Risk factors for and outcomes of postoperative complications in adult patients with moyamoya disease

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The risk factors and clinical significance of postoperative complications in moyamoya disease are still unclear. The aim of this study was to investigate the predictors of postoperative complications in moyamoya disease and examine the impact of complications on outcomes.


The authors reviewed consecutive cases involving adult moyamoya disease patients who underwent indirect, direct, or combined bypass surgery in their hospital between 2009 and 2015. Preoperative clinical characteristics and radiographic features were recorded. Postoperative complications within 14 days after surgery were examined. Multivariate logistic regression analyses were performed to identify the risk factors for either postoperative ischemia or postoperative cerebral hyperperfusion. Outcome data, including recurrent strokes and neurological status (modified Rankin Scale [mRS]) during follow-up, were collected. Outcomes were compared between patients who had complications with those without complications, using propensity-score analysis to account for between-group differences in baseline characteristics.


A total of 500 patients (610 hemispheres) were included in this study. Postoperative complications were observed in 74 operations (12.1%), including new postoperative ischemia in 30 cases (4.9%), hyperperfusion in 27 (4.4%), impaired wound healing in 12 (2.0%), and subdural effusion in 6 (1.0%). The complication rates for different surgery types were as follows: 12.6% (n = 25) for indirect bypass, 12.7% (n = 37) for direct bypass, and 10.0% (n = 12) for combined bypass (p = 0.726). Postoperative ischemic complications occurred in 30 hemispheres (4.9%) in 30 different patients, and postoperative symptomatic hyperperfusion occurred after 27 procedures (4.4%). Advanced Suzuki stage (OR 1.669, 95% CI 1.059–2.632, p = 0.027) and preoperative ischemic presentation (OR 5.845, 95% CI 1.654–20.653, p = 0.006) were significantly associated with postoperative ischemia. Preoperative ischemic presentation (OR 5.73, 95% CI 1.27–25.88, p = 0.023) and admission modified Rankin Scale (mRS) score (OR 1.81, 95% CI 1.06–3.10, p = 0.031) were significantly associated with symptomatic postoperative cerebral hyperperfusion syndrome (CHS). Compared with patients without postoperative complications, patients who experienced any postoperative complications had longer hospital stays and worse mRS scores at discharge (both p < 0.0001). At the final follow-up, no significant differences in functional disability (mRS score 3–6, 11.9% vs 4.5%, p = 0.116) and future stroke events (p = 0.513) between the 2 groups were detected.


Advanced Suzuki stage and preoperative ischemic presentation were independent risk factors for postoperative ischemia; the mRS score on admission and preoperative ischemic presentation were independently associated with postoperative CHS. Although patients with postoperative complications had worse neurological status at discharge, postoperative complications had no associations with future stroke events or functional disability during follow-up.

ABBREVIATIONS CHS = cerebral hyperperfusion syndrome; DSA = digital subtraction angiography; EDAS = encephaloduroarteriosynangiosis; ICA = internal carotid artery; MCA = middle cerebral artery; MMD = moyamoya disease; MRA = MR angiography; mRS = modified Rankin Scale; PCA = posterior cerebral artery; STA = superficial temporal artery; TIA = transient ischemic attack.

Article Information

Correspondence Jizong Zhao: Beijing Tiantan Hospital, Capital Medical University, Beijing, China. zhaojz205@163.com.

INCLUDE WHEN CITING Published online March 30, 2018; DOI: 10.3171/2017.10.JNS171749.

Disclosures The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

© AANS, except where prohibited by US copyright law.



  • View in gallery

    Kaplan-Meier plot showing freedom from stroke per hemisphere treated for adult MMD patients with and without complications after propensity-score matching. Tick marks indicate time points after which data were censored for a particular patient-hemisphere in the group (point of last follow-up). There was no significant difference in freedom from stroke between the 2 groups (p = 0.513, log-rank test). Figure is available in color online only.

  • View in gallery

    Comparison of mRS scores of patients with and without complications. The proportions of patients with mRS scores ranging from 0 (yellow) to 6 (dark red) are shown for all patients at discharge (A), patients in the propensity-score matched groups—scores at discharge (B), all patients at last follow-up (C), and patients in the propensity-score matched groups—scores at last follow-up (D). Figure is available in color online only.


  • 1

    Antonucci MUBurns TCPulling TMRosenberg JMarks MPSteinberg GK: Acute preoperative infarcts and poor cerebrovascular reserve are independent risk factors for severe ischemic complications following direct extracranial-intracranial bypass for moyamoya disease. AJNR Am J Neuroradiol 37:2282352016

  • 2

    Cho WSKim JEKim CHBan SPKang HSSon YJ: Long-term outcomes after combined revascularization surgery in adult moyamoya disease. Stroke 45:302530312014

  • 3

    Cho WSLee HYKang HSKim JEBang JSOh CW: Symptomatic cerebral hyperperfusion on SPECT after indirect revascularization surgery for moyamoya disease. Clin Nucl Med 38:44462013

  • 4

    Deng XGao FZhang DZhang YWang RWang S: Effects of different surgical modalities on the clinical outcome of patients with moyamoya disease: a prospective cohort study. J Neurosurg [epub ahead of print July 7 2017. DOI: 10.3171/2016.12.JNS162626] 2017

  • 5

    Fujimura MBang OYKim JS: Moyamoya disease. Front Neurol Neurosci 40:2042202016

  • 6

    Fujimura MInoue TShimizu HSaito AMugikura STominaga T: Efficacy of prophylactic blood pressure lowering according to a standardized postoperative management protocol to prevent symptomatic cerebral hyperperfusion after direct revascularization surgery for moyamoya disease. Cerebrovasc Dis 33:4364452012

  • 7

    Fujimura MKaneta TShimizu HTominaga T: Cerebral ischemia owing to compression of the brain by swollen temporal muscle used for encephalo-myo-synangiosis in moyamoya disease. Neurosurg Rev 32:245249discussion 249 2009

  • 8

    Fujimura MKaneta TTominaga T: Efficacy of superficial temporal artery-middle cerebral artery anastomosis with routine postoperative cerebral blood flow measurement during the acute stage in childhood moyamoya disease. Childs Nerv Syst 24:8278322008

  • 9

    Fujimura MMugikura SKaneta TShimizu HTominaga T: Incidence and risk factors for symptomatic cerebral hyperperfusion after superficial temporal artery-middle cerebral artery anastomosis in patients with moyamoya disease. Surg Neurol 71:4424472009

  • 10

    Fujimura MShimizu HInoue TMugikura SSaito ATominaga T: Significance of focal cerebral hyperperfusion as a cause of transient neurologic deterioration after extracranial-intracranial bypass for moyamoya disease: comparative study with non-moyamoya patients using N-isopropyl-p-[123I]iodoamphetamine single-photon emission computed tomography. Neurosurgery 68:9579652011

  • 11

    Fujimura MTominaga T: Current status of revascularization surgery for moyamoya disease: special consideration for its ‘internal carotid-external carotid (IC-EC) conversion’ as the physiological reorganization system. Tohoku J Exp Med 236:45532015

  • 12

    Guzman RLee MAchrol ABell-Stephens TKelly MDo HM: Clinical outcome after 450 revascularization procedures for moyamoya disease. Clinical article. J Neurosurg 111:9279352009

  • 13

    Hayashi KHorie NSuyama KNagata I: Incidence and clinical features of symptomatic cerebral hyperperfusion syndrome after vascular reconstruction. World Neurosurg 78:4474542012

  • 14

    Hayashi TShirane RFujimura MTominaga T: Postoperative neurological deterioration in pediatric moyamoya disease: watershed shift and hyperperfusion. J Neurosurg Pediatr 6:73812010

  • 15

    Hirooka ROgasawara KSasaki MYamadate KKobayashi MSuga Y: Magnetic resonance imaging in patients with cerebral hyperperfusion and cognitive impairment after carotid endarterectomy. J Neurosurg 108:117811832008

  • 16

    Houkin KNakayama NKuroda SIshikawa TNonaka T: How does angiogenesis develop in pediatric moyamoya disease after surgery? A prospective study with MR angiography. Childs Nerv Syst 20:7347412004

  • 17

    Ishii YTanaka YMomose TYamashina MSato AWakabayashi S: Chronological evaluation of cerebral hemodynamics by dynamic susceptibility contrast magnetic resonance imaging after indirect bypass surgery for moyamoya disease. World Neurosurg 108:4274352017

  • 18

    Iwama THashimoto NTsukahara TMurai B: Peri-operative complications in adult moyamoya disease. Acta Neurochir (Wien) 132:26311995

  • 19

    Jeon JPKim JECho WSBang JSSon YJOh CW: Meta-analysis of the surgical outcomes of symptomatic moyamoya disease in adults. J Neurosurg 128:7937992018

  • 20

    Jung YJAhn JSKwon DHKwun BD: Ischemic complications occurring in the contralateral hemisphere after surgical treatment of adults with moyamoya disease. J Korean Neurosurg Soc 50:4924962011

  • 21

    Kazumata KIto MTokairin KIto YHoukin KNakayama N: The frequency of postoperative stroke in moyamoya disease following combined revascularization: a single-university series and systematic review. J Neurosurg 121:4324402014

  • 22

    Khan NAchrol ASGuzman RBurns TCDodd RBell-Stephens T: Sex differences in clinical presentation and treatment outcomes in moyamoya disease. Neurosurgery 71:5875932012

  • 23

    Kim JEJeon JS: An update on the diagnosis and treatment of adult Moyamoya disease taking into consideration controversial issues. Neurol Res 36:4074162014

  • 24

    Kim JEOh CWKwon OKPark SQKim SEKim YK: Transient hyperperfusion after superficial temporal artery/middle cerebral artery bypass surgery as a possible cause of postoperative transient neurological deterioration. Cerebrovasc Dis 25:5805862008

  • 25

    Kim SHChoi JUYang KHKim TGKim DS: Risk factors for postoperative ischemic complications in patients with moyamoya disease. J Neurosurg 103 (5 Suppl):4334382005

  • 26

    Kim TOh CWBang JSKim JECho WS: Moyamoya disease: treatment and outcomes. J Stroke 18:21302016

  • 27

    Kim TOh CWKwon OKHwang GKim JEKang HS: Stroke prevention by direct revascularization for patients with adult-onset moyamoya disease presenting with ischemia. J Neurosurg 124:178817932016

  • 28

    Kuroda SHoukin KNunomura MAbe H: Frontal lobe infarction due to hemodynamic change after surgical revascularization in moyamoya disease—two case reports. Neurol Med Chir (Tokyo) 40:3153202000

  • 29

    Liu XZhang DShuo WZhao YWang RZhao J: Long term outcome after conservative and surgical treatment of haemorrhagic moyamoya disease. J Neurol Neurosurg Psychiatry 84:2582652013

  • 30

    Mallory GWBower RSNwojo METaussky PWetjen NMVarzoni TC: Surgical outcomes and predictors of stroke in a North American white and African American moyamoya population. Neurosurgery 73:9849922013

  • 31

    Nakamura MImai HKonno KKubota CSeki KPuentes S: Experimental investigation of encephalomyosynangiosis using gyrencephalic brain of the miniature pig: histopathological evaluation of dynamic reconstruction of vessels for functional anastomosis. Laboratory investigation. J Neurosurg Pediatr 3:4884952009

  • 32

    Ogasawara KInoue TKobayashi MEndo HFukuda TOgawa A: Pretreatment with the free radical scavenger edaravone prevents cerebral hyperperfusion after carotid endarterectomy. Neurosurgery 55:106010672004

  • 33

    Ohue SKumon YKohno KWatanabe HIwata SOhnishi T: Postoperative temporary neurological deficits in adults with moyamoya disease. Surg Neurol 69:2812872008

  • 34

    Pandey PSteinberg GK: Neurosurgical advances in the treatment of moyamoya disease. Stroke 42:330433102011

  • 35

    Qian CYu XLi JChen JWang LChen G: The efficacy of surgical treatment for the secondary prevention of stroke in symptomatic moyamoya disease: a meta-analysis. Medicine (Baltimore) 94:e22182015

  • 36

    Research Committee on the Pathology and Treatment of Spontaneous Occlusion of the Circle of Willis: Guidelines for diagnosis and treatment of moyamoya disease (spontaneous occlusion of the circle of Willis). Neurol Med Chir (Tokyo) 52:2452662012

  • 37

    Sato KShirane RYoshimoto T: Perioperative factors related to the development of ischemic complications in patients with moyamoya disease. Childs Nerv Syst 13:68721997

  • 38

    Scott RMSmith ER: Moyamoya disease and moyamoya syndrome. N Engl J Med 360:122612372009

  • 39

    Sun HWilson COzpinar ASafavi-Abbasi SZhao YNakaji P: Perioperative complications and long-term outcomes after bypasses in adults with moyamoya disease: a systematic review and meta-analysis. World Neurosurg 92:1791882016

  • 40

    Suzuki JTakaku A: Cerebrovascular “moyamoya” disease. Disease showing abnormal net-like vessels in base of brain. Arch Neurol 20:2882991969

  • 41

    Uchino HKuroda SHirata KShiga THoukin KTamaki N: Predictors and clinical features of postoperative hyperperfusion after surgical revascularization for moyamoya disease: a serial single photon emission CT/positron emission tomography study. Stroke 43:261026162012

  • 42

    Uno MNakajima NNishi KShinno KNagahiro S: Hyperperfusion syndrome after extracranial-intracranial bypass in a patient with moyamoya disease—case report. Neurol Med Chir (Tokyo) 38:4204241998

  • 43

    van Mook WNRennenberg RJSchurink GWvan Oostenbrugge RJMess WHHofman PA: Cerebral hyperperfusion syndrome. Lancet Neurol 4:8778882005

  • 44

    Zhao WGLuo QJia JBYu JL: Cerebral hyperperfusion syndrome after revascularization surgery in patients with moyamoya disease. Br J Neurosurg 27:3213252013


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