Combined endovascular embolization and stereotactic radiosurgery in the treatment of large arteriovenous malformations

Clinical article

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Large cerebral arteriovenous malformations (AVMs) are often not amenable to direct resection or stereotactic radiosurgery (SRS) treatment. An alternative treatment strategy is staged endovascular embolization followed by SRS (Embo/SRS). The object of this study was to examine the experience at Washington University in St. Louis with Embo/SRS for large AVMs and review the results in earlier case series.


Twenty-one cases involving patients with large AVMs treated with Embo/SRS between 1994 and 2006 were retrospectively evaluated. The AVM size (before and after embolization), procedural complications, radiological outcome, and neurological outcome were examined. Radiological success was defined as AVM obliteration as demonstrated by catheter angiography, CT angiography, or MR angiography. Radiological failure was defined as residual AVM as demonstrated by catheter angiography, CT angiography, or MR angiography performed at least 3 years after SRS.


The maximum diameter of all AVMs in this series was > 3 cm (mean 4.2 cm); 12 (57%) were Spetzler-Martin Grade IV or V. Clinical follow-up was available in 20 of 21 cases; radiological follow-up was available in 19 of 21 cases (mean duration of follow-up 3.6 years). Forty-three embolization procedures were performed; 8 embolization-related complications occurred, leading to transient neurological deficits in 5 patients (24%), minor permanent neurological deficits in 3 patients (14%), and major permanent neurological deficits in none (0%). Twenty-one SRS procedures were performed; 1 radiation-induced complication occurred (5%), leading to a permanent minor neurological deficit. Of the 20 patients with clinical follow-up, none experienced cerebral hemorrhage. In the 19 patients with radiological follow-up, AVM obliteration was confirmed by catheter angiography in 13, MR angiography in 2, and CT angiography in 1. Residual nidus was found in 3 patients. In patients with follow-up catheter angiography, the AVM obliteration rate was 81% (13 of 16 cases).


Staged endovascular embolization followed by SRS provides an effective means of treating large AVMs not amenable to standard surgical or SRS treatment. The outcomes and complication rates reported in this series compare favorably to the results of other reported therapeutic strategies for this very challenging patient population.

Abbreviations used in this paper: AVM = arteriovenous malformation; Embo/SRS = staged endovascular embolization followed by SRS; GKS = Gamma Knife surgery; NBCA = n-butyl cyanoacrylate; PVA = polyvinyl alcohol; SRS = stereotactic radiosurgery.

Article Information

Address correspondence to: Gregory J. Zipfel, M.D., Department of Neurosurgery, Washington University School of Medicine, 660 South Euclid Avenue, Campus Box 8057, St. Louis, Missouri 63110. email:

Please include this information when citing this paper: published online February 18, 2011; DOI: 10.3171/2011.1.JNS10571.

© AANS, except where prohibited by US copyright law.



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    Case 9. This 56-year-old woman presented with seizures and an unruptured Spetzler-Martin Grade III AVM. A: Pretreatment angiograms showing a large AVM nidus, feeding arteries that were primarily from the right ACA, and superficial venous drainage that drained into the superior sagittal sinus and vein of Labbé. B: Angiograms obtained immediately after the first embolization, which was performed via an ACA branch, showing reduction of the nidus size by the area outlined in yellow. C: Angiograms obtained immediately after the second embolization, which was performed via 2 ACA branches, showing further peripheral reduction of the AVM nidus. D: Gamma Knife treatment plan. The original AVM volume of 18 cm3 was reduced to 10 cm3 for radiosurgery. E: Follow-up angiograms obtained 1.5 years after GKS showing complete obliteration of the patient's AVM.


  • 1

    Andrade-Souza YMRamani MScora DTsao MNter-Brugge KSchwartz ML: Embolization before radiosurgery reduces the obliteration rate of arteriovenous malformations. Neurosurgery 60:4434522007

  • 2

    Chang JHChang JWPark YGChung SS: Factors related to complete occlusion of arteriovenous malformations after gamma knife radiosurgery. J Neurosurg 93:Suppl 3961012000

  • 3

    Chang SDMarcellus MLMarks MPLevy RPDo HMSteinberg GK: Multimodality treatment of giant intracranial arteriovenous malformations. Neurosurgery 53:1132003

  • 4

    Colombo FPozza FChierego GCasentini LDe Luca GFrancescon P: Linear accelerator radiosurgery of cerebral arteriovenous malformations: an update. Neurosurgery 34:14211994

  • 5

    Dawson RC IIITarr RWHecht STJungreis CALunsford LDCoffey R: Treatment of arteriovenous malformations of the brain with combined embolization and stereotactic radiosurgery: results after 1 and 2 years. AJNR Am J Neuroradiol 11:8578641990

  • 6

    Debrun GMAletich VAusman JICharbel FDujovny M: Embolization of the nidus of brain arteriovenous malformations with n-butyl cyanoacrylate. Neurosurgery 40:1121211997

  • 7

    Ellis TLFriedman WABova FJKubilis PSBuatti JM: Analysis of treatment failure after radiosurgery for arteriovenous malformations. J Neurosurg 89:1041101998

  • 8

    Fiorella DAlbuquerque FCWoo HHMcDougall CGRasmussen PA: The role of neuroendovascular therapy for the treatment of brain arteriovenous malformations. Neurosurgery 59:5 Suppl 3S1631772006

  • 9

    Firlik ADLevy EIKondziolka DYonas H: Staged volume radiosurgery followed by microsurgical resection: a novel treatment for giant cerebral arteriovenous malformations: technical case report. Neurosurgery 43:122312281998

  • 10

    Flickinger JC: An integrated logistic formula for prediction of complications from radiosurgery. Int J Radiat Oncol Biol Phys 17:8798851989

  • 11

    Flickinger JCKondziolka DLunsford LDKassam APhuong LKLiscak R: Development of a model to predict permanent symptomatic postradiosurgery injury for arteriovenous malformation patients. Int J Radiat Oncol Biol Phys 46:114311482000

  • 12

    Foote KDFriedman WAEllis TLBova FJBuatti JMMeeks SL: Salvage retreatment after failure of radiosurgery in patients with arteriovenous malformations. J Neurosurg 98:3373412003

  • 13

    Fox AJGirvin JPViñuela FDrake CG: Rolandic arteriovenous malformations: improvement in limb function by IBC embolization. AJNR Am J Neuroradiol 6:5755821985

  • 14

    Fox AJPelz DMLee DH: Arteriovenous malformations of the brain: recent results of endovascular therapy. Radiology 177:51571990

  • 15

    Friedman WA: Radiosurgery for arteriovenous malformations. Clin Neurosurg 42:3283471995

  • 16

    Frizzel RTFisher WS III: 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 37:103110401995

  • 17

    Gobin YPLaurent AMerienne LSchlienger MAymard AHoudart E: Treatment of brain arteriovenous malformations by embolization and radiosurgery. J Neurosurg 85:19281996

  • 18

    Guo WYWikholm GKarlsson BLindquist CSvendsen PEricson K: Combined embolization and gamma knife radiosurgery for cerebral arteriovenous malformations. Acta Radiol 34:6006061993

  • 19

    Hadjipanayis CGLevy EINiranjan AFirlik ADKondziolka DFlickinger JC: Stereotactic radiosurgery for motor cortex region arteriovenous malformations. Neurosurgery 48:70772001

  • 20

    Hamilton MGSpetzler RF: The prospective application of a grading system for arteriovenous malformations. Neurosurgery 34:271994

  • 21

    Hartmann APile-Spellman JStapf CSciacca RRFaulstich AMohr JP: Risk of endovascular treatment of brain arteriovenous malformations. Stroke 33:181618202002

  • 22

    He HWJiang CHLiu HBLi YXZhang JBWu ZX: Endovascular treatment of cerebral arteriovenous malformations with Onyx embolization. Chin Med J (Engl) 118:204120452005

  • 23

    Henkes HNahser HCBerg-Dammer EWeber WLange SKühne D: Endovascular therapy of brain AVMs prior to radiosurgery. Neurol Res 20:4794921998

  • 24

    Heros RCKorosue KDiebold PM: Surgical excision of cerebral arteriovenous malformations: late results. Neurosurgery 26:5705781990

  • 25

    Izawa MHayashi MChernov MNakaya KOchiai TMurata N: Long-term complications after gamma knife surgery for arteriovenous malformations. J Neurosurg 102:Suppl34372005

  • 26

    Jayaraman MVMarcellus MLHamilton SDo HMCampbell DChang SD: Neurologic complications of arteriovenous malformation embolization using liquid embolic agents. AJNR Am J Neuroradiol 29:2422462008

  • 27

    Karlsson BJokura HYamamoto MSöderman MLax I: Is repeated radiosurgery an alternative to staged radiosurgery for very large brain arteriovenous malformations?. J Neurosurg 107:7407442007

  • 28

    Karlsson BLax ISöderman M: Can the probability for obliteration after radiosurgery for arteriovenous malformations be accurately predicted?. Int J Radiat Oncol Biol Phys 43:3133191999

  • 29

    Karlsson BLindquist CSteiner L: Prediction of obliteration after gamma knife surgery for cerebral arteriovenous malformations. Neurosurgery 40:4254311997

  • 30

    Katsaridis VPapagiannaki CAimar E: Curative embolization of cerebral arteriovenous malformations (AVMs) with Onyx in 101 patients. Neuroradiology 50:5895972008

  • 31

    Kusske JAKelly WA: Embolization and reduction of the “steal” syndrome in cerebral arteriovenous malformations. J Neurosurg 40:3133211974

  • 32

    Loy DNRich KMSimpson JDorward ISantanam LDerdeyn CP: Time-of-flight magnetic resonance angiography imaging of a residual arteriovenous malformation nidus after Onyx embolization for stereotactic radiosurgery planning. Technical note. Neurosurg Focus 26:5E132009

  • 33

    Luessenhop AJMujica PH: Embolization of segments of the circle of Willis and adjacent branches for management of certain inoperable cerebral arteriovenous malformations. J Neurosurg 54:5735821981

  • 34

    Lundqvist CWikholm GSvendsen P: Embolization of cerebral arteriovenous malformations: Part II—Aspects of complications and late outcome. Neurosurgery 39:4604691996

  • 35

    Lunsford LDKondziolka DFlickinger JCBissonette DJJungreis CAMaitz AH: Stereotactic radiosurgery for arteriovenous malformations of the brain. J Neurosurg 75:5125241991

  • 36

    Marks LBSpencer DP: The influence of volume on the tolerance of the brain to radiosurgery. J Neurosurg 75:1771801991

  • 37

    Mathis JABarr JDHorton JAJungreis CALunsford LDKondziolka DS: The efficacy of particulate embolization combined with stereotactic radiosurgery for treatment of large arteriovenous malformations of the brain. AJNR Am J Neuroradiol 16:2993061995

  • 38

    Miyachi SNegoro MOkamoto TKobayashi TKida YTanaka T: Embolisation of cerebral arteriovenous malformations to assure successful subsequent radiosurgery. J Clin Neurosci 7:Suppl 182852000

  • 39

    Miyawaki LDowd CWara WGoldsmith BAlbright NGutin P: Five year results of LINAC radiosurgery for arteriovenous malformations: outcome for large AVMS. Int J Radiat Oncol Biol Phys 44:108911061999

  • 40

    Mizoi KJokura HYoshimoto TTakahashi AEzura MKinouchi H: Multimodality treatment for large and critically located arteriovenous malformations. Neurol Med Chir (Tokyo) 38:Suppl1861921998

  • 41

    Mounayer CHammami NPiotin MSpelle LBenndorf GKessler I: Nidal embolization of brain arteriovenous malformations using Onyx in 94 patients. AJNR Am J Neuroradiol 28:5185232007

  • 42

    Nataf FMerienne LSchlienger MLefkopoulos DMeder JFTouboul E: Cerebral arteriovenous malformations treated by radiosurgery: a series of 705 cases. Neurochirurgie 47:2682822001

  • 43

    Pan DHGuo WYChung WYShiau CYChang YCWang LW: Gamma knife radiosurgery as a single treatment modality for large cerebral arteriovenous malformations. J Neurosurg 93:Suppl 31131192000

  • 44

    Panagiotopoulos VGizewski EAsgari SRegel JForsting MWanke I: Embolization of ntracranial arteriovenous malformations with ethylene-vinyl alcohol copolymer (Onyx). AJNR Am J Neuroradiol 30:991062008

  • 45

    Pollock BEFlickinger JCLunsford LDMaitz AKondziolka D: Factors associated with successful arteriovenous malformation radiosurgery. Neurosurgery 42:123912471998

  • 46

    Pollock BEKline RWStafford SLFoote RLSchomberg PJ: The rationale and technique of staged-volume arteriovenous malformation radiosurgery. Int J Radiat Oncol Biol Phys 48:8178242000

  • 47

    Schlienger MAtlan DLefkopoulos DMerienne LTouboul EMissir O: Linac radiosurgery for cerebral arteriovenous malformations: results in 169 patients. Int J Radiat Oncol Biol Phys 46:113511422000

  • 48

    Sirin SKondziolka DNiranjan AFlickinger JCMaitz AHLunsford LD: Prospective staged volume radiosurgery for large arteriovenous malformations: indications and outcomes in otherwise untreatable patients. Neurosurgery 58:17272006

  • 49

    Sorimachi TKoike TTakeuchi SMinakawa TAbe HNishimaki K: Embolization of cerebral arteriovenous malformations achieved with polyvinyl alcohol particles: angiographic reappearance and complications. AJNR Am J Neuroradiol 20:132313281999

  • 50

    Spetzler RFMartin NA: A proposed grading system for arteriovenous malformations. J Neurosurg 65:4764831986

  • 51

    Steinberg GKFabrikant JIMarks MPLevy RPFrankel KAPhillips MH: Stereotactic heavy-charged-particle Braggpeak radiation for intracranial arteriovenous malformations. N Engl J Med 323:961011990

  • 52

    Steinmeier RSchramm JMüller HGFahlbusch R: Evaluation of prognostic factors in cerebral arteriovenous malformations. Neurosurgery 24:1932001989

  • 53

    Taylor CLDutton KRappard GPride GLReplogle RPurdy PD: Complications of preoperative embolization of cerebral arteriovenous malformations. J Neurosurg 100:8108122004

  • 54

    van Rooij WJSluzewski MBeute GN: Brain AVM embolization with Onyx. AJNR Am J Neuroradiol 28:1721782007

  • 55

    Viñuela FDion JEDuckwiler GMartin NALylyk PFox A: Combined endovascular embolization and surgery in the management of cerebral arteriovenous malformations: experience with 101 cases. J Neurosurg 75:8568641991

  • 56

    Weber WKis BSiekmann RJans PLaumer RKühne D: Preoperative embolization of intracranial arteriovenous malformations with Onyx. Neurosurgery 61:2442542007

  • 57

    Wikholm GLundqvist CSvendsen P: The Göteborg cohort of embolized cerebral arteriovenous malformations: a 6-year follow-up. Neurosurgery 49:7998062001




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