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Postoperative vascular event prediction using angiography and ultrasonography in patients with Moyamoya disease

Published:September 05, 2022DOI:https://doi.org/10.1016/j.jns.2022.120408

      Abstract

      Objective

      Indirect revascularization surgery reduce the risk of recurrent vascular events in patients with moyamoya disease (MMD), but the roles of postoperative angiography and ultrasonography in predicting these events remain unclear.

      Methods

      This prospective study enrolled patients with MMD who would undergo their first unilateral indirect revascularization surgery. They received preoperative and postoperative ultrasound examination at 1, 3, and 6 months and conventional cerebral angiography. On ultrasonography, postoperative emerging flow (PEF) in an intracranial artery was defined as emerging flow postoperatively with absence of flow preoperatively. Predictors of vascular event frequency reduction were identified from angiographic and ultrasonographic parameters.

      Results

      In total, 52 patients (including 24 pediatric and 24 male patients), who underwent 52 preoperative and 82 postoperative ultrasound examinations, were enrolled. Significant postoperative changes were noted in all the ultrasonographic parameters of ipsilateral superficial temporal artery (STA) and the end-diastolic velocity and flow volume in contralateral STA. During a median follow-up of 5.3 years, indirect revascularization surgery significantly reduced the occurrence of ipsilateral vascular events. Predictors of vascular event frequency reduction included Matsushima grade A or B on the ipsilateral side on angiography (odds ratio [OR] = 22.00, P = 0.002) and lower resistance index (RI) in ipsilateral STA (OR = 0.0001, P = 0.012) but no PEF pattern in ipsilateral middle cerebral artery (OR = 0.14, P = 0.029) on ultrasonography performed within 6 months.

      Conclusions

      Reduction of long-term vascular event frequency probably can be predicted through postoperative angiography and ultrasonography within 6 months after indirect revascularization surgery.

      Keywords

      Abbreviations:

      ACA (anterior cerebral artery), ECA (external carotid artery), EDAS (encephaloduroarteriosynangiosis), EDV (end-diastolic velocity), EMS (encephalomyosynangiosis), EPS (encephalopericraniosynangiosis), FV (flow volume), MCA (middle cerebral artery), MMD (Moyamoya disease.), PEF (postoperative emerging flow.), PSV (peak systolic velocity), RI (resistance index), STA (superficial temporal artery), TIA (transient ischemic attack)
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      References

        • Fujimura M.
        • Bang O.Y.
        • Kim J.S.
        Moyamoya disease.
        Front. Neurol. Neurosci. 2016; 40: 204-220https://doi.org/10.1159/000448314
        • Matsuo S.
        • Amano T.
        • Miyamatsu Y.
        • Yamashita S.
        • Yasaka M.
        • Okada Y.
        • Nakamizo A.
        Carotid ultrasonography predicts collateral development following combined direct and indirect revascularization surgery in adult ischemic moyamoya disease.
        Clin. Neurol. Neurosurg. 2021; 203106590https://doi.org/10.1016/j.clineuro.2021.106590
        • Bao X.Y.
        • Zhang Y.
        • Wang Q.N.
        • Zhang Q.
        • Wang H.
        • Zhang Z.S.
        • Li D.S.
        • Duan L.
        Long-term outcomes after encephaloduroarteriosynangiosis in adult patients with moyamoya disease presenting with ischemia.
        World Neurosurg. 2018; 115: e482-e489https://doi.org/10.1016/j.wneu.2018.04.076
        • Park S.E.
        • Kim J.S.
        • Park E.K.
        • Shim K.W.
        • Kim D.S.
        Direct versus indirect revascularization in the treatment of moyamoya disease.
        J. Neurosurg. 2018; 129: 480-489https://doi.org/10.3171/2017.5.JNS17353
        • Macyszyn L.
        • Attiah M.
        • Ma T.S.
        • Ali Z.
        • Faught R.
        • Hossain A.
        • Man K.
        • Patel H.
        • Sobota R.
        • Zager E.L.
        • Stein S.C.
        Direct versus indirect revascularization procedures for moyamoya disease: a comparative effectiveness study.
        J. Neurosurg. 2017; 126: 1523-1529https://doi.org/10.3171/2015.8.JNS15504
        • Matsushima Y.
        • Inaba Y.
        Moyamoya disease in children and its surgical treatment. Introduction of a new surgical procedure and its follow-up angiograms.
        Childs Brain. 1984; 11: 155-170https://doi.org/10.1159/000120172
        • Yeh S.J.
        • Tang S.C.
        • Tsai L.K.
        • Lee C.W.
        • Chen Y.F.
        • Liu H.M.
        • Yang S.H.
        • Kuo M.F.
        • Jeng J.S.
        Color Doppler ultrasonography as an alternative tool for postoperative evaluation of collaterals after indirect revascularization surgery in moyamoya disease.
        PLoS One. 2017; 12e0188948https://doi.org/10.1371/journal.pone.0188948
        • Lee Y.S.
        • Jung K.H.
        • Roh J.K.
        Diagnosis of moyamoya disease with transcranial Doppler sonography: correlation study with magnetic resonance angiography.
        J. Neuroimaging. 2004; 14: 319-323https://doi.org/10.1177/1051228404264958
        • Pan H.
        • Shi W.
        • Li H.
        • Zhang H.
        • Li C.
        • Wang Y.
        Clinical prediction of surgical revascularization outcome in moyamoya disease via transcranial color sonography.
        J. Stroke Cerebrovasc. Dis. 2020; 29105154https://doi.org/10.1016/j.jstrokecerebrovasdis.2020.105154
        • Lin Y.H.
        • Kuo M.F.
        • Lu C.J.
        • Lee C.W.
        • Yang S.H.
        • Huang Y.C.
        • Liu H.M.
        • Chen Y.F.
        Standardized MR perfusion scoring system for evaluation of sequential perfusion changes and surgical outcome of moyamoya disease.
        AJNR Am. J. Neuroradiol. 2019; 40: 260-266https://doi.org/10.3174/ajnr.A5945
        • Chou S.C.
        • Chen Y.F.
        • Lee C.W.
        • Hsu H.C.
        • Wang K.C.
        • Yang S.H.
        • Liu H.M.
        • Kuo M.F.
        Long-term outcomes of moyamoya disease following indirect revascularization in middle adulthood: a prospective, quantitative study.
        J. Formos. Med. Assoc. 2022; S0929-6646: 00007-00009https://doi.org/10.1016/j.jfma.2022.01.007
        • Deckers P.T.
        • van Hoek W.
        • Kronenburg A.
        • Yaqub M.
        • Siero J.C.W.
        • Bhogal A.A.
        • van Berckel B.N.M.
        • van der Zwan A.
        • Braun K.P.J.
        Contralateral improvement of cerebrovascular reactivity and TIA frequency after unilateral revascularization surgery in moyamoya vasculopathy.
        Neuroimage Clin. 2021; 30102684https://doi.org/10.1016/j.nicl.2021.102684
        • Suzuki J.
        • Kodama N.
        Moyamoya disease--a review.
        Stroke. 1983; 14: 104-109https://doi.org/10.1161/01.str.14.1.104
        • Matsushima T.
        • Inoue T.
        • Suzuki S.O.
        • Fujii K.
        • Fukui M.
        • Hasuo K.
        Surgical treatment of moyamoya disease in pediatric patients--comparison between the results of indirect and direct revascularization procedures.
        Neurosurgery. 1992; 31: 401-405https://doi.org/10.1227/00006123-199209000-00003
        • Yeh S.J.
        • Tang S.C.
        • Tsai L.K.
        • Lee C.W.
        • Chen Y.F.
        • Liu H.M.
        • Yang S.H.
        • Hsieh Y.L.
        • Kuo M.F.
        • Jeng J.S.
        Greater ultrasonographic changes in pediatric moyamoya patients compared with adults after indirect revascularization surgeries.
        J. Neurosurg. Pediatr. 2018; 22: 663-671https://doi.org/10.3171/2018.6.PEDS18151
        • Wang G.
        • Wen Y.
        • Chen S.
        • Zhang G.
        • Li M.
        • Zhang S.
        • Qi S.
        • Feng W.
        Use of a panel of four microRNAs in CSF as a predicted biomarker for postoperative neoangiogenesis in moyamoya disease.
        CNS Neurosci. Ther. 2021; 27: 908-918https://doi.org/10.1111/cns.13646
        • He J.
        • Wang R.
        • Zhang D.
        • Zhang Y.
        • Zhang Q.
        • Zhao J.
        Expression of circulating vascular endothelial growth factor-antagonizing cytokines and vascular stabilizing factors prior to and following bypass surgery in patients with moyamoya disease.
        Exp. Ther. Med. 2014; 8: 302-308https://doi.org/10.3892/etm.2014.1713
        • Zhao M.
        • Zhang D.
        • Wang S.
        • Zhang Y.
        • Deng X.
        • Zhao J.
        The collateral circulation in Moyamoya disease: a single-center experience in 140 pediatric patients.
        Pediatr. Neurol. 2017; 77: 78-83https://doi.org/10.1016/j.pediatrneurol.2017.08.016
        • Ha E.J.
        • Kim K.H.
        • Wang K.C.
        • Phi J.H.
        • Lee J.Y.
        • Choi J.W.
        • Cho B.K.
        • Yang J.
        • Byun Y.H.
        • Kim S.K.
        Long-term outcomes of indirect bypass for 629 children with moyamoya disease: longitudinal and cross-sectional analysis.
        Stroke. 2019; 50: 3177-3183https://doi.org/10.1161/STROKEAHA.119.025609
        • Noh H.J.
        • Kim S.J.
        • Kim J.S.
        • Hong S.C.
        • Kim K.H.
        • Jun P.
        • Bang O.Y.
        • Chung C.S.
        • Lee K.H.
        • Lee K.H.
        • Kim G.M.
        Long term outcome and predictors of ischemic stroke recurrence in adult moyamoya disease.
        J. Neurol. Sci. 2015; 359: 381-388https://doi.org/10.1016/j.jns.2015.11.018
        • Yu L.
        • Ma L.
        • Huang Z.
        • Shi Z.
        • Wang R.
        • Zhao Y.
        • Zhang D.
        Revascularization surgery in patients with ischemic-type moyamoya disease: predictors for postoperative stroke and long-term outcomes.
        World Neurosurg. 2019; 128: e582-e596https://doi.org/10.1016/j.wneu.2019.04.214