{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,13]],"date-time":"2026-06-13T01:52:47Z","timestamp":1781315567097,"version":"3.54.1"},"reference-count":39,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2022,5,13]],"date-time":"2022-05-13T00:00:00Z","timestamp":1652400000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100004731","name":"Natural Science Foundation of Zhejiang Province","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100004731","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Neurol."],"abstract":"<jats:sec><jats:title>Objective<\/jats:title><jats:p>Cerebral ischemia and intracranial hemorrhage are the two main phenotypes of moyamoya disease (MMD). However, the pathophysiological processes of these two MMD phenotypes are still largely unknown. Here, we aimed to use multimodal neuroimaging techniques to explore the brain structural and functional differences between the two MMD subtypes.<\/jats:p><\/jats:sec><jats:sec><jats:title>Methods<\/jats:title><jats:p>We included 12 patients with ischemic MMD, 10 patients with hemorrhagic MMD, and 10 healthy controls (HCs). Each patient underwent MRI scans and cognitive assessment. The cortical thickness of two MMD subtypes and HC group were compared. Arterial spin labeling (ASL) and diffusion tensor imaging (DTI) were used to inspect the cerebral blood flow (CBF) of cortical regions and the integrity of related white matter fibers, respectively. Correlation analyses were then performed among the MRI metrics and cognitive function scores.<\/jats:p><\/jats:sec><jats:sec><jats:title>Results<\/jats:title><jats:p>We found that only the cortical thickness in the right middle temporal gyrus (MTG) of hemorrhagic MMD was significantly greater than both ischemic MMD and HC (<jats:italic>p<\/jats:italic> &amp;lt; 0.05). In addition, the right MTG showed higher ASL-CBF, and its associated fiber tract (arcuate fasciculus, AF) exhibited higher fractional anisotropy (FA) values in hemorrhagic MMD. Furthermore, the cortical thickness of the right MTG was positively correlated with its ASL-CBF values (<jats:italic>r<\/jats:italic> = 0.37, <jats:italic>p<\/jats:italic> = 0.046) and the FA values of right AF (<jats:italic>r<\/jats:italic> = 0.67, <jats:italic>p<\/jats:italic> &amp;lt; 0.001). At last, the FA values of right AF were found to be significantly correlated with cognitive performances within patients with MMD.<\/jats:p><\/jats:sec><jats:sec><jats:title>Conclusions<\/jats:title><jats:p>Hemorrhagic MMD shows increased cortical thickness on the right MTG in comparison with ischemic MMD and HCs. The increased cortical thickness is associated with the higher CBF values and the increased integrity of the right AF. These findings are important to understand the clinical symptoms and pathophysiology of MMD and further applied to clinical practice.<\/jats:p><\/jats:sec>","DOI":"10.3389\/fneur.2022.871421","type":"journal-article","created":{"date-parts":[[2022,5,13]],"date-time":"2022-05-13T06:24:51Z","timestamp":1652423091000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":6,"title":["Moyamoya Disease With Initial Ischemic or Hemorrhagic Attack Shows Different Brain Structural and Functional Features: A Pilot Study"],"prefix":"10.3389","volume":"13","author":[{"given":"Junwen","family":"Hu","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yin","family":"Li","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yun","family":"Tong","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhaoqing","family":"Li","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jingyin","family":"Chen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yang","family":"Cao","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yifan","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Duo","family":"Xu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Leilei","family":"Zheng","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ruiliang","family":"Bai","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lin","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2022,5,13]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"288","DOI":"10.1001\/archneur.1969.00480090076012","article-title":"Cerebrovascular \u201cmoyamoya\u201d disease. Disease showing abnormal net-like vessels in base of brain","volume":"20","author":"Suzuki","year":"1969","journal-title":"Arch Neurol."},{"key":"B2","doi-asserted-by":"publisher","first-page":"392","DOI":"10.3171\/2014.10.JNS132369","article-title":"Clinical features and long-term outcomes of moyamoya disease: a single-center experience with 528 cases in China","volume":"122","author":"Liu","year":"2015","journal-title":"J Neurosurg."},{"key":"B3","doi-asserted-by":"publisher","first-page":"1415","DOI":"10.1161\/STROKEAHA.113.004386","article-title":"Effects of extracranial-intracranial bypass for patients with hemorrhagic moyamoya disease: results of the Japan Adult Moyamoya Trial","volume":"45","author":"Miyamoto","year":"2014","journal-title":"Stroke."},{"key":"B4","doi-asserted-by":"publisher","first-page":"151","DOI":"10.1186\/s12967-020-02317-9","article-title":"Towards individualized cortical thickness assessment for clinical routine","volume":"18","author":"Tahedl","year":"2020","journal-title":"J Transl Med."},{"key":"B5","doi-asserted-by":"publisher","first-page":"469","DOI":"10.3389\/fnhum.2018.00469","article-title":"Changes in cortical thickness in patients with early Parkinson's disease at different Hoehn and Yahr Stages","volume":"12","author":"Gao","year":"2018","journal-title":"Front Hum Neurosci."},{"key":"B6","doi-asserted-by":"publisher","first-page":"1155","DOI":"10.3171\/2020.1.JNS193260","article-title":"Combined structural and diffusion tensor imaging detection of ischemic injury in moyamoya disease: relation to disease advancement and cerebral hypoperfusion","volume":"134","author":"Kazumata","year":"2020","journal-title":"J Neurosurg."},{"key":"B7","doi-asserted-by":"publisher","first-page":"858","DOI":"10.4103\/1673-5374.249234","article-title":"Microstructural damage pattern of vascular cognitive impairment: a comparison between moyamoya disease and cerebrovascular atherosclerotic disease","volume":"14","author":"Su JB Xi","year":"2019","journal-title":"Neural Regen Res."},{"key":"B8","doi-asserted-by":"publisher","first-page":"71","DOI":"10.1016\/j.clinimag.2017.07.005","article-title":"Cortical thickness changes in adult moyamoya disease assessed by structural magnetic resonance imaging","volume":"46","author":"Qiao","year":"2017","journal-title":"Clin Imaging."},{"key":"B9","doi-asserted-by":"publisher","first-page":"487","DOI":"10.1177\/0284185119866808","article-title":"Precentral and cerebellar atrophic changes in moyamoya disease using 7-T magnetic resonance imaging","volume":"61","author":"Moon","year":"2020","journal-title":"Acta Radiol."},{"key":"B10","doi-asserted-by":"publisher","first-page":"51","DOI":"10.1007\/s12031-007-0029-0","article-title":"Diffusion tensor imaging (DTI)-based white matter mapping in brain research: a review","volume":"34","author":"Assaf","year":"2008","journal-title":"J Mol Neurosci."},{"key":"B11","doi-asserted-by":"publisher","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."},{"key":"B12","doi-asserted-by":"publisher","first-page":"337","DOI":"10.1148\/radiol.2016150789","article-title":"Arterial spin labeling perfusion of the brain: emerging clinical applications","volume":"281","author":"Haller","year":"2016","journal-title":"Radiology."},{"key":"B13","doi-asserted-by":"publisher","first-page":"E5","DOI":"10.3171\/2019.9.FOCUS19567","article-title":"Clinical utility of arterial spin labeling imaging in disorders of the nervous system","volume":"47","author":"Soldozy","year":"2019","journal-title":"Neurosurg Focus."},{"key":"B14","doi-asserted-by":"publisher","first-page":"541","DOI":"10.3760\/cma.j.issn.1001-2346.2017.06.001","article-title":"Consensus of Chinese experts on the diagnosis and treatment of moyamoya disease and moyamoya syndrome","volume":"33","year":"2017","journal-title":"Chin J Neurosur."},{"key":"B15","doi-asserted-by":"publisher","first-page":"438","DOI":"10.1017\/S1355617709090626","article-title":"Construct validity of the Trail Making Test: role of task-switching, working memory, inhibition\/interference control, and visuomotor abilities","volume":"15","author":"Sanchez-Cubillo","year":"2009","journal-title":"J Int Neuropsychol Soc."},{"key":"B16","doi-asserted-by":"publisher","first-page":"1027","DOI":"10.3233\/JAD-170380","article-title":"Delayed recall and working memory MMSE domains predict delirium following cardiac surgery","volume":"59","author":"Price","year":"2017","journal-title":"J Alzheimers Dis."},{"key":"B17","doi-asserted-by":"publisher","first-page":"1402","DOI":"10.1016\/j.neuroimage.2012.02.084","article-title":"Within-subject template estimation for unbiased longitudinal image analysis","volume":"61","author":"Reuter","year":"2012","journal-title":"Neuroimage."},{"key":"B18","doi-asserted-by":"publisher","first-page":"95","DOI":"10.1038\/s41398-021-01237-6","article-title":"Cortical thinning and associated connectivity changes in patients with anorexia nervosa","volume":"11","author":"de la Cruz","year":"2021","journal-title":"Transl Psychiatry."},{"key":"B19","doi-asserted-by":"publisher","first-page":"116137","DOI":"10.1016\/j.neuroimage.2019.116137","article-title":"MRtrix3: A fast, flexible and open software framework for medical image processing and visualisation","volume":"202","author":"Tournier","year":"2019","journal-title":"Neuroimage."},{"key":"B20","doi-asserted-by":"publisher","first-page":"57","DOI":"10.1016\/j.neuroimage.2018.05.027","article-title":"Population-averaged atlas of the macroscale human structural connectome and its network topology","volume":"178","author":"Yeh","year":"2018","journal-title":"Neuroimage."},{"key":"B21","doi-asserted-by":"publisher","first-page":"258","DOI":"10.1016\/j.jocn.2019.11.026","article-title":"Detection of hemodynamic impairment on (15)O gas PET using visual assessment of arterial spin-labeling MR imaging in patients with moyamoya disease","volume":"72","author":"Hara","year":"2020","journal-title":"J Clin Neurosci."},{"key":"B22","doi-asserted-by":"publisher","first-page":"889","DOI":"10.1007\/s00276-019-02244-5","article-title":"Anatomical variability of the arcuate fasciculus: a systematical review","volume":"41","author":"Bernard","year":"2019","journal-title":"Surg Radiol Anat."},{"key":"B23","doi-asserted-by":"publisher","first-page":"119","DOI":"10.3389\/fnana.2015.00119","article-title":"Asymmetric projections of the arcuate fasciculus to the temporal cortex underlie lateralized language function in the human brain","volume":"9","author":"Takaya","year":"2015","journal-title":"Front Neuroanat."},{"key":"B24","doi-asserted-by":"publisher","first-page":"354","DOI":"10.1161\/STROKEAHA.114.007407","article-title":"Chronic ischemia alters brain microstructural integrity and cognitive performance in adult moyamoya disease","volume":"46","author":"Kazumata","year":"2015","journal-title":"Stroke."},{"key":"B25","doi-asserted-by":"publisher","first-page":"423","DOI":"10.1038\/nrn845","article-title":"Modes of neuronal migration in the developing cerebral cortex","volume":"3","author":"Nadarajah","year":"2002","journal-title":"Nat Rev Neurosci."},{"key":"B26","doi-asserted-by":"publisher","first-page":"709","DOI":"10.1007\/s00062-020-00928-9","article-title":"Microstructural alterations analogous to accelerated aging of the cerebral cortex in carotid occlusive disease","volume":"21","author":"Seiler","year":"2020","journal-title":"Clin Neuroradiol."},{"key":"B27","doi-asserted-by":"publisher","first-page":"1631","DOI":"10.1161\/STROKEAHA.110.608521","article-title":"Surgical revascularization reverses cerebral cortical thinning in patients with severe cerebrovascular steno-occlusive disease","volume":"42","author":"Fierstra","year":"2011","journal-title":"Stroke."},{"key":"B28","doi-asserted-by":"publisher","first-page":"27","DOI":"10.1016\/j.neuropsychologia.2014.11.033","article-title":"Increased cortical thickness and altered functional connectivity of the right superior temporal gyrus in left-handers","volume":"67","author":"Li","year":"2015","journal-title":"Neuropsychologia."},{"key":"B29","doi-asserted-by":"publisher","first-page":"1815","DOI":"10.1002\/hbm.23484","article-title":"Cortical thickness and functional connectivity abnormality in chronic headache and low back pain patients","volume":"38","author":"Yang","year":"2017","journal-title":"Hum Brain Mapp."},{"key":"B30","first-page":"564","volume-title":"Fundamentals of Cognitive Neuroscience: A Beginner's Guide 2nd Edition. Chapter 2 - The Brain.","author":"Gage","year":"2018"},{"key":"B31","doi-asserted-by":"publisher","first-page":"884","DOI":"10.3171\/2017.9.JNS172231","article-title":"Longitudinal anterior-to-posterior shift of collateral channels in patients with moyamoya disease: an implication for its hemorrhagic onset","volume":"130","author":"Yamamoto","year":"2018","journal-title":"J Neurosurg."},{"key":"B32","doi-asserted-by":"publisher","first-page":"2243","DOI":"10.3174\/ajnr.A6861","article-title":"Cortical distribution of fragile periventricular anastomotic collateral vessels in moyamoya disease: an exploratory cross-sectional study of Japanese patients with moyamoya disease","volume":"41","author":"Miyakoshi","year":"2020","journal-title":"AJNR Am J Neuroradiol."},{"key":"B33","doi-asserted-by":"publisher","first-page":"90","DOI":"10.1161\/01.STR.0000047120.67507.0D","article-title":"Angiographic dilatation and branch extension of the anterior choroidal and posterior communicating arteries are predictors of hemorrhage in adult moyamoya patients","volume":"34","author":"Morioka","year":"2003","journal-title":"Stroke."},{"key":"B34","doi-asserted-by":"publisher","first-page":"2708","DOI":"10.1161\/STROKEAHA.119.024487","article-title":"Collateral circulation in moyamoya disease: a new grading system","volume":"50","author":"Liu","year":"2019","journal-title":"Stroke."},{"key":"B35","doi-asserted-by":"publisher","first-page":"517","DOI":"10.2176\/nmc.tn.2019-0162","article-title":"The targeted bypass strategy for preventing hemorrhage in moyamoya disease: technical note","volume":"59","author":"Funaki","year":"2019","journal-title":"Neurol Med Chir (Tokyo)."},{"key":"B36","doi-asserted-by":"publisher","first-page":"527","DOI":"10.3171\/2015.12.JNS151499","article-title":"Postoperative executive function in adult moyamoya disease: a preliminary study of its functional anatomy and behavioral correlates","volume":"126","author":"Lei","year":"2017","journal-title":"J Neurosurg."},{"key":"B37","doi-asserted-by":"publisher","first-page":"1947","DOI":"10.1161\/STROKEAHA.112.654004","article-title":"Moyamoya disease-related versus primary intracerebral hemorrhage: [corrected] location and outcomes are different","volume":"43","author":"Nah","year":"2012","journal-title":"Stroke."},{"key":"B38","doi-asserted-by":"publisher","first-page":"117731","DOI":"10.1016\/j.neuroimage.2021.117731","article-title":"Virtual brain grafting: Enabling whole brain parcellation in the presence of large lesions","volume":"229","author":"Radwan","year":"2021","journal-title":"Neuroimage."},{"key":"B39","doi-asserted-by":"publisher","first-page":"102160","DOI":"10.1016\/j.nicl.2019.102160","article-title":"Anatomical assessment of trigeminal nerve tractography using diffusion MRI: A comparison of acquisition b-values and single- and multi-fiber tracking strategies","volume":"25","author":"Xie","year":"2020","journal-title":"Neuroimage Clin."}],"container-title":["Frontiers in Neurology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fneur.2022.871421\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,5,13]],"date-time":"2022-05-13T06:24:57Z","timestamp":1652423097000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fneur.2022.871421\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,5,13]]},"references-count":39,"alternative-id":["10.3389\/fneur.2022.871421"],"URL":"https:\/\/doi.org\/10.3389\/fneur.2022.871421","relation":{},"ISSN":["1664-2295"],"issn-type":[{"value":"1664-2295","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,5,13]]},"article-number":"871421"}}