptomatology was optimized using binary logistic regression and receiver operating characteristic curve analysis with bootstrapping. The PIRAMD finding was scored from 0 to 10. For each hemisphere, 1 point was assigned for prior infarct, 3 points for reduced CVR, 3 points for a modified Suzuki Score ≥ Grade II, and 3 points for flow impairment in ≥ 2 of 7 predefined vascular territories. Hemispheres were divided into 3 severity grades based on total PIRAMD score, as follows: Grade 1, 0–5 points; Grade 2, 6–9 points; and Grade 3, 10 points. Results: In 28 of 46 (60.9%) hemispheres the findings met clinical symptomatic criteria. With decreased CVR, the odds ratio of having a symptomatic hemisphere was 13 (95% CI 1.1–22.6, p = 0.002). The area under the curve for individual PIRAMD factors was 0.67–0.72, and for the PIRAMD grade it was 0.845. There were 0/8 (0%), 10/18 (55.6%), and 18/20 (90%) symptomatic PIRAMD Grade 1, 2, and 3 hemispheres, respectively. Conclusions: A scoring system for total impairment is proposed that uses noninvasive MRI parameters. This scoring system correlates with symptomatology and may provide a measure of hemodynamic severity in moyamoya, which could be used for guiding management decisions and evaluating intervention response.

Neuroimaging of vascular reserve in patients with cerebrovascular diseases

“…In response to vasoactive stimuli, SPECT imaging originally demonstrated that CBF reactivity was reduced in moyamoya patients (Hoshi et al, 1994;Tatemichi et al, 1988), and more recently using MRI in conjunction with hypercapnic stimuli, CVR magnitude has been consistently shown to be reduced, and onset of hemodynamic responses delayed, in patients with moyamoya (Cogswell et al, 2017;Donahue et al, 2015a;Liu et al, 2017b). CVR timing values have been shown to correlate with arterial circulation times measured from catheter angiography (Donahue et al, 2013) and preliminary scoring systems have been proposed that include CVR as a relevant variable in addition to standard anatomical information from angiography and FLAIR (Ladner et al, 2017). Importantly, when short stimulus paradigms are used (e.g., breath holds or hypercapnic stimuli with durations less than 60s), delays in maximal hemodynamic responses due to delayed arterial blood circulation times and/or smooth muscle relaxation are frequently observed in moyamoya patients.…”

Development and validation of a risk scoring model for postoperative adult moyamoya disease

“…Although a few studies have evaluated risk factors of MMD or propose a scoring system, these systems were mainly focused on radiological results. [5][6][7][8][9]29,30 Moreover, the efficiency of these scoring systems was not externally validated. To the best of our knowledge, the current study is the first to address the scoring system of MMD preoperatively, using various parameters to predict postoperative outcome in relatively large internal and external cohorts and validate its clinical value.…”

Standardized MR Perfusion Scoring System for Evaluation of Sequential Perfusion Changes and Surgical Outcome of Moyamoya Disease

“…The authors used ROIs to measure different cortical areas and obtain the MTT relative to the cerebellum. Ladner et al 25 developed a complex scoring system to incorporate the prior infarcts, angiography, and cerebral reactivity to measure hemodynamic severity in MMD. We used the standardized TTP map, which is an easily obtainable method to evaluate perfusion independent of the deconvolution algorithms.…”