REVIEW

Bypass, Minimally Invasive and Endoscopic Procedures in Moyamoya Disease: current clinical impact and future perspectives

Bypass, Procedimentos Minimamente Invasivos e Endoscópicos na Doença de Moyamoya: impacto clínico atual e perspectivas para o futuro

  • Thiago de Mendonça Nonato Oliveira    Thiago de Mendonça Nonato Oliveira
  • André Giacomelli Leal    André Giacomelli Leal
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Resumo

Doença de Moyamoya (DMM) é uma arteriopatia cerebrovascular progressiva caracterizada por estenose da artéria carótida interna e seus ramos, associada à formação de circulação colateral anômala. Apresenta distribuição etária bimodal, com maior prevalência em populações do Leste Asiático e risco variável entre grupos populacionais. O manejo clínico visa reduzir eventos isquêmicos e hemorrágicos, enquanto a revascularização cirúrgica constitui a principal estratégia terapêutica. Este estudo objetiva analisar criticamente as evidências sobre revascularização direta e indireta, bem como abordagens menos invasivas, avaliando benefícios funcionais, riscos, limitações e perspectivas futuras em neurocirurgia. Foram revisados estudos clínicos recentes e revisões sobre bypass direto (ATC-ACM, AO-ACM e enxertos) e indireto (EDAS, EMS, EAS, EDS, EMAS). Os desfechos incluíram perfusão cerebral, eventos isquêmicos/hemorrágicos, desenvolvimento de colaterais, função neurológica (escala de Rankin modificada) e complicações perioperatórias, com ênfase em síndrome de hiperperfusão cerebral. O bypass direto oferece restauração imediata do fluxo e melhora funcional precoce, tornando-o preferível em adultos com alto risco de isquemia. O bypass indireto, menos invasivo, promove angiogênese gradual e maior segurança em crianças. Abordagens híbridas e técnicas minimamente invasivas emergem como alternativas promissoras. A seleção do procedimento deve ser individualizada, considerando idade, anatomia vascular e risco clínico.

Palavras-chave

Doença de Moyamoya; Revascularização cerebral; Neurocirurgia; Cirurgia minimamente invasiva; Neuroendoscopia

Abstract

Moyamoya disease (MMD) is a progressive cerebrovascular arteriopathy characterized by stenosis of the internal carotid artery and its branches, associated with the formation of anomalous collateral circulation. It presents a bimodal age distribution, with a higher prevalence in East Asian populations and variable risk among population groups. Clinical management aims to reduce ischemic and hemorrhagic events, while surgical revascularization constitutes the main therapeutic strategy. This study aims to critically analyze the evidence on direct and indirect revascularization, as well as less invasive approaches, evaluating functional benefits, risks, limitations, and future perspectives in neurosurgery. Recent clinical studies and reviews on direct (STA-MCA, OA-MCA and grafts) and indirect (EDAS, EMS, EAS, EDS, EMAS) bypass were reviewed. Outcomes included cerebral perfusion, ischemic/hemorrhagic events, collateral development, neurological function (mRS), and perioperative complications, with emphasis on cerebral hyperperfusion syndrome. Direct bypass offers immediate restoration of flow and early functional improvement, making it preferable in adults with a high risk of ischemia. Indirect bypass, which is less invasive, promotes gradual angiogenesis and greater safety in children. Hybrid approaches and minimally invasive techniques are emerging as promising alternatives. The selection of the procedure should be individualized, considering age, vascular anatomy, and clinical risk.

Keywords

Moyamoya disease; Cerebral revascularization; Neurosurgery; Minimally invasive surgical procedures; Neuroendoscopy

References

1. Koc NA, Rakowski M, Pettersson SD, Skrzypkowska P, Szmuda T, Zieliński P. Ultrasonographic assessment of bypass capacity after revascularization surgery in moyamoya disease: a systematic review and single-arm meta-analysis. Acta Neurochir (Wien). 2025;167(1):242. https://doi.org/10.1007/s00701-025-06658-6. PMid:40928552.

2. Takahashi T, Ito Y, Hirata K, et al. Evaluation of cortical microvascularization by preoperative maximum intensity projection method in moyamoya disease reflects the increase of pial arteries on the brain surface. Neurol Med Chir (Tokyo). 2025;65(11):510-6. https:// doi.org/10.2176/jns-nmc.2025-0107. PMid:40967775.

9. Cui J, Lu C, Xu Z, Yao L. The impact of anesthesia methods on early postoperative cognitive function in Moyamoya disease patients after vascular bypass surgery. Medicine (Baltimore). 2025;104(35):e43317. https://doi.org/10.1097/MD.0000000000043317. PMid:40898529.

10. Zhang J, Zhang J, Yang L, et al. Anesthetic management in combined off-pump CABG and EC-IC bypass for CAD and Moyamoya disease. 

JACC Case Rep. 2025;30(24):104752. https://doi.org/10.1016/j. jaccas.2025.104752. PMid:40846375.

11. Ikezawa M, Takasu S, Nishihori M, et al. A case of anastomotic aneurysm after superficial temporal artery-middle cerebral artery bypass for moyamoya disease treated with coil embolization. J Neuroendovasc Ther. 2025;19(1):2025-0051. https://doi.org/10.5797/jnet.cr.2025-0051. PMid:40766792.

12. Ajala RT, Nguyen A, Lyon K, Qaiser R. Indirect bypass with pericranial transposition for moyamoya syndrome in an infant. Cureus. 2023;15(8):e44073. https://doi.org/10.7759/cureus.4407 . PMid:37750109.

13. Wang JZ, Mu J, Zhang D, Zheng S, Zhu X, Wei X. Clinical use of color Doppler ultrasonography to predict and evaluate the collateral development of two common revascularizations in patients with moyamoya disease. Front Neurol. 2022;13:976695. https://doi.

org/10.3389/fneur.2022.976695. PMid:36388226.

14. Kameno K, Kaku Y, Ohmori Y, Takemoto Y, Uekawa K, Mukasa A. Artificial dural regeneration matrix as a substitute for autologous tissue in indirect bypass in Moyamoya disease: investigation of a rat model of chronic cerebral hypoperfusion. Neurosurg Rev. 2025;48(1):48. https://doi.org/10.1007/s10143-025-03185-x. PMid:39810057.

15. Greenberg MS. Greenberg’s Handbook of Neurosurgery. 10th ed. New York: Georg Thieme Verlag; 2023. https://doi.org/10.1055/b000000751.

16. Nguyen VN, Parikh KA, Motiwala M, et al. Surgical techniques and indications for treatment of adult moyamoya disease. Front Surg. 2022;9:966430. https://doi.org/10.3389/fsurg.2022.966430. PMid:36061058.

17. Nguyen VN, Motiwala M, Elarjani T, et al. Direct, indirect, and combined extracranial-to-intracranial bypass for adult moyamoya disease: an updated systematic review and meta-analysis. Stroke. 2022;53(12):3572-82. https://doi.org/10.1161/STROKEAHA.122.03958 . PMid:36134563.

18. Ayyad A, Al-Salihi MM, Ahmed A, Hajali AA, Hammadi F, Horn P. Combined direct and indirect revascularization for adults with moyamoya disease: a single-center retrospective study. Asian J Neurosurg. 2024;19(3):445-51. https://doi.org/10.1055/s-0044-178779 . PMid:39205883.

19. Nielsen TH, Abhinav K, Sussman ES, et al. Direct versus indirect bypass procedure for the treatment of ischemic moyamoya disease: results of an individualized selection strategy. J Neurosurg. 2020;134(5): 1578-89. https://doi.org/10.3171/2020.3.JNS19284 . PMid:32534489.

20. Sadigh Y, de Haan Y, Haasdijk EJ, et al. Indications and outcomes of intracranial bypass: a systematic review and meta-analysis. 

World Neurosurg. 2025;201:124308. https://doi.org/10.1016/j. wneu.2025.12430 . PMid:40701362.

21. Ogawa S, Ogiwara H. Indirect revascularization for pediatric moyamoya disease. J Neurosurg Pediatr. 2024;34(1):111-7. https://doi. org/10.3171/2024.2.PEDS23414. PMid:38608297.

22. Shi Z, Wu L, Li W, et al. The intraoperative hemodynamic and clinical research of three direct bypasses in moyamoya disease a prospective cohort of 98 cases. Sci Rep. 2025;15(1):30463. https://doi.org/10.1038/ s41598-025-15654-w. PMid:40830192.

23. Gao P, Chen D, Yuan S, et al. Follow-up outcomes of different bypass surgical modalities for adults with ischaemic-type moyamoya disease. Br J Neurosurg. 2023;37(2):148-57. https://doi.org/10.1080/02688697 .2021.1981239. PMid:34553657.

24. Lu L, Huang Y, Han Y, et al. Clinical effect of a modified superficial temporal artery-middle cerebral artery bypass surgery in Moyamoya disease treatment. Front Neurol. 2023;14:1273822. https://doi. org/10.3389/fneur.2023.1273822. PMid:37941571.

25. Lim YC, Lee E, Song J. Outcomes of bypass surgery in adult moyamoya disease by onset type. JAMA Netw Open. 2024;7(6):e2415102. https:// doi.org/10.1001/jamanetworkopen.2024.15102. PMid:38842810.

26. Park H, Han M, Jang DK, et al. Association of bypass surgery and mortality in Moyamoya disease. J Am Heart Assoc. 2023;12(22):e030834. https://doi.org/10.1161/JAHA.123.030834. PMid:37947101.

27. Kimata J, Tokairin K, Uchino H, Ito M, Fujimura M. Symptomatic cerebral hyperperfusion after occipital artery-posterior cerebral artery bypass in a patient with moyamoya disease: illustrative case. J Neurosurg Case Lessons. 2025;10(9):CASE25486. https://doi.org/10.3171/ CASE25486. PMid:40889378.

28. Khan ZM, Kiran S, Anwar K, et al. The role of encephaloduroarteriosynangiosis in Moyamoya Disease: a consecutive case series from Pakistan. Cureus. 2025;17(5):e83665. https://doi.org/10.7759/ cureus.83665. PMid:40486313.

29. Talahma I, Abusabha SE, Abu Ali RM, Hrainy MJ, Sarahna OK, Nu’man MF. Moyamoya disease in a 10-year-old male patient in the Middle East with the outcome of the surgery: A case report and literature review. Int J Surg Case Rep. 2025;133(C):111557. https://doi. org/10.1016/j.ijscr.2025.111557. PMid:40554934.

30. Atai NA, Nguyen VN, Kammen A, Sternbach S, Rennert RC, Russin JJ. A novel interhemispheric dural inversion technique for indirect parafalcine cerebral revascularization: case report. Neurosurg Pract. 2024;5(2):e00085. https://doi.org/10.1227/neuprac.0000000000000085. PMid:39958238.



1Centro Universitário Aparício Carvalho – FIMCA, Porto Velho, RO, Brasil.

2Chief of Vascular Neurosurgery Department, Instituto de Neurologia de Curitiba – INC, Curitiba, PR, Brasil.

 

Received Jan 6, 2026 

Corrected Jan 22, 2026 

Accepted Mar 21, 2026


JBNC  Brazilian Journal of Neurosurgery

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