Skip to main content

Advertisement

SpringerLink
Log in

How to reduce the complication rate of multiple burr holes surgery in moyamoya angiopathy

  • Technical Note
  • Published:
Acta Neurochirurgica Aims and scope Submit manuscript

Abstract

Purpose

This study is aimed at analyzing clinical outcome, absence of stroke recurrence, revascularization, and complications and long-term follow-up in the surgical treatment of moyamoya angiopathy (MMA) using the multiple burr holes (MBH) technique with dura opening and arachnoid preservation as a single procedure. To the best of our knowledge, this is the first to describe an MBH technique with arachnoid preservation.

Method

We retrospectively reviewed all patients operated from June 2001 to March 2021, for a symptomatic and progressive MMA operated with opening of the dura but arachnoid preservation. Clinical examinations were obtained in all patients, and radiological monitoring was performed by cerebral 3D-magnetic resonance angiography (MRA) with perfusion or single-photon emission computed tomography (SPECT) with acetazolamide.

Results

In total, 21 consecutive patients (6 children and 15 adults) were included with a mean age of 7.4 years in the pediatric group and 36.9 years in the adult group. Initial presentation was permanent ischemic stroke in 15 cases, transient ischemic attack (TIA) in 5 cases, and cerebral hemorrhage in one case. The MBH with dura opening and arachnoid preservation was performed bilaterally in 9 cases (43%) and unilaterally in 12 cases (57%). One patient died due to intraoperative bilateral ischemic stroke. Of the 20 other patients, 30% demonstrated clinical stability and 70% showed partial or complete recovery. Although one patient experienced a perioperative stroke, we did not observe any pseudomeningocele or postoperative ischemic stroke (IS) recurrence in all surviving cases during the average follow-up period of 55.5 months (range: 1–195). These outcomes emphasize the importance of preoperative monitoring to ensure the effectiveness and safety of the intervention. Postoperative angiography studies showed revascularization in 96.3% of treated hemispheres (100% in the adult group vs 80% in the pediatric group).

Conclusions

Our results on this small cohort suggest that the MBH technique with opening of the dura and arachnoids preservation can prevent recurrent strokes and reduce the risk of pseudomeningocele.

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

Abbreviations

ASL:

Arterial spin labeling

ACA:

Anterior carotid artery

BH:

Burr holes

CTA:

Computed tomography angiography

DSA:

Digital subtraction angiography

F:

Female

FLAIR:

Fluid-Attenuated Inversion Recovery

Ha:

Headache

IS:

Ischemic stroke

L:

Left

M:

Male

MBH:

Multiple burr holes

MCA:

Middle cerebral artery

MMA:

Moyamoya angiopathy

MRA:

Cerebral 3D-magnetic resonance angiography

MRI:

Magnetic resonance imaging

mRS:

Modified Rankin scale

NA:

Not available

N:

Number patient

NIHSS:

National Institutes of Health Stroke Scale

PCO2 :

Carbon dioxide pressure

Pt:

Patients

R:

Right

SPECT:

Single photon emission computed tomography (rest + Diamox)

TIA:

Transient ischemic attack

TH:

Treated hemisphere

References

  1. Blauwblomme T, Lemaitre H, Naggara O et al (2016) Cerebral blood flow improvement after indirect revascularization for pediatric moyamoya disease: a statistical analysis of arterial spin-labeling MRI. AJNR Am J Neuroradiol 37(4):706–712. https://doi.org/10.3174/ajnr.A4592

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Blauwblomme T, Mathon B, Naggara O, Kossorotoff M, Sainte-Rose C (2017) Long-term outcome after multiple burr hole surgery in children with moyamoya angiopathy: a single-center experience in 108 hemispheres. Neurosurgery 0:1–7. https://doi.org/10.1093/neuros/nyw161

  3. Bonita R, Beaglehole R (1988) Modification of rankin scale: recovery of motor function after stroke. 19(12):1497–1500. https://doi.org/10.1161/01.str.19.12.1497

  4. Brott T, Adams HP Jr, Olinger CP, Marler JR, Barsan WG, Biller J, Spilker J, Holleran R, Eberle R, Hertzberg V et al (1989) Measurements of acute cerebral infarction: a clinical examination scale. Stroke 20(7):864–70. https://doi.org/10.1161/01.str.20.7.864

    Article  CAS  PubMed  Google Scholar 

  5. De Oliveira RS, Amato MCM, Simao GN, 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(6):260–264. https://doi.org/10.1055/s-0030-1249069

    Article  PubMed  Google Scholar 

  6. Dong Wei D, Wen Yuan Z, Yong Wei Z, Zhi Gang Y, Qiang L, Bing X, Xiao L, Jian Min L (2013) Role of CT perfusion imaging in evaluating the effects of multiple burr hole surgery on adult ischemic Moyamoya disease. Neuroradiology 55:1431–1438. https://doi.org/10.1007/s00234-013-1291-1

    Article  Google Scholar 

  7. Dusick JR, Gonzalez NR, Martin NA (2011) Clinical and angiographic outcomes from indirect revascularization surgery for Moyamoya disease in adults and children: a review of 63 procedures. Neurosurgery 68:34–43. https://doi.org/10.1227/NEU.0b013e3181fc5ec2

    Article  PubMed  Google Scholar 

  8. Ehrenreich H, Hasselblatt M, Dembowski C, Cepek L, Lewczuk P, Stiefel M et al (2002) Erythropoietin therapy for acute stroke is both safe and beneficial. Mol Med 8:495–505. https://doi.org/10.1007/bf03402029

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Endo M, Kawano N, Miyasika Y (1989) Cranial burr hole for revascularization in moyamoya disease. J Neurosurg 71(8):180–185. https://doi.org/10.3171/jns.1989.71.2.0180

    Article  CAS  PubMed  Google Scholar 

  10. Hawk MW, Kim KD (2000) Review of spinal pseudomeningoceles and cerebrospinal fluid fistulas. Neurosurg Focus 9(1):1–8. https://doi.org/10.3171/foc.2000.9.1.5

    Article  Google Scholar 

  11. Houkin K, Nakayama N, Kuroda S, Nonaka T,Shonai T, Yoshimoto T (2005) Novel magnetic resonance angiography stage grading for moyamoya disease cerebrovascular diseases. 20:347–354. https://doi.org/10.1159/000087935

  12. Kawaguchi T, Fujita S, Hosoda K et al (1996) Multiple burr-hole operation for adult moyamoya disease. J Neurosurg 84(3):468–476. https://doi.org/10.3171/jns.1996.84.3.0468

    Article  CAS  PubMed  Google Scholar 

  13. Lehman L, Kaseka ML, Stout J, See AP, Pabst L, Sun LR, Hassanein SA, Waak M, Vossough A, Smith ER, Dlamini N (2022) Pediatric moyamoya biomarkers: narrowing the knowledge gap. Semin Pediatr Neurol 43:101002. https://doi.org/10.1016/j.spen.2022.101002

    Article  PubMed  Google Scholar 

  14. Ma Y, Zhao M, Deng X, Zhang D, Wang S, Zeng Z, Zhang Q, Zhao J (2020) Comparison of clinical outcomes and characteristics between patients with and without hypertension in moyamoya disease. J Clin Neurosci 75:163–167. https://doi.org/10.1016/j.jocn.2019.12.016

    Article  PubMed  Google Scholar 

  15. Man Hong J, Cheol LimY MD (2018) Feasibility of multiple burr hole with erythropoietin in acute moyamoya patients. Stroke 49:1290–1295. https://doi.org/10.1161/STROKEAHA.117.020566

    Article  CAS  Google Scholar 

  16. Matsushima T, Inoue TK, Suzuki SO et al (1997) Surgical techniques and the results of a fronto-temporo-parietal combined indirect bypass procedure for children with moyamoya disease: a comparison with the results of encephalo-duro-arteriosynangiosis alone. Clin Neurol Neurosurg 99(Suppl 2):S123–S127. https://doi.org/10.4103/1817-1745.76102

    Article  PubMed  Google Scholar 

  17. 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(1):91–98. https://doi.org/10.1016/j.wneu.2013.05.010

    Article  PubMed  Google Scholar 

  18. Noguchi T, Kawashima M, Irie H, Ootsuka T, Nishihara M, Matsushima T, Kudo S (2011) Arterial spin-labeling MR imaging in moyamoya disease compared with SPECT imaging. Eur J Radiol 80(3):e557-62. https://doi.org/10.1016/j.ejrad.2011.01.016

    Article  PubMed  Google Scholar 

  19. Nael K, Mossadeghi B, Boutelier T, Kubal W, Krupinski EA, Dagher J, Villablanca JP (2015) Bayesian estimation of cerebral perfusion using reduced-contrast-dose dynamic susceptibility contrast perfusion at 3T. AJNR Am J Neuroradiol 36(4):710. https://doi.org/10.3174/ajnr.A4184

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Pires PW, Dams Ramos CM, Matin N, Dorrance AM (2013) The effects of hypertension on the cerebral circulation. Am J Physiol Heart Circ Physiol 304(12):H1598–H1614. https://doi.org/10.1152/ajpheart.00490.2012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Sainte-Rose C, Oliveira R, Puget S et al (2006) Multiple bur hole surgery for the treatment of moyamoya disease in children. J Neurosurg 105(6 suppl):437–443. https://doi.org/10.7150/ijms.11719

    Article  CAS  PubMed  Google Scholar 

  22. See AP, Stout JN (2023) Cerebrovascular reserve in moyamoya requires more standardization: editorial on ASL-MRI guided evaluation of multiple burr hole revascularization surgery in moyamoya disease. Acta Neurochir 165(8):2071–2072. https://doi.org/10.1007/s00701-023-05646-y

    Article  PubMed  Google Scholar 

  23. Scott RM, Smith JL, Robertson RL et al (2004) Long-term outcome in children with moyamoya syndrome after cranial revascularization by pial synangiosis. J Neurosurg 100:142–149. https://doi.org/10.3171/ped.2004.100.2.0142

    Article  PubMed  Google Scholar 

  24. Sollmann N, Liebl H, Preibisch C, Zimmer C, Helle M, Obara M, Kirschke JS, Kaczmarz S (2021) Super-selective ASL and 4D ASL-based MR angiography in a patient with moyamoya disease: case report. Clin Neuroradiol 31(2):515–519. https://doi.org/10.1007/s00062-020-00961-8

    Article  PubMed  Google Scholar 

  25. Sumikawa K, Nagai H (1983) Moyamoya disease and anesthesia. Anesthesiology 58(2):204–205. https://doi.org/10.1097/00000542-198302000-00033

  26. Suzuki J, Takaku A, Kodama N, Sato S (1975) An attempt to treat cerebrovascular “moyamoya” disease in children. Childs Brain 1(4):193–206. https://doi.org/10.1159/000119568

    Article  CAS  PubMed  Google Scholar 

  27. Takahashi A, Houkin K, Kamiyama H et al (1994) Elevated levels of basic fibroblast growth factor in the cerebrospinal fluid of patients with moyamoya disease. Jpn J Stroke 16:201–205. https://doi.org/10.1016/0304-3940(93)90416-i

    Article  Google Scholar 

  28. Velo M, Grasso G, Fujimura M, Torregrossa F, Longo M, Granat F, Pitrone A, Vinci SL, Ferraù L, La Spina P (2022) Moyamoya vasculopathy: cause, clinical manifestations, neuroradiologic features, and surgical management. World Neurosurg 159:409–425. https://doi.org/10.1016/j.wneu.2021.11.026

    Article  PubMed  Google Scholar 

  29. Wintermark M, Sesay M, Barbier E, Borbély K, Dillon WP, Eastwood JD, Glenn TC, Grandin CB, Pedraza S, Soustiel JF, Nariai T, Zaharchuk G, Caillé JM, Dousset V, Yonas H (2005) Comparative overview of brain perfusion imaging techniques. Stroke 36:e83–e99. https://doi.org/10.1161/01.STR.0000177884.72657.8b

    Article  PubMed  Google Scholar 

  30. Yilmaz N, Kiymaz N, Yilmaz C et al (2006) Surgical treatment outcomes in subdural effusion: a clinical study. Pediatr Neurosurg 42:1–3. https://doi.org/10.1159/000089502

    Article  CAS  PubMed  Google Scholar 

  31. Ko YS, Kim C (2004) Surgical results of multiple burr hole operation in adult moyamoya disease - preliminary report. J Korean Neurosurg Soc 35:17–22

    Google Scholar 

  32. Yu J, Shi L, Guo Y, Xu B, Xu K (2016) Progress on complications of direct bypass for moyamoya disease. Int J Med Sci 13(8):578–87. https://doi.org/10.7150/ijms.15390

    Article  PubMed  PubMed Central  Google Scholar 

  33. Zhang H, Zheng L, Feng L (2019) Epidemiology, diagnosis and treatment of moyamoya disease. Exp Ther Med 17(3):1977–1984. https://doi.org/10.3892/etm.2019.7198

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Neurosurgery Department, St-Luc Hospital, Université Catholique de Louvain, Brussels, Belgium

    M. Soler-Rico, M. Di Santo, G. Vaz, V. Joris, E. Fomekong & C. Raftopoulos

  2. Medical Imaging Department, St-Luc Hospital, Université Catholique de Louvain, Brussels, Belgium

    S. Guillaume

  3. Anesthesiology Department, St-Luc Hospital, Université Catholique de Louvain, Brussels, Belgium

    M. Van Boven

Authors
  1. M. Soler-Rico
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. Di Santo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. G. Vaz
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. V. Joris
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. E. Fomekong
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. S. Guillaume
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. M. Van Boven
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. C. Raftopoulos
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to C. Raftopoulos.

Ethics declarations

Ethics approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the Local Ethics Committee (Comité d’Ethique Hospitalo-Facultaire Saint-Luc, CE B 403) and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Competing interests

The authors declare no competing interests.

Additional information

Publisher's Note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Soler-Rico, M., Di Santo, M., Vaz, G. et al. How to reduce the complication rate of multiple burr holes surgery in moyamoya angiopathy. Acta Neurochir 165, 3613–3622 (2023). https://doi.org/10.1007/s00701-023-05876-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00701-023-05876-0

Keywords

Search

Navigation