Acta Neurochirurgica

, Volume 161, Issue 5, pp 947–954 | Cite as

Restoration of periventricular vasculature after direct bypass for moyamoya disease: intra-individual comparison

  • Akinori Miyakoshi
  • Takeshi FunakiEmail author
  • Jun C Takahashi
  • Yasushi Takagi
  • Takayuki Kikuchi
  • Kazumichi Yoshida
  • Hiroharu Kataoka
  • Yohei Mineharu
  • Masakazu Okawa
  • Yukihiro Yamao
  • Yasutaka Fushimi
  • Tomohisa Okada
  • Kaori Togashi
  • Susumu Miyamoto
Original Article - Vascular Neurosurgery - Other
Part of the following topical collections:
  1. Vascular Neurosurgery – Other



While periventricular anastomosis, a unique abnormal vasculature in moyamoya disease, has been studied in relation to intracranial hemorrhage, no study has addressed its change after bypass surgery. The authors sought to test whether direct bypass surgery could restore normal periventricular vasculature.


Patients who had undergone direct bypass surgery for moyamoya disease at a single institution were eligible for the study. Baseline, postoperative, and follow-up magnetic resonance angiography (MRA) scans were scheduled before surgery, after the first surgery, and 3 to 6 months after contralateral second surgery, respectively. Sliding-thin-slab maximum-intensity-projection coronal MRA images of periventricular anastomoses were scored according to the three subtypes (lenticulostriate, thalamic, and choroidal anastomosis). Baseline and postoperative MRA images were compared to obtain a matched comparison of score changes in the surgical and nonsurgical hemispheres within individuals (intra-individual comparison).


Of 110 patients, 42 were identified for intra-individual comparisons. The periventricular anastomosis score decreased significantly in the surgical hemispheres (median, 2 versus 1; p < 0.001), whereas the score remained unchanged in the nonsurgical hemispheres (median, 2 versus 2; p = 0.57); the score change varied significantly between the surgical and nonsurgical hemispheres (p < 0.001). Of the 104 periventricular-anastomosis-positive hemispheres undergoing surgery, 47 (45.2%) were assessed as negative in the follow-up MRA. Among the subtypes, choroidal anastomosis was most likely to be assessed as negative (79.7% of positive hemispheres).


Periventricular vasculature can be restored after direct bypass. The likelihood of correction of choroidal anastomosis is a subject requiring further studies.


Moyamoya disease Intracranial hemorrhage Cerebral revascularization Periventricular anastomosis 



Middle cerebral artery


Magnetic resonance angiography


Posterior cerebral artery


Single photon emission tomography


Superficial temporal artery


Sliding-thin-slab maximum-intensity-projection


Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

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

Informed consent

All subjects gave opt-out consent.


  1. 1.
    Akashi T, Takahashi S, Mugikura S, Sato S, Murata T, Umetsu A, Takase K (2017) Ischemic white matter lesions associated with medullary arteries: classification of MRI findings based on the anatomic arterial distributions. AJR Am J Roentgenol 209:W160–W168CrossRefGoogle Scholar
  2. 2.
    Ding J, Zhou D, Paul Cosky EE, Pan L, Ya J, Wang Z, Jin K, Guan J, Ding Y, Ji X, Meng R (2018) Hemorrhagic moyamoya disease treatment: a network meta-analysis. World Neurosurg 117:e557–e562CrossRefGoogle Scholar
  3. 3.
    Fujimura M, Funaki T, Houkin K, Takahashi JC, Kuroda S, Tomata Y, Tominaga T, Miyamoto S (2018) Intrinsic development of choroidal and thalamic collaterals in hemorrhagic-onset moyamoya disease: case control study of the Japan Adult Moyamoya Trial. J Neurosurg 1:1–7. CrossRefGoogle Scholar
  4. 4.
    Funaki T, Fushimi Y, Takahashi JC, Takagi Y, Araki Y, Yoshida K, Kikuchi T, Miyamoto S (2015) Visualization of periventricular collaterals in moyamoya disease with flow-sensitive black-blood magnetic resonance angiography: preliminary experience. Neurol Med Chir (Tokyo) 55:204–209CrossRefGoogle Scholar
  5. 5.
    Funaki T, Takahashi JC, Houkin K, Kuroda S, Takeuchi S, Fujimura M, Tomata Y, Miyamoto S (2018) Angiographic features of hemorrhagic moyamoya disease with high recurrence risk: a supplementary analysis of the Japan Adult Moyamoya Trial. J Neurosurg 128:777–784CrossRefGoogle Scholar
  6. 6.
    Funaki T, Takahashi JC, Houkin K, Kuroda S, Takeuchi S, Fujimura M, Tomata Y, Miyamoto S (2018) 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 1:1–8. Google Scholar
  7. 7.
    Funaki T, Takahashi JC, Takagi Y, Yoshida K, Araki Y, Kikuchi T, Kataoka H, Iihara K, Miyamoto S (2013) Impact of posterior cerebral artery involvement on long-term clinical and social outcome of pediatric moyamoya disease. J Neurosurg Pediatr 12:626–632CrossRefGoogle Scholar
  8. 8.
    Funaki T, Takahashi JC, Yoshida K, Takagi Y, Fushimi Y, Kikuchi T, Mineharu Y, Okada T, Morimoto T, Miyamoto S (2016) Periventricular anastomosis in moyamoya disease: detecting fragile collateral vessels with MR angiography. J Neurosurg 124:1766–1772CrossRefGoogle Scholar
  9. 9.
    Han DH, Kwon OK, Byun BJ, Choi BY, Choi CW, Choi JU, Choi SG, Doh JO, Han JW, Jung S, Kang SD, Kim DJ, Kim HI, Kim HD, Kim MC, Kim SC, Kim SC, Kim Y, Kwun BD, Lee BG, Lim YJ, Moon JG, Park HS, Shin MS, Song JH, Suk JS, Yim MB, Korean Society for Cerebrovascular D (2000) A co-operative study: clinical characteristics of 334 Korean patients with moyamoya disease treated at neurosurgical institutes (1976–1994). The Korean Society for Cerebrovascular Disease. Acta Neurochir 142:1263–1273 discussion 1273–1264CrossRefGoogle Scholar
  10. 10.
    Houkin K, Kamiyama H, Abe H, Takahashi A, Kuroda S (1996) Surgical therapy for adult moyamoya disease. Can surgical revascularization prevent the recurrence of intracerebral hemorrhage. Stroke 27:1342–1346CrossRefGoogle Scholar
  11. 11.
    Irikura K, Miyasaka Y, Kurata A, Tanaka R, Yamada M, Kan S, Fujii K (2000) The effect of encephalo-myo-synangiosis on abnormal collateral vessels in childhood moyamoya disease. Neurol Res 22:341–346CrossRefGoogle Scholar
  12. 12.
    Jang DK, Lee KS, Rha HK, Huh PW, Yang JH, Park IS, Ahn JG, Sung JH, Han YM (2017) Bypass surgery versus medical treatment for symptomatic moyamoya disease in adults. J Neurosurg 127:492–502CrossRefGoogle Scholar
  13. 13.
    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 128:793–799CrossRefGoogle Scholar
  14. 14.
    Jiang H, Ni W, Xu B, Lei Y, Tian Y, Xu F, Gu Y, Mao Y (2014) Outcome in adult patients with hemorrhagic moyamoya disease after combined extracranial-intracranial bypass. J Neurosurg 121:1048–1055CrossRefGoogle Scholar
  15. 15.
    Karasawa J, Touho H, Ohnishi H, Miyamoto S, Kikuchi H (1992) Long-term follow-up study after extracranial-intracranial bypass surgery for anterior circulation ischemia in childhood moyamoya disease. J Neurosurg 77:84–89CrossRefGoogle Scholar
  16. 16.
    Liu X, Zhang D, Shuo W, Zhao Y, Wang R, Zhao J (2013) Long term outcome after conservative and surgical treatment of haemorrhagic moyamoya disease. J Neurol Neurosurg Psychiatry 84:258–265CrossRefGoogle Scholar
  17. 17.
    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 45:1415–1421CrossRefGoogle Scholar
  18. 18.
    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 Intractable Diseases (2012) Guidelines for diagnosis and treatment of moyamoya disease (spontaneous occlusion of the circle of Willis). Neurol Med Chir (Tokyo) 52:245–266CrossRefGoogle Scholar
  19. 19.
    Suzuki J, Kodama N (1983) Moyamoya disease--a review. Stroke 14:104–109CrossRefGoogle Scholar
  20. 20.
    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 47:37–43CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2019

Authors and Affiliations

  • Akinori Miyakoshi
    • 1
  • Takeshi Funaki
    • 1
    Email author
  • Jun C Takahashi
    • 2
  • Yasushi Takagi
    • 3
  • Takayuki Kikuchi
    • 1
  • Kazumichi Yoshida
    • 1
  • Hiroharu Kataoka
    • 1
  • Yohei Mineharu
    • 1
  • Masakazu Okawa
    • 1
  • Yukihiro Yamao
    • 1
  • Yasutaka Fushimi
    • 4
  • Tomohisa Okada
    • 5
  • Kaori Togashi
    • 4
  • Susumu Miyamoto
    • 1
  1. 1.Department of NeurosurgeryKyoto University Graduate School of MedicineKyotoJapan
  2. 2.Department of NeurosurgeryNational Cerebral and Cardiovascular CenterOsakaJapan
  3. 3.Department of NeurosurgeryTokushima University Graduate School of Biomedical SciencesTokushimaJapan
  4. 4.Department of Diagnostic Imaging and Nuclear MedicineKyoto University Graduate School of MedicineKyotoJapan
  5. 5.Department of Human Brain Research CenterKyoto University Graduate School of MedicineKyotoJapan

Personalised recommendations