Combined cerebral revascularization for moyamoya disease

Shulgina A.A.; Lukshin V.A.; Usachev D.Yu.; Korshunov A.E.; Belousova O.B.; Pronin I.N.

doi:https://doi.org/10.17116/neiro20218502147

Shulgina A.A.

Burdenko Neurosurgical Center

ORCID: 0000-0002-2887-1583

Lukshin V.A.

Burdenko Neurosurgical Center

ORCID: 0000-0001-5787-484X

Usachev D.Yu.

Burdenko Neurosurgical Center

ORCID: 0000-0002-9811-9442

Korshunov A.E.

Burdenko Neurosurgical Center

Belousova O.B.

Burdenko Neurosurgical Center

ORCID: 0000-0003-4908-8923

Pronin I.N.

Burdenko Neurosurgical Center

SPIN RSCI: 9223-9217
Scopus AuthorID: 7006011755
ORCID: 0000-0002-4480-0275

Combined cerebral revascularization for moyamoya disease

Authors:

Shulgina A.A., Lukshin V.A., Usachev D.Yu., Korshunov A.E., Belousova O.B., Pronin I.N.

More about the authors

Journal: Burdenko's Journal of Neurosurgery. 2021;85(2): 47‑59

DOI: 10.17116/neiro20218502147

Read: 6004 times

To cite this article:

Shulgina AA, Lukshin VA, Usachev DYu, Korshunov AE, Belousova OB, Pronin IN. Combined cerebral revascularization for moyamoya disease. Burdenko's Journal of Neurosurgery. 2021;85(2):47‑59. (In Russ., In Engl.)
https://doi.org/10.17116/neiro20218502147

Подписка 2025 Журнал «Вопросы нейрохирургии» имени Н.Н. Бурденко (Burdenko's Journal of Neurosurgery)

Использование инфографики авторами научных работ

Close metadata

INTRODUCTION

Combined cerebral revascularization with direct and indirect components is recognized as the most appropriate method for treating patients with Moyamoya disease all over the world, however, large studies on its effectiveness in Russia have not yet been conducted.

THE AIM OF THE STUDY

Was to evaluate the results of combined cerebral revascularization in patients with Moyamoya disease with an analysis of the clinical state and perfusion and angiographic features of neoangiogenesis.

MATERIAL AND METHODS

For the period from 2013 to 2020 in N.N. Burdenko National Medical Research Center of Neurosurgery 79 combined revascularizations were performed in 55 patients with Moyamoya disease. The average age was 13.9±10.11 years. All patients were examined according to a single protocol, including a comprehensive assessment of the clinical symptoms, the state of the brain tissue, the cerebral vascular system, and cerebral blood flow. The results of surgical treatment were evaluated in the early postoperative and long-term periods. The average follow-up period was 14.66±13.17 months. In the postoperative period, the dynamics of neurological status and cerebral blood flow were assessed and the features of neoangiogenesis from various components of revascularization were studied.

RESULTS

In the early postoperative period, in 77.2% of cases, a good treatment result was observed, with no negative dynamics of the neurological status. Ischemic stroke in the operated hemisphere developed in 4 cases (5.1%). In the follow-up period, an improvement in neurological symptoms was observed in 76.6%. Improvement of cerebral blood flow was noted in 92.4% of cases, direct anastomoses functioned in 94.3%, and signs of neovascularization in the area of indirect synangiosis were observed in 80.0%. At the same time, a complementary influence of direct and indirect components of revascularization was revealed in ensuring good general angiographic and perfusion results.

CONCLUSIONS

Combined revascularization is a highly effective method of surgical treatment of all patients with Moyamoya disease.

Keywords:

Moyamoya disease

ischemic stroke

surgical revascularization

combined revascularization

extra-intracranial microanastomosis

Authors:

Shulgina A.A.

Burdenko Neurosurgical Center

ORCID: 0000-0002-2887-1583

Lukshin V.A.

Burdenko Neurosurgical Center

ORCID: 0000-0001-5787-484X

Usachev D.Yu.

Burdenko Neurosurgical Center

ORCID: 0000-0002-9811-9442

Korshunov A.E.

Burdenko Neurosurgical Center

Belousova O.B.

Burdenko Neurosurgical Center

ORCID: 0000-0003-4908-8923

Pronin I.N.

Burdenko Neurosurgical Center

SPIN RSCI: 9223-9217
Scopus AuthorID: 7006011755
ORCID: 0000-0002-4480-0275

Received:

24.05.2020

Accepted:

05.02.2021

Close metadata

References:

Baba T, Houkin K, Kuroda S. Novel epidemiological features of moyamoya disease. Journal of Neurology, Neurosurgery and Psychiatry. 2008;79(8):900-904. https://doi.org/10.1136/jnnp.2007.130666
Kuroda S, Houkin K. Moyamoya disease: current concepts and future perspectives. The Lancet. Neurology. 2008;7(11):1056-1066. https://doi.org/10.1016/S1474-4422(08)70240-0
Kuroda S, Hashimoto N, Yoshimoto T, Iwasaki Y; Research Committee on Moyamoya Disease in Japan. Radiological Findings, Clinical Course, and Outcome in Asymptomatic Moyamoya Disease. Stroke. 2007;38(5):1430-1435. https://doi.org/10.1161/STROKEAHA.106.478297
Kobayashi E, Saeki N, Oishi H, Hirai S, Yamaura A. Long-term natural history of hemorrhagic moyamoya disease in 42 patients. Journal of Neurosurgery. 2000;93(6):976-980. https://doi.org/10.3171/jns.2000.93.6.0976
Guzman R, Lee M, Achrol A, Bell-Stephens T, Kelly M, Do HM, Marks MP, Steinberg GK. Clinical outcome after 450 revascularization procedures for moyamoya disease. Clinical article. Journal of Neurosurgery. 2009;111(5):927-935. https://doi.org/10.3171/2009.4.JNS081649
Miyamoto S, Yoshimoto T, Hashimoto N, Okada Y, Tsuji I, Tominaga T, Nakagawara J, Takahashi JC; JAM Trial Investigators. Effects of extracranial-intracranial bypass for patients with hemorrhagic moyamoya disease: results of the Japan Adult Moyamoya Trial. Stroke. 2014;45(5):1415-1421. https://doi.org/10.1161/STROKEAHA.113.004386
Shulgina AA, Lukshin VA, Korshunov AE, Belousova OB, Pronin IN, Usachev DY. Modern trends in diagnosis and surgical treatment of moyamoya disease. Voprosy nejrohirurgii im. N.N. Burdenko. 2020;84(4):90-103. (In Russ). https://doi.org/10.17116/neiro20208404190
Houkin K, Kamiyama H, Takahashi A, Kuroda S, Abe H. Combined revascularization surgery for childhood moyamoya disease: STA-MCA and encephalo-duro-arterio-myo-synangiosis. Child’s Nervous System: ChNS. 1997;13(1):24-29. https://doi.org/10.1007/s003810050034
Sun H, Wilson C, Ozpinar A, Safavi-Abbasi S, Zhao Y, Nakaji P, Wanebo JE, Spetzler RF. Perioperative Complications and Long-Term Outcomes After Bypasses in Adults with Moyamoya Disease: A Systematic Review and Meta-Analysis. World Neurosurgery. 2016;92:179-188. https://doi.org/10.1016/j.wneu.2016.04.083
Korshunov AE, Pronin IN, Golovteev AL. Moyamoya disease is a treatable cause of repeated ischemic strokes in children. Russkij zhurnal detskoj nevrologii. 2010;5(1):27-34. (In Russ.).
Samitova ER, Mazankova LN, Mosin IM, Osmanov IM, Zykov VP, Akhadov TA, Melnikov IA, Koroid NV, Tambiev IE, Dikova EA, Elfimova OI, Getmanchenko YuG. Moyamoya disease in the practice of a pediatric infectious disease specialist. Rossijskij vestnik perinatologii i pediatrii. 2017;62(2):78-83. (In Russ.). https://doi.org/10.21508/1027-4065-2017-62-2-78-83
Kovalenko AP, Shopin VN, Penner VA, Scherbin AV. Moyamoya disease: a case from practice. Endovaskulyarna nejrorentgenohіrurgіya. 2013;5(3):54-61. (In Russ.).
Lvova OA, Gusev VV, Kovtun OP. Is Moyamoya disease the only and sufficient reason for acute cerebrovascular accident? Nejrohirurgiya i nevrologiya detskogo vozrasta. 2013;35(1):50-56. (In Russ.).
Petrukhin AS, Mukhin KYu, Alikhanov AA, Kulikov SV, Abbasova AA. Moyamoya syndrome in a patient with type I neurofibromatosis. Nevrologicheskij zhurnal. 1999;6:16-18. (In Russ.).
Panuntsev VS, Khristoforova MI. Moyamoya disease and syndrome. Nejrohirurgiya. 2001;3:6-11. (In Russ.).
Khachatryan VA, Samochernykh KA, Trofimova TN. Cerebrovaskulyarnaya patologiya u detej. SPb.: Desyatka; 2006. (In Russ.).
Ovsyannikov KS, Dubovoy AV, Galaktionov DM. Combined (direct and indirect) revascularization in moiamoia disease in adult patients. Nejrohirurgiya. 2018;20(3):57-66. (In Russ.). https://doi.org/10.17650/1683-3295-2018-20-3-57-66
Shulgina AA, Lukshin VA, Korshunov AE, Usachev DY, Pronin IN. Combination of double and indirect two-sided revascularization of the brain in the treatment of moyamoya disease. Voprosy nejrohirurgii im. N.N. Burdenko. 2020;84(2):93-102. (In Russ.). https://doi.org/10.17116/neiro20208402193
Kwah LK, Diong J. National Institutes of Health Stroke Scale (NIHSS). Journal of Physiotherapy. 2014;60(1):61. https://doi.org/10.1016/j.jphys.2013.12.012
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. Guidelines for diagnosis and treatment of moyamoya disease (spontaneous occlusion of the circle of Willis). Neurologia Medico-Chirurgica. 2012;52(5):245-66. https://doi.org/10.2176/nmc.52.245
Houkin K, Nakayama N, Kuroda S, Nonaka T, Shonai T, Yoshimoto T. Novel Magnetic Resonance Angiography Stage Grading for Moyamoya Disease. Cerebrovascular Diseases. 2005;20(5):347-354. https://doi.org/10.1159/000087935
Suzuki J, Takaku A. Cerebrovascular «moyamoya» disease. Disease showing abnormal net-like vessels in base of brain. Archives of Neurology. 1969;20(3):288-299. https://doi.org/10.1001/archneur.1969.00480090076012
Zhao Y, Yu S, Lu J, Yu L, Li J, Zhang Y, Zhang D, Wang R, Zhao Y. Direct Bypass Surgery Vs. Combined Bypass Surgery for Hemorrhagic Moyamoya Disease: A Comparison of Angiographic Outcomes. Frontiers in Neurology. 2018;9:1121. https://doi.org/10.3389/fneur.2018.01121
Robertson RL, Burrows PE, Barnes PD, Robson CD, Poussaint TY, Scott RM. Angiographic changes after pial synangiosis in childhood moyamoya disease. AJNR American Journal of Neuroradiology. 1997;18(5):837-845.
Jeon JP, Kim JE, Cho WS, Bang JS, Son YJ, Oh CW. Meta-analysis of the surgical outcomes of symptomatic moyamoya disease in adults. Journal of Neurosurgery. 2018;128(3):793-799. https://doi.org/10.3171/2016.11.JNS161688
Ge P, Ye X, Liu X, Deng X, Wang J, Wang R, Zhang Y, Zhang D, Zhang Q, Zhao J. Angiographic Outcomes of Direct and Combined Bypass Surgery in Moyamoya Disease. Frontiers in Neurology. 2019;10:1267. https://doi.org/10.3389/fneur.2019.01267
Czabanka M, Peña-Tapia P, Scharf J, Schubert GA, Münch E, Horn P, Schmiedek P, Vajkoczy P. Characterization of direct and indirect cerebral revascularization for the treatment of European patients with moyamoya disease. Cerebrovascular Diseases. 2011;32(4):361-369. https://doi.org/10.1159/000330351
Ishii D, Okazaki T, Matsushige T, Shinagawa K, Sakamoto S, Oshita J, Kurisu K. Chronic Dilatation of Superficial Temporal Artery and Middle Meningeal Artery Associated with Development of Collateral Circulation After Bypass Surgery for Moyamoya Angiopathy. World Neurosurgery. 2018;119:864-873. https://doi.org/10.1016/j.wneu.2018.07.287
Honda M, Kitagawa N, Tsutsumi K, Morikawa M, Nagata I, Kaminogo M. Magnetic resonance angiography evaluation of external carotid artery tributaries in moyamoya disease. Surgical Neurology. 2005;64(4):325-330. https://doi.org/10.1016/j.surneu.2004.12.020
Hasuo K, Mihara F, Matsushima T. MRI and MR angiography in moyamoya disease. Journal of Magnetic Resonance Imaging: JMRI. 1998;8(4):762-766. https://doi.org/10.1002/jmri.1880080403
Yoon HK, Shin HJ, Lee M, Byun HS, Na DG, Han BK. MR angiography of moyamoya disease before and after encephaloduroarteriosynangiosis. AJR American Journal of Roentgenology. 2000;174(1):195-200. https://doi.org/10.2214/ajr.174.1.1740195
Matsushima T, Inoue T, Ikezaki K, Matsukado K, Natori Y, Inamura T, Fukui M. Multiple combined indirect procedure for the surgical treatment of children with moyamoya disease. A comparison with single indirect anastomosis and direct anastomosis. Neurosurgical Focus. 1998;5(5):4. https://doi.org/10.3171/foc.1998.5.5.7
Bang JS, Kwon OK, Kim JE, Kang HS, Park H, Cho SY, Oh CW. Quantitative angiographic comparison with the OSIRIS program between the direct and indirect revascularization modalities in adult moyamoya disease. Neurosurgery. 2012;70(3):625-632; discussion 632-633. https://doi.org/10.1227/NEU.0b013e3182333c47