Abstract
Objective
To investigate the feasibility and clinical effectiveness of performing multiple burr hole surgery in pediatric moyamoya patients as a response to failed modified encephaloduroarteriosynangiosis (mEDAS).
Methods
From January 2014 to May 2018, multiple burr hole surgery (MBS) was conducted on 16 hemispheres in 12 patients as a secondary treatment following mEDAS. The male-to-female ratio was 1:2 and the average age at the time of mEDAS was 6 years old. The average patient age was 9 ± 3 years olds (range 7–17) at the time of MBS which occurred an average of 46 months after mEDAS. An average of 10 ± 1 holes (range 8–13) were made. Time-to-peak (TTP) magnetic resonance images (MRI) were taken along 20 axial cuts. Of these cuts, two consecutive cuts on the lateral ventricle were selected to calculate the average value of the region of interest (ROI). The value of the cerebellum was subtracted from the average value of two consecutive cuts. The ROI value was analyzed using a paired t test by SPSS 20 (SPSS Inc., Chicago, IL, USA).
Results
All 16 cases presented improvement of clinical symptoms as determined by ROI analysis of the TTP MRI images. The average ROI value was 5.03 ± 6.36 before MBS and − 15.54 ± 9.42 after MBS. The average change in the ROI value was − 20.58 ± 12.59. The ROI value decreased in all cases after MBS. Magnetic resonance angiography (MRA) also showed a positive effect on vascularization.
Conclusion
In pediatric moyamoya patients, MBS is recommended as secondary option as a response to failed mEDAS. Its clinical effectiveness was shown by analyzing TTP images and assisted by MRA and digital subtraction angiography.
This is a preview of subscription content, access via your institution.




References
Calamante F, Thomas DL, Pell GS, Wiersma J, Turner R (1999) Measuring cerebral blood flow using magnetic resonance imaging techniques. J Cereb Blood Flow Metab 19:701–735
Choi HS, Kim DS, Shim KW, Kim J, Kim ES, Lee SK (2011) Focal time-to-peak changes on perfusion MRI in children with Moyamoya disease: correlation with conventional angiography. Acta Radiol 52:675–679
Czabanka M, Pena-Tapia P, Scharf J, Schubert GA, Munch E, Horn P et al (2011) Characterization of direct and indirect cerebral revascularization for the treatment of European patients with moyamoya disease. Cerebrovasc Dis 32:361–369
Endo M, Kawano N, Miyaska Y, Yada K (1989) Cranial burr hole for revascularization in moyamoya disease. J Neurosurg 71:180–185
Fung LW, Thompson D, Ganesan V (2005) Revascularisation surgery for paediatric moyamoya: a review of the literature. Childs Nerv Syst 21:358–364
Ganesan V (2010) Moyamoya: to cut or not to cut is not the only question. A paediatric neurologist’s perspective. Dev Med Child Neurol 52:10–13
Hirai S, Inaji M, Tanaka Y, Hara S, Nariai T, Maehara T (2017) Correlation between clinical presentations and hemodynamic parameters measured by dynamic susceptibility contrast magnetic resonance imaging in adult patients with moyamoya disease. J Stroke Cerebrovasc Dis 26:2814–2820
Kim CY, Wang KC, Kim SK, Chung YN, Kim HS, Cho BK (2003) Encephaloduroarteriosynangiosis with bifrontal encephalogaleo(periosteal)synangiosis in the pediatric moyamoya disease: the surgical technique and its outcomes. Childs Nerv Syst 19:316–324
Lin YH, Kuo MF, Lu CJ, Lee CW, Yang SH, Huang YC et al (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
Liu JJ, Steinberg GK (2017) Direct versus indirect bypass for moyamoya disease. Neurosurg Clin N Am 28:361–374
Ma Y, Zhao M, Zhang Q, Liu X, Zhang D, Wang S, Zhang Y, Li M, Zhao J (2018) Risk factors for epilepsy recurrence after revascularization in pediatric patients with moyamoya disease. J Stroke Cerebrovasc Dis 27:740–746
Matsushima Y, Inaba Y (1984) Moyamoya disease in children and its surgical treatment. Introduction of a new surgical procedure and its follow-up angiograms. Childs Brain 11:155–170
McLaughlin N, Martin NA (2014) Effectiveness of burr holes for indirect revascularization in patients with moyamoya disease-a review of the literature. World Neurosurg 81:91–98
Mizoi K, Kayama T, Yoshimoto T, Nagamine Y (1996) Indirect revascularization for moyamoya disease: is there a beneficial effect for adult patients? Surg Neurol 45:541–548; discussion 548-549
Ogiwara H, Morota N (2012) Bifrontal encephalogaleosynangiosis for children with moyamoya disease. J Neurosurg Pediatr 10:246–251
Park SE, Kim JS, Park EK, Shim KW, Kim DS (2018) Direct versus indirect revascularization in the treatment of moyamoya disease. J Neurosurg 129:480–489
Quon JL, Kim LH, Lober RM, Maleki M, Steinberg GK, Yeom KW (2019) Arterial spin-labeling cerebral perfusion changes after revascularization surgery in pediatric moyamoya disease and syndrome. J Neurosurg Pediatr:1–7
Suzuki J, Takaku A (1969) Cerebrovascular “moyamoya” disease. Disease showing abnormal net-like vessels in base of brain. Arch Neurol 20:288–299
Suzuki J, Kodama N (1983) Moyamoya disease--a review. Stroke 14:104–109
Tanaka Y, Nariai T, Nagaoka T, Akimoto H, Ishiwata K, Ishii K, Matsushima Y, Ohno K (2006) Quantitative evaluation of cerebral hemodynamics in patients with moyamoya disease by dynamic susceptibility contrast magnetic resonance imaging--comparison with positron emission tomography. J Cereb Blood Flow Metab 26:291–300
Thines L, Petyt G, Aguettaz P, Bodenant M, Himpens FX, Lenci H, Henon H, Gauthier C, Hossein-Foucher C, Cordonnier C, Lejeune JP (2015) Surgical management of Moyamoya disease and syndrome: current concepts and personal experience. Rev Neurol (Paris) 171:31–44
Togao O, Mihara F, Yoshiura T, Tanaka A, Noguchi T, Kuwabara Y, Kaneko K, Matsushima T, Honda H (2006) Cerebral hemodynamics in Moyamoya disease: correlation between perfusion-weighted MR imaging and cerebral angiography. AJNR Am J Neuroradiol 27:391–397
Wang KC, Phi JH, Lee JY, Kim SK, Cho BK (2012) Indirect revascularization surgery for moyamoya disease in children and its special considerations. Korean J Pediatr 55:408–413
Yamada I, Himeno Y, Nagaoka T, Akimoto H, Matsushima Y, Kuroiwa T, Shibuya H (1999) Moyamoya disease: evaluation with diffusion-weighted and perfusion echo-planar MR imaging. Radiology 212:340–347
Yun TJ, Cheon JE, Na DG, Kim WS, Kim IO, Chang KH, Yeon KM, Song IC, Wang KC (2009) Childhood moyamoya disease: quantitative evaluation of perfusion MR imaging--correlation with clinical outcome after revascularization surgery. Radiology 251:216–223
Zhang H, Zheng L, Feng L (2019) Epidemiology, diagnosis and treatment of moyamoya disease. Exp Ther Med 17:1977–1984
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
On behalf of all authors, the corresponding author states that there were no conflicts of interest in this study.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Hwang, J.K., Park, E.K., Kim, J. et al. The feasibility of performing multiple burr hole surgery in pediatric moyamoya patients as a response to failed mEDAS. Childs Nerv Syst 37, 2233–2238 (2021). https://doi.org/10.1007/s00381-021-05093-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00381-021-05093-z
Keywords
- Moyamoya disease
- Revascularization
- Time to peak map