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

Robert M. StarkeDepartment of Neurological Surgery, University of Miami, Florida;

Search for other papers by Robert M. Starke in
Current site
Google Scholar
PubMed
Close
 MD, MSc
,
David J. McCarthyDepartment of Neurological Surgery, University of Miami, Florida;

Search for other papers by David J. McCarthy in
Current site
Google Scholar
PubMed
Close
 MSc
,
Ching-Jen ChenDepartment of Neurological Surgery, University of Virginia, Charlottesville, Virginia;

Search for other papers by Ching-Jen Chen in
Current site
Google Scholar
PubMed
Close
 MD
,
Hideyuki KanoDepartment of Neurological Surgery, University of Pittsburgh;

Search for other papers by Hideyuki Kano in
Current site
Google Scholar
PubMed
Close
 MD, PhD
,
Brendan J. McShaneDepartment of Neurological Surgery, University of Pennsylvania, Philadelphia, Pennsylvania;

Search for other papers by Brendan J. McShane in
Current site
Google Scholar
PubMed
Close
 BA
,
John LeeDepartment of Neurological Surgery, University of Pennsylvania, Philadelphia, Pennsylvania;

Search for other papers by John Lee in
Current site
Google Scholar
PubMed
Close
 MD
,
Mohana Rao PatibandlaDepartment of Neurological Surgery, University of Virginia, Charlottesville, Virginia;

Search for other papers by Mohana Rao Patibandla in
Current site
Google Scholar
PubMed
Close
 MCh
,
David MathieuDepartment of Neurological Surgery, University of Sherbrooke, Quebec, Canada,

Search for other papers by David Mathieu in
Current site
Google Scholar
PubMed
Close
 MD
,
Lucas T. VasasDepartment of Neurological Surgery, University of Manitoba, Winnipeg, Manitoba, Canada;

Search for other papers by Lucas T. Vasas in
Current site
Google Scholar
PubMed
Close
 BS
,
Anthony M. KaufmannDepartment of Neurological Surgery, University of Manitoba, Winnipeg, Manitoba, Canada;

Search for other papers by Anthony M. Kaufmann in
Current site
Google Scholar
PubMed
Close
 MD, MSc, FRCSC
,
Wei Gang WangDepartment of Radiation Oncology, Beaumont Health System, Royal Oak, Michigan;

Search for other papers by Wei Gang Wang in
Current site
Google Scholar
PubMed
Close
 MD
,
Inga S. GrillsDepartment of Radiation Oncology, Beaumont Health System, Royal Oak, Michigan;

Search for other papers by Inga S. Grills in
Current site
Google Scholar
PubMed
Close
 MD
,
Christopher P. CifarelliDepartments of Neurological Surgery and

Search for other papers by Christopher P. Cifarelli in
Current site
Google Scholar
PubMed
Close
 MD, PhD
,
Gabriella PaisanDepartment of Neurological Surgery, University of Virginia, Charlottesville, Virginia;

Search for other papers by Gabriella Paisan in
Current site
Google Scholar
PubMed
Close
 MD
,
John VargoRadiation Oncology, West Virginia University, Morgantown, West Virginia;

Search for other papers by John Vargo in
Current site
Google Scholar
PubMed
Close
 MD
,
Tomas ChytkaDepartment of Neurological Surgery, Na Homolce Hospital, Prague, Czech Republic;

Search for other papers by Tomas Chytka in
Current site
Google Scholar
PubMed
Close
 MD
,
Ladislava JanouskovaDepartment of Neurological Surgery, Na Homolce Hospital, Prague, Czech Republic;

Search for other papers by Ladislava Janouskova in
Current site
Google Scholar
PubMed
Close
 MD
,
Caleb E. FelicianoDepartment of Neurological Surgery, University of Puerto Rico, San Juan, Puerto Rico; and

Search for other papers by Caleb E. Feliciano in
Current site
Google Scholar
PubMed
Close
 MD
,
Nanthiya SujijantaratDepartment of Neurological Surgery, Yale University School of Medicine, New Haven, Connecticut

Search for other papers by Nanthiya Sujijantarat in
Current site
Google Scholar
PubMed
Close
 MD
,
Charles MatoukDepartment of Neurological Surgery, Yale University School of Medicine, New Haven, Connecticut

Search for other papers by Charles Matouk in
Current site
Google Scholar
PubMed
Close
 MD
,
Veronica ChiangDepartment of Neurological Surgery, Yale University School of Medicine, New Haven, Connecticut

Search for other papers by Veronica Chiang in
Current site
Google Scholar
PubMed
Close
 MD
,
Judith HessDepartment of Neurological Surgery, Yale University School of Medicine, New Haven, Connecticut

Search for other papers by Judith Hess in
Current site
Google Scholar
PubMed
Close
 BA
,
Rafael Rodriguez-MercadoDepartment of Neurological Surgery, University of Puerto Rico, San Juan, Puerto Rico; and

Search for other papers by Rafael Rodriguez-Mercado in
Current site
Google Scholar
PubMed
Close
 MD
,
Daniel A. TonettiDepartment of Neurological Surgery, University of Pittsburgh;

Search for other papers by Daniel A. Tonetti in
Current site
Google Scholar
PubMed
Close
 MD
,
L. Dade LunsfordDepartment of Neurological Surgery, University of Pittsburgh;

Search for other papers by L. Dade Lunsford in
Current site
Google Scholar
PubMed
Close
 MD
, and
Jason P. SheehanDepartment of Neurological Surgery, University of Virginia, Charlottesville, Virginia;

Search for other papers by Jason P. Sheehan in
Current site
Google Scholar
PubMed
Close
 MD, PhD
View More View Less
Restricted access

Purchase Now

USD  $45.00

JNS + Pediatrics - 1 year subscription bundle (Individuals Only)

USD  $525.00

JNS + Pediatrics + Spine - 1 year subscription bundle (Individuals Only)

USD  $624.00
USD  $45.00
USD  $525.00
USD  $624.00
Print or Print + Online Sign in

OBJECTIVE

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).

METHODS

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.

RESULTS

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).

CONCLUSIONS

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.
  • Collapse
  • Expand

Illustration from Duan et al. (pp 1174–1181).

  • 1

    Altman DG: Practical Statistics for Medical Research. Boca Raton, FL: CRC Press, 1990

  • 2

    Awad IA, Little JR, Akarawi WP, Ahl J: Intracranial dural arteriovenous malformations: factors predisposing to an aggressive neurological course. J Neurosurg 72:839850, 1990

    • Search Google Scholar
    • Export Citation
  • 3

    Barcia-Salorio JL, Soler F, Barcia JA, Hernández G: Stereotactic radiosurgery for the treatment of low-flow carotid-cavernous fistulae: results in a series of 25 cases. Stereotact Funct Neurosurg 63:266270, 1994

    • Search Google Scholar
    • Export Citation
  • 4

    Borden JA, Wu JK, Shucart WA: A proposed classification for spinal and cranial dural arteriovenous fistulous malformations and implications for treatment. J Neurosurg 82:166179, 1995

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Brown RD Jr, Wiebers DO, Nichols DA: Intracranial dural arteriovenous fistulae: angiographic predictors of intracranial hemorrhage and clinical outcome in nonsurgical patients. J Neurosurg 81:531538, 1994

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    Bulters DO, Mathad N, Culliford D, Millar J, Sparrow OC: The natural history of cranial dural arteriovenous fistulae with cortical venous reflux—the significance of venous ectasia. Neurosurgery 70:312319, 2012

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7

    Chen CJ, Buell TJ, Diamond J, Ding D, Kumar JS, Taylor DG, et al.: Stereotactic radiosurgery for high-grade intracranial dural arteriovenous fistulas. World Neurosurg 116:e640e648, 2018

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    Cifarelli CP, Kaptain G, Yen CP, Schlesinger D, Sheehan JP: Gamma Knife radiosurgery for dural arteriovenous fistulas. Neurosurgery 67:12301235, 2010

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Cognard C, Gobin YP, Pierot L, Bailly AL, Houdart E, Casasco A, et al.: Cerebral dural arteriovenous fistulas: clinical and angiographic correlation with a revised classification of venous drainage. Radiology 194:671680, 1995

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    Cohen-Inbar O, Starke RM, Kano H, Bowden G, Huang P, Rodriguez-Mercado R, et al.: Stereotactic radiosurgery for cerebellar arteriovenous malformations: an international multicenter study. J Neurosurg 127:512521, 2017

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Cohen-Inbar O, Starke RM, Paisan G, Kano H, Huang PP, Rodriguez-Mercado R, et al.: Early versus late arteriovenous malformation responders after stereotactic radiosurgery: an international multicenter study. J Neurosurg 127:503511, 2017

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Daniels DJ, Vellimana AK, Zipfel GJ, Lanzino G: Intracranial hemorrhage from dural arteriovenous fistulas: clinical features and outcome. Neurosurg Focus 34(5):E15, 2013

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Della Pepa GM, Parente P, D’Argento F, Pedicelli A, Sturiale CL, Sabatino G, et al.: Angio-architectural features of high-grade intracranial dural arteriovenous fistulas: correlation with aggressive clinical presentation and hemorrhagic risk. Neurosurgery 81:315330, 2017

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Dmytriw AA, Schwartz ML, Cusimano MD, Mendes Pereira V, Krings T, Tymianski M, et al.: Gamma Knife radiosurgery for the treatment of intracranial dural arteriovenous fistulas. Interv Neuroradiol 23:211220, 2017

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    Elhammady MS, Ambekar S, Heros RC: Epidemiology, clinical presentation, diagnostic evaluation, and prognosis of cerebral dural arteriovenous fistulas. Handb Clin Neurol 143:99105, 2017

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    Fine JP, Gray RJ: A proportional hazards model for the subdistribution of a competing risk. J Am Stat Assoc 94:496509, 1999

  • 17

    Friedman JA, Pollock BE, Nichols DA, Gorman DA, Foote RL, Stafford SL: Results of combined stereotactic radiosurgery and transarterial embolization for dural arteriovenous fistulas of the transverse and sigmoid sinuses. J Neurosurg 94:886891, 2001

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18

    Gray RJ: A class of K-sample tests for comparing the cumulative incidence of a competing risk. Ann Stat 16:11411154, 1988

  • 19

    Gross BA, Albuquerque FC, McDougall CG, Jankowitz BT, Jadhav AP, Jovin TG, et al.: A multi-institutional analysis of the untreated course of cerebral dural arteriovenous fistulas. J Neurosurg 129:11141119, 2018

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20

    Gross BA, Du R: Natural history of cerebral arteriovenous malformations: a meta-analysis. J Neurosurg 118:437443, 2013

  • 21

    Gross BA, Du R: The natural history of cerebral dural arteriovenous fistulae. Neurosurgery 71:594603, 2012

  • 22

    Gross BA, Ropper AE, Popp AJ, Du R: Stereotactic radiosurgery for cerebral dural arteriovenous fistulas. Neurosurg Focus 32(5):E18, 2012

  • 23

    Hai J, Ding M, Guo Z, Wang B: A new rat model of chronic cerebral hypoperfusion associated with arteriovenous malformations. J Neurosurg 97:11981202, 2002

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24

    Hanakita S, Koga T, Shin M, Shojima M, Igaki H, Saito N: Role of Gamma Knife surgery in the treatment of intracranial dural arteriovenous fistulas. J Neurosurg 117 Suppl:158163, 2012

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25

    Jung HH, Chang JH, Whang K, Pyen JS, Chang JW, Park YG: Gamma Knife surgery for low-flow cavernous sinus dural arteriovenous fistulas. J Neurosurg 113 Suppl:2127, 2010

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26

    Koebbe CJ, Singhal D, Sheehan J, Flickinger JC, Horowitz M, Kondziolka D, et al.: Radiosurgery for dural arteriovenous fistulas. Surg Neurol 64:392399, 2005

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27

    Lewis AI, Tomsick TA, Tew JM Jr: Management of tentorial dural arteriovenous malformations: transarterial embolization combined with stereotactic radiation or surgery. J Neurosurg 81:851859, 1994

    • Search Google Scholar
    • Export Citation
  • 28

    Li C, Wang Y, Li Y, Jiang C, Yang X, Wu Z: Clinical and angioarchitectural risk factors associated with intracranial hemorrhage in dural arteriovenous fistulas: a single-center retrospective study. PLoS One 10:e0131235, 2015

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29

    Link MJ, Coffey RJ, Nichols DA, Gorman DA: The role of radiosurgery and particulate embolization in the treatment of dural arteriovenous fistulas. J Neurosurg 84:804809, 1996

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30

    O’Leary S, Hodgson TJ, Coley SC, Kemeny AA, Radatz MW: Intracranial dural arteriovenous malformations: results of stereotactic radiosurgery in 17 patients. Clin Oncol (R Coll Radiol) 14:97102, 2002

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31

    Pan DH, Wu HM, Kuo YH, Chung WY, Lee CC, Guo WY: Intracranial dural arteriovenous fistulas: natural history and rationale for treatment with stereotactic radiosurgery. Prog Neurol Surg 27:176194, 2013

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32

    Park KS, Kang DH, Park SH, Kim YS: The efficacy of gamma knife radiosurgery alone as a primary treatment for intracranial dural arteriovenous fistulas. Acta Neurochir (Wien) 158:821828, 2016

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33

    Peng T, Liu A, Jia J, Jiang C, Li Y, Wu Z, et al.: Risk factors for dural arteriovenous fistula intracranial hemorrhage. J Clin Neurosci 21:769772, 2014

  • 34

    Piippo A, Laakso A, Seppä K, Rinne J, Jääskeläinen JE, Hernesniemi J, et al.: Early and long-term excess mortality in 227 patients with intracranial dural arteriovenous fistulas. J Neurosurg 119:164171, 2013

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35

    Pollock BE, Nichols DA, Garrity JA, Gorman DA, Stafford SL: Stereotactic radiosurgery and particulate embolization for cavernous sinus dural arteriovenous fistulae. Neurosurgery 45:459467, 1999

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36

    Schneider BF, Eberhard DA, Steiner LE: Histopathology of arteriovenous malformations after gamma knife radiosurgery. J Neurosurg 87:352357, 1997

  • 37

    Shah MN, Botros JA, Pilgram TK, Moran CJ, Cross DT III, Chicoine MR, et al.: Borden-Shucart Type I dural arteriovenous fistulas: clinical course including risk of conversion to higher-grade fistulas. J Neurosurg 117:539545, 2012

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 38

    Sheehan JP, Starke RM, Kano H, Barnett GH, Mathieu D, Chiang V, et al.: Gamma Knife radiosurgery for posterior fossa meningiomas: a multicenter study. J Neurosurg 122:14791489, 2015

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 39

    Söderman M, Edner G, Ericson K, Karlsson B, Rähn T, Ulfarsson E, et al.: Gamma knife surgery for dural arteriovenous shunts: 25 years of experience. J Neurosurg 104:867875, 2006

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 40

    Söderman M, Pavic L, Edner G, Holmin S, Andersson T: Natural history of dural arteriovenous shunts. Stroke 39:17351739, 2008

  • 41

    Starke RM, Kano H, Ding D, Lee JYK, Mathieu D, Whitesell J, et al.: Stereotactic radiosurgery for cerebral arteriovenous malformations: evaluation of long-term outcomes in a multicenter cohort. J Neurosurg 126:3644, 2017

    • Search Google Scholar
    • Export Citation
  • 42

    Strom RG, Botros JA, Refai D, Moran CJ, Cross DT III, Chicoine MR, et al.: Cranial dural arteriovenous fistulae: asymptomatic cortical venous drainage portends less aggressive clinical course. Neurosurgery 64:241248, 2009

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 43

    Tonetti DA, Gross BA, Jankowitz BT, Atcheson KM, Kano H, Monaco EA, et al.: Stereotactic radiosurgery for dural arteriovenous fistulas without cortical venous reflux. World Neurosurg 107:371375, 2017

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 44

    Tonetti DA, Gross BA, Jankowitz BT, Kano H, Monaco EA, Niranjan A, et al.: 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]

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 45

    van Dijk JM, terBrugge KG, Willinsky RA, Wallace MC: Clinical course of cranial dural arteriovenous fistulas with long-term persistent cortical venous reflux. Stroke 33:12331236, 2002

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 46

    van Dijk JMC, Terbrugge KG, Willinsky RA, Wallace MC: The natural history of dural arteriovenous shunts: the Toronto experience. Stroke 40:e412e414, 2009

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 47

    Willinsky R, Goyal M, terBrugge K, Montanera W: Tortuous, engorged pial veins in intracranial dural arteriovenous fistulas: correlations with presentation, location, and MR findings in 122 patients. AJNR Am J Neuroradiol 20:10311036, 1999

    • Search Google Scholar
    • Export Citation
  • 48

    Zipfel GJ, Shah MN, Refai D, Dacey RG Jr, Derdeyn CP: Cranial dural arteriovenous fistulas: modification of angiographic classification scales based on new natural history data. Neurosurg Focus 26(5):E14, 2009

    • PubMed
    • Search Google Scholar
    • Export Citation

Metrics

All Time Past Year Past 30 Days
Abstract Views 1110 328 17
Full Text Views 215 36 3
PDF Downloads 234 46 3
EPUB Downloads 0 0 0