Embolization of Cerebral Arteriovenous Malformations

  • Bruno C. Flores
  • Alfred P. See
  • Andrew F. Ducruet
  • Felipe C. AlbuquerqueEmail author


Effective treatment of cerebral arteriovenous malformations (AVMs) requires a multidisciplinary approach that appropriately applies the complementary modalities of microsurgical resection, endovascular embolization, and radiosurgery. Embolization is most commonly used as an adjunct to reduce the arterial supply to the AVM before surgery or radiosurgery. Additional indications for embolization include an attempt to achieve complete AVM obliteration, targeted treatment to eliminate high-risk features, and subtotal occlusion to palliate symptoms caused by an otherwise incurable AVM. In all cases, the risks and benefits of treatment must be weighed carefully when formulating a treatment strategy. For optimal management of cerebral AVMs, patients should have access to physicians experienced in open cerebrovascular surgery, endovascular embolization, and radiosurgery.



The authors would like to thank the Neuroscience Publications staff of Barrow Neurological Institute for their invaluable assistance in the preparation of this chapter.


  1. 1.
    Berman MF, Sciacca RR, Pile-Spellman J, Stapf C, Connolly ES Jr, Mohr JP, et al. The epidemiology of brain arteriovenous malformations. Neurosurgery. 2000;47(2):389–96; discussion 397.CrossRefPubMedGoogle Scholar
  2. 2.
    Luessenhop AJ, Spence WT. Artificial embolization of cerebral arteries. Report of use in a case of arteriovenous malformation. J Am Med Assoc. 1960;172:1153–5.CrossRefPubMedGoogle Scholar
  3. 3.
    Al-Shahi R, Warlow C. A systematic review of the frequency and prognosis of arteriovenous malformations of the brain in adults. Brain. 2001;124(Pt 10):1900–26.CrossRefPubMedGoogle Scholar
  4. 4.
    Leblanc GG, Golanov E, Awad IA, Young WL. Biology of vascular malformations of the brain NWC. Biology of vascular malformations of the brain. Stroke. 2009;40(12):e694–702. Scholar
  5. 5.
    Brown RD Jr, Wiebers DO, Torner JC, O'Fallon WM. Incidence and prevalence of intracranial vascular malformations in Olmsted County, Minnesota, 1965 to 1992. Neurology. 1996;46(4):949–52.CrossRefPubMedGoogle Scholar
  6. 6.
    Stapf C, Mast H, Sciacca RR, Berenstein A, Nelson PK, Gobin YP, et al. The New York Islands AVM Study: design, study progress, and initial results. Stroke. 2003;34(5):e29–33. Scholar
  7. 7.
    Crawford PM, West CR, Chadwick DW, Shaw MD. Arteriovenous malformations of the brain: natural history in unoperated patients. J Neurol Neurosurg Psychiatry. 1986;49(1):1–10.CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Mast H, Young WL, Koennecke HC, Sciacca RR, Osipov A, Pile-Spellman J, et al. Risk of spontaneous haemorrhage after diagnosis of cerebral arteriovenous malformation. Lancet. 1997;350(9084):1065–8.CrossRefPubMedGoogle Scholar
  9. 9.
    Graf CJ, Perret GE, Torner JC. Bleeding from cerebral arteriovenous malformations as part of their natural history. J Neurosurg. 1983;58(3):331–7. Scholar
  10. 10.
    Itoyama Y, Uemura S, Ushio Y, Kuratsu J, Nonaka N, Wada H, et al. Natural course of unoperated intracranial arteriovenous malformations: study of 50 cases. J Neurosurg. 1989;71(6):805–9. Scholar
  11. 11.
    Jane JA, Kassell NF, Torner JC, Winn HR. The natural history of aneurysms and arteriovenous malformations. J Neurosurg. 1985;62(3):321–3. Scholar
  12. 12.
    Ondra SL, Troupp H, George ED, 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. Scholar
  13. 13.
    Al-Shahi R, Warlow CP. Quality of evidence for management of arteriovenous malformations of the brain. Lancet. 2002;360(9338):1022–23; author reply 3. Scholar
  14. 14.
    Mohr JP, Parides MK, Stapf C, Moquete E, Moy CS, Overbey JR, 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. Scholar
  15. 15.
    Flores BC, Klinger DR, Rickert KL, Barnett SL, Welch BG, White JA, et al. Management of intracranial aneurysms associated with arteriovenous malformations. Neurosurg Focus. 2014;37(3):E11. Scholar
  16. 16.
    Redekop G, TerBrugge K, Montanera W, Willinsky R. Arterial aneurysms associated with cerebral arteriovenous malformations: classification, incidence, and risk of hemorrhage. J Neurosurg. 1998;89(4):539–46. Scholar
  17. 17.
    Starke RM, Komotar RJ, Otten ML, Hahn DK, Fischer LE, Hwang BY, 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. Scholar
  18. 18.
    Natarajan SK, Ghodke B, Britz GW, Born DE, Sekhar LN. Multimodality treatment of brain arteriovenous malformations with microsurgery after embolization with Onyx single-center experience and technical nuances. Neurosurgery. 2008;62(6):1213–25; discussion 25–6. Scholar
  19. 19.
    Spetzler RF, Martin NA. A proposed grading system for arteriovenous malformations. J Neurosurg. 1986;65(4):476–83. Scholar
  20. 20.
    Andrade-Souza YM, Ramani M, Scora D, Tsao MN, ter Brugge K, Schwartz ML. Embolization before radiosurgery reduces the obliteration rate of arteriovenous malformations. Neurosurgery. 2007;60(3):443–51; discussion 51–2. Scholar
  21. 21.
    Kano H, Kondziolka D, Flickinger JC, Park KJ, Iyer A, Yang HC, et al. Stereotactic radiosurgery for arteriovenous malformations after embolization: a case-control study. J Neurosurg. 2012;117(2):265–75. Scholar
  22. 22.
    Schwyzer L, Yen CP, Evans A, Zavoian S, Steiner L. Long-term results of Gamma Knife surgery for partially embolized arteriovenous malformations. Neurosurgery. 2012;71(6):1139–47; discussion 47–8. Scholar
  23. 23.
    Bing F, Doucet R, Lacroix F, Bahary JP, Darsaut T, Roy D, et al. Liquid embolization material reduces the delivered radiation dose: clinical myth or reality? AJNR Am J Neuroradiol. 2012;33(2):320–2. Scholar
  24. 24.
    Sanborn MR, Park MS, McDougall CG, Albuquerque FC. Endovascular approaches to pial arteriovenous malformations. Neurosurg Clin N Am. 2014;25(3):529–37. Scholar
  25. 25.
    Abud DG, Riva R, Nakiri GS, 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. Scholar
  26. 26.
    van Rooij WJ, Jacobs S, Sluzewski M, van der Pol B, Beute GN, Sprengers ME. Curative embolization of brain arteriovenous malformations with Onyx: patient selection, embolization technique, and results. AJNR Am J Neuroradiol. 2012;33(7):1299–304.
  27. 27.
    de Castro-Afonso LH, Nakiri GS, Oliveira RS, Santos MV, Santos AC, Machado HR, 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. Scholar
  28. 28.
    Brown RD Jr, Wiebers DO, Forbes GS. Unruptured intracranial aneurysms and arteriovenous malformations: frequency of intracranial hemorrhage and relationship of lesions. J Neurosurg. 1990;73(6):859–63. Scholar
  29. 29.
    Kim EJ, Halim AX, Dowd CF, Lawton MT, Singh V, Bennett J, et al. The relationship of coexisting extranidal aneurysms to intracranial hemorrhage in patients harboring brain arteriovenous malformations. Neurosurgery. 2004;54(6):1349–57; discussion 57–8.CrossRefPubMedGoogle Scholar
  30. 30.
    Lasjaunias P, Piske R, Terbrugge K, Willinsky R. Cerebral arteriovenous malformations (C. AVM) and associated arterial aneurysms (AA). Analysis of 101 C. AVM cases, with 37 AA in 23 patients. Acta Neurochir (Wien). 1988;91(1–2):29–36.CrossRefGoogle Scholar
  31. 31.
    Marks MP, Lane B, Steinberg GK, Chang PJ. Hemorrhage in intracerebral arteriovenous malformations: angiographic determinants. Radiology. 1990;176(3):807–13. Scholar
  32. 32.
    Fox AJ, Girvin JP, Vinuela F, Drake CG. Rolandic arteriovenous malformations: improvement in limb function by IBC embolization. AJNR Am J Neuroradiol. 1985;6(4):575–82.PubMedGoogle Scholar
  33. 33.
    Kusske JA, Kelly WA. Embolization and reduction of the “steal” syndrome in cerebral arteriovenous malformations. J Neurosurg. 1974;40(3):313–21. Scholar
  34. 34.
    Luessenhop AJ, Mujica PH. Embolization of segments of the circle of Willis and adjacent branches for management of certain inoperable cerebral arteriovenous malformations. J Neurosurg. 1981;54(5):573–82. Scholar
  35. 35.
    Mast H, Mohr JP, Osipov A, Pile-Spellman J, Marshall RS, Lazar RM, et al. ‘Steal’ is an unestablished mechanism for the clinical presentation of cerebral arteriovenous malformations. Stroke. 1995;26(7):1215–20.CrossRefPubMedGoogle Scholar
  36. 36.
    Rosenkranz M, Regelsberger J, Zeumer H, Grzyska U. Management of cerebral arteriovenous malformations associated with symptomatic congestive intracranial hypertension. Eur Neurol. 2008;59(1–2):62–6. Scholar
  37. 37.
    Simon SD, Yao TL, Rosenbaum BP, Reig A, Mericle RA. Resolution of trigeminal neuralgia after palliative embolization of a cerebellopontine angle arteriovenous malformation. Cent Eur Neurosurg. 2009;70(3):161–3. Scholar
  38. 38.
    Han PP, Ponce FA, Spetzler RF. Intention-to-treat analysis of Spetzler-Martin grades IV and V arteriovenous malformations: natural history and treatment paradigm. J Neurosurg. 2003;98(1):3–7. Scholar
  39. 39.
    Miyamoto S, Hashimoto N, Nagata I, Nozaki K, Morimoto M, Taki W, et al. Posttreatment sequelae of palliatively treated cerebral arteriovenous malformations. Neurosurgery. 2000;46(3):589–94; discussion 94–5.CrossRefPubMedGoogle Scholar
  40. 40.
    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.CrossRefPubMedGoogle Scholar
  41. 41.
    Spetzler RF, Wilson CB, Weinstein P, Mehdorn M, Townsend J, Telles D. Normal perfusion pressure breakthrough theory. Clin Neurosurg. 1978;25:651–72.CrossRefPubMedGoogle Scholar
  42. 42.
    Luessenhop AJ, Presper JH. Surgical embolization of cerebral arteriovenous malformations through internal carotid and vertebral arteries. Long-term results. J Neurosurg. 1975;42(4):443–51. Scholar
  43. 43.
    Spetzler RF, Martin NA, Carter LP, Flom RA, Raudzens PA, Wilkinson E. Surgical management of large AVM’s by staged embolization and operative excision. J Neurosurg. 1987;67(1):17–28. Scholar
  44. 44.
    Brothers MF, Kaufmann JC, Fox AJ, Deveikis JP. n-Butyl 2-cyanoacrylate – substitute for IBCA in interventional neuroradiology: histopathologic and polymerization time studies. AJNR Am J Neuroradiol. 1989;10(4):777–86.PubMedGoogle Scholar
  45. 45.
    Spiegel SM, Vinuela F, Goldwasser JM, Fox AJ, Pelz DM. Adjusting the polymerization time of isobutyl-2 cyanoacrylate. AJNR Am J Neuroradiol. 1986;7(1):109–12.PubMedGoogle Scholar
  46. 46.
    Taki W, Yonekawa Y, Iwata H, Uno A, Yamashita K, Amemiya H. A new liquid material for embolization of arteriovenous malformations. AJNR Am J Neuroradiol. 1990;11(1):163–8.PubMedGoogle Scholar
  47. 47.
    Chaloupka JC, Vinuela F, Vinters HV, Robert J. Technical feasibility and histopathologic studies of ethylene vinyl copolymer (EVAL) using a swine endovascular embolization model. AJNR Am J Neuroradiol. 1994;15(6):1107–15.PubMedGoogle Scholar
  48. 48.
    Murayama Y, Vinuela F, Ulhoa A, Akiba Y, Duckwiler GR, Gobin YP, et al. Nonadhesive liquid embolic agent for cerebral arteriovenous malformations: preliminary histopathological studies in swine rete mirabile. Neurosurgery. 1998;43(5):1164–75.CrossRefPubMedGoogle Scholar
  49. 49.
    Jahan R, Murayama Y, Gobin YP, Duckwiler GR, Vinters HV, Vinuela F. Embolization of arteriovenous malformations with Onyx: clinicopathological experience in 23 patients. Neurosurgery. 2001;48(5):984–95; discussion 95–7.PubMedGoogle Scholar
  50. 50.
    Weber W, Kis B, Siekmann R, Jans P, Laumer R, Kuhne D. Preoperative embolization of intracranial arteriovenous malformations with Onyx. Neurosurgery. 2007;61(2):244–52; discussion 52–4. Scholar
  51. 51.
    U.S. Food and Drug Administration. Catheter entrapment with the ev3 Onyx liquid embolic system. FDA Safety Communication. 2016. Archived at Accessed November 1, 2017.
  52. 52.
    Ozturk MH, Unal H, Dinc H. Embolization of an AVM with acrylic glue through a new microcatheter with detachable tip: an amazing experience. Neuroradiology. 2008;50(10):903–4. Scholar
  53. 53.
    Altschul D, Paramasivam S, Ortega-Gutierrez S, Fifi JT, Berenstein A. Safety and efficacy using a detachable tip microcatheter in the embolization of pediatric arteriovenous malformations. Childs Nerv Syst. 2014;30(6):1099–107. Scholar
  54. 54.
    Herial NA, Khan AA, Suri MF, Sherr GT, Qureshi AI. Liquid embolization of brain arteriovenous malformation using novel detachable tip micro catheter: a technical report. J Vasc Interv Neurol. 2014;7(5):64–8.PubMedPubMedCentralGoogle Scholar
  55. 55.
    Herial NA, Khan AA, Sherr GT, Qureshi MH, Suri MF, Qureshi AI. Detachable-tip microcatheters for liquid embolization of brain arteriovenous malformations and fistulas: a United States single-center experience. Neurosurgery. 2015;11(Suppl 3):404–11; discussion 11. Scholar
  56. 56.
    Fifi JT. Experience with detachable tip microcatheter. Oral presentation. Center for Endovascular Surgery: Mount Sinai; 2014.Google Scholar
  57. 57.
    Jafar JJ, Davis AJ, Berenstein A, Choi IS, Kupersmith MJ. The effect of embolization with N-butyl cyanoacrylate prior to surgical resection of cerebral arteriovenous malformations. J Neurosurg. 1993;78(1):60–9. Scholar
  58. 58.
    DeMeritt JS, Pile-Spellman J, Mast H, Moohan N, Lu DC, Young WL, et al. Outcome analysis of preoperative embolization with N-butyl cyanoacrylate in cerebral arteriovenous malformations. AJNR Am J Neuroradiol. 1995;16(9):1801–7.PubMedGoogle Scholar
  59. 59.
    Kwon Y, Jeon SR, Kim JH, Lee JK, Ra DS, Lee DJ, et al. Analysis of the causes of treatment failure in Gamma Knife radiosurgery for intracranial arteriovenous malformations. J Neurosurg. 2000;93(Suppl 3):104–6.
  60. 60.
    Starke RM, Komotar RJ, Hwang BY, Fischer LE, Otten ML, Merkow MB, et al. A comprehensive review of radiosurgery for cerebral arteriovenous malformations: outcomes, predictive factors, and grading scales. Stereotact Funct Neurosurg. 2008;86(3):191–9. Scholar
  61. 61.
    Lunsford LD, Kondziolka D, Flickinger JC, Bissonette DJ, Jungreis CA, Maitz AH, et al. Stereotactic radiosurgery for arteriovenous malformations of the brain. J Neurosurg. 1991;75(4):512–24. Scholar
  62. 62.
    Steiner L, Lindquist C, Adler JR, Torner JC, Alves W, Steiner M. Clinical outcome of radiosurgery for cerebral arteriovenous malformations. J Neurosurg. 1992;77(1):1–8. Scholar
  63. 63.
    Gobin YP, Laurent A, Merienne L, Schlienger M, Aymard A, Houdart E, et al. Treatment of brain arteriovenous malformations by embolization and radiosurgery. J Neurosurg. 1996;85(1):19–28. Scholar
  64. 64.
    Henkes H, Nahser HC, Berg-Dammer E, Weber W, Lange S, Kuhne D. Endovascular therapy of brain AVMs prior to radiosurgery. Neurol Res. 1998;20(6):479–92.CrossRefPubMedGoogle Scholar
  65. 65.
    Back AG, Vollmer D, Zeck O, Shkedy C, Shedden PM. Retrospective analysis of unstaged and staged Gamma Knife surgery with and without preceding embolization for the treatment of arteriovenous malformations. J Neurosurg. 2008;109(Suppl):57–64. Scholar
  66. 66.
    Blackburn SL, Ashley WW Jr, Rich KM, Simpson JR, Drzymala RE, Ray WZ, et al. Combined endovascular embolization and stereotactic radiosurgery in the treatment of large arteriovenous malformations. J Neurosurg. 2011;114(6):1758–67. Scholar
  67. 67.
    Valavanis A, Yasargil MG. The endovascular treatment of brain arteriovenous malformations. Adv Tech Stand Neurosurg. 1998;24:131–214.CrossRefPubMedGoogle Scholar
  68. 68.
    Fournier D, TerBrugge KG, Willinsky R, Lasjaunias P, Montanera W. Endovascular treatment of intracerebral arteriovenous malformations: experience in 49 cases. J Neurosurg. 1991;75(2):228–33. Scholar
  69. 69.
    Vinuela F, Duckwiler G, Guglielmi G. Contribution of interventional neuroradiology in the therapeutic management of brain arteriovenous malformations. J Stroke Cerebrovasc Dis. 1997;6(4):268–71.CrossRefPubMedGoogle Scholar
  70. 70.
    Yu SC, Chan MS, Lam JM, Tam PH, Poon WS. Complete obliteration of intracranial arteriovenous malformation with endovascular cyanoacrylate embolization: initial success and rate of permanent cure. AJNR Am J Neuroradiol. 2004;25(7):1139–43.PubMedGoogle Scholar
  71. 71.
    Elsenousi A, Aletich VA, Alaraj A. Neurological outcomes and cure rates of embolization of brain arteriovenous malformations with n-butyl cyanoacrylate or Onyx: a meta-analysis. J Neurointerv Surg. 2016;8(3):265–72. Epub 2014 Dec 24.CrossRefPubMedGoogle Scholar
  72. 72.
    Katsaridis V, Papagiannaki C, Aimar E. Curative embolization of cerebral arteriovenous malformations (AVMs) with Onyx in 101 patients. Neuroradiology. 2008;50(7):589–97. Scholar
  73. 73.
    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. Scholar
  74. 74.
    Saatci I, Geyik S, Yavuz K, Cekirge HS. 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. Scholar
  75. 75.
    Iosif C, Mendes GA, Saleme S, Ponomarjova S, Silveira EP, Caire F, et al. Endovascular transvenous cure for ruptured brain arteriovenous malformations in complex cases with high Spetzler-Martin grades. J Neurosurg. 2015;122(5):1229–38. Scholar
  76. 76.
    Martinez-Galdamez M, Saura P, Saura J, Muniz J, Albisua J, Perez-Higueras A. Transvenous Onyx embolization of a subependymal deep arteriovenous malformation with a single drainage vein: technical note. J Neurointerv Surg. 2014;6(3):e20. Scholar
  77. 77.
    Pereira VM, Marcos-Gonzalez A, Radovanovic I, Bijlenga P, Narata AP, Moret J, et al. Transvenous embolization of a ruptured deep cerebral arteriovenous malformation. A technical note. Interv Neuroradiol. 2013;19(1):27–34.CrossRefPubMedPubMedCentralGoogle Scholar
  78. 78.
    Renieri L, Limbucci N, Consoli A, Rosi A, Nappini S, Giordano F, et al. Transvenous embolization: a report of 4 pediatric cases. J Neurosurg Pediatr. 2015;15(4):445–50. Scholar
  79. 79.
    Crowley RW, Ducruet AF, Kalani MY, Kim LJ, Albuquerque FC, McDougall CG. Neurological morbidity and mortality associated with the endovascular treatment of cerebral arteriovenous malformations before and during the Onyx era. J Neurosurg. 2015;122(6):1492–7. Scholar
  80. 80.
    Debrun GM, Aletich V, Ausman JI, Charbel F, Dujovny M. Embolization of the nidus of brain arteriovenous malformations with n-butyl cyanoacrylate. Neurosurgery. 1997;40(1):112–20; discussion 20–1.PubMedGoogle Scholar
  81. 81.
    Hartmann A, Pile-Spellman J, Stapf C, Sciacca RR, Faulstich A, Mohr JP, et al. Risk of endovascular treatment of brain arteriovenous malformations. Stroke. 2002;33(7):1816–20.CrossRefPubMedGoogle Scholar
  82. 82.
    Taylor CL, Dutton K, Rappard G, Pride GL, Replogle R, Purdy PD, et al. Complications of preoperative embolization of cerebral arteriovenous malformations. J Neurosurg. 2004;100(5):810–2. Scholar
  83. 83.
    Frizzel RT, Fisher WS 3rd. Cure, morbidity, and mortality associated with embolization of brain arteriovenous malformations: a review of 1246 patients in 32 series over a 35-year period. Neurosurgery. 1995;37(6):1031–9; discussion 9-40.CrossRefPubMedGoogle Scholar
  84. 84.
    Loh Y, Duckwiler GR, Onyx Trial Investigators. A prospective, multicenter, randomized trial of the Onyx liquid embolic system and N-butyl cyanoacrylate embolization of cerebral arteriovenous malformations. Clinical article. J Neurosurg. 2010;113(4):733–41. Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Bruno C. Flores
    • 1
  • Alfred P. See
    • 1
  • Andrew F. Ducruet
    • 1
  • Felipe C. Albuquerque
    • 1
    • 2
    Email author
  1. 1.Department of NeurosurgeryBarrow Neurological Institute, St. Joseph’s Hospital and Medical CenterPhoenixUSA
  2. 2.c/o Neuroscience Publications; Barrow Neurological Institute, St. Joseph’s Hospital and Medical CenterPhoenixUSA

Personalised recommendations