Predictors of neoangiogenesis after indirect revascularization in moyamoya disease: a multicenter retrospective study

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OBJECTIVE

The effect of indirect revascularization to improve cerebral perfusion for moyamoya disease (MMD) is based on ingrowth of new vessels into the cortical brain. Preoperative indicators for neoangiogenesis would be helpful to the selection of appropriate procedures for MMD patients but have not yet been investigated. Our study aimed to identify potential predictors for neovascularization after indirect bypass surgery.

METHODS

The authors reviewed consecutive cases with complete clinical and radiological documentation of patients who had undergone surgery between December 2010 and January 2018. Patients who were treated with indirect bypass surgery were included. Cerebrovascular characteristics were evaluated by catheter angiography. Neoangiogenesis after indirect bypass was determined as “good” or “poor” based on the Matsushima standard. Univariate and multivariate analyses were performed to identify predictors for neoangiogenesis after indirect bypass. Subgroup analyses by onset type and surgical type were carried out to identify specific predictors for different populations.

RESULTS

In total, 231 hemispheres of 209 patients (mean ± SD age 23.06 ± 15.09 years, range 3–61 years) were retrospectively included. In 146 (63.2%) hemispheres, good neoangiogenesis was observed after indirect revascularization. Multivariate analysis showed that the status of ICA moyamoya vessels (p < 0.001, OR [95% CI] 3.242 [2.007–5.236]) is a predictor of favorable neoangiogenesis after indirect bypass surgery, whereas hemorrhagic onset (p < 0.001, OR [95% CI] 0.138 [0.054–0.353]) is a risk factor for poor neoangiogenesis. In addition, younger age was significantly associated with good neovascularization in patients with hemorrhagic onset (p = 0.027, OR [95% CI] 0.893 [0.808–0.987]), whereas age was not a significant predictor for neovascularization in non–hemorrhagic-onset patients (p = 0.955). Hemispheres with good revascularization had lower incidence of rebleeding, lower modified Rankin Scale scores, and more improvement of symptoms during long-term follow-up (p = 0.026, 0.006, and 0.013, respectively).

CONCLUSIONS

Hemorrhagic onset predicts poor neovascularization after indirect bypass surgery for MMD patients. Abundant ICA moyamoya vessels indicate good neoangiogenesis after indirect bypass and vice versa, whereas absent ICA moyamoya vessels predict poor revascularization. Good neovascularization was associated with better long-term outcome. Future studies are needed to further address this issue and clarify the underlying pathophysiological mechanisms.

ABBREVIATIONS ACA = anterior cerebral artery; DSA = digital subtraction angiography; EC-IC = extracranial-intracranial; EDAS = encephaloduroarteriosynangiosis; EDGS = encephalodurogaleo(periosteal)synangiosis; ICA = internal carotid artery; MBH = multiple burr hole; MD = moyamoya disease; mRS = modified Rankin Scale; OphA = ophthalmic artery; PCA = posterior cerebral artery; STA = superficial temporal artery; TIA = transient ischemic attack.
Article Information

Contributor Notes

Correspondence Yuanli Zhao: Beijing Tiantan Hospital, Capital Medical University, Beijing, China. zhaoyuanli@126.com.INCLUDE WHEN CITING Published online January 25, 2019; DOI: 10.3171/2018.9.JNS181562.Disclosures The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.
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References
  • 1

    Acker GFekonja LVajkoczy P: Surgical management of moyamoya disease. Stroke 49:4764822018

  • 2

    Adelson PDScott RM: Pial synangiosis for moyamoya syndrome in children. Pediatr Neurosurg 23:26331995

  • 3

    Aoki N: Cerebrovascular bypass surgery for the treatment of moyamoya disease: unsatisfactory outcome in the patients presenting with intracranial hemorrhage. Surg Neurol 40:3723771993

    • Search Google Scholar
    • Export Citation
  • 4

    Arias EJDunn GPWashington CWDerdeyn CPChicoine MRGrubb RL Jr: Surgical revascularization in North American adults with moyamoya phenomenon: long-term angiographic follow-up. J Stroke Cerebrovasc Dis 24:159716082015

    • Search Google Scholar
    • Export Citation
  • 5

    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 128:132713372018

    • Search Google Scholar
    • Export Citation
  • 6

    Fujimura MTominaga T: Lessons learned from moyamoya disease: outcome of direct/indirect revascularization surgery for 150 affected hemispheres. Neurol Med Chir (Tokyo) 52:3273322012

    • Search Google Scholar
    • Export Citation
  • 7

    Ge PYe XZhang QZhang DWang SZhao J: Encephaloduroateriosynangiosis versus conservative treatment for patients with moyamoya disease at late Suzuki stage. J Clin Neurosci 50:2772802018

    • Search Google Scholar
    • Export Citation
  • 8

    Goda MIsono MIshii KKamida TAbe TKobayashi H: Long-term effects of indirect bypass surgery on collateral vessel formation in pediatric moyamoya disease. J Neurosurg 100 (2 Suppl Pediatrics):1561622004

    • Search Google Scholar
    • Export Citation
  • 9

    Imai HMiyawaki SOno HNakatomi HYoshimoto YSaito N: The importance of encephalo-myo-synangiosis in surgical revascularization strategies for moyamoya disease in children and adults. World Neurosurg 83:6916992015

    • Search Google Scholar
    • Export Citation
  • 10

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

    • Search Google Scholar
    • Export Citation
  • 11

    Kawamoto HKiya KMizoue TOhbayashi N: A modified burr-hole method ‘galeoduroencephalosynangiosis’ in a young child with moyamoya disease. A preliminary report and surgical technique. Pediatr Neurosurg 32:2722752000

    • Search Google Scholar
    • Export Citation
  • 12

    Kim SKWang KCKim IOLee DSCho BK: Combined encephaloduroarteriosynangiosis and bifrontal encephalogaleo (periosteal) synangiosis in pediatric moyamoya disease. Neurosurgery 62 (6 Suppl 3):145614642008

    • Search Google Scholar
    • Export Citation
  • 13

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

  • 14

    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

    • Search Google Scholar
    • Export Citation
  • 15

    Macyszyn LAttiah MMa TSAli ZFaught RHossain A: Direct versus indirect revascularization procedures for moyamoya disease: a comparative effectiveness study. J Neurosurg 126:152315292017

    • Search Google Scholar
    • Export Citation
  • 16

    Matsushima TInoue TSuzuki SOFujii KFukui MHasuo K: Surgical treatment of moyamoya disease in pediatric patients—comparison between the results of indirect and direct revascularization procedures. Neurosurgery 31:4014051992

    • Search Google Scholar
    • Export Citation
  • 17

    Nakashima HMeguro TKawada SHirotsune NOhmoto T: Long-term results of surgically treated moyamoya disease. Clin Neurol Neurosurg 99 (Suppl 2):S156S1611997

    • Search Google Scholar
    • Export Citation
  • 18

    Ogiwara HMorota N: Bifrontal encephalogaleosynangiosis for children with moyamoya disease. J Neurosurg Pediatr 10:2462512012

  • 19

    Park SEKim JSPark EKShim KWKim DS: Direct versus indirect revascularization in the treatment of moyamoya disease. J Neurosurg 129:4804892018

    • Search Google Scholar
    • Export Citation
  • 20

    Patel NNMangano FTKlimo P Jr: Indirect revascularization techniques for treating moyamoya disease. Neurosurg Clin N Am 21:5535632010

    • Search Google Scholar
    • Export Citation
  • 21

    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

    • Search Google Scholar
    • Export Citation
  • 22

    Scott RMSmith JLRobertson RLMadsen JRSoriano SGRockoff MA: Long-term outcome in children with moyamoya syndrome after cranial revascularization by pial synangiosis. J Neurosurg 100 (2 Suppl Pediatrics):1421492004

    • Search Google Scholar
    • Export Citation
  • 23

    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

    • Search Google Scholar
    • Export Citation
  • 24

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

    • Search Google Scholar
    • Export Citation
  • 25

    Teo MKMadhugiri VSSteinberg GK: Editorial. Direct versus indirect bypass for moyamoya disease: ongoing controversy. J Neurosurg 126:152015222017

    • Search Google Scholar
    • Export Citation
  • 26

    Zhao JLiu HZou YZhang WHe S: Clinical and angiographic outcomes after combined direct and indirect bypass in adult patients with moyamoya disease: a retrospective study of 76 procedures. Exp Ther Med 15:357035762018

    • Search Google Scholar
    • Export Citation
  • 27

    Zhao MDeng XZhang DWang SZhang YWang R: Risk factors for and outcomes of postoperative complications in adult patients with moyamoya disease. J Neurosurg 130:5315422019

    • Search Google Scholar
    • Export Citation
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