Skip to main content

Advertisement

Log in

Posterior cerebral territory ischemia in pediatric moyamoya: Surgical techniques and long-term clinical and radiographic outcomes

  • Research
  • Published:
Child's Nervous System Aims and scope Submit manuscript

Abstract

Purpose

To describe a surgical technique for posterior cerebral revascularization in pediatric patients with moyamoya arteriopathy. Here, we describe the clinical characteristics, surgical indications, operative techniques, and clinical and radiographic outcomes in a series of pediatric patients with moyamoya disease affecting the posterior cerebral artery (PCA) territory.

Methods

A retrospective single-center series of all pediatric patients with moyamoya disease who presented to our institute between July 2009 through August 2019 were reviewed. The clinical characteristics, surgical indications, operative techniques, and long-term clinical and radiographic outcomes of pediatric moyamoya patients with PCA territory ischemia were collected and analyzed.

Results

A total of 10 PCA revascularization procedures were performed in 9 patients, 5 female, ages 1 to 11.1 years (average 5.2 years). Complications included 1 stroke, with no infections, hemorrhages, seizures, or deaths. One patient had less than 1 year of radiographic and clinical follow-up. In 8 of 9 patients with at least 1 year of radiographic follow-up, there was engraftment of surgical vessels present in all cases. No new strokes were identified on long-term follow-up despite the radiographic progression of the disease. In the 8 cases available for analysis, the average follow-up was 50.8 months with a range of 12 to 117 months.

Conclusions

PCA territory ischemia in patients with progressive moyamoya disease can be surgically treated with indirect revascularization. Here, we describe our experience with PCA revascularization procedures for moyamoya disease, including pial pericranial dural (PiPeD) revascularization and pial synangiosis utilizing the occipital artery. These surgical options may be useful for decreasing the risk of stroke in pediatric moyamoya patients with severe posterior circulation disease.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Takeuchi K (1957) Hypoplasia of bilateral internal carotid arteries. No To Shinkei 9:37–43

    Google Scholar 

  2. Suzuki J, Takaku A (1969) Cerebrovascular moyamoya disease: disease showing abnormal net-like vessels in base of brain. Arch Neurol 20:288–299

    Article  CAS  PubMed  Google Scholar 

  3. Scott RM, Smith ER (2009) Moyamoya disease and moyamoya syndrome. N Engl J Med 360:1226–1237

    Article  CAS  PubMed  Google Scholar 

  4. Wanebo JE, Khan N, Zabramski JM (2013) Moyamoya disease: diagnosis and treatment. Thieme

    Google Scholar 

  5. Miyamoto S, Kikuchi H, Karasawa J, Nagata I, Ikota T, Takeuchi S (1984) Study of the posterior circulation in moyamoya disease. Clinical and neuroradiological evaluation J Neurosurg 61:1032–1037

    CAS  PubMed  Google Scholar 

  6. Miyamoto S, Kikuchi H, Karasawa J, Nagata I, Ihara I, Yamagata S (1986) Study of the posterior circulation in moyamoya disease. Part 2: Visual disturbances and surgical treatment. J Neurosurg 65:454–460

    Article  CAS  PubMed  Google Scholar 

  7. Kim WH, Kim SD, Nam MH, Jung JM, Jin SW, Ha SK, Lim DJ, Lee HB (2019) Posterior circulation involvement and collateral flow pattern in moyamoya disease with the RNF213 polymorphism. Childs Nerv Syst 35:309–314

    Article  PubMed  Google Scholar 

  8. Karasawa J, Kikuchi H, Kawamura J, Sakai T (1980) Intracranial transplantation of the omentum for cerebrovascular moyamoya disease: a two-year follow-up study. Surg Neurol 14:444–449

    CAS  PubMed  Google Scholar 

  9. Karasawa J, Touho H, Ohnishi H, Miyamoto S, Kikuchi H (1993) Cerebral revascularization using omental transplantation for childhood moyamoya disease. J Neurosurg 79:192–196

    Article  CAS  PubMed  Google Scholar 

  10. Havlik RJ, Fried I, Chyatte D, Modlin IM (1992) Encephalo-omental synangiosis in the management of moyamoya disease. Surgery 111:156–162

    CAS  PubMed  Google Scholar 

  11. Kinugasa K, Mandai S, Tokunaga K, Kamata I, Sugiu K, Handa A, Ohmoto T (1994) Ribbon enchephalo-duro-arterio-myo-synangiosis for moyamoya disease. Surg Neurol 41:455–461

    Article  CAS  PubMed  Google Scholar 

  12. Kim SK, Wang KC, Kim IO, Lee DS, Cho BK (2008) Combined encephaloduroarteriosynangiosis and bifrontal encephalogaleo (periosteal) synangiosis in pediatric moyamoya disease. Neurosurgery 62:1456–1464

    Article  PubMed  Google Scholar 

  13. Kuroda S, Houkin K, Ishikawa T, Nakayama N, Iwasaki Y (2010) Novel bypass surgery for moyamoya disease using pericranial flap: its impacts on cerebral hemodynamics and long-term outcome. Neurosurgery 66:1093–1101; discussion 1101

  14. Kimiwada T, Hayashi T, Shirane R, Tominaga T (2018) Posterior cerebral artery stenosis and posterior circulation revascularization surgery in pediatric patients with moyamoya disease. J Neurosurg Pediatr 21:632–638

    Article  PubMed  Google Scholar 

  15. Pandey P, Steinberg GK (2011) Outcome of repeat revascularization surgery for moyamoya disease after an unsuccessful indirect revascularization. Clinical article J Neurosurg 115:328–336

    Article  PubMed  Google Scholar 

  16. Endo M, Kawano N, Miyaska Y, Yada K (1989) Cranial burr hole for revascularization in moyamoya disease. J Neurosurg 71:180–185

    Article  CAS  PubMed  Google Scholar 

  17. McLaughlin N, Cutler A, Martin NA (2013) Technical nuances of temporal muscle dissection and reconstruction for the pterional keyhole craniotomy. J Neurosurg 118:309–314

    Article  PubMed  Google Scholar 

  18. Kapu R, Symss NP, Cugati G, Pande A, Vasudevan CM, Ramamurthi R (2010) Multiple burr hole surgery as a treatment modality for pediatric moyamoya disease. J Pediatr Neurosci 5:115–120

    Article  PubMed  PubMed Central  Google Scholar 

  19. Oliveira RS, Amato MC, Simão GN, Abud DG, Avidago EB, Specian CM, Machado HR (2009) Effect of multiple cranial burr hole surgery on prevention of recurrent ischemic attacks in children with moyamoya disease. Neuropediatrics 40:260–264

    Article  PubMed  Google Scholar 

  20. Montaser AS, Lalgudi Srinivasan H, Staffa SJ, Zurakowski D, Slingerland AL, Orbach DB, Hausman-Kedem M, Roth J, Smith ER (2022) Ivy sign: a diagnostic and prognostic biomarker for pediatric moyamoya. J Neurosurg Pediatr 29:458–466

    Article  PubMed  Google Scholar 

  21. Adelson PD, Scott RM (1995) Pial synangiosis for moyamoya syndrome in children. Pediatr Neurosurg 23:26–33

    Article  CAS  PubMed  Google Scholar 

  22. Kim SK, Cho BK, Phi JH, Lee JY, Chae JH, Kim KJ, Hwang YS, Kim IO, Lee DS, Lee J, Wang KC (2010) Pediatric moyamoya disease: an analysis of 410 consecutive cases. Ann Neurol 68:92–101

    Article  PubMed  Google Scholar 

  23. Mugikura S, Takahashi S, Higano S, Shirane R, Sakurai Y, Yamada S (2002) Predominant involvement of ipsilateral anterior and posterior circulations in moyamoya disease. Stroke 33:1497–1500

    Article  PubMed  Google Scholar 

  24. Yamada I, Himeno Y, Suzuki S, Matsushima Y (1995) Posterior circulation in moyamoya disease: angiographic study. Radiology 197:239–246

    Article  CAS  PubMed  Google Scholar 

  25. Lee JY, Choi YH, Cheon JE, Paeng JC, Ryu HW, Kim KJ, Phi JH, Wang KC, Cho BK, Chae JH, Kim SK (2014) Delayed posterior circulation insufficiency in pediatric moyamoya disease. J Neurol 261:2305–2313

    Article  PubMed  Google Scholar 

  26. Ferriero DM, Fullerton HJ, Bernard TJ, Billinghurst L, Daniels SR, DeBaun MR, deVeber G, Ichord RN, Jordan LC, Massicotte P, Meldau J, Roach ES, Smith ER (2019) Management of stroke in neonates and children: a scientific statement from the American Heart Association/American Stroke Association. Stroke 50:e51–e96

    Article  PubMed  Google Scholar 

  27. Riordan CP, Storey A, Cote DJ, Smith ER, Scott RM (2019) Results of more than 20 years of follow-up in pediatric patients with moyamoya disease undergoing pial synangiosis. J Neurosurg Pediatr 1–7

  28. Storey A, Michael Scott R, Robertson R, Smith E (2017) Preoperative transdural collateral vessels in moyamoya as radiographic biomarkers of disease. J Neurosurg Pediatr 19:289–295

    Article  PubMed  Google Scholar 

  29. 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

    Article  PubMed  Google Scholar 

  30. 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

    CAS  PubMed  Google Scholar 

  31. Chang SD, Steinberg GK (2000) Surgical management of moyamoya disease. Contemporary Neurosurgery 22:1–8

    Article  Google Scholar 

  32. Coert BA, Chang SD, Marks MP, Steinberg GK (2005) Revascularization of the posterior circulation. Skull Base 15:43–62

    Article  PubMed  PubMed Central  Google Scholar 

  33. Lee J, Steinberg GK (2010) Omental to cerebral transposition for the treatment of cerebral ischemia. The Omentum: Basic Research and Clinical Application Woodbury, CT: Ciné-Med Inc 137–149

  34. Montaser A, Driscoll J, Smith H, Karsten MB, Day E, Mounlavongsy T, Orbach DB, Smith ER (2021) Long-term clinical and radiographic outcomes after pial pericranial dural revascularization: a hybrid surgical technique for treatment of anterior cerebral territory ischemia in pediatric moyamoya disease. J Neurosurg Pediatr 28:351–359

    Article  PubMed  Google Scholar 

  35. Scott RM, Smith JL, Robertson RL, Madsen JR, Soriano SG, Rockoff MA (2004) Long-term outcome in children with moyamoya syndrome after cranial revascularization by pial synangiosis. J Neurosurg 100:142–149

    PubMed  Google Scholar 

  36. Ha EJ, Kim KH, Wang KC, Phi JH, Lee JY, Choi JW, Cho BK, Yang J, Byun YH, Kim SK (2019) Long-term outcomes of indirect bypass for 629 children with moyamoya disease: longitudinal and cross-sectional analysis. Stroke 50:3177–3183

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Contributions

ERS, AM, DBO, and APS contributed to conception and design of the study. AM was responsible for data collection, analysis, and initial draft of the manuscript. ADK was responsible for data collection, preparing figures, analysis and additional manuscript drafts and revisions. JD, ED, and MK were responsible for chart abstraction, data collection, and initial analysis. All authors contributed to cohort ascertainment and data collection. All authors contributed to writing and reviewing the manuscript.

Corresponding author

Correspondence to Edward R. Smith.

Ethics declarations

Conflict of interest

The authors have no relevant financial or non-financial interests to disclose.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Montaser, A., Kappel, A.D., Driscoll, J. et al. Posterior cerebral territory ischemia in pediatric moyamoya: Surgical techniques and long-term clinical and radiographic outcomes. Childs Nerv Syst 40, 791–800 (2024). https://doi.org/10.1007/s00381-023-06219-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00381-023-06219-1

Keywords

Navigation