{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,23]],"date-time":"2026-10-23T09:11:51Z","timestamp":1792746711421,"version":"4.5.0"},"reference-count":90,"publisher":"Journal of Neurosurgery Publishing Group (JNSPG)","issue":"1","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2025,7,1]]},"abstract":"\n OBJECTIVE<\/jats:title>\n Both direct and indirect surgical revascularization techniques are commonly applied for the treatment of moyamoya disease and syndrome; however, responses can be heterogeneous and efficacy in the context of ischemic disease is not yet formally known from randomized clinical trials. Here, a prospective, longitudinal interventional study was performed to test the hypothesis that presenting 1) parenchymal cerebrovascular reactivity (CVR) and 2) CVR response times portend hemodynamic improvements after direct and indirect revascularization.<\/jats:p>\n <\/jats:sec>\n \n METHODS<\/jats:title>\n \n Catheter angiography and hypercapnic blood oxygenation\u2013weighted 3-T MRI (spatial resolution 3.5 \u00d7 3.5 \u00d7 3.5 mm, repetition time 2000 msec) were acquired before and 11.0 \u00b1 7.9 months and 12.6 \u00b1 6.9 months after surgery, respectively. In response to a 5% fixed-inspired CO\n 2<\/jats:sub>\n respiratory challenge, time regression analyses were utilized to quantify maximal cerebrovascular reactivity (CVR\n max<\/jats:sub>\n ) and time to reach maximal cerebrovascular reactivity (CVR\n delay<\/jats:sub>\n ) to test the overarching hypothesis that presurgical measures predicted postsurgical CVR\n max<\/jats:sub>\n increases and CVR\n delay<\/jats:sub>\n reductions. Age, sex, surgical type, and preoperative impairment were considered as relevant explanatory variables in the regression analysis (significance criterion p < 0.05).\n <\/jats:p>\n <\/jats:sec>\n \n RESULTS<\/jats:title>\n \n A total of 47 operative hemispheres (32 indirect-only and 15 direct or combined direct-indirect revascularization) from 30 adult patients (median [range] age 43 [20\u201359] years) were evaluated. Direct\/combined versus indirect revascularized brain hemispheres were matched for age (44.1 \u00b1 11.1 vs 44.7 \u00b1 13.8 years, p = 0.864), prior infarct (92.9% vs 92.6%, p = 0.976), and Suzuki stage within 1 stage on the 6-point staging scale (4.1 \u00b1 0.7 vs 3.4 \u00b1 0.6). Across all hemispheres and surgical procedures, CVR\n max<\/jats:sub>\n increased (p = 0.022) and CVR\n delay<\/jats:sub>\n decreased (p = 0.009) after surgery; however, responses varied considerably across hemispheres and surgical procedures. On multiple regression analysis, extent of preoperative impairment, quantified as preoperative CVR\n max<\/jats:sub>\n and moderated by the type of surgery performed, was an indicator of intervention-induced outcome in hemodynamics (p = 0.015). No effect of preoperative CVR\n delay<\/jats:sub>\n or age was found for outcomes.\n <\/jats:p>\n <\/jats:sec>\n \n CONCLUSIONS<\/jats:title>\n The findings confirm heterogeneous CVR responses approximately 1 year after revascularization across patients, albeit moderated by type of revascularization. Of the variables considered, lower presurgical CVR provided the most significant indicator of the likelihood of postsurgical hemodynamic improvement.<\/jats:p>\n <\/jats:sec>","DOI":"10.3171\/2024.10.jns24697","type":"journal-article","created":{"date-parts":[[2025,2,14]],"date-time":"2025-02-14T20:35:55Z","timestamp":1739565355000},"page":"274-284","source":"Crossref","is-referenced-by-count":4,"title":["Presenting cerebrovascular reactivity as a determinant of direct and indirect surgical revascularization success in North American patients with moyamoya vasculopathy"],"prefix":"10.3171","volume":"143","author":[{"given":"Shuhei","family":"Shiino","sequence":"first","affiliation":[{"name":"Departments of Neurology,"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Caleb","family":"Han","sequence":"additional","affiliation":[{"name":"Departments of Neurology,"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Maria","family":"Garza","sequence":"additional","affiliation":[{"name":"Departments of Neurology,"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Matthew","family":"Fusco","sequence":"additional","affiliation":[{"name":"Neurosurgery,"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rohan","family":"Chitale","sequence":"additional","affiliation":[{"name":"Neurosurgery,"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"L. Taylor","family":"Davis","sequence":"additional","affiliation":[{"name":"Radiology and Radiological Sciences,"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wesley","family":"Richerson","sequence":"additional","affiliation":[{"name":"Departments of Neurology,"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mark","family":"Rodeghier","sequence":"additional","affiliation":[{"name":"Rodeghier Consulting, Chicago, Illinois; and"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Abigail R.","family":"Dubois","sequence":"additional","affiliation":[{"name":"Departments of Neurology,"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Melanie","family":"Leguizamon","sequence":"additional","affiliation":[{"name":"Departments of Neurology,"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kilian","family":"Hett","sequence":"additional","affiliation":[{"name":"Departments of Neurology,"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lori C.","family":"Jordan","sequence":"additional","affiliation":[{"name":"Radiology and Radiological Sciences,"},{"name":"Department of Pediatrics, Division of Neurology, Vanderbilt University Medical Center, Nashville, Tennessee"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Manus J.","family":"Donahue","sequence":"additional","affiliation":[{"name":"Departments of Neurology,"},{"name":"Psychiatry and Behavioral Sciences, and"},{"name":"Electrical and Computer Engineering, Vanderbilt University Medical Center, Nashville, Tennessee;"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1754","reference":[{"issue":"8","key":"b1","series-title":"Lancet Neurol","first-page":"747","article-title":"Moyamoya disease: diagnosis and interventions","volume":"21","author":"Ihara M","year":"2022","unstructured":"Ihara M, Yamamoto Y, Hattori Y, Moyamoya disease: diagnosis and interventions. Lancet Neurol. 2022;21(8):747\u2013758."},{"issue":"12","key":"b2","series-title":"N Engl J Med","first-page":"1226","article-title":"Moyamoya disease and moyamoya syndrome","volume":"360","author":"Scott RM","year":"2009","unstructured":"Scott RM, Smith ER. Moyamoya disease and moyamoya syndrome. N Engl J Med. 2009;360(12):1226\u20131237."},{"issue":"4","key":"b3","series-title":"Neuroepidemiology","first-page":"282","article-title":"Epidemiological and clinical features of moyamoya disease in the USA","volume":"40","author":"Kainth D","year":"2013","unstructured":"Kainth D, Chaudhry SA, Kainth H, Suri FK, Qureshi AI. Epidemiological and clinical features of moyamoya disease in the USA. Neuroepidemiology. 2013;40(4):282\u2013287."},{"issue":"1","key":"b4","series-title":"Neurosurgery","first-page":"93","article-title":"Moyamoya disorder in the United States","volume":"71","author":"Starke RM","year":"2012","unstructured":"Starke RM, Crowley RW, Maltenfort M, Moyamoya disorder in the United States. Neurosurgery. 2012;71(1):93\u201399."},{"issue":"6","key":"b5","series-title":"Stroke","first-page":"1490","article-title":"Clinical features and outcome in North American adults with moyamoya phenomenon","volume":"37","author":"Hallemeier CL","year":"2006","unstructured":"Hallemeier CL, Rich KM, Grubb RL Jr, Clinical features and outcome in North American adults with moyamoya phenomenon. Stroke. 2006;37(6):1490\u20131496."},{"issue":"5","key":"b6","series-title":"Childs Nerv Syst","first-page":"358","article-title":"Revascularisation surgery for paediatric moyamoya: a review of the literature","volume":"21","author":"Fung LWE","year":"2005","unstructured":"Fung LWE, Thompson D, Ganesan V. Revascularisation surgery for paediatric moyamoya: a review of the literature. Childs Nerv Syst. 2005;21(5):358\u2013364."},{"issue":"3","key":"b7","series-title":"Neurosurg Clin N Am","first-page":"361","article-title":"Direct versus indirect bypass for moyamoya disease","volume":"28","author":"Liu JJ","year":"2017","unstructured":"Liu JJ, Steinberg GK. Direct versus indirect bypass for moyamoya disease. 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Neurosurgery. 2019;84(1):261\u2013271."},{"issue":"9","key":"b14","series-title":"AJNR Am J Neuroradiol","first-page":"1709","article-title":"Unilateral hemispheric proliferation of ivy sign on fluid-attenuated inversion recovery images in moyamoya disease correlates highly with ipsilateral hemispheric decrease of cerebrovascular reserve","volume":"30","author":"Kawashima M","year":"2009","unstructured":"Kawashima M, Noguchi T, Takase Y, Ootsuka T, Kido N, Matsushima T. Unilateral hemispheric proliferation of ivy sign on fluid-attenuated inversion recovery images in moyamoya disease correlates highly with ipsilateral hemispheric decrease of cerebrovascular reserve. AJNR Am J Neuroradiol. 2009;30(9):1709\u20131716."},{"issue":"4","key":"b15","series-title":"J Cereb Blood Flow Metab","first-page":"705","article-title":"Classifying intracranial stenosis disease severity from functional MRI data using machine learning","volume":"40","author":"Waddle SL","year":"2020","unstructured":"Waddle SL, Juttukonda MR, Lants SK, Classifying intracranial stenosis disease severity from functional MRI data using machine learning. J Cereb Blood Flow Metab. 2020;40(4):705\u2013719."},{"issue":"8","key":"b16","series-title":"Stroke","first-page":"2335","article-title":"Routine clinical evaluation of cerebrovascular reserve capacity using carbogen in patients with intracranial stenosis","volume":"45","author":"Donahue MJ","year":"2014","unstructured":"Donahue MJ, Dethrage LM, Faraco CC, Routine clinical evaluation of cerebrovascular reserve capacity using carbogen in patients with intracranial stenosis. 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Stroke. 2012;43(3):903\u2013915."},{"issue":"7","key":"b19","series-title":"Stroke","first-page":"2021","article-title":"Mapping cerebrovascular reactivity using blood oxygen level-dependent MRI in patients with arterial steno-occlusive disease: comparison with arterial spin labeling MRI","volume":"39","author":"Mandell DM","year":"2008","unstructured":"Mandell DM, Han JS, Poublanc J, Mapping cerebrovascular reactivity using blood oxygen level-dependent MRI in patients with arterial steno-occlusive disease: comparison with arterial spin labeling MRI. Stroke. 2008;39(7):2021\u20132028."},{"issue":"4","key":"b20","series-title":"J Cereb Blood Flow Metab","first-page":"1213","article-title":"Imaging of cerebrovascular reserve and oxygenation in Moyamoya disease","volume":"37","author":"Ni WW","year":"2017","unstructured":"Ni WW, Christen T, Rosenberg J, Zun Z, Moseley ME, Zaharchuk G. Imaging of cerebrovascular reserve and oxygenation in Moyamoya disease. J Cereb Blood Flow Metab. 2017;37(4):1213\u20131222."},{"issue":"7","key":"b21","series-title":"NMR Biomed","first-page":"779","article-title":"On the assessment of cerebrovascular reactivity using hypercapnia BOLD MRI","volume":"22","author":"Yezhuvath US","year":"2009","unstructured":"Yezhuvath US, Lewis-Amezcua K, Varghese R, Xiao G, Lu H. On the assessment of cerebrovascular reactivity using hypercapnia BOLD MRI. NMR Biomed. 2009;22(7):779\u2013786."},{"issue":"5","key":"b22","series-title":"J Magn Reson Imaging","first-page":"1129","article-title":"Relationships between hypercarbic reactivity, cerebral blood flow, and arterial circulation times in patients with moyamoya disease","volume":"38","author":"Donahue MJ","year":"2013","unstructured":"Donahue MJ, Ayad M, Moore R, Relationships between hypercarbic reactivity, cerebral blood flow, and arterial circulation times in patients with moyamoya disease. J Magn Reson Imaging. 2013;38(5):1129\u20131139."},{"issue":"10","key":"b23","series-title":"J Cereb Blood Flow Metab","first-page":"1767","article-title":"Time delay processing of hypercapnic fMRI allows quantitative parameterization of cerebrovascular reactivity and blood flow delays","volume":"36","author":"Donahue MJ","year":"2016","unstructured":"Donahue MJ, Strother MK, Lindsey KP, Hocke LM, Tong Y, Frederick BD. Time delay processing of hypercapnic fMRI allows quantitative parameterization of cerebrovascular reactivity and blood flow delays. J Cereb Blood Flow Metab. 2016;36(10):1767\u20131779."},{"issue":"13","key":"b24","series-title":"N Engl J Med","first-page":"1305","article-title":"Comparison of warfarin and aspirin for symptomatic intracranial arterial stenosis","volume":"352","author":"Chimowitz MI","year":"2005","unstructured":"Chimowitz MI, Lynn MJ, Howlett-Smith H, Comparison of warfarin and aspirin for symptomatic intracranial arterial stenosis. 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J Neurosurg. 2017;126(5):1520\u20131522."},{"issue":"6","key":"b31","series-title":"Stroke","first-page":"1170","article-title":"Effects of surgical revascularization on outcome of patients with pediatric moyamoya disease","volume":"28","author":"Ishikawa T","year":"1997","unstructured":"Ishikawa T, Houkin K, Kamiyama H, Abe H. Effects of surgical revascularization on outcome of patients with pediatric moyamoya disease. Stroke. 1997;28(6):1170\u20131173."},{"issue":"2","key":"b32","series-title":"Neurosurgery","first-page":"315","article-title":"Direct vs indirect revascularization in a North American cohort of moyamoya disease","volume":"89","author":"Lai PMR","year":"2021","unstructured":"Lai PMR, Patel NJ, Frerichs KU, Direct vs indirect revascularization in a North American cohort of moyamoya disease. Neurosurgery. 2021;89(2):315\u2013322."},{"issue":"7","key":"b33","series-title":"J Stroke Cerebrovasc Dis","first-page":"1597","article-title":"Surgical revascularization in North American adults with moyamoya phenomenon: long-term angiographic follow-up","volume":"24","author":"Arias EJ","year":"2015","unstructured":"Arias EJ, Dunn GP, Washington CW, Surgical revascularization in North American adults with moyamoya phenomenon: long-term angiographic follow-up. J Stroke Cerebrovasc Dis. 2015;24(7):1597\u20131608."},{"issue":"3","key":"b34","series-title":"Neurosurgery","first-page":"625","article-title":"Quantitative angiographic comparison with the OSIRIS program between the direct and indirect revascularization modalities in adult moyamoya disease","volume":"70","author":"Bang JS","year":"2012","unstructured":"Bang JS, Kwon OK, Kim JE, Quantitative angiographic comparison with the OSIRIS program between the direct and indirect revascularization modalities in adult moyamoya disease. 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Neurosurgery. 2013;73(3):430\u2013439."},{"issue":"3","key":"b36","series-title":"J Neurosurg","first-page":"397","article-title":"Effect of direct arterial bypass on the prevention of future stroke in patients with the hemorrhagic variety of moyamoya disease","volume":"93","author":"Kawaguchi S","year":"2000","unstructured":"Kawaguchi S, Okuno S, Sakaki T. Effect of direct arterial bypass on the prevention of future stroke in patients with the hemorrhagic variety of moyamoya disease. J Neurosurg. 2000;93(3):397\u2013401."},{"issue":"5","key":"b37","series-title":"J Cereb Blood Flow Metab","first-page":"842","article-title":"Comparison of cerebral blood flow measurement with [15O]-water positron emission tomography and arterial spin labeling magnetic resonance imaging: a systematic review","volume":"36","author":"Fan AP","year":"2016","unstructured":"Fan AP, Jahanian H, Holdsworth SJ, Zaharchuk G. 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J Cereb Blood Flow Metab. 2022;42(8):1493\u20131506."},{"key":"b39","series-title":"Neuroimage","first-page":"296","article-title":"Investigating the non-linearity of the BOLD cerebrovascular reactivity response to targeted hypo\/hypercapnia at 7T","volume":"98","author":"Bhogal AA","year":"2014","unstructured":"Bhogal AA, Siero JCW, Fisher JA, Investigating the non-linearity of the BOLD cerebrovascular reactivity response to targeted hypo\/hypercapnia at 7T. Neuroimage. 2014;98:296\u2013305."},{"issue":"8","key":"b40","series-title":"Stroke","first-page":"1610","article-title":"Impaired cerebrovascular reactivity with steal phenomenon is associated with increased diffusion in white matter of patients with Moyamoya disease","volume":"41","author":"Conklin J","year":"2010","unstructured":"Conklin J, Fierstra J, Crawley AP, Impaired cerebrovascular reactivity with steal phenomenon is associated with increased diffusion in white matter of patients with Moyamoya disease. Stroke. 2010;41(8):1610\u20131616."},{"issue":"3","key":"b41","series-title":"J Magn Reson Imaging","first-page":"912","article-title":"A prospective, longitudinal magnetic resonance imaging evaluation of cerebrovascular reactivity and infarct development in patients with intracranial stenosis","volume":"54","author":"Juttukonda MR","year":"2021","unstructured":"Juttukonda MR, Davis LT, Lants SK, A prospective, longitudinal magnetic resonance imaging evaluation of cerebrovascular reactivity and infarct development in patients with intracranial stenosis. J Magn Reson Imaging. 2021;54(3):912\u2013922."},{"issue":"2","key":"b42","series-title":"Radiology","first-page":"419","article-title":"Cerebrovascular reactivity mapping using resting-state BOLD functional MRI in healthy adults and patients with moyamoya disease","volume":"299","author":"Liu P","year":"2021","unstructured":"Liu P, Liu G, Pinho MC, Cerebrovascular reactivity mapping using resting-state BOLD functional MRI in healthy adults and patients with moyamoya disease. Radiology. 2021;299(2):419\u2013425."},{"issue":"9","key":"b43","series-title":"J Cereb Blood Flow Metab","first-page":"1391","article-title":"Consensus statement on current and emerging methods for the diagnosis and evaluation of cerebrovascular disease","volume":"38","author":"Donahue MJ","year":"2018","unstructured":"Donahue MJ, Achten E, Cogswell PM, Consensus statement on current and emerging methods for the diagnosis and evaluation of cerebrovascular disease. 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Neuroimage. 2015;114:239\u2013248."},{"issue":"8","key":"b1","series-title":"Lancet Neurol","first-page":"747","article-title":"Moyamoya disease: diagnosis and interventions","volume":"21","author":"Ihara M","year":"2022","unstructured":"Ihara M, Yamamoto Y, Hattori Y, Moyamoya disease: diagnosis and interventions. Lancet Neurol. 2022;21(8):747\u2013758."},{"issue":"12","key":"b2","series-title":"N Engl J Med","first-page":"1226","article-title":"Moyamoya disease and moyamoya syndrome","volume":"360","author":"Scott RM","year":"2009","unstructured":"Scott RM, Smith ER. Moyamoya disease and moyamoya syndrome. N Engl J Med. 2009;360(12):1226\u20131237."},{"issue":"4","key":"b3","series-title":"Neuroepidemiology","first-page":"282","article-title":"Epidemiological and clinical features of moyamoya disease in the USA","volume":"40","author":"Kainth D","year":"2013","unstructured":"Kainth D, Chaudhry SA, Kainth H, Suri FK, Qureshi AI. 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