Hemorrhage risk of cerebral dural arteriovenous fistulas following Gamma Knife radiosurgery in a multicenter international consortium

Restricted access


The authors performed a study to evaluate the hemorrhagic rates of cerebral dural arteriovenous fistulas (dAVFs) and the risk factors of hemorrhage following Gamma Knife radiosurgery (GKRS).


Data from a cohort of patients undergoing GKRS for cerebral dAVFs were compiled from the International Radiosurgery Research Foundation. The annual posttreatment hemorrhage rate was calculated as the number of hemorrhages divided by the patient-years at risk. Risk factors for dAVF hemorrhage prior to GKRS and during the latency period after radiosurgery were evaluated in a multivariate analysis.


A total of 147 patients with dAVFs were treated with GKRS. Thirty-six patients (24.5%) presented with hemorrhage. dAVFs that had any cortical venous drainage (CVD) (OR = 3.8, p = 0.003) or convexity or torcula location (OR = 3.3, p = 0.017) were more likely to present with hemorrhage in multivariate analysis. Half of the patients had prior treatment (49.7%). Post-GRKS hemorrhage occurred in 4 patients, with an overall annual risk of 0.84% during the latency period. The annual risks of post-GKRS hemorrhage for Borden type 2–3 dAVFs and Borden type 2–3 hemorrhagic dAVFs were 1.45% and 0.93%, respectively. No hemorrhage occurred after radiological confirmation of obliteration. Independent predictors of hemorrhage following GKRS included nonhemorrhagic neural deficit presentation (HR = 21.6, p = 0.027) and increasing number of past endovascular treatments (HR = 1.81, p = 0.036).


Patients have similar rates of hemorrhage before and after radiosurgery until obliteration is achieved. dAVFs that have any CVD or are located in the convexity or torcula were more likely to present with hemorrhage. Patients presenting with nonhemorrhagic neural deficits and a history of endovascular treatments had higher risks of post-GKRS hemorrhage.

ABBREVIATIONS AVM = arteriovenous malformation; CVD = cortical venous drainage; dAVF = dural arteriovenous fistula; GKRS = Gamma Knife radiosurgery; NHND = nonhemorrhagic neural deficit.

Article Information

Correspondence David McCarthy: University of Miami Miller School of Medicine, Miami, FL. djm77@med.miami.edu.

INCLUDE WHEN CITING Published online March 15, 2019; DOI: 10.3171/2018.12.JNS182208.

Disclosures Dr. Vargo reports receiving speaking honoraria from Brainlab. Dr. Lunsford reports stock ownership in Elekta and being a consultant for Insightec, DSMB. Dr. Kano reports he has an Elekta Research Grant and is an Elekta AB grant recipient.

© AANS, except where prohibited by US copyright law.




Altman DG: Practical Statistics for Medical Research. Boca Raton, FL: CRC Press1990


Awad IALittle JRAkarawi WPAhl J: Intracranial dural arteriovenous malformations: factors predisposing to an aggressive neurological course. J Neurosurg 72:8398501990


Barcia-Salorio JLSoler FBarcia JAHernández G: Stereotactic radiosurgery for the treatment of low-flow carotid-cavernous fistulae: results in a series of 25 cases. Stereotact Funct Neurosurg 63:2662701994


Borden JAWu JKShucart WA: A proposed classification for spinal and cranial dural arteriovenous fistulous malformations and implications for treatment. J Neurosurg 82:1661791995


Brown RD JrWiebers DONichols DA: Intracranial dural arteriovenous fistulae: angiographic predictors of intracranial hemorrhage and clinical outcome in nonsurgical patients. J Neurosurg 81:5315381994


Bulters DOMathad NCulliford DMillar JSparrow OC: The natural history of cranial dural arteriovenous fistulae with cortical venous reflux—the significance of venous ectasia. Neurosurgery 70:3123192012


Chen CJBuell TJDiamond JDing DKumar JSTaylor DG: Stereotactic radiosurgery for high-grade intracranial dural arteriovenous fistulas. World Neurosurg 116:e640e6482018


Cifarelli CPKaptain GYen CPSchlesinger DSheehan JP: Gamma Knife radiosurgery for dural arteriovenous fistulas. Neurosurgery 67:123012352010


Cognard CGobin YPPierot LBailly ALHoudart ECasasco A: Cerebral dural arteriovenous fistulas: clinical and angiographic correlation with a revised classification of venous drainage. Radiology 194:6716801995


Cohen-Inbar OStarke RMKano HBowden GHuang PRodriguez-Mercado R: Stereotactic radiosurgery for cerebellar arteriovenous malformations: an international multicenter study. J Neurosurg 127:5125212017


Cohen-Inbar OStarke RMPaisan GKano HHuang PPRodriguez-Mercado R: Early versus late arteriovenous malformation responders after stereotactic radiosurgery: an international multicenter study. J Neurosurg 127:5035112017


Daniels DJVellimana AKZipfel GJLanzino G: Intracranial hemorrhage from dural arteriovenous fistulas: clinical features and outcome. Neurosurg Focus 34(5):E152013


Della Pepa GMParente PD’Argento FPedicelli ASturiale CLSabatino G: Angio-architectural features of high-grade intracranial dural arteriovenous fistulas: correlation with aggressive clinical presentation and hemorrhagic risk. Neurosurgery 81:3153302017


Dmytriw AASchwartz MLCusimano MDMendes Pereira VKrings TTymianski M: Gamma Knife radiosurgery for the treatment of intracranial dural arteriovenous fistulas. Interv Neuroradiol 23:2112202017


Elhammady MSAmbekar SHeros RC: Epidemiology, clinical presentation, diagnostic evaluation, and prognosis of cerebral dural arteriovenous fistulas. Handb Clin Neurol 143:991052017


Fine JPGray RJ: A proportional hazards model for the subdistribution of a competing risk. J Am Stat Assoc 94:4965091999


Friedman JAPollock BENichols DAGorman DAFoote RLStafford SL: Results of combined stereotactic radiosurgery and transarterial embolization for dural arteriovenous fistulas of the transverse and sigmoid sinuses. J Neurosurg 94:8868912001


Gray RJ: A class of K-sample tests for comparing the cumulative incidence of a competing risk. Ann Stat 16:114111541988


Gross BAAlbuquerque FCMcDougall CGJankowitz BTJadhav APJovin TG: A multi-institutional analysis of the untreated course of cerebral dural arteriovenous fistulas. J Neurosurg 129:111411192018


Gross BADu R: Natural history of cerebral arteriovenous malformations: a meta-analysis. J Neurosurg 118:4374432013


Gross BADu R: The natural history of cerebral dural arteriovenous fistulae. Neurosurgery 71:5946032012


Gross BARopper AEPopp AJDu R: Stereotactic radiosurgery for cerebral dural arteriovenous fistulas. Neurosurg Focus 32(5):E182012


Hai JDing MGuo ZWang B: A new rat model of chronic cerebral hypoperfusion associated with arteriovenous malformations. J Neurosurg 97:119812022002


Hanakita SKoga TShin MShojima MIgaki HSaito N: Role of Gamma Knife surgery in the treatment of intracranial dural arteriovenous fistulas. J Neurosurg 117 Suppl:1581632012


Jung HHChang JHWhang KPyen JSChang JWPark YG: Gamma Knife surgery for low-flow cavernous sinus dural arteriovenous fistulas. J Neurosurg 113 Suppl:21272010


Koebbe CJSinghal DSheehan JFlickinger JCHorowitz MKondziolka D: Radiosurgery for dural arteriovenous fistulas. Surg Neurol 64:3923992005


Lewis AITomsick TATew JM Jr: Management of tentorial dural arteriovenous malformations: transarterial embolization combined with stereotactic radiation or surgery. J Neurosurg 81:8518591994


Li CWang YLi YJiang CYang XWu Z: Clinical and angioarchitectural risk factors associated with intracranial hemorrhage in dural arteriovenous fistulas: a single-center retrospective study. PLoS One 10:e01312352015


Link MJCoffey RJNichols DAGorman DA: The role of radiosurgery and particulate embolization in the treatment of dural arteriovenous fistulas. J Neurosurg 84:8048091996


O’Leary SHodgson TJColey SCKemeny AARadatz MW: Intracranial dural arteriovenous malformations: results of stereotactic radiosurgery in 17 patients. Clin Oncol (R Coll Radiol) 14:971022002


Pan DHWu HMKuo YHChung WYLee CCGuo WY: Intracranial dural arteriovenous fistulas: natural history and rationale for treatment with stereotactic radiosurgery. Prog Neurol Surg 27:1761942013


Park KSKang DHPark SHKim YS: The efficacy of gamma knife radiosurgery alone as a primary treatment for intracranial dural arteriovenous fistulas. Acta Neurochir (Wien) 158:8218282016


Peng TLiu AJia JJiang CLi YWu Z: Risk factors for dural arteriovenous fistula intracranial hemorrhage. J Clin Neurosci 21:7697722014


Piippo ALaakso ASeppä KRinne JJääskeläinen JEHernesniemi J: Early and long-term excess mortality in 227 patients with intracranial dural arteriovenous fistulas. J Neurosurg 119:1641712013


Pollock BENichols DAGarrity JAGorman DAStafford SL: Stereotactic radiosurgery and particulate embolization for cavernous sinus dural arteriovenous fistulae. Neurosurgery 45:4594671999


Schneider BFEberhard DASteiner LE: Histopathology of arteriovenous malformations after gamma knife radiosurgery. J Neurosurg 87:3523571997


Shah MNBotros JAPilgram TKMoran CJCross DT IIIChicoine MR: Borden-Shucart Type I dural arteriovenous fistulas: clinical course including risk of conversion to higher-grade fistulas. J Neurosurg 117:5395452012


Sheehan JPStarke RMKano HBarnett GHMathieu DChiang V: Gamma Knife radiosurgery for posterior fossa meningiomas: a multicenter study. J Neurosurg 122:147914892015


Söderman MEdner GEricson KKarlsson BRähn TUlfarsson E: Gamma knife surgery for dural arteriovenous shunts: 25 years of experience. J Neurosurg 104:8678752006


Söderman MPavic LEdner GHolmin SAndersson T: Natural history of dural arteriovenous shunts. Stroke 39:173517392008


Starke RMKano HDing DLee JYKMathieu DWhitesell J: Stereotactic radiosurgery for cerebral arteriovenous malformations: evaluation of long-term outcomes in a multicenter cohort. J Neurosurg 126:36442017


Strom RGBotros JARefai DMoran CJCross DT IIIChicoine MR: Cranial dural arteriovenous fistulae: asymptomatic cortical venous drainage portends less aggressive clinical course. Neurosurgery 64:2412482009


Tonetti DAGross BAJankowitz BTAtcheson KMKano HMonaco EA: Stereotactic radiosurgery for dural arteriovenous fistulas without cortical venous reflux. World Neurosurg 107:3713752017


Tonetti DAGross BAJankowitz BTKano HMonaco EANiranjan A: Reconsidering an important subclass of high-risk dural arteriovenous fistulas for stereotactic radiosurgery. J Neurosurg [epub ahead of print March 1 2018. DOI: 10.3171/2017.10.JNS171802]


van Dijk JMterBrugge KGWillinsky RAWallace MC: Clinical course of cranial dural arteriovenous fistulas with long-term persistent cortical venous reflux. Stroke 33:123312362002


van Dijk JMCTerbrugge KGWillinsky RAWallace MC: The natural history of dural arteriovenous shunts: the Toronto experience. Stroke 40:e412e4142009


Willinsky RGoyal MterBrugge KMontanera W: Tortuous, engorged pial veins in intracranial dural arteriovenous fistulas: correlations with presentation, location, and MR findings in 122 patients. AJNR Am J Neuroradiol 20:103110361999


Zipfel GJShah MNRefai DDacey RG JrDerdeyn CP: Cranial dural arteriovenous fistulas: modification of angiographic classification scales based on new natural history data. Neurosurg Focus 26(5):E142009




All Time Past Year Past 30 Days
Abstract Views 249 249 249
Full Text Views 68 68 68
PDF Downloads 22 22 22
EPUB Downloads 0 0 0


Google Scholar