Abstract
Background
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.
Methods
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).
Results
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).
Conclusions
Periventricular vasculature can be restored after direct bypass. The likelihood of correction of choroidal anastomosis is a subject requiring further studies.
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Abbreviations
- MCA:
-
Middle cerebral artery
- MRA:
-
Magnetic resonance angiography
- PCA:
-
Posterior cerebral artery
- SPECT:
-
Single photon emission tomography
- STA:
-
Superficial temporal artery
- STS-MIP:
-
Sliding-thin-slab maximum-intensity-projection
References
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–W168
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–e562
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. https://doi.org/10.3171/2017.11.jns171990
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) 55:204–209
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 128:777–784
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. https://doi.org/10.3171/2017.9.jns17576
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 12:626–632
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 124:1766–1772
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 1273–1264
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 27:1342–1346
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 22:341–346
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 127:492–502
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
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 121:1048–1055
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 77:84–89
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 84:258–265
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
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) 52:245–266
Suzuki J, Kodama N (1983) Moyamoya disease--a review. Stroke 14:104–109
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
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In this study, the authors used MRA to evaluate the periventricular anastomosis in patients with moyamoya disease and score the changes after direct bypass surgery including intra-individual comparison. The study nicely demonstrated the beneficial effect of direct EC-IC bypass on periventricular anastomosis in patients with moyamoya disease. This effect has long been purported to occur and described anecdotally, but this is the first study to demonstrate this effect as related to direct bypass surgery. Further work aiming to elucidate the factors influencing the degree of improvement would be welcome. For example, measuring flow in the bypass during surgery and afterwards and determining whether a robust bypass with greater flow augmentation, might be a factor, would be of great value. Also, longer term correlation of the changes in anastomosis patterns with the risk of bleeding and outcomes would be most welcome. But for the time being, the authors are to be congratulated on this novel work which nicely adds to our understanding of this elusive disease.
Fady Charbel
Illinois, USA
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This article is part of the Topical Collection on Vascular Neurosurgery - Other
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Miyakoshi, A., Funaki, T., Takahashi, J.C. et al. Restoration of periventricular vasculature after direct bypass for moyamoya disease: intra-individual comparison. Acta Neurochir 161, 947–954 (2019). https://doi.org/10.1007/s00701-019-03866-9
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DOI: https://doi.org/10.1007/s00701-019-03866-9