Neuropediatrics 2022; 53(03): 188-194
DOI: 10.1055/a-1753-2634
Original Article

Vascular Architecture Characters and Changes of Pediatric Moyamoya Disease after Combined Bypass Surgery

Yan Ma
1   Department of Neurosurgery, Capital Medical University, Xuanwu Hospital, Beijing, China
,
Xia Lu
1   Department of Neurosurgery, Capital Medical University, Xuanwu Hospital, Beijing, China
,
Gao Zeng
1   Department of Neurosurgery, Capital Medical University, Xuanwu Hospital, Beijing, China
,
Bin Yang
1   Department of Neurosurgery, Capital Medical University, Xuanwu Hospital, Beijing, China
,
Liqun Jiao
1   Department of Neurosurgery, Capital Medical University, Xuanwu Hospital, Beijing, China
,
Feng Ling
1   Department of Neurosurgery, Capital Medical University, Xuanwu Hospital, Beijing, China
› Author Affiliations
Funding This work was supported by the National Key Research and Development Project (2016YFC1301703) and the Beijing Scientific and Technologic Project (D161100003816002).

Abstract

Objective We aimed to analyze the angioarchitecture characters and changes after combined bypass surgery (CBS) in pediatric moyamoya disease (MMD).

Methods We retrospectively analyzed our database of consecutive patients with moyamoya angiopathy who received treatment. Only pediatric MMD cases aged between 3 and 19 years with pre- and post-operative imaging examinations including digital subtraction angiography and magnetic resonance imaging were enrolled in this study. The main trunk vessels' stenosis and the collaterals from the superficial-meningeal system and deep parenchymal system were evaluated before and after CBS.

Results During short-term follow-up period after the unilateral CBS, the stenosis of main trunk vessels both in operative (5.7 ± 2.1 vs. 6.8 ± 1.8; p < 0.001) and non-operative hemisphere (non-operative side 4.3 ± 1.9 vs. 5.7 ± 2.1; p < 0.001) progressed obviously. During the median follow-up period of 28.5 months after CBS, the decrease of posterior cerebral artery middle cerebral artery (PCA-MCA) anastomoses was much more significant (26 vs. 6, p < 0.001) than that of the PCA anterior cerebral artery anastomoses (18 vs. 19, p = 0.807). Meanwhile, the subependymal anastomotic network could be relieved obviously (27 vs. 2, p < 0.001), while the inner thalamic and striatal anastomotic network showed no significant change (31 vs. 25, p = 0.109).

Conclusions The successful CBS could decrease the collaterals from the PCA-MCA leptomeningeal system and the subependymal compensations in deep parenchyma significantly, while the main trunk stenosis would aggravate rapidly both in operative and non-operative hemisphere in short-term follow-up after unilateral CBS. Therefore, strict and regular follow-ups for the changes of vascular architecture and prompt surgical intervention for the contralateral side might be of benefit to pediatric MMD.

Author Contributions

L.J. and F.L. contributed to conception and design. X.L. and B.Y. contributed to the acquisition of data. Y.M., G.Z., and X.L. contributed to the analysis and interpretation of data. Y.M. and X.L. contributed to the article drafting. All authors critically revised the article and reviewed the submitted version of manuscript. L.J. approved the final version of the manuscript on behalf of all authors. X.L. and Y.M. contributed to statistical analysis. L.J. and F.L. contributed to study supervision.


Supplementary Material



Publication History

Received: 21 June 2021

Accepted: 24 January 2022

Accepted Manuscript online:
27 January 2022

Article published online:
16 March 2022

© 2022. Thieme. All rights reserved.

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

 
  • References

  • 1 Lee S, Rivkin MJ, Kirton A, deVeber G, Elbers J. International Pediatric Stroke Study. Moyamoya disease in children: results from the international pediatric stroke study. J Child Neurol 2017; 32 (11) 924-929
  • 2 Lasjaunias P, ter Brugge KG, Berenstein A. Surgical Neuroangiography. Vol II. Berlin Heidelberg, German: Springer; 2006. 885.
  • 3 Irikura K, Miyasaka Y, Kurata A. et al. A source of haemorrhage in adult patients with moyamoya disease: the significance of tributaries from the choroidal artery. Acta Neurochir (Wien) 1996; 138 (11) 1282-1286
  • 4 Morioka M, Hamada J, Kawano T. et al. Angiographic dilatation and branch extension of the anterior choroidal and posterior communicating arteries are predictors of hemorrhage in adult moyamoya patients. Stroke 2003; 34 (01) 90-95
  • 5 Veeravagu A, Guzman R, Patil CG, Hou LC, Lee M, Steinberg GK. Moyamoya disease in pediatric patients: outcomes of neurosurgical interventions. Neurosurg Focus 2008; 24 (02) E16
  • 6 Park SE, Kim JS, Park EK, Shim KW, Kim DS. Direct versus indirect revascularization in the treatment of moyamoya disease. J Neurosurg 2018; 129 (02) 480-489
  • 7 Kuroda S, Houkin K, Kamiyama H, Abe H. Effects of surgical revascularization on peripheral artery aneurysms in moyamoya disease: report of three cases. Neurosurgery 2001; 49 (02) 463-467 , discussion 467–468
  • 8 Yoshida Y, Yoshimoto T, Shirane R, Sakurai Y. Clinical course, surgical management, and long-term outcome of moyamoya patients with rebleeding after an episode of intracerebral hemorrhage: an extensive follow-up study. Stroke 1999; 30 (11) 2272-2276
  • 9 Kim H, Jang DK, Han YM. et al. Direct bypass versus indirect bypass in adult moyamoya angiopathy with symptoms or hemodynamic instability: a meta-analysis of comparative studies. World Neurosurg 2016; 94: 273-284
  • 10 Baltsavias G, Khan N, Valavanis A. The collateral circulation in pediatric moyamoya disease. Childs Nerv Syst 2015; 31 (03) 389-398
  • 11 Kim WH, Kim SD, Nam MH. et al. Posterior circulation involvement and collateral flow pattern in moyamoya disease with the RNF213 polymorphism. Childs Nerv Syst 2019; 35 (02) 309-314
  • 12 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). Neurol Med Chir (Tokyo) 2012; 52 (05) 245-266
  • 13 Houkin K, Nakayama N, Kuroda S, Nonaka T, Shonai T, Yoshimoto T. Novel magnetic resonance angiography stage grading for moyamoya disease. Cerebrovasc Dis 2005; 20 (05) 347-354
  • 14 Matsushima T, Fukui M, Kitamura K, Hasuo K, Kuwabara Y, Kurokawa T. Encephalo-duro-arterio-synangiosis in children with moyamoya disease. Acta Neurochir (Wien) 1990; 104 (3-4): 96-102
  • 15 Ryu J, Hamano E, Nishimura M, Satow T, Takahashi JC. Difference in periventricular anastomosis in child and adult moyamoya disease: a vascular morphology study. Acta Neurochir (Wien) 2020; 162 (06) 1333-1339
  • 16 Takagi Y, Kikuta K, Nozaki K. et al. Expression of hypoxia-inducing factor-1 alpha and endoglin in intimal hyperplasia of the middle cerebral artery of patients with moyamoya disease. Neurosurgery 2007; 60 (02) 338-345 , discussion 345
  • 17 Arikan F, Vilalta J, Torne R, Noguer M, Lorenzo-Bosquet C, Sahuquillo J. Rapid resolution of brain ischemic hypoxia after cerebral revascularization in moyamoya disease. Neurosurgery 2015; 76 (03) 302-312 , discussion 312
  • 18 Kim SJ, Son TO, Kim KH. et al. Neovascularization precedes occlusion in moyamoya disease: angiographic findings in 172 pediatric patients. Eur Neurol 2014; 72 (5-6): 299-305
  • 19 Kang HS, Kim JH, Phi JH. et al. Plasma matrix metalloproteinases, cytokines and angiogenic factors in moyamoya disease. J Neurol Neurosurg Psychiatry 2010; 81 (06) 673-678
  • 20 Rafat N, Beck GCh, Peña-Tapia PG, Schmiedek P, Vajkoczy P. Increased levels of circulating endothelial progenitor cells in patients with moyamoya disease. Stroke 2009; 40 (02) 432-438
  • 21 Takahashi JC, Funaki T, Houkin K. et al; JAM Trial Investigators. Significance of the hemorrhagic site for recurrent bleeding: prespecified analysis in the Japan adult moyamoya trial. Stroke 2016; 47 (01) 37-43
  • 22 Yu L-B, Ma Y-G, Zhang D. Cerebral revascularization accelerates the angiographic staging progression of the operated hemisphere in a pediatric patient with moyamoya disease. J Craniofac Surg 2019; 30 (04) 1180-1183
  • 23 Ma Y, Li M, Jiao LQ, Zhang HQ, Ling F. Contralateral cerebral hemodynamic changes after unilateral direct revascularization in patients with moyamoya disease. Neurosurg Rev 2011; 34 (03) 347-353 , discussion 353–354