Long-term complications and outcomes of therapeutic embolization of cerebral arteriovenous malformations: a systematic review
Keywords:
Central nervous system vascular malformations, Embolization, therapeutic, Cerebrovascular disorders, Neurosurgery, Brain arteriovenous malformations, Endovascular treatment, Complications, Outcomes, Long term, Vascular disordersAbstract
BACKGROUND: Embolization is a promising treatment strategy for cerebral arteriovenous malformations (AVMs). However, consensus regarding the main complications or long-term outcomes of embolization in AVMs remains lacking. OBJECTIVE: To characterize the most prevalent complications and long-term outcomes in patients with AVM undergoing therapeutic embolization. DESIGN AND SETTING: This systematic review was conducted at the Federal University of Alagoas, Arapiraca, Brazil. METHODS: This systematic review was conducted according to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses criteria. Data were obtained from MEDLINE, PubMed, LILACS, and SciELO databases, which included the epidemiological profile of the population, characteristics of the proposed therapy, complications (hemorrhagic events and neurological deficits), and long-term outcomes (modified Rankin scale pre- and post-treatment, AVM recanalization, complete obliteration, and deaths). RESULTS: Overall, the analysis included 34 articles (2,799 patients). Grade III Spetzler–Martin AVMs were observed in 34.2% of cases. Notably, 39.3% of patients underwent embolization combined with radiosurgery. The most frequently reported long-term complication was hemorrhage, which occurred in 8.7% of patients at a mean follow-up period of 58.6 months. Further, 6.3% of patients exhibited neurological deficits after an average of 34.7 months. Complete obliteration was achieved in 51.4% of the cases after a mean period of 36 months. Recanalization of AVMs was observed in 3.5% of patients. Long-term death occurred in 4.0% of patients. CONCLUSION: Embolization of AVMs is an increasingly safe strategy with low long-term complications and satisfactory outcomes, especially in patients who have undergone combination therapies. SYSTEMATIC REVIEW REGISTRATION: https://www.crd.york.ac.uk/prospero/ Registration number
CRD42020204867
Downloads
References
Finby N, Begg CF. Arteriovenous malformation of the brain. N Y State J Med. 1965;65:554-8. PMID: 14276301.
Mast H, Young WL, Koennecke HC, et al. Risk of spontaneous haemorrhage after diagnosis of cerebral arteriovenous malformation. Lancet. 1997;350(9084):1065-8. PMID: 10213548; https://doi.org/10.1016/s0140-6736(97)05390-7.
Laakso A, Hernesniemi J. Arteriovenous malformations: epidemiology and clinical presentation. Neurosurg Clin N Am. 2012;23(1):1-6. PMID: 2210785; https://doi.org/10.1016/j.nec.2011.09.012.
Galaktionov DM, Dubovoy AV, Kiselev VS, etal. Kombinirovannoe lechenie arteriovenoznykh mal'formatsiĭ golovnogo mozga s ispol'zovaniem éndovaskuliarnogo i mikrokhirurgicheskogo metodov [Combination treatment of cerebral arteriovenous malformations using endovascular and microsurgical techniques]. Zh Vopr Neirokhir Im N N Burdenko. 2017;81(4):26-32. PMID: 28914868; https://doi.org/10.17116/neiro201781426-32.
van Beijnum J, van der Worp HB, Buis DR, et al. Treatment of brain arteriovenous malformations: a systematic review and meta-analysis. JAMA. 2011;306(18):2011-9. PMID: 22068993; https://doi.org/10.1001/jama.2011.1632.
Zuurbier SM, Al-Shahi Salman R. Interventions for treating brain arteriovenous malformations in adults. Cochrane Database Syst Rev. 2019;9(9):CD003436. PMID: 31503327; https://doi.org/10.1002/14651858.CD003436.pub4.
Mohr JP, Parides MK, Stapf C, et al. 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; https://doi.org/10.1016/S0140-6736(13)62302-8.
Ogilvy CS, Stieg PE, Awad I, et al. Recommendations for the management of intracranial arteriovenous malformations: a statement for healthcare professionals from a special writing group of the Stroke Council, American Stroke Association. Circulation. 2001;103(21):2644-57. PMID: 11382737; https://doi.org/10.1161/01.cir.103.21.2644.
Bendok BR, El Tecle NE, El Ahmadieh TY, et al. Advances and innovations in brain arteriovenous malformation surgery. Neurosurgery. 2014;74 Suppl 1:S60-73. PMID: 24402494; https://doi.org/10.1227/NEU.0000000000000230.
Wells G, Shea B, O’Connell D, et al. The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomized studies in meta-analyses. 2013. Available from: http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp. Accessed in 2022 (Nov 16).
Yang W, Wei Z, Wang JY, et al. Long-term Outcomes of Patients With Giant Intracranial Arteriovenous Malformations. Neurosurgery. 2016;79(1):116-24. PMID: 26695091; https://doi.org/10.1227/NEU.0000000000001189.
Yang W, Hung AL, Caplan JM, et al. Delayed Hemorrhage After Treatment of Brain Arteriovenous Malformations (AVMs). World Neurosurg. 2016;87:98-109. PMID: 26704216; https://doi.org/10.1016/j.wneu.2015.11.057.
Dehdashti AR, Thines L, Willinsky RA, et al. Multidisciplinary care of occipital arteriovenous malformations: effect on nonhemorrhagic headache, vision, and outcome in a series of 135 patients. Clinical article. J Neurosurg. 2010;113(4):742-8. PMID: 20059323; https://doi.org/10.3171/2009.11.JNS09884.
Singfer U, Hemelsoet D, Vanlangenhove P, et al. Unruptured Brain Arteriovenous Malformations: Primary ONYX Embolization in ARUBA (A Randomized Trial of Unruptured Brain Arteriovenous Malformations)-Eligible Patients. Stroke. 2017;48(12):3393-6. PMID: 29114088; https://doi.org/10.1161/STROKEAHA.117.018605.
Xu F, Ni W, Liao Y, et al. Onyx embolization for the treatment of brain arteriovenous malformations. Acta Neurochir (Wien). 2011;153(4):869-78. PMID: 21046174; https://doi.org/10.1007/s00701-010-0848-6.
Abud DG, Riva R, Nakiri GS, et al. 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.
Iosif C, de Lucena AF, Abreu-Mattos LG, et al. Curative endovascular treatment for low-grade Spetzler-Martin brain arteriovenous malformations: a single-center prospective study. J Neurointerv Surg. 2019;11(7):699-705. PMID: 30602485; https://doi.org/10.1136/neurintsurg-2018-014390.
Mendes GA, Iosif C, Silveira EP, et al. Transvenous Embolization in Pediatric Plexiform Arteriovenous Malformations. Neurosurgery. 2016;78(3):458-65. PMID: 26457485; https://doi.org/10.1227/NEU.0000000000001057.
Weber W, Kis B, Siekmann R, et al. Preoperative embolization of intracranial arteriovenous malformations with Onyx. Neurosurgery. 2007;61(2):244-52; discussion 252-4 PMID: 17762736; https://doi.org/10.1227/01.NEU.0000255473.60505.84.
Cronqvist M, Wirestam R, Ramgren B, et al. Endovascular treatment of intracerebral arteriovenous malformations: procedural safety, complications, and results evaluated by MR imaging, including diffusion and perfusion imaging. AJNR Am J Neuroradiol. 2006;27(1):162-76. PMID: 16418378.
Lv X, Wu Z, Jiang C, et al. Endovascular treatment accounts for a change in brain arteriovenous malformation natural history risk. Interv Neuroradiol. 2010;16(2):127-32. PMID: 20642886; https://doi.org/10.1177/159101991001600203.
Pierot L, Kadziolka K, Litré F, Rousseaux P. Combined treatment of brain AVMs with use of Onyx embolization followed by radiosurgery. AJNR Am J Neuroradiol. 2013;34(7):1395-400. PMID: 23391837; https://doi.org/10.3174/ajnr.A3409.
Shekhtman OD, Maryashev SA, Eliava SS, et al. Combined treatment of cerebral arteriovenous malformations. Experience of the Burdenko Neurosurgical Institute. Zh Vopr Neirokhir Im N N Burdenko. 2015;79(4):4-18. PMID: 26529618; https://doi.org/10.17116/neiro20157944-18.
da Costa L, Wallace MC, Ter Brugge KG, et al. The natural history and predictive features of hemorrhage from brain arteriovenous malformations. Stroke. 2009;40(1):100-5. PMID: 19008469; https://doi.org/10.1161/STROKEAHA.108.524678.
Halim AX, Johnston SC, Singh V, et al. Longitudinal risk of intracranial hemorrhage in patients with arteriovenous malformation of the brain within a defined population. Stroke. 2004;35(7):1697-702. PMID: 15166396; https://doi.org/10.1161/01.STR.0000130988.44824.29.
Zabel-du Bois A, Milker-Zabel S, Huber P, Schlegel W, Debus J. Risk of hemorrhage and obliteration rates of LINAC-based radiosurgery for cerebral arteriovenous malformations treated after prior partial embolization. Int J Radiat Oncol Biol Phys. 2007;68(4):999-1003. PMID: 17398029; https://doi.org/10.1016/j.ijrobp.2007.01.027.
Choi JH, Mohr JP. Brain arteriovenous malformations in adults. Lancet Neurol. 2005;4(5):299-308. PMID: 15847843; https://doi.org/10.1016/S1474-4422(05)70073-9.
Hartmann A, Pile-Spellman J, Stapf C, et al. Risk of endovascular treatment of brain arteriovenous malformations. Stroke. 2002;33(7):1816-20. PMID: 12105359; https://doi.org/10.1161/01.str.0000020123.80940.b2.
Starke RM, Komotar RJ, Otten ML, et al. Adjuvant embolization with N-butyl cyanoacrylate in the treatment of cerebral arteriovenous malformations: outcomes, complications, and predictors of neurologic deficits. Stroke. 2009;40(8):2783-90. PMID: 19478232; https://doi.org/10.1161/STROKEAHA.108.539775. 24
Blauwblomme T, Bourgeois M, Meyer P, et al. Long-term outcome of 106 consecutive pediatric ruptured brain arteriovenous malformations after combined treatment. Stroke. 2014;45(6):1664-71. PMID: 24788975; https://doi.org/10.1161/STROKEAHA.113.004292.
Kano H, Kondziolka D, Flickinger JC, et al. Stereotactic radiosurgery for arteriovenous malformations after embolization: a case-control study. J Neurosurg. 2012;117(2):265-75. PMID: 22631689; https://doi.org/10.3171/2012.4.JNS111935.
Singfer U, Hemelsoet D, Vanlangenhove P, et al. Unruptured Brain Arteriovenous Malformations: Primary ONYX Embolization in ARUBA (A Randomized Trial of Unruptured Brain Arteriovenous Malformations)-Eligible Patients. Stroke. 2017;48(12):3393-6. PMID: 29114088; https://doi.org/10.1161/STROKEAHA.117.018605.
Liu J, Lv M, Lv X, et al. Curative glubran 2 embolization of cerebral arteriovenous malformations patient selection and initial results. Interv Neuroradiol. 2014;20(6):722-8. PMID: 25496682; https://doi.org/10.15274/INR-2014-10063.
Aboukaïs R, Vinchon M, Quidet M, et al. Reappearance of arteriovenous malformations after complete resection of ruptured arteriovenous malformations: true recurrence or false-negative early postoperative imaging result? J Neurosurg. 2017;126(4):1088-93. PMID: 27231973; https://doi.org/10.3171/2016.3.JNS152846.
Panagiotopoulos V, Gizewski E, Asgari S, et al. Embolization of intracranial arteriovenous malformations with ethylene-vinyl alcohol copolymer (Onyx). AJNR Am J Neuroradiol. 2009;30(1):99-106. PMID: 18842759; https://doi.org/10.3174/ajnr.A1314.
Valavanis A, Schwarz U, Baumann CR, Weller M, Linnebank M. Amyotrophic lateral sclerosis after embolization of cerebral arterioveneous malformations. J Neurol. 2014;261(4):732-7. PMID: 24509642; https://doi.org/10.1007/s00415-014-7260-8.
Al-Smadi AS, Ansari SA, Shokuhfar T, et al. Safety and outcome of combined endovascular and surgical management of low grade cerebral arteriovenous malformations in children compared to surgery alone. Eur J Radiol. 2019;116:8-13. PMID: 31153578; https://doi.org/10.1016/j.ejrad.2019.02.016.
Consoli A, Scarpini G, Rosi A, et al. Endovascular treatment of unruptured and ruptured brain arteriovenous malformations with Onyx18: a monocentric series of 84 patients. J Neurointerv Surg. 2014;6(8):600-6. PMID: 24126640; https://doi.org/10.1136/neurintsurg-2013-010869.
de Castro-Afonso LH, Nakiri GS, Oliveira RS, et al. Curative embolization of pediatric intracranial arteriovenous malformations using Onyx: the role of new embolization techniques on patient outcomes. Neuroradiology. 2016;58(6):585-94. PMID: 26909692; https://doi.org/10.1007/s00234-016-1666-1.
Lee CC, Chen CJ, Ball B, et al. Stereotactic radiosurgery for arteriovenous malformations after Onyx embolization: a case-control study. J Neurosurg. 2015;123(1):126-35. PMID: 25658780; https://doi.org/10.3171/2014.12.JNS141437.
Lv X, Li Y, Jiiang C, Yang X, Wu Z. Brain arteriovenous malformations and endovascular treatment: effect on seizures. Interv Neuroradiol. 2010;16(1):39-45. PMID: 20377978; https://doi.org/10.1177/159101991001600105.
Mathis JA, Barr JD, Horton JA, et al. The efficacy of particulate embolization combined with stereotactic radiosurgery for treatment of large arteriovenous malformations of the brain. AJNR Am J Neuroradiol. 1995;16(2):299-306. PMID: 7726076.
Pérez-Higueras A, López RR, Tapia DQ. Endovascular Treatment of Cerebral AVM: Our Experience with Onyx. Interv Neuroradiol. 2005;11(Suppl 1):141-57. PMID: 20584469; https://doi.org/10.1177/15910199050110S118.
Pierot L, Cognard C, Herbreteau D, et al. Endovascular treatment of brain arteriovenous malformations using a liquid embolic agent: results of a prospective, multicentre study (BRAVO). Eur Radiol. 2013;23(10):2838-45. PMID: 23652849; https://doi.org/10.1007/s00330-013-2870-6.
Raupp EF, Fernandes J. Does treatment with N-butyl cyanoacrylate embolization protect against hemorrhage in cerebral arteriovenous malformations? Arq Neuropsiquiatr. 2005;63(1):34-9. PMID: 15830062; https://doi.org/10.1590/s0004-282x2005000100007.
Sahlein DH, Mora P, Becske T, Nelson PK. Nidal embolization of brain arteriovenous malformations: rates of cure, partial embolization, and clinical outcome. J Neurosurg. 2012;117(1):65-77. PMID: 22540403; https://doi.org/10.3171/2012.3.JNS111405.
Umansky D, Corn BW, Strauss I, et al. Combined treatment approach to cerebral arteriovenous malformation in pediatric patients: stereotactic radiosurgery to partially Onyx-embolized AVM. Childs Nerv Syst. 2018;34(11):2269-74. PMID: 29882061; https://doi.org/10.1007/s00381-018-3854-2.
van Rooij WJ, Jacobs S, Sluzewski M, et al. Curative embolization of brain arteriovenous malformations with onyx: patient selection, embolization technique, and results. AJNR Am J Neuroradiol. 2012;33(7):1299-304. PMID: 22383233; https://doi.org/10.3174/ajnr.A2947.
Wikholm G, Lundqvist C, Svendsen P. The Göteborg cohort of embolized cerebral arteriovenous malformations: a 6-year follow-up. Neurosurgery. 2001;49(4):799-805; discussion 805-6. PMID: 11564239; https://doi.org/10.1097/00006123-200110000-00004.
Jordan J, Llibre JC, Vazquez F. Predictors of neurological deficit after endovascular treatment of cerebral arteriovenous malformations and functional repercussions in prospective follow-up. Neuroradiol J. 2014;27(6):718-24. PMID: 25489896; https://doi.org/10.15274/NRJ-2014-10095.
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2025 São Paulo Medical Journal

This work is licensed under a Creative Commons Attribution 4.0 International License.