{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,11]],"date-time":"2026-09-11T02:00:58Z","timestamp":1789092058007,"version":"build-2803163510"},"reference-count":28,"publisher":"MDPI AG","issue":"13","license":[{"start":{"date-parts":[[2024,7,5]],"date-time":"2024-07-05T00:00:00Z","timestamp":1720137600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Medical Faculty T\u00fcbingen","award":["2723-0-0"],"award-info":[{"award-number":["2723-0-0"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Diagnostics"],"abstract":"<jats:p>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.<\/jats:p>","DOI":"10.3390\/diagnostics14131437","type":"journal-article","created":{"date-parts":[[2024,7,5]],"date-time":"2024-07-05T03:48:56Z","timestamp":1720151336000},"page":"1437","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":10,"title":["MRI-Based Assessment of Risk for Stroke in Moyamoya Angiopathy (MARS-MMA): An MRI-Based Scoring System for the Severity of Moyamoya Angiopathy"],"prefix":"10.3390","volume":"14","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-4105-5131","authenticated-orcid":false,"given":"Leonie","family":"Zerweck","sequence":"first","affiliation":[{"name":"Department of Diagnostic and Interventional Neuroradiology, University Hospital Tuebingen, 72076 Tuebingen, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4487-2807","authenticated-orcid":false,"given":"Constantin","family":"Roder","sequence":"additional","affiliation":[{"name":"Department of Neurosurgery, University Hospital Tuebingen, 72076 Tuebingen, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ganna","family":"Blazhenets","sequence":"additional","affiliation":[{"name":"Department of Nuclear Medicine, Medical Center, Medical Faculty, University of Freiburg, 79106 Freiburg im Breisgau, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Peter","family":"Martus","sequence":"additional","affiliation":[{"name":"Institute for Clinical Epidemiology and Applied Biometry, University Hospital Tuebingen, 72076 Tuebingen, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Johannes","family":"Thurow","sequence":"additional","affiliation":[{"name":"Department of Nuclear Medicine, Medical Center, Medical Faculty, University of Freiburg, 79106 Freiburg im Breisgau, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Patrick","family":"Haas","sequence":"additional","affiliation":[{"name":"Department of Neurosurgery, University Hospital Tuebingen, 72076 Tuebingen, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1930-7497","authenticated-orcid":false,"given":"Arne","family":"Estler","sequence":"additional","affiliation":[{"name":"Department of Diagnostic and Interventional Neuroradiology, University Hospital Tuebingen, 72076 Tuebingen, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7596-5139","authenticated-orcid":false,"given":"Georg","family":"Gohla","sequence":"additional","affiliation":[{"name":"Department of Diagnostic and Interventional Neuroradiology, University Hospital Tuebingen, 72076 Tuebingen, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Christer","family":"Ruff","sequence":"additional","affiliation":[{"name":"Department of Diagnostic and Interventional Neuroradiology, University Hospital Tuebingen, 72076 Tuebingen, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nadja","family":"Selo","sequence":"additional","affiliation":[{"name":"Department of Diagnostic and Interventional Neuroradiology, University Hospital Tuebingen, 72076 Tuebingen, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2507-9160","authenticated-orcid":false,"given":"Urs","family":"W\u00fcrtemberger","sequence":"additional","affiliation":[{"name":"Department of Neuroradiology, Medical Center, Faculty of Medicine, University of Freiburg, 79106 Freiburg im Breisgau, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nadia","family":"Khan","sequence":"additional","affiliation":[{"name":"Department of Neurosurgery, University Hospital Tuebingen, 72076 Tuebingen, Germany"},{"name":"Moyamoya Center, University Children\u2019s Hospital Zurich, 8032 Zurich, Switzerland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5236-3450","authenticated-orcid":false,"given":"Uwe","family":"Klose","sequence":"additional","affiliation":[{"name":"Department of Diagnostic and Interventional Neuroradiology, University Hospital Tuebingen, 72076 Tuebingen, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ulrike","family":"Ernemann","sequence":"additional","affiliation":[{"name":"Department of Diagnostic and Interventional Neuroradiology, University Hospital Tuebingen, 72076 Tuebingen, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Philipp","family":"Meyer","sequence":"additional","affiliation":[{"name":"Department of Nuclear Medicine, Medical Center, Medical Faculty, University of Freiburg, 79106 Freiburg im Breisgau, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7604-3419","authenticated-orcid":false,"given":"Till-Karsten","family":"Hauser","sequence":"additional","affiliation":[{"name":"Department of Diagnostic and Interventional Neuroradiology, University Hospital Tuebingen, 72076 Tuebingen, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2024,7,5]]},"reference":[{"key":"ref_1","first-page":"288","article-title":"Cerebrovascular \u201cMoyamoya\u201d Disease: Disease Showing Abnormal Net-Like Vessels in Base of Brain","volume":"20","author":"Suzuki","year":"1969","journal-title":"JAMA Neurol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1226","DOI":"10.1056\/NEJMra0804622","article-title":"Moyamoya disease and moyamoya syndrome","volume":"360","author":"Scott","year":"2009","journal-title":"N. Engl. J. Med."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"23969873221144089","DOI":"10.1177\/23969873221144089","article-title":"European Stroke Organisation (ESO) Guidelines on Moyamoya angiopathy: Endorsed by Vascular European Reference Network (VASCERN)","volume":"8","author":"Bersano","year":"2023","journal-title":"Eur. Stroke J."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"2","DOI":"10.5853\/jos.2015.01627","article-title":"Moyamoya Disease: Epidemiology, Clinical Features, and Diagnosis","volume":"18","author":"Kim","year":"2016","journal-title":"J. Stroke"},{"key":"ref_5","first-page":"73","article-title":"Moyamoya disease: Diagnostic imaging","volume":"76","author":"Tarasow","year":"2011","journal-title":"Pol. J. Radiol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"292","DOI":"10.2174\/1570159X19666210716114016","article-title":"Progression in Moyamoya Disease: Clinical Features, Neuroimaging Evaluation, and Treatment","volume":"20","author":"Zhang","year":"2022","journal-title":"Curr. Neuropharmacol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"1845","DOI":"10.3171\/2019.2.JNS19106","article-title":"Arterial wall contrast enhancement in progressive moyamoya disease","volume":"132","author":"Roder","year":"2019","journal-title":"J. Neurosurg."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"332","DOI":"10.1159\/000513301","article-title":"Longitudinal Reproducibility of CO2-Triggered BOLD MRI for the Hemodynamic Evaluation of Adult Patients with Moyamoya Angiopathy","volume":"50","author":"Roder","year":"2021","journal-title":"Cerebrovasc. Dis."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"1061","DOI":"10.1007\/s00701-003-0148-5","article-title":"Moyamoya disease and Moyamoya syndrome: Experience in Europe; choice of revascularisation procedures","volume":"145","author":"Khan","year":"2003","journal-title":"Acta Neurochir."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"101713","DOI":"10.1016\/j.nicl.2019.101713","article-title":"Hypercapnic BOLD MRI compared to H215O PET\/CT for the hemodynamic evaluation of patients with Moyamoya Disease","volume":"22","author":"Hauser","year":"2019","journal-title":"NeuroImage Clin."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"e75","DOI":"10.1016\/j.wneu.2018.05.163","article-title":"Estimation of Severity of Moyamoya Disease with [(15)O]Water-Positron Emission Tomography Compared with Magnetic Resonance Imaging and Angiography","volume":"117","author":"Roder","year":"2018","journal-title":"World Neurosurg."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1131","DOI":"10.1007\/s00234-024-03338-7","article-title":"Evaluation of the contribution of individual arteries to the cerebral blood supply in patients with Moyamoya angiopathy: Comparison of vessel-encoded arterial spin labeling and digital subtraction angiography","volume":"66","author":"Zerweck","year":"2024","journal-title":"Neuroradiology"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"46","DOI":"10.1016\/j.mri.2019.03.003","article-title":"Evaluation of cerebrovascular reserve in patients with cerebrovascular diseases using resting-state MRI: A feasibility study","volume":"59","author":"Taneja","year":"2019","journal-title":"Magn. Reson. Imaging"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"621","DOI":"10.1161\/STROKEAHA.117.020010","article-title":"Staging Hemodynamic Failure With Blood Oxygen-Level-Dependent Functional Magnetic Resonance Imaging Cerebrovascular Reactivity: A Comparison Versus Gold Standard ((15)O-)H2O-Positron Emission Tomography","volume":"49","author":"Fierstra","year":"2018","journal-title":"Stroke"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"539","DOI":"10.1007\/s00234-022-03088-4","article-title":"Evaluation of the cerebrovascular reactivity in patients with Moyamoya Angiopathy by use of breath-hold fMRI: Investigation of voxel-wise hemodynamic delay correction in comparison to [(15)O]water PET","volume":"65","author":"Zerweck","year":"2023","journal-title":"Neuroradiology"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"553","DOI":"10.1007\/s00234-021-02814-8","article-title":"Hemodynamic evaluation of patients with Moyamoya Angiopathy: Comparison of resting-state fMRI to breath-hold fMRI and [(15)O]water PET","volume":"64","author":"Zerweck","year":"2022","journal-title":"Neuroradiology"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"495","DOI":"10.3171\/2015.11.JNS15562","article-title":"Prior Infarcts, Reactivity, and Angiography in Moyamoya Disease (PIRAMD): A scoring system for moyamoya severity based on multimodal hemodynamic imaging","volume":"126","author":"Ladner","year":"2017","journal-title":"J. Neurosurg."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"4618","DOI":"10.21037\/qims-22-1062","article-title":"A dual-center validation of the PIRAMD scoring system for assessing the severity of ischemic Moyamoya disease","volume":"13","author":"Sebok","year":"2023","journal-title":"Quant. Imaging Med. Surg."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"1699","DOI":"10.1212\/WNL.50.6.1699","article-title":"Arterial territories of the human brain: Cerebral hemispheres","volume":"50","author":"Tatu","year":"1998","journal-title":"Neurology"},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Mutsaerts, H.J., van Dalen, J.W., Heijtel, D.F., Groot, P.F., Majoie, C.B., Petersen, E.T., Richard, E., and Nederveen, A.J. (2015). Cerebral Perfusion Measurements in Elderly with Hypertension Using Arterial Spin Labeling. PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0133717"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1551","DOI":"10.1007\/s42399-020-00442-6","article-title":"Investigation of the BOLD-Based MRI Signal Time Course During Short Breath-Hold Periods for Estimation of the Cerebrovascular Reactivity","volume":"2","author":"Zerweck","year":"2020","journal-title":"SN Compr. Clin. Med."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"315","DOI":"10.1007\/s00062-023-01363-2","article-title":"Breath-Hold-Triggered BOLD fMRI in Drug-Resistant Nonlesional Focal Epilepsy-A Pilot Study","volume":"34","author":"Bosselmann","year":"2023","journal-title":"Clin. Neuroradiol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"458","DOI":"10.3171\/2021.11.PEDS21384","article-title":"Ivy sign: A diagnostic and prognostic biomarker for pediatric moyamoya","volume":"29","author":"Montaser","year":"2022","journal-title":"J. Neurosurg. Pediatr."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"2040622320960004","DOI":"10.1177\/2040622320960004","article-title":"What and why: The current situation and future prospects of \u201civy sign\u201d in moyamoya disease","volume":"11","author":"Yu","year":"2020","journal-title":"Ther. Adv. Chronic Dis."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"74","DOI":"10.1038\/s41597-022-01923-0","article-title":"Digital 3D Brain MRI Arterial Territories Atlas","volume":"10","author":"Liu","year":"2023","journal-title":"Sci. Data"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1097\/00006231-199801000-00006","article-title":"Subtraction ictal SPET co-registered to MRI in partial epilepsy: Description and technical validation of the method with phantom and patient studies","volume":"19","author":"Mullan","year":"1998","journal-title":"Nucl. Med. Commun."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"1557","DOI":"10.1007\/s002590000319","article-title":"Simplified quantitative determination of cerebral perfusion reserve with H2(15)O PET and acetazolamide","volume":"27","author":"Arigoni","year":"2000","journal-title":"Eur. J. Nucl. Med. Mol. Imaging"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"E6","DOI":"10.3171\/2019.9.FOCUS19616","article-title":"Contemporary and emerging magnetic resonance imaging methods for evaluation of moyamoya disease","volume":"47","author":"Lehman","year":"2019","journal-title":"Neurosurg. Focus"}],"container-title":["Diagnostics"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2075-4418\/14\/13\/1437\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T15:10:29Z","timestamp":1760109029000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2075-4418\/14\/13\/1437"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,7,5]]},"references-count":28,"journal-issue":{"issue":"13","published-online":{"date-parts":[[2024,7]]}},"alternative-id":["diagnostics14131437"],"URL":"https:\/\/doi.org\/10.3390\/diagnostics14131437","relation":{},"ISSN":["2075-4418"],"issn-type":[{"value":"2075-4418","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,7,5]]}}}