Vol. 23 No. 1 (2019)
NEUROSURGERY

Efficiency of endovascular embolization and predictors of postoperative complications in patients with different types of brain arteriovenous malformations

A. Brusyanskaya
Meshalkin National Medical Research Center, Novosibirsk, Russian Federation
Bio
A. Krivoshapkin
Meshalkin National Medical Research Center, Novosibirsk, Russian Federation; Novosibirsk State Medical University, Novosibirsk, Russian Federation; European Medical Center, Moscow, Russian Federation
K. Orlov
Meshalkin National Medical Research Center, Novosibirsk, Russian Federation; Novosibirsk State Medical University, Novosibirsk, Russian Federation
A. Alshevskaya
Biostatistics and Clinical Trials Center, Novosibirsk, Russian Federation
A. Moskalev
Biostatistics and Clinical Trials Center, Novosibirsk, Russian Federation
G. Sergeev
European Medical Center, Moscow, Russian Federation
A. Gaytan
Novosibirsk State Medical University, Novosibirsk, Russian Federation; European Medical Center, Moscow, Russian Federation
A. Simonovich
Novosibirsk State Medical University, Novosibirsk, Russian Federation

Published 2019-03-09

Keywords

  • brain arteriovenous malformations,
  • endovascular embolization,
  • hemorrhage,
  • seizure

How to Cite

Brusyanskaya, A., Krivoshapkin, A., Orlov, K., Alshevskaya, A., Moskalev, A., Sergeev, G., Gaytan, A., & Simonovich, A. (2019). Efficiency of endovascular embolization and predictors of postoperative complications in patients with different types of brain arteriovenous malformations. Patologiya Krovoobrashcheniya I Kardiokhirurgiya, 23(1), 54–60. https://doi.org/10.21688/1681-3472-2019-1-54-60

Abstract

Aim. (1) To evaluate the efficiency of endovascular embolization of brain arteriovenous malformations (AVMs) with seizure or hemorrhage in relation to radicalness and postoperative complication development and (2) to determine the predictors of postoperative complications after endovascular embolization of AVMs.

Methods. In this retrospective study, we examined the treatment of 192 patients with brain AVMs with seizure (seizure group; n = 85) or hemorrhage (hemorrhage group; n = 107). All the patients underwent total endovascular embolization of the malformations, and the follow-up period was 12 months. The two different patient groups were identified, and the predictors of the development of adverse events (hemorrhagic and ischemic complications) in the early postoperative period (hospital stay) were determined.

Results. Twelve months after control cerebral angiography was performed, recanalization was observed in 7 (8.2%) and 14 (13.1%) patients in the seizure and hemorrhage groups, respectively (p = 0.432). The frequency of complications was 20% and 29.9% in the seizure and hemorrhage groups, respectively (p = 0.162). The mortality rate during hospitalization was 0% and 9.3% in the seizure and hemorrhage groups, respectively (p = 0.026). Multivariate regression analysis revealed that a history of hemorrhage, the location of AVMs in functionally significant zones, and a large maximum size of AVMs are predictors of the development of postoperative complications.

Conclusion. Endovascular embolization is an effective, minimally invasive approach for the treatment of different types of brain AVMs. Considering the natural risks of brain AVMs according to the literature, endovascular embolization is associated with a low frequency of early postoperative complications.

Received 14 February 2019. Revised 24 May 2019. Accepted 28 May 2019.

Funding: The study did not have sponsorship.

Conflict of interest: Authors declare no conflict of interest.

References

  1. Rutledge W.C., Ko N.U., Lawton M.T., Kim H. Hemorrhage rates and risk factors in the natural history course of brain arteriovenous malformations. Transl Stroke Res. 2014;5(5):538-42. PMID: 24930128, PMCID: PMC4139097. https://doi.org/10.1007/s12975-014-0351-0
  2. Brown R.D. Jr., Wiebers D.O., Torner J.C., O'Fallon W.M. Frequency of intracranial hemorrhage as a presenting symptom and subtype analysis: A population-based study of intracranial vascular malformation in Olmsted County, Minnesota. J Neurosurg. 1996;85(1):29-32. PMID: 8683279. https://doi.org/10.3171/jns.1996.85.1.0029
  3. Свистов Д.В., Кандыба Д.В., Савелло А.В. Артериовенозные мальформации головного мозга: клиника, диагностика, комплексное лечение. Санкт-Петербург: Фолиант, 2002. С. 199–260. [Svistov D.V., Kandyba D.V., Savello A.V. Arteriovenous malformations of the brain: clinic, diagnostics, complex treatment. St. Petersburg: Foliant; 2002. P. 199-260. (in Russ.)]
  4. Шанько Ю.Г., Смеянович В.А. Современные принципы диагностики и лечения церебральных артериовенозных мальформаций. ARS MEDICA. 2009;(13):16-29. [Shanko Yu.G., Smeyanovich V.A. Modern principles of diagnostics and treatment of cerebral arteriovenous malformations. ARS MEDICA. 2009;(13):16-29].
  5. Ассоциация нейрохирургов Российской Федерации. Клинические рекомендации по диагностике и лечению артериовенозных мальформаций центральной нервной системы. М., 2014. 35 с. [Association of Neurosurgeons of the Russian Federation. Clinical guidelines for the diagnostics and treatment of arteriovenous malformations of the central nervous system. Moscow; 2014. 35 p.]
  6. Zheng T., Wang Q.J., Liu Y.Q., Cui X.B., Gao Y.Y., Lai L.F., Su S.X., Zhang X., Li X.F., He X.Y., Duan C.Z. Clinical features and endovascular treatment of intracranial arteriovenous malformations in pediatric patients. Child Nerv Syst. 2014;30(4):647-53. PMID: 24013265. https://doi.org/10.1007/s00381-013-2277-3
  7. Филатов Ю.М. Артериовенозные аневризмы больших полушарий головного мозга. М., 1972. 32 с. [Filatov Yu.M. Arteriovenous aneurysm of the cerebral hemispheres. Moscow; 1972. 32 p.]
  8. Crawford P.M., West C.R., Chadwick D.W., Shaw M.D. Arteriovenous malformations of the brain: Natural history in unoperated patients. J Neurol Neurosurg Psychiatry. 1986;49(1):1-10. PMID: 3958721, PMCID: PMC1028639. https://doi.org/10.1136/jnnp.49.1.1
  9. Sisti M.B., Stein B.M. Arteriovenous malformations of the brain stem. Neurosurgery clinics of North America. 1993;4(3):497-505.
  10. Hofmeister C., Stapf C., Hartmann A., Sciacca R.R., Mansmann U., terBrugge K., Lasjaunias P., Mohr J.P., Mast H., Meisel J. Demographic, morphological, and clinical characteristics of 1289 patients with brain arteriovenous malformation. Stroke. 2000;31(6):1307-10. PMID: 10835449.
  11. Ondra S.L., Troupp H., George E.D., Schwab K. The natural history of symptomatic arteriovenous malformations of the brain: a 24-year follow-up assessment. J Neurosurg. 1990;73(3):387-91. PMID: 2384776. https://doi.org/10.3171/jns.1990.73.3.0387
  12. Laakso A., Dashti R., Seppänen J., Juvela S., Väärt K., Niemelä M., Sankila R., Hernesniemi J.A. Long-term excess mortality in 623 patients with brain arteriovenous malformations. Neurosurgery. 2008;63(2):244-55. PMID: 18797354. https://doi.org/10.1227/01.NEU.0000320439.27895.24
  13. Cockroft K.M., Hwang S.-K., Rosenwasser R.H. Endovascular treatment of cerebral arteriovenous malformations: Indications, techniques, outcome, and complications. Neurosurg Clin N Am. 2005;16(2):367-80. PMID: 15694168. https://doi.org/10.1016/j.nec.2004.08.001
  14. Crowley R.W., Ducruet A.F., McDougall C.G., Albuquerque F.C. Endovascular advances for brain arteriovenous malformations. Neurosurgery. 2014;74(Suppl. 1):74–82. PMID: 24402496. https://doi.org/10.1227/NEU.0000000000000176
  15. Danaila L. Microsurgical treatment of the interhemispheric arteriovenous malformations. Chirurgia (Bucur). 2012;107(6):701-14. PMID: 23294947.
  16. Кривошапкин А.Л, Брусянская А.С., Орлов К.Ю., Гайтан А.С., Сергеев Г.С. Контроль эпилептических приступов у больных с артериовенозными мальформациями после эндоваскулярного лечения. Нейрохирургия. 2017;(3):27-33. Режим доступа: https://www.therjn.com/jour/article/view/447 [Krivoshapkin A.L., Brusyanskaya A.S., Orlov K.Y., Gaitan A.S., Sergeev G.S. Control of epileptic seizures at patients with arteriovenous malformations after endovascular treatment. Russian Journal of Neurosurgery. 2017;(3):27-33. (In Russ.) Available from: https://www.therjn.com/jour/article/view/447]
  17. Кривошапкин А.Л., Орлов К.Ю., Брусянская А.С., Сергеев Г.С., Гайтан А.С., Симонович А.Е. Результаты инвазивного лечения больных с эпилептическим типом течения артериовенозных мальформаций головного мозга. Сибирский научный медицинский журнал. 2018;38(6):145-53. https://doi.org/10.15372/SSMJ20180621 [Krivoshapkin A.L., Orlov K.Y., Brusyanskaya A.S., Sergeev G.S., Gaytan A.S., Simonovich A.E. The results of invasive treatment of patients with brain arteriovenous malformations with seizure. Siberian Scientific Medical Journal. 2018;38(6):145-153. (In Russ.) https://doi.org/10.15372/SSMJ20180621]
  18. Mohr J.P., Parides M.K., Stapf C., Moquete E., Moy C.S., Overbey J.R., Al-Shahi Salman R., Vicaut E., Young W.L., Houdart E., Cordonnier C., Stefani M.A., Hartmann A., von Kummer R., Biondi A., Berkefeld J., Klijn C.J., Harkness K., Libman R., Barreau X., Moskowitz A.J.; international ARUBA investigators. Medical management with or without interventional therapy for unruptured brain arteriovenous malformations (ARUBA): a multicentre, non-blinded, randomised trial. Lancet. 2014;383(9917):614-21. PMID: 24268105 PMCID: PMC4119885 https://doi.org/10.1016/S0140-6736(13)62302-8
  19. Abud D.G., Riva R., Nakiri G.S., Padovani F., Khawaldeh M., Mounayer C. Treatment of brain arteriovenous malformations by double arterial catheterization with simultaneous injection of Onyx: Retrospective series of 17 patients. AJNR Am J Neuroradiol. 2011;32(1):152-8. PMID: 20966066. https://doi.org/10.3174/ajnr.A2247
  20. Elhammady M.S., Heros R.C. Onyx and arteriovenous malformations. J Neurosurg. 2011;115(1):75-6. PMID: 21476803. https://doi.org/10.3171/2010.3.JNS091626
  21. Lv X., Wu Z., Jiang C., Li Y., Yang X., Zhang Y., Lv M., Zhang N. Endovascular treatment accounts for a change in brain arteriovenous malformation natural history risk. Interv Neuroradiol. 2010;16(2):127-32. PMCID: PMC3277980, PMID: 20642886. https://doi.org/10.1177/159101991001600203
  22. Maimon S., Strauss I., Frolov V., Margalit N., Ram Z. Brain arteriovenous malformation treatment using a combination of onyx and a new detachable tip microcatheter, SONIC: Short-term results. AJNR Am J Neuroradiol. 2010;31(5):947-54. PMID: 20190210. https://doi.org/10.3174/ajnr.A1959
  23. Natarajan S.K., Britz G.W., Born D.E., Sekhar L.N. Multimodality treatment of brain arteriovenous malformations with microsurgery after embolization with onyx: single-center experience and technical nuances. Neurosurgery. 2008;62(6):1213-25. PMID: 18824988. https://doi.org/10.1227/01.neu.0000333293.74986.e5
  24. Saatci I., Geyik S., Yavuz K., Cekirge H.S. Endovascular treatment of brain arteriovenous malformations with prolonged intranidal Onyx injection technique: long-term results in 350 consecutive patients with completed endovascular treatment course. J Neurosurg. 2011;115(1):78-88. PMID: 21476804. https://doi.org/10.3171/2011.2.JNS09830
  25. Zhang C.-G., Yang H. Embolization with Onyx for treatment of cerebral arteriovenous malformation. Chinese Journal of Interventional Imaging and Therapy. 2011;8(3):179-81.
  26. Bakhtiyarovna M.L. Clinical-pathogenic analysis of brain arteriovenous malformation neurologic manifestations. European Science Review. 2016;2(4):72-4.
  27. Al-Shahi Salman R., White P.M., Counsell C.E., du Plessis J., van Beijnum J., Josephson C.B., Wilkinson T., Wedderburn C.J., Chandy Z., St George E.J., Sellar R.J., Warlow C.P.; Scottish Audit of Intracranial Vascular Malformations Collaborators. Outcome after conservative management or intervention for unruptured brain arteriovenous malformations. JAMA. 2014;311(16):1661-9. PMID: 24756516. https://doi.org/10.1001/jama.2014.3200
  28. Baranoski J.F., Grant R.A., Hirsch L.J., Visintainer P., Gerrard J.L., Günel M., Matouk C.C., Spencer D.D., Bulsara K.R. Seizure control for intracranial arteriovenous malformations is directly related to treatment modality: a meta-analysis. J NeuroInterv Surg. 2014;6(9):684-90. PMID: 24319021. https://doi.org/10.1136/neurintsurg-2013-010945
  29. Ding D., Quigg M., Starke R.M., Xu Z., Yen C.P., Przybylowski C.J., Dodson B.K., Sheehan J.P. Radiosurgery for temporal lobe arteriovenous malformations: effect of temporal location on seizure outcomes. J Neurosurg. 2015;123(4):924-34. PMID: 25884262 https://doi.org/10.3171/2014.10.JNS141807
  30. Englot D.J., Young W.L., Han S.J., McCulloch C.E., Chang E.F., Lawton M.T. Seizure predictors and control after microsurgical resection of supratentorial arteriovenous malformations in 440 patients. Neurosurgery. 2012;71(3):572-80. PMID: 22592327, PMCID: PMC5815296. https://doi.org/10.1227/NEU.0b013e31825ea3ba
  31. Krivoshapkin A.L., Orlov K.Yu., Brusyanskaya A.S., Berestov V.V., Gaytan A.S. Effect of first line endovascular embolization and subsequent microsurgery to control seizure in patients with cerebral arteriovenous malformations (AVM) [ePoster]. The 6th World Intracranial Hemorrhage Conference 2017 (WICH 2017). Baltimore, USA; 2017.
  32. de los Reyes K., Patel A., Doshi A., Egorova N., Panov F., Bederson J.B., Frontera J.A. Seizures after Onyx embolization for the treatment of cerebral arteriovenous malformation. Interv Neuroradiol. 2011;17(3):331-8. PMCID: PMC3396045, PMID: 22005695. https://doi.org/10.1177/159101991101700308
  33. von der Brelie C., Simon M., Esche J., Schramm J., Boström A. Seizure outcomes in patients with surgically treated cerebral arteriovenous malformations. Neurosurgery. 2015;77(5):762-8. PMID: 26225856. https://doi.org/10.1227/NEU.0000000000000919
  34. Schramm J. Seizures associated with cerebral arteriovenous malformations. Handb Clin Neurol. 2017;143:31-40. PMID: 28552156. https://doi.org/10.1016/B978-0-444-63640-9.00004-7