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HomeRadiologyVol. 297, No. 3 PreviousNext Reviews and CommentaryFree AccessEditorialDistribution of Cerebral Blood Flow: The Role of Superselective Arterial Spin Labeling MRIJeroen Hendrikse Jeroen Hendrikse Author AffiliationsFrom the Department of Radiology, University Medical Center Utrecht, Utrecht University, Postbox 85500, 3508 GA Utrecht, the Netherlands.Address correspondence to the author (e-mail: [email protected]).Jeroen Hendrikse Published Online:Sep 22 2020https://doi.org/10.1148/radiol.2020203578MoreSectionsPDF ToolsImage ViewerAdd to favoritesCiteTrack CitationsPermissionsReprints ShareShare onFacebookTwitterLinked In See also the article by Hwang and Cho et al in this issue.Dr Hendrikse is a professor in neuroradiology and chair of the Department of Radiology at the University Medical Center Utrecht, the Netherlands. His research focuses on optimizing clinical use of brain MRI methods, including intracranial vessel wall imaging, arterial spin labeling perfusion MRI, and high spatial resolution 7-T MRI of brain parenchyma. He is principal investigator of several national and European grants.Download as PowerPointOpen in Image Viewer In patients with moyamoya disease, the intracranial arterial circulation becomes compromised by a typical chronic, progressive stenosis (narrowing) of the distal internal carotid arteries. For these patients, revascularization surgery can provide an alternative blood supply for brain perfusion and can prevent cerebral ischemia and infarction. Imaging plays an important role in the evaluation of the intracranial vasculature and perfusion. MR angiography and CT angiography show the presence and extent of distal carotid stenosis, and digital subtraction angiography (DSA) shows in detail the presence of collateral blood supply before and after revascularization surgery.In this issue of Radiology, Hwang and colleagues (1) investigate the opportunity of an innovative MRI method, superselective (SS) arterial spin labeling (ASL), to evaluate the extent of the area perfused by the bypass. The SS-ASL perfusion MRI method used by Hwang et al pinpoints the labeling to one specific artery at a time. By doing so, Hwang et al magnetically labeled the arterial blood in each side of the external carotid arteries (proximal to the bypass) and internal carotid arteries (left and right separately) and one dominant side vertebral artery. The method had a scanning time of approximately 3 minutes per artery, with 15 minutes total MRI scanning time using SS labeling of five arteries (internal carotid arteries, external carotid arteries, and the dominant vertebral artery). Similar to normal (nonselective) ASL, the superselectively labeled image is subtracted from a control image, thus showing the perfused area of the labeled artery on the cross-sectional MRI scan.Hwang et al performed this SS-ASL method in a large group of 33 patients with moyamoya disease. The main research question was the performance of SS-ASL relative to DSA as the reference standard. The authors performed several detailed comparisons of the brain areas perfused by the bypass as evaluated with SS-ASL and DSA. In general, they found good agreements between SS-ASL and DSA with only a few disagreements. The intermodality agreement of the revascularization area grading was substantial (weighted κ, 0.70; 95% confidence interval: 0.37, 1.00). The authors found moderate agreements between the methods for the changes in perfusion territories before and after the bypass surgery (weighted κ, 0.59; 95% confidence interval: 0.54, 65). In the Discussion section, Hwang et al conclude that, based on their findings in “approximately 70% of patients,” the revascularization territory “could be accurately evaluated with SS-ASL imaging alone, thus avoiding postoperative DSA, to identify bypass perfusion territory.”This study distinguishes itself by combining the advanced SS-ASL perfusion MRI method, the large group of 33 patients with moyamoya disease, the comparison with the reference standard DSA, the clinical setting with bypass surgery, and the question of the extent of the brain tissue area perfused by the bypass.Several methods for perfusion territory imaging with selective and SS-ASL approaches exist (2–4). For instance, the “slab-based” selective ASL methods use a labeling slab similar to that with pulsed ASL that is angulated to label a single artery in the neck region (4). The selective labeling of a single artery with this slab-based approach can be difficult given the anatomy of the arteries in the neck. The separate labeling of the external and the internal carotid arteries with the slab-based approach can be impossible because the common carotid artery is also labeled within the labeling slab. With SS-ASL, the labeling can be pinpointed to a single artery (5), such as the external or internal carotid artery or the vertebral artery. Hwang et al succeeded in using this advanced SS-ASL method in a large group of patients, with the planning performed primarily by MRI technicians. The feasibility of planning in a clinical MRI workflow with planning by MRI technicians is important to allow SS-ASL to become an alternative for DSA. With the head-to-head comparison with DSA, the authors show that SS-ASL perfusion MRI can replace DSA for the follow-up evaluation of territory revascularization after bypass surgery in the majority of patients with moyamoya disease. MRI is often a standard part of the follow-up evaluations in these patients, and it is clear that avoiding additional DSA follow-up examinations is both patient friendly and cost-effective.In historical overviews (2,3), the first MRI methods with saturation slabs were used in 1990 to describe the distribution of the blood flow of the proximal intracranial vasculature around the circle of Willis (6), with later slab-based perfusion territory methods described in 2004 (4) and the SS method described in 2005 (5). Recent studies also showed that both selective and nonselective ASL MRI provide angiographic and perfusion information at multiple delay times between the labeling and imaging (3). With selective ASL MRI, the location of infarctions can be compared cross-sectionally with the extent of the revascularization and perfusion territories. Also, selective ASL MRI can be combined into a single MRI examination with many methods: time-of-flight MR angiography information of the larger intracranial arteries and T2-weighted fluid-attenuated inversion recovery and diffusion-weighted imaging information of the presence and location of old and recent infarctions. In patients with cerebrovascular disease and patients with arteriovenous malformations, perfusion territory imaging can show the blood supply of individual arteries to the arteriovenous malformations. When requiring quantitative perfusion information, nonselective (normal) ASL should be used to quantify the regional cerebral blood flow (7).To conclude, Hwang and colleagues show that SS-ASL can be performed in the clinical radiologic workflow with planning performed primarily by MRI technicians. Their results show that SS-ASL perfusion MRI provides similar information as DSA and can replace DSA in the follow-up evaluation of territory revascularization after bypass surgery in approximately 70% of patients with moyamoya disease. Similar to the use in moyamoya disease, SS-ASL can also play a role in other clinical settings, including arteriovenous malformations and other cerebrovascular disorders.Disclosure of Conflicts of Interest: J.H. disclosed no relevant relationships.Supported by the European Research Council under the European Union’s Horizon 2020 Framework Programme and European Research Council grant agreement no. 637024.References1. Hwang I, Cho WS, Yoo RE, et al. Revascularization evaluation in adult-onset moyamoya disease after bypass surgery: superselective arterial spin labeling perfusion MRI compared with digital subtraction angiography. Radiology 2020;297:630–637. Link, Google Scholar2. van Laar PJ, van der Grond J, Hendrikse J. Brain perfusion territory imaging: methods and clinical applications of selective arterial spin-labeling MR imaging. Radiology 2008;246(2):354–364. Link, Google Scholar3. van Osch MJP, Teeuwisse WM, Chen Z, Suzuki Y, Helle M, Schmid S. Advances in arterial spin labelling MRI methods for measuring perfusion and collateral flow. J Cereb Blood Flow Metab 2018;38(9):1461–1480. Crossref, Medline, Google Scholar4. Hendrikse J, van der Grond J, Lu H, van Zijl PCM, Golay X. Flow territory mapping of the cerebral arteries with regional perfusion MRI. Stroke 2004;35(4):882–887. Crossref, Medline, Google Scholar5. Werner R, Norris DG, Alfke K, Mehdorn HM, Jansen O. Continuous artery-selective spin labeling (CASSL). Magn Reson Med 2005;53(5):1006–1012. Crossref, Medline, Google Scholar6. Edelman RR, Mattle HP, O’Reilly GV, Wentz KU, Liu C, Zhao B. Magnetic resonance imaging of flow dynamics in the circle of Willis. Stroke 1990;21(1):56–65. Crossref, Medline, Google Scholar7. Alsop DC, Detre JA, Golay X, et al. Recommended implementation of arterial spin-labeled perfusion MRI for clinical applications: A consensus of the ISMRM perfusion study group and the European consortium for ASL in dementia. Magn Reson Med 2015;73(1):102–116. Crossref, Medline, Google ScholarArticle HistoryReceived: Aug 28 2020Revision requested: Aug 31 2020Revision received: Sept 1 2020Accepted: Sept 2 2020Published online: Sept 22 2020Published in print: Dec 2020 FiguresReferencesRelatedDetailsAccompanying This ArticleRevascularization Evaluation in Adult-Onset Moyamoya Disease after Bypass Surgery: Superselective Arterial Spin Labeling Perfusion MRI Compared with Digital Subtraction AngiographySep 22 2020RadiologyRecommended Articles Acceleration-selective Arterial Spin-labeling MR Angiography Used to Visualize Distal Cerebral Arteries and Collateral Vessels in Moyamoya DiseaseRadiology2017Volume: 286Issue: 2pp. 611-621Revascularization Evaluation in Adult-Onset Moyamoya Disease after Bypass Surgery: Superselective Arterial Spin Labeling Perfusion MRI Compared with Digital Subtraction AngiographyRadiology2020Volume: 297Issue: 3pp. 630-637Monitoring Cerebral Perfusion Changes after Revascularization in Patients with Moyamoya Disease by Using Arterial Spin-labeling MR ImagingRadiology2018Volume: 288Issue: 2pp. 565-572Arterial Spin Labeling Perfusion of the Brain: Emerging Clinical ApplicationsRadiology2016Volume: 281Issue: 2pp. 337-356Predicting PET Cerebrovascular Reserve with Deep Learning by Using Baseline MRI: A Pilot Investigation of a Drug-Free Brain Stress TestRadiology2020Volume: 296Issue: 3pp. 627-637See More RSNA Education Exhibits Puff of Smoke: Moyamoya DiseaseDigital Posters2019Going Against the Flow: Arterial Spin Labelled Imaging Provides Key Functional Diagnostic InformationDigital Posters2019Angiographic Neurovascular Anatomy (part 1): Internal Carotid Artery, Important Branches And VariantsDigital Posters2021 RSNA Case Collection Moyamoya DiseaseRSNA Case Collection2021Dural arteriovenous fistulaRSNA Case Collection2020Ischemic stroke in moyamoya diseaseRSNA Case Collection2020 Vol. 297, No. 3 Metrics Altmetric Score PDF download