Clinical outcome after 450 revascularization procedures for moyamoya disease

Clinical article

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Object

Moyamoya disease (MMD) is a rare cerebrovascular disease mainly described in the Asian literature. To address a lack of data on clinical characteristics and long-term outcomes in the treatment of MMD in North America, the authors analyzed their experience at Stanford University Medical Center. They report on a consecutive series of patients treated for MMD and detail their demographics, clinical characteristics, and long-term surgical outcomes.

Methods

Data obtained in consecutive series of 329 patients with MMD treated microsurgically by the senior author (G.K.S.) between 1991 and 2008 were analyzed. Demographic, clinical, and surgical data were prospectively gathered and neurological outcomes assessed in postoperative follow-up using the modified Rankin Scale. Association of demographic, clinical, and surgical data with postoperative outcome was assessed by chi-square, uni- and multivariate logistic regression, and Kaplan-Meier survival analyses.

Results

The authors treated a total of 233 adult patients undergoing 389 procedures (mean age 39.5 years) and 96 pediatric patients undergoing 168 procedures (mean age 10.1 years). Direct revascularization technique was used in 95.1% of adults and 76.2% of pediatric patients. In 264 patients undergoing 450 procedures (mean follow-up 4.9 years), the surgical morbidity rate was 3.5% and the mortality rate was 0.7% per treated hemisphere. The cumulative 5-year risk of perioperative or subsequent stroke or death was 5.5%. Of the 171 patients presenting with a transient ischemic attack, 91.8% were free of transient ischemic attacks at 1 year or later. Overall, there was a significant improvement in quality of life in the cohort as measured using the modified Rankin Scale (p < 0.0001).

Conclusions

Revascularization surgery in patients with MMD carries a low risk, is effective at preventing future ischemic events, and improves quality of life. Patients in whom symptomatic MMD is diagnosed should be offered revascularization surgery.

Abbreviations used in this paper: EEG = electroencephalography; MCA = middle cerebral artery; MELAS = myopathy, encephalopathy, lactic acidosis, and stroke; MMD = moyamoya disease; mRS = modified Rankin Scale; STA = superficial temporal artery; TIA = transient ischemic attack.

Article Information

Address correspondence to: Gary K. Steinberg, M.D., Ph.D., Department of Neurosurgery, Stanford University School of Medicine, 300 Pasteur Drive, R281 Stanford, California 94305-5487. email: gsteinberg@stanford.edu.

Please include this information when citing this paper: published online May 22, 2009; DOI: 10.3171/2009.4.JNS081649.

© AANS, except where prohibited by US copyright law.

Headings

Figures

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    A: Bimodal distribution of age at initial presentation, with peaks in the 10–19 and 30–39 bins. B: Sex breakdown of each bin: consistently two-thirds female and one-third male in each bin except for the 0–9 bin where the ratio is nearly 1:1. C and D: Ethnic distribution (C) and percentage of adult and pediatric patients at presentation in the ethnic subgroups (D).

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    Upper and Lower: Bar graphs showing presenting symptoms in 96 pediatric (upper) and 233 adult (lower) patients consisting of stroke, TIAs, intracerebral hemorrhage (ICH), seizures, and headaches. Adults presented significantly more often with intracerebral hemorrhage than pediatric patients (p < 0.05). A = Asian; AA = African-American; C = Caucasian; H = Hispanic.

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    Bar graphs demonstrating presurgical (A) and postsurgical (B) mRS scores obtained in 264 patients with a minimum of 6 months of follow-up. C: Overall 67% of the patients improved by 1–2 points on the mRS scale (change in mRS score of −1 or −2), whereas 23% remained unchanged (no change in mRS = 0). Status in only a few patients worsened after surgery (change in mRS score of 1–4). Values to the left of the dashed line represent no change or improvement in the mRS score.

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    Kaplan-Meier survival curve for any stroke or hemorrhage. The overall 5-year risk of any stroke or hemorrhage was 5.5%.

References

  • 1

    Anonymous: United Kingdom transient ischaemic attack (UKTIA) aspirin trial: interim results. UK-TIA Study Group. Br Med J (Clin Res Ed) 296:3163201988

    • Search Google Scholar
    • Export Citation
  • 2

    Baba THoukin KKuroda S: Novel epidemiological features of moyamoya disease. J Neurol Neurosurg Psychiatry 79:9009042008

  • 3

    Chang SDSteinberg GK: Superficial temporal artery to middle cerebral artery anastomosis. Techniques in Neurosurgery 6:861002000

  • 4

    Chang SDSteinberg GK: Surgical management of moyamoya disease. Contemporary Neurosurgery 22:192000

  • 5

    Chiu DShedden PBratina PGrotta JC: Clinical features of moyamoya disease in the United States. Stroke 29:134713511998

  • 6

    Choi JUKim DSKim EYLee KC: Natural history of moyamoya disease: comparison of activity of daily living in surgery and non surgery groups. Clin Neurol Neurosurg 99:2 SupplS11S181997

    • Search Google Scholar
    • Export Citation
  • 7

    Fujii KIkezaki KIrikura KMiyasaka YFukui M: The efficacy of bypass surgery for the patients with hemorrhagic moyamoya disease. Clin Neurol Neurosurg 99:2 SupplS194S1951997

    • Search Google Scholar
    • Export Citation
  • 8

    Fukui M: Current state of study on moyamoya disease in Japan. Surg Neurol 47:1381431997

  • 9

    Fukui M: Guidelines for the diagnosis and treatment of spontaneous occlusion of the circle of Willis (‘moyamoya’ disease). Research Committee on Spontaneous Occlusion of the Circle of Willis (Moyamoya Disease) of the Ministry of Health and Welfare, Japan. Clin Neurol Neurosurg 2 Suppl99:S238S2401997

    • Search Google Scholar
    • Export Citation
  • 10

    Golby AJMarks MPThompson RCSteinberg GK: Direct and combined revascularization in pediatric moyamoya disease. Neurosurgery 45:50601999

    • Search Google Scholar
    • Export Citation
  • 11

    Hallemeier CLRich KMGrubb RL JrChicoine MRMoran CJCross DT III: Clinical features and outcome in North American adults with moyamoya phenomenon. Stroke 37:149014962006

    • Search Google Scholar
    • Export Citation
  • 12

    Hankinson TCBohman L-EHeyer GLicursi MGhatan SFeldstein NA: Surgical treatment of moyamoya syndrome in patients with sickle cell anemia: outcome following encephaloduroarteriosynangiosis. J Neurosurg Pediatr 1:2112162008

    • Search Google Scholar
    • Export Citation
  • 13

    Hoffman HJ: Moyamoya disease and syndrome. Clin Neurol Neurosurg 99:2 SupplS39S441997

  • 14

    Houkin KKamiyama HAbe HTakahashi AKuroda S: Surgical therapy for adult moyamoya disease. Can surgical revascularization prevent the recurrence of intracerebral hemorrhage?. Stroke 27:134213461996

    • Search Google Scholar
    • Export Citation
  • 15

    Hung CCTu YKSu CFLin LSShih CJ: Epidemiological study of Moyamoya disease in Taiwan. Clin Neurol Neurosurg 99:S23S251997

  • 16

    Ikezaki KFukui MInamura TKinukawa NWakai KOno Y: The current status of the treatment for hemorrhagic type moyamoya disease based on a 1995 nationwide survey in Japan. Clin Neurol Neurosurg 99:2 SupplS183S1861997

    • Search Google Scholar
    • Export Citation
  • 17

    Iwama THashimoto NYonekawa Y: The relevance of hemodynamic factors to perioperative ischemic complications in childhood moyamoya disease. Neurosurgery 38:112011261996

    • Search Google Scholar
    • Export Citation
  • 18

    Iwama TYoshimura S: Present status of Moyamoya disease in Japan. Acta Neurochir Suppl 103:1151182008

  • 19

    Jea ASmith ERRobertson RScott RM: Moyamoya syndrome associated with Down syndrome: outcome after surgical revascularization. Pediatrics 116:e694e7012005

    • Search Google Scholar
    • Export Citation
  • 20

    Karasawa JTouho HOhnishi HMiyamoto SKikuchi H: Long-term follow-up study after extracranial-intracranial bypass surgery for anterior circulation ischemia in childhood moyamoya disease. J Neurosurg 77:84891992

    • Search Google Scholar
    • Export Citation
  • 21

    Kawaguchi SOkuno SSakaki T: Effect of direct arterial bypass on the prevention of future stroke in patients with the hemorrhagic variety of moyamoya disease. J Neurosurg 93:3974012000

    • Search Google Scholar
    • Export Citation
  • 22

    Kelly MEBell-Stephens TEMarks MPDo HMSteinberg GK: Progression of unilateral moyamoya disease: a clinical series. Cerebrovasc Dis 22:1091152006

    • Search Google Scholar
    • Export Citation
  • 23

    Khan NSchuknecht BBoltshauser ECapone ABuck AImhof HG: Moyamoya disease and Moyamoya syndrome: experience in Europe; choice of revascularisation procedures. Acta Neurochir (Wien) 145:106110712003

    • Search Google Scholar
    • Export Citation
  • 24

    Kim SHChoi JYang KKim TKim D: Risk factors for postoperative ischemic complications in patients with moyamoya disease. J Neurosurg 103:4334382005

    • Search Google Scholar
    • Export Citation
  • 25

    Kim SKWang KCKim DGPaek SHChung HTHan MH: Clinical feature and outcome of pediatric cerebrovascular disease: a neurosurgical series. Childs Nerv Syst 16:4214282000

    • Search Google Scholar
    • Export Citation
  • 26

    Kobayashi ESaeki NOishi HHirai SYamaura A: Long-term natural history of hemorrhagic moyamoya disease in 42 patients. J Neurosurg 93:9769802000

    • Search Google Scholar
    • Export Citation
  • 27

    Kraemer MHeienbrok WBerlit P: Moyamoya disease in Europeans. Stroke 39:319332002008

  • 28

    Kuriyama SKusaka YFujimura MWakai KTamakoshi AHashimoto S: Prevalence and clinicoepidemiological features of moyamoya disease in Japan: findings from a nationwide epidemiological survey. Stroke 39:42472008

    • Search Google Scholar
    • Export Citation
  • 29

    Kuroda SHashimoto NYoshimoto TIwasaki Y: Radiological findings, clinical course, and outcome in asymptomatic moyamoya disease: results of multicenter survey in Japan. Stroke 38:143014352007

    • Search Google Scholar
    • Export Citation
  • 30

    Kuroda SIshikawa THoukin KNanba RHokari MIwasaki Y: Incidence and clinical features of disease progression in adult moyamoya disease. Stroke 36:214821532005

    • Search Google Scholar
    • Export Citation
  • 31

    Longo NSchrijver IVogel HPique LMCowan TMPasquali M: Progressive cerebral vascular degeneration with mitochondrial encephalopathy. Am J Med Genet A 146:3613672008

    • Search Google Scholar
    • Export Citation
  • 32

    Matsushima YAoyagi MNariai TTakada YHirakawa K: Long-term intelligence outcome of post-encephalo-duro-arterio-synangiosis childhood moyamoya patients. Clin Neurol Neurosurg 2 Suppl99:S147S1501997

    • Search Google Scholar
    • Export Citation
  • 33

    Olesen JFriberg LOlsen TSAndersen ARLassen NAHansen PE: Ischaemia-induced (symptomatic) migraine attacks may be more frequent than migraine-induced ischaemic insults. Brain 116:1872021993

    • Search Google Scholar
    • Export Citation
  • 34

    Otawara YOgasawara KSeki KKibe MKubo YOgawa A: Intracerebral hemorrhage after prophylactic revascularization in a patient with adult moyamoya disease. Surg Neurol 68:3353372007

    • Search Google Scholar
    • Export Citation
  • 35

    Park-Matsumoto YCTazawa TShimizu J: Migraine with aura-like headache associated with moyamoya disease. Acta Neurol Scand 100:1191211999

    • Search Google Scholar
    • Export Citation
  • 36

    Sakamoto TKawaguchi MKurehara KKitaguchi KFuruya HKarasawa J: Risk factors for neurologic deterioration after revascularization surgery in patients with moyamoya disease. Anesth Analg 85:106010651997

    • Search Google Scholar
    • Export Citation
  • 37

    Scott RMSmith JLRobertson RLMadsen JRSoriano SGRockoff MA: Long-term outcome in children with moyamoya syndrome after cranial revascularization by pial synangiosis. J Neurosurg 100:1421492004

    • Search Google Scholar
    • Export Citation
  • 38

    Seol HJWang KCKim SKHwang YSKim KJCho BK: Headache in pediatric moyamoya disease: review of 204 consecutive cases. J Neurosurg 103:4394422005

    • Search Google Scholar
    • Export Citation
  • 39

    Steinberg GKOgilvy CSShuer LMConnolly ES JrSolomon RALam A: Comparison of endovascular and surface cooling during unruptured cerebral aneurysm repair. Neurosurgery 55:3073152004

    • Search Google Scholar
    • Export Citation
  • 40

    Suzuki JKodama N: Moyamoya disease—a review. Stroke 14:1041091983

  • 41

    Takanashi JSugita KHonda ANiimi H: Moyamoya syndrome in a patient with Down syndrome presenting with chorea. Pediatr Neurol 9:3963981993

    • Search Google Scholar
    • Export Citation
  • 42

    Takeuchi KShimizu K: Hypogenesis of bilateral internal carotid arteries. No To Shinkei 9:37431957

  • 43

    Uchino KJohnston SCBecker KJTirschwell DL: Moyamoya disease in Washington State and California. Neurology 65:9569582005

  • 44

    Veeravagu AGuzman RPatil CGHou LCLee MSteinberg GK: Moyamoya disease in pediatric patients: outcomes of neurosurgical interventions. Neurosurg Focus 24:E162008

    • Search Google Scholar
    • Export Citation
  • 45

    Wakai KTamakoshi AIkezaki KFukui MKawamura TAoki R: Epidemiological features of moyamoya disease in Japan: findings from a nationwide survey. Clin Neurol Neurosurg 99:2 SupplS1S51997

    • Search Google Scholar
    • Export Citation
  • 46

    Wang MYSteinberg GK: Rapid and near-complete resolution of moyamoya vessels in a patient with moyamoya disease treated with superficial temporal artery-middle cerebral artery bypass. Pediatr Neurosurg 24:1451501996

    • Search Google Scholar
    • Export Citation
  • 47

    Yilmaz EYPritz MBBruno ALopez-Yunez ABiller J: Moyamoya: Indiana University Medical Center experience. Arch Neurol 58:127412782001

    • Search Google Scholar
    • Export Citation
  • 48

    Yoshida YYoshimoto TShirane RSakurai Y: Clinical course, surgical management, and long-term outcome of moyamoya patients with rebleeding after an episode of intracerebral hemorrhage: an extensive follow-up study. Stroke 30:227222761999

    • Search Google Scholar
    • Export Citation

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