Ipsilateral late stroke after revascularization surgery for patients with Moyamoya disease



Ipsilateral late stroke events occurring after cerebral revascularization for Moyamoya disease (MMD) and their risk factors have not been fully investigated.


We retrospectively analyzed 123 patients with MMD who underwent 212 revascularizations. We investigated preoperative demographic data, surgical procedures, and ipsilateral stroke events occurring more than 1 month after surgery. The effect of revascularization and the residual Moyamoya vessel (MMV) score were examined using magnetic resonance angiography (MRA). Then, predictive factors for postoperative late stroke occurrence were evaluated by logistic regression.


The mean age was 26 ± 18.4 years (range 1 to 66 years). Ipsilateral late stroke events were present in 11 of 123 (9%) patients. Stroke occurred in 11 out of 212 surgeries (5.2%) on a hemispheric basis. During the 1300.1 hemisphere-years of follow-up more than 1 month after surgery, the annual stroke rate was 0.84%. The postoperative MRA time-of-flight image showed a mean revascularization score of 1.82 ± 0.6 and a mean residual MMV score of 1.91 ± 0.83. Postoperative strokes occurring within 1 month after cerebral revascularization (36.4%, p = 0.0026) and lower revascularization scores (1.82 ± 0.6 vs 2.51 ± 0.59, p = 0.0006) were significant factors related to the presence of ipsilateral late stroke. Logistic regression showed that stroke events within 1 month after revascularization (odds ratio [OR], 9.79; 95% confidence interval [CI], 0.02–0.57; p = 0.0103), low revascularization score (OR, 0.15; 95% CI, 0.001–0.37; p = 0.0069), and high residual MMV score (OR, 16.2; 95% CI, 1.88–187.4; p = 0.0107) were risk factors for ipsilateral stroke more than 1 month after revascularization.


MMD patients who have a stroke within 1 month after cerebral revascularization are at high risk for late strokes. Less effective revascularization or remarkable residual MMV are risk factors for late stroke events. Additional revascularization may be considered for patients in such situations.

Clinical trial registration

This study was approved by the Bioethics Review Committee of Nagoya University Hospital for the treatment and prognosis of Moyamoya disease (2016-0327).

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2


  1. 1.

    Suzuki J, Takaku A (1969) Cerebrovascular “moyamoya” disease. Disease showing abnormal net-like vessels in base of brain. Arch Neurol 20:288–299

    CAS  Article  Google Scholar 

  2. 2.

    Kuroda S, Houkin K (2008) Moyamoya disease: current concepts and future perspectives. Lancet Neurol 7:1056–1066

    Article  Google Scholar 

  3. 3.

    Kuroda S, Houkin K (2012) Bypass surgery for moyamoya disease: concept and essence of surgical techniques. Neurol Med Chir (Tokyo) 52:287–294

    Article  Google Scholar 

  4. 4.

    Miyamoto S, Yoshimoto T, Hashimoto N, Okada Y, Tsuji I, Tominaga T, Nakagawara J, Takahashi JC (2014) Effects of extracranial-intracranial bypass for patients with hemorrhagic moyamoya disease: results of the Japan Adult Moyamoya Trial. Stroke 45:1415–1421

    Article  Google Scholar 

  5. 5.

    Jeon JP, Kim JE, Cho WS, Bang JS, Son YJ, Oh CW (2018) Meta-analysis of the surgical outcomes of symptomatic moyamoya disease in adults. J Neurosurg 128:793–799

    Article  Google Scholar 

  6. 6.

    Kang K, Lu J, Ju Y, Ji R, Wang D, Shen Y, Yu L, Gao B, Zhang D, Zhao X (2020) Clinical and radiological outcomes after revascularization of hemorrhagic moyamoya disease. Front Neurol 11:382

    Article  Google Scholar 

  7. 7.

    Kuroda S, Nakayama N, Yamamoto S, Kashiwazaki D, Uchino H, Saito H, Hori E, Akioka N, Kuwayama N, Houkin K (2020) Late (5-20 years) outcomes after STA-MCA anastomosis and encephalo-duro-myo-arterio-pericranial synangiosis in patients with moyamoya disease. J Neurosurg:1–8. https://doi.org/10.3171/2019.12.jns192938

  8. 8.

    Lee SB, Kim DS, Huh PW, Yoo DS, Lee TG, Cho KS (2012) Long-term follow-up results in 142 adult patients with moyamoya disease according to management modality. Acta Neurochir (Wien) 154:1179–1187

    Article  Google Scholar 

  9. 9.

    Fujimura M, Tominaga T (2015) 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 236:45–53

    Article  Google Scholar 

  10. 10.

    Research Committee on the Pathology and Treatment of Spontaneous Occlusion of the Circle of Willis; Health Labour Sciences Research Grant for Research on Measures for Infractable Diseases (2012) Guidelines for diagnosis and treatment of moyamoya disease (spontaneous occlusion of the circle of Willis). Neurol Med Chir (Tokyo) 52:245–266

    Article  Google Scholar 

  11. 11.

    Araki Y, Uda K, Yokoyama K, Kanamori F, Mamiya T, Nishihori M, Izumi T, Tanahashi K, Sumitomo M, Okamoto S, Wakabayashi T, Natsume A (2020) Surgical designs of revascularization for moyamoya disease: 15 years of experience in a single center. World Neurosurg 139:e325–e334

    Article  Google Scholar 

  12. 12.

    Maruwaka M, Yoshikawa K, Okamoto S, Araki Y, Sumitomo M, Kawamura A, Yokoyama K, Wakabayashi T (2015) Biomarker research for moyamoya disease in cerebrospinal fluid using surface-enhanced laser desorption/ionization time-of-flight mass spectrometry. J Stroke Cerebrovasc Dis 24:104–111

    Article  Google Scholar 

  13. 13.

    Yokoyama K, Maruwaka M, Yoshikawa K, Araki Y, Okamoto S, Sumitomo M, Kawamura A, Sakamoto Y, Shimizu K, Izumi T, Wakabayashi T (2018) Elevation of Proenkephalin 143-183 in cerebrospinal fluid in moyamoya disease. World Neurosurg 109:e446–e459

    Article  Google Scholar 

  14. 14.

    Houkin K, Nakayama N, Kuroda S, Ishikawa T, Nonaka T (2004) How does angiogenesis develop in pediatric moyamoya disease after surgery? A prospective study with MR angiography. Childs Nerv Syst 20:734–741

    PubMed  Google Scholar 

  15. 15.

    Lin Y, Kuo M, Lu C, Lee C, Yang S, Huang Y, Liu H, Chen Y (2019) Standardized MR perfusion scoring system for evaluation of sequential perfusion changes and surgical outcome of moyamoya disease. AJNR Am J Neuroradiol 40:260–266

    Article  Google Scholar 

  16. 16.

    Deng X, Gao F, Zhang D, Zhang Y, Wang R, Wang S, Cao Y, Zhao Y, Pan Y, Liu X, Zhang Q, Zhao J (2018) Direct versus indirect bypasses for adult ischemic-type moyamoya disease: a propensity score-matched analysis. J Neurosurg 128:1785–1791

    Article  Google Scholar 

  17. 17.

    Funaki T, Takahashi JC, Houkin K, Kuroda S, Fujimura M, Tomata Y, Miyamoto S (2019) Effect of choroidal collateral vessels on de novo hemorrhage in moyamoya disease: analysis of nonhemorrhagic hemispheres in the Japan Adult Moyamoya Trial. J Neurosurg 132:408–414

    Article  Google Scholar 

  18. 18.

    Funaki T, Takahashi JC, Houkin K, Kuroda S, Takeuchi S, Fujimura M, Tomata Y, Miyamoto S (2019) High rebleeding risk associated with choroidal collateral vessels in hemorrhagic moyamoya disease: analysis of a nonsurgical cohort in the Japan adult moyamoya trial. J Neurosurg 130:337–673

    Article  Google Scholar 

  19. 19.

    Takahashi JC, Funaki T, Houkin K, Inoue T, Ogasawara K, Nakagawara J, Kuroda S, Yamada K, Miyamoto S (2016) Significance of the hemorrhagic site for recurrent bleeding: prespecified analysis in the Japan adult moyamoya trial. Stroke 47:37–43

    Article  Google Scholar 

  20. 20.

    Kanamori F, Araki Y, Yokoyama K et al (2020) Characteristics of periventricular anastomosis after surgical revascularization in pediatric patients with Moyamoya disease. Jpn J Neurosurg 29:442–447

    Article  Google Scholar 

  21. 21.

    Li Y, Esene I, Mandel M, Bigder M, Steinberg GK (2020) Incidental De novo cerebral microhemorrhages are predictive of future symptomatic macrohemorrhages after surgical revascularization in Moyamoya disease. Neurosurgery. https://doi.org/10.1093/neuros/nyaa319

  22. 22.

    Kikuta K, Takagi Y, Nozaki K, Hanakawa T, Okada T, Mikuni N, Miki Y, Fushmi Y, Yamamoto A, Yamada K, Fukuyama H, Hashimoto N (2005) Asymptomatic microbleeds in moyamoya disease: T2*-weighted gradient-echo magnetic resonance imaging study. J Neurosurg 102:470–475

    Article  Google Scholar 

  23. 23.

    Kikuta K, Takagi Y, Nozaki K, Okada T, Hashimoto N (2007) Histological analysis of microbleed after surgical resection in a patient with moyamoya disease. Neurol Med Chir (Tokyo) 47:564–567

    Article  Google Scholar 

  24. 24.

    Kuroda S, Kashiwazaki D, Ishikawa T, Nakayama N, Houkin K (2013) Incidence, locations, and longitudinal course of silent microbleeds in moyamoya disease: a prospective T2*-weighted MRI study. Stroke 44:516–518

    Article  Google Scholar 

  25. 25.

    Teo M, Johnson J, Steinberg GK (2017) Strategies for and outcome of repeat revascularization surgery for moyamoya disease: an American institutional series. Neurosurgery 81:852–859

    PubMed  Google Scholar 

  26. 26.

    Uchino H, Kashiwazaki D, Akioka N, Koh M, Kuwayama N, Houkin K, Kuroda S (2019) Strategy and effect of repeat bypass surgery for anterior/posterior circulation in refractory moyamoya disease. J Neurosurg:1–11. https://doi.org/10.3171/2019.3.jns181979

  27. 27.

    Funaki T, Takahashi JC, Takagi Y, Yoshida K, Araki Y, Kikuchi T, Kataoka H, Iihara K, Sano N, Miyamoto S (2014) Incidence of late cerebrovascular events after direct bypass among children with moyamoya disease: a descriptive longitudinal study at a single center. Acta Neurochir (Wien) 156:551–559 discussion 559

    Article  Google Scholar 

  28. 28.

    Takahashi JC, Funaki T, Houkin K, Kuroda S, Fujimura M, Tomata Y, Miyamoto S (2020) Impact of cortical hemodynamic failure on both subsequent hemorrhagic stroke and effect of bypass surgery in hemorrhagic moyamoya disease: a supplementary analysis of the Japan Adult Moyamoya Trial. J Neurosurg:1–6. https://doi.org/10.3171/2020.1.jns192392

Download references


This work was funded by a grant from the Japan Society for the Promotion of Science (No. 7118 K08967, https://www.jsps.go.jp).

Author information




All authors contributed to the study conception and design. Material preparation, data collection, and analysis were performed by YA, KY, and KU. The first draft of the manuscript was written by YA, and all authors commented on the previous versions of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Yoshio Araki.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Ethical approval

All the procedures in studies involving human participants were performed in accordance with the ethical standards of the institutional or national research committee and with either the 1964 Declaration of Helsinki and its later amendments or comparable ethical standards. For this type of study, formal consent was not required.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Previous presentation

No portion of the content of this manuscript has been presented or published previously.

This article is part of the Topical Collection on Vascular Neurosurgery

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Araki, Y., Yokoyama, K., Uda, K. et al. Ipsilateral late stroke after revascularization surgery for patients with Moyamoya disease. Acta Neurochir (2021). https://doi.org/10.1007/s00701-021-04773-8

Download citation


  • Moyamoya disease,
  • Moyamoya vessel,
  • Postoperative stroke,
  • Revascularization surgeries