Skip to main content

Advertisement

SpringerLink
Log in

Incidence of late cerebrovascular events after direct bypass among children with moyamoya disease: a descriptive longitudinal study at a single center

  • Clinical Article - Vascular
  • Published:
Acta Neurochirurgica Aims and scope Submit manuscript

Abstract

Background

The potential for late cerebrovascular events following surgical revascularization presents a challenge in the treatment of pediatric moyamoya disease. Limited information is available on the incidence of such events after direct bypass. The objective of this descriptive study was to examine the incidence of late cerebrovascular events after direct bypass for pediatric moyamoya disease.

Methods

The study cohort comprised consecutive patients with moyamoya disease who had undergone direct bypass at less than 18 years of age in the authors’ institute between 1978 and 2003. They were prospectively followed until the end of the study period or, if applicable, the time of death.

Results

Fifty-six of 58 enrolled patients (96.6 %) were followed for a mean period of 18.1 years. Four patients experienced late cerebrovascular events, comprising one stroke and three hemorrhages, an average of 13 years after surgery, one of whom experienced a fatal second hemorrhage. The only late ischemic stroke in the cohort occurred after a severe head injury and emergent craniotomy. The incidence of late cerebrovascular events was 0.41 % per year (95 % confidence interval, 0.15–1.08); 10-year, 20-year, and 30-year cumulative incidences were 1.8 %, 7.3 %, and 13.1 %, respectively.

Conclusions

Despite the efficacy of surgical revascularization, pediatric patients remain at risk of future cerebrovascular events, especially hemorrhage, after reaching adulthood and thus require careful long-term follow-up.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Baba T, Houkin K, Kuroda S (2008) Novel epidemiological features of moyamoya disease. J Neurol Neurosurg Psychiatry 79:900–904

    Article  CAS  PubMed  Google Scholar 

  2. Choi JU, Kim DS, Kim EY, Lee KC (1997) Natural history of moyamoya disease: comparison of activity of daily living in surgery and non surgery groups. Clin Neurol Neurosurg 99(Suppl 2):S11–S18

    Article  PubMed  Google Scholar 

  3. Czabanka M, Pena-Tapia P, Scharf J, Schubert GA, Munch E, Horn P, Schmiedek P, Vajkoczy P (2011) Characterization of direct and indirect cerebral revascularization for the treatment of European patients with moyamoya disease. Cerebrovasc Dis 32:361–369

    Article  CAS  PubMed  Google Scholar 

  4. Darwish B, Besser M (2005) Long term outcome in children with Moyamoya disease: experience with 16 patients. J Clin Neurosci 12:873–877

    Article  CAS  PubMed  Google Scholar 

  5. Fukui M (1997) Guidelines for the diagnosis and treatment of spontaneous occlusion of the circle of Willis (‘moyamoya’ disease). Research Committee on Spontaneous Occlusion of the Circle of Willis (Moyamoya Disease) of the Ministry of Health and Welfare, Japan. Clin Neurol Neurosurg 99(2):S238–S240

    Article  PubMed  Google Scholar 

  6. Fung LW, Thompson D, Ganesan V (2005) Revascularisation surgery for paediatric moyamoya: a review of the literature. Childs Nerv Syst 21:358–364

    Article  PubMed  Google Scholar 

  7. Goda M, Isono M, Ishii K, Kamida T, Abe T, Kobayashi H (2004) Long-term effects of indirect bypass surgery on collateral vessel formation in pediatric moyamoya disease. J Neurosurg 100:156–162

    PubMed  Google Scholar 

  8. Guzman R, Lee M, Achrol A, Bell-Stephens T, Kelly M, Do HM, Marks MP, Steinberg GK (2009) Clinical outcome after 450 revascularization procedures for moyamoya disease. Clinical article. J Neurosurg 111:927–935

    Article  PubMed  Google Scholar 

  9. Hayashi T, Shirane R, Tominaga T (2009) Additional surgery for postoperative ischemic symptoms in patients with moyamoya disease: the effectiveness of occipital artery-posterior cerebral artery bypass with an indirect procedure: technical case report. Neurosurgery 64:E195–E196, discussion E196

    Article  PubMed  Google Scholar 

  10. Iida H, Itoh H, Bloomfield PM, Munaka M, Higano S, Murakami M, Inugami A, Eberl S, Aizawa Y, Kanno I et al (1994) A method to quantitate cerebral blood flow using a rotating gamma camera and iodine-123 iodoamphetamine with one blood sampling. Eur J Nucl Med 21:1072–1084

    Article  CAS  PubMed  Google Scholar 

  11. Ikeda A, Yamamoto I, Sato O, Morota N, Tsuji T, Seguchi T (1991) Revascularization of the calcarine artery in moyamoya disease: OA-cortical PCA anastomosis—case report. Neurol Med Chir (Tokyo) 31:658–661

    Article  CAS  Google Scholar 

  12. Imaizumi T, Hayashi K, Saito K, Osawa M, Fukuyama Y (1998) Long-term outcomes of pediatric moyamoya disease monitored to adulthood. Pediatr Neurol 18:321–325

    Article  CAS  PubMed  Google Scholar 

  13. Ishii R, Takeuchi S, Ibayashi K, Tanaka R (1984) Intelligence in children with moyamoya disease: evaluation after surgical treatments with special reference to changes in cerebral blood flow. Stroke 15:873–877

    Article  CAS  PubMed  Google Scholar 

  14. Karasawa J, Kikuchi H, Furuse S, Sakaki T, Yoshida Y (1977) A surgical treatment of “moyamoya” disease “encephalo-myo synangiosis”. Neurol Med Chir (Tokyo) 17:29–37

    Article  CAS  Google Scholar 

  15. Karasawa J, Kikuchi H, Kuriyama Y, Sawada T, Kuro M, Kobayashi K, Koike T, Mitsugi T (1981) Cerebral hemodynamics in “moyamoya” disease—II. Measurements of cerebral circulation and metabolism by use of the argon desaturation method in pre- and post-neurosurgical procedures. Neurol Med Chir (Tokyo) 21:1161–1168

    Article  CAS  Google Scholar 

  16. Karasawa J, Touho H, Ohnishi H, Miyamoto S, Kikuchi H (1992) Long-term follow-up study after extracranial-intracranial bypass surgery for anterior circulation ischemia in childhood moyamoya disease. J Neurosurg 77:84–89

    Article  CAS  PubMed  Google Scholar 

  17. 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 

  18. Kobayashi E, Saeki N, Oishi H, Hirai S, Yamaura A (2000) Long-term natural history of hemorrhagic moyamoya disease in 42 patients. J Neurosurg 93:976–980

    Article  CAS  PubMed  Google Scholar 

  19. Kruskal WH, Wallis WA (1952) Use of Ranks in One-Criterion Variance Analysis. J Am Stat Assoc 47:583–621

    Article  Google Scholar 

  20. Kuriyama S, Kusaka Y, Fujimura M, Wakai K, Tamakoshi A, Hashimoto S, Tsuji I, Inaba Y, Yoshimoto T (2008) Prevalence and clinicoepidemiological features of moyamoya disease in Japan: findings from a nationwide epidemiological survey. Stroke 39:42–47

    Article  PubMed  Google Scholar 

  21. 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

    Article  PubMed  Google Scholar 

  22. Kuroda S, Houkin K, Kamiyama H, Abe H (2001) Effects of surgical revascularization on peripheral artery aneurysms in moyamoya disease: report of three cases. Neurosurgery 49:463–467, discussion 467–468

    CAS  PubMed  Google Scholar 

  23. Miyamoto S (2004) Study design for a prospective randomized trial of extracranial-intracranial bypass surgery for adults with moyamoya disease and hemorrhagic onset—the Japan Adult Moyamoya Trial Group. Neurol Med Chir (Tokyo) 44:218–219

    Article  Google Scholar 

  24. Miyamoto S, Akiyama Y, Nagata I, Karasawa J, Nozaki K, Hashimoto N, Kikuchi H (1998) Long-term outcome after STA-MCA anastomosis for moyamoya disease. Neurosurg Focus 5:e5

    Article  CAS  PubMed  Google Scholar 

  25. Morioka M, Hamada J, Todaka T, Yano S, Kai Y, Ushio Y (2003) High-risk age for rebleeding in patients with hemorrhagic moyamoya disease: long-term follow-up study. Neurosurgery 52:1049–1054, discussion 1054–1045

    Article  PubMed  Google Scholar 

  26. 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 

  27. Mukawa M, Nariai T, Matsushima Y, Tanaka Y, Inaji M, Maehara T, Aoyagi M, Ohno K (2012) Long-term follow-up of surgically treated juvenile patients with moyamoya disease. J Neurosurg Pediatr 10:451–456

    Article  PubMed  Google Scholar 

  28. Okada Y, Shima T, Nishida M, Yamane K, Yamada T, Yamanaka C (1998) Effectiveness of superficial temporal artery-middle cerebral artery anastomosis in adult moyamoya disease: cerebral hemodynamics and clinical course in ischemic and hemorrhagic varieties. Stroke 29:625–630

    Article  CAS  PubMed  Google Scholar 

  29. Phi JH, Wang KC, Cho BK, Lee MS, Lee JH, Yu KS, Hahm BJ, Kim SK (2011) Long-term social outcome in children with moyamoya disease who have reached adulthood. J Neurosurg Pediatr 8:303–309

    Article  PubMed  Google Scholar 

  30. 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 Intractable Diseases (2012) Guidelines for diagnosis and treatment of moyamoya disease (Spontaneous Occlusion of the Circle of Willis). Neurol Med Chir (Tokyo) 52:245–266

    Article  Google Scholar 

  31. 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 

  32. Starke RM, Komotar RJ, Hickman ZL, Paz YE, Pugliese AG, Otten ML, Garrett MC, Elkind MS, Marshall RS, Festa JR, Meyers PM, Connolly ES Jr (2009) Clinical features, surgical treatment, and long-term outcome in adult patients with moyamoya disease. Clinical article. J Neurosurg 111:936–942

    Article  PubMed Central  PubMed  Google Scholar 

  33. Suzuki K, Sarti C, Tuomilehto J, Kutsuzowa T, Narva EV, Sivenius J, Salmi K, Kaarsalo E, Torppa J, Kuulasmaa K (1994) Stroke incidence and case fatality in Finland and in Akita, Japan: a comparative study. Neuroepidemiology 13:236–244

    Article  CAS  PubMed  Google Scholar 

  34. Takikawa S, Kamiyama H, Abe H, Mitsumori K, Tsuru M (1990) Hemodynamic evaluation of vascular reconstructive surgery for childhood moyamoya disease using single photon emission computed tomography. Neurol Med Chir (Tokyo) 30:389–395

    Article  CAS  Google Scholar 

  35. Uchino H, Kuroda S, Hirata K, Shiga T, Houkin K, Tamaki N (2012) Predictors and clinical features of postoperative hyperperfusion after surgical revascularization for moyamoya disease: a serial single photon emission CT/positron emission tomography study. Stroke 43:2610–2616

    Article  PubMed  Google Scholar 

  36. Ulrich PT, Januschek E (2011) Revascularisation surgery and long-term follow-up in juvenile Moyamoya syndrome: a retrospective analysis. Acta Neurochir Suppl 112:39–43

    Article  PubMed  Google Scholar 

  37. Wakai K, Tamakoshi A, Ikezaki K, Fukui M, Kawamura T, Aoki R, Kojima M, Lin Y, Ohno Y (1997) Epidemiological features of moyamoya disease in Japan: findings from a nationwide survey. Clin Neurol Neurosurg 99(Suppl 2):S1–S5

    Article  PubMed  Google Scholar 

  38. Yoshida Y, Yoshimoto T, Shirane R, Sakurai Y (1999) 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 30:2272–2276

    Google Scholar 

Download references

Acknowledgments

We are grateful to Dr. Takeo Nakayama, Professor at the Department of Health Informatics, Kyoto University School of Public Health, for providing statistical advice. We also thank Yuko Tanaka for her efforts at collecting patient records.

Conflicts of interest

None.

Author information

Authors and Affiliations

  1. Department of Neurosurgery, Kyoto University Graduate School of Medicine, 54 Kawahara-cho, Shogoin, Sakyo-ku, Kyoto, 606-8507, Japan

    Takeshi Funaki, Jun C. Takahashi, Yasushi Takagi, Kazumichi Yoshida, Takayuki Kikuchi, Noritaka Sano & Susumu Miyamoto

  2. Department of Neurosurgery, Nagoya University Graduate School of Medicine, Nagoya, Japan

    Yoshio Araki

  3. Department of Neurosurgery, National Cerebral and Cardiovascular Center, Osaka, Japan

    Hiroharu Kataoka & Koji Iihara

Authors
  1. Takeshi Funaki
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jun C. Takahashi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yasushi Takagi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kazumichi Yoshida
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yoshio Araki
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Takayuki Kikuchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Hiroharu Kataoka
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Koji Iihara
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Noritaka Sano
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Susumu Miyamoto
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Takeshi Funaki.

Additional information

Comment

The natural history of patients with moyamoya disease after revascularisation is still not well known. This manuscript deals with 56 children with a mean follow-up interval of 18.1 years; one ischemic stroke and three hemorrhages were observed. One of three hemorrhages was due to rupture of a small aneurysm at the posterior choroidal artery. These four events occurred after 13 years on average after revascuralisation surgery. The reviewer read this report with great interest as he had experience recently of an adult female patient (50 years old) who had suffered a huge hemorrhage in the right temporal lobe and right ventricle around 24 months after revascularisation surgery (bilateral STA-MCA bypass plus one STA-ACA bypass in one stage and patency of all the bypasses were confirmed with DSA). Whether revascularisation surgery prevents future hemorrhagic event or not—and, if yes, to what extent—has to be resolved. Interestingly, the hemorrhages reported in this paper and also in our patient were only in adults, occurring 18 years later and 1 year later respectively.

The mechanism of failure of prevention of hemorrhage that occurred so long after revascularisation surgery in the former case and so shortly after in the latter has also to be solved. Anyway, occurrence of hemorrhage seems to be associated with adulthood irrespective of revascularisation surgery.

By the way, fatal rerupture of the small intraventricular aneurysm of the posterior choroidal artery could have been prevented by its surgical removal, although some papers propose its shrinkage or disappearance by revascularisation.

Reference

Sadatoh A. Yonekawa Y, Morooka Y, Imakita T: A case of moyamoya disease with repeated intraventricular hemorrhage due to a ruptured pseudoaneurysm. No Shinkeigeka (1989)17:755-758 (Japanese, English abstract)

Yasuhiro Yonekawa

Zurich, Switzerland

Rights and permissions

Reprints and permissions

About this article

Cite this article

Funaki, T., Takahashi, J.C., Takagi, Y. et al. Incidence of late cerebrovascular events after direct bypass among children with moyamoya disease: a descriptive longitudinal study at a single center. Acta Neurochir 156, 551–559 (2014). https://doi.org/10.1007/s00701-013-1975-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00701-013-1975-7

Keywords

Search

Navigation