Radiosurgery for low-grade intracranial arteriovenous malformations

Clinical article

Dale Ding M.D., Chun-Po Yen M.D., Zhiyuan Xu M.D., Robert M. Starke M.D., M.Sc. and Jason P. Sheehan M.D., Ph.D.
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  • Department of Neurological Surgery, University of Virginia, Charlottesville, Virginia
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Object

Low-grade, or Spetzler-Martin (SM) Grades I and II, arteriovenous malformations (AVMs) are associated with lower surgical morbidity rates than higher-grade lesions. While radiosurgery is now widely accepted as an effective treatment approach for AVMs, the risks and benefits of the procedure for low-grade AVMs, as compared with microsurgery, remain poorly understood. The authors of this study present the outcomes for a large cohort of low-grade AVMs treated with radiosurgery.

Methods

From an institutional radiosurgery database comprising approximately 1450 AVM cases, all patients with SM Grade I and II lesions were identified. Patients with less than 2 years of radiological follow-up, except those with complete AVM obliteration, were excluded from analysis. Univariate and multivariate Cox proportional-hazards and logistic regression analyses were used to determine factors associated with obliteration, radiation-induced changes (RICs), and hemorrhage following radiosurgery.

Results

Five hundred two patients harboring low-grade AVMs were eligible for analysis. The median age was 35 years, 50% of patients were male, and the most common presentation was hemorrhage (47%). The median AVM volume and prescription dose were 2.4 cm3 and 23 Gy, respectively. The median radiological and clinical follow-up intervals were 48 and 62 months, respectively. The cumulative obliteration rate was 76%. The median time to obliteration was 40 months, and the actuarial obliteration rates were 66% and 80% at 5 and 10 years, respectively. Independent predictors of obliteration were no preradiosurgery embolization (p < 0.001), decreased AVM volume (p = 0.005), single draining vein (p = 0.013), lower radiosurgery-based AVM scale score (p = 0.016), and lower Virginia Radiosurgery AVM Scale (Virginia RAS) score (p = 0.001). The annual postradiosurgery hemorrhage rate was 1.4% with increased AVM volume (p = 0.034) and lower prescription dose (p = 0.006) as independent predictors. Symptomatic and permanent RICs were observed in 8.2% and 1.4% of patients, respectively. No preradiosurgery hemorrhage (p = 0.011), a decreased prescription dose (p = 0.038), and a higher Virginia RAS score (p = 0.001) were independently associated with postradiosurgery RICs.

Conclusions

Spetzler-Martin Grade I and II AVMs are very amenable to successful treatment with stereotactic radiosurgery. While patient, physician, and institutional preferences frequently dictate the final course of treatment, radiosurgery offers a favorable risk-to-benefit profile for the management of low-grade AVMs.

Abbreviations used in this paper:AVM = arteriovenous malformation; DSA = digital subtraction angiography; RBAS = radiosurgery-based AVM scale; RIC = radiation-induced change; SM = Spetzler-Martin; Virginia RAS = Virginia Radiosurgery AVM Scale.

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Contributor Notes

Address correspondence to: Jason P. Sheehan, M.D., Ph.D., University of Virginia, Department of Neurosurgery, P.O. Box 800212, Charlottesville, VA 22908. email: jps2f@virginia.edu.

Please include this information when citing this paper: published online March 7, 2014; DOI: 10.3171/2014.1.JNS131713.

  • 1

    Achrol AS, , Guzman R, , Varga M, , Adler JR, , Steinberg GK, & Chang SD: Pathogenesis and radiobiology of brain arteriovenous malformations: implications for risk stratification in natural history and posttreatment course. Neurosurg Focus 26:5 E9, 2009

    • Search Google Scholar
    • Export Citation
  • 2

    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 60:443452, 2007

    • Search Google Scholar
    • Export Citation
  • 3

    Bing F, , Doucet R, , Lacroix F, , Bahary JP, , Darsaut T, & Roy D, : Liquid embolization material reduces the delivered radiation dose: clinical myth or reality?. AJNR Am J Neuroradiol 33:320322, 2012

    • Search Google Scholar
    • Export Citation
  • 4

    Brown RD Jr, , Wiebers DO, , Forbes G, , O'Fallon WM, , Piepgras DG, & Marsh WR, : The natural history of unruptured intracranial arteriovenous malformations. J Neurosurg 68:352357, 1988

    • Search Google Scholar
    • Export Citation
  • 5

    Choi JH, & Mohr JP: Brain arteriovenous malformations in adults. Lancet Neurol 4:299308, 2005

  • 6

    Cockroft KM: Unruptured brain arteriovenous malformations should be treated conservatively: no. Stroke 38:33103311, 2007

  • 7

    Davidson AS, & Morgan MK: How safe is arteriovenous malformation surgery? A prospective, observational study of surgery as first-line treatment for brain arteriovenous malformations. Neurosurgery 66:498505, 2010

    • Search Google Scholar
    • Export Citation
  • 8

    Ding D, , Yen CP, , Xu Z, , Starke RM, & Sheehan JP: Radiosurgery for patients with unruptured intracranial arteriovenous malformations. Clinical article. J Neurosurg 118:958966, 2013

    • Search Google Scholar
    • Export Citation
  • 9

    Fiehler J, & Stapf C: ARUBA—beating natural history in unruptured brain AVMs by intervention. Neuroradiology 50:465467, 2008

  • 10

    Friedman WA, , Bova FJ, & Mendenhall WM: Linear accelerator radiosurgery for arteriovenous malformations: the relationship of size to outcome. J Neurosurg 82:180189, 1995

    • Search Google Scholar
    • Export Citation
  • 11

    Graf CJ, , Perret GE, & Torner JC: Bleeding from cerebral arteriovenous malformations as part of their natural history. J Neurosurg 58:331337, 1983

    • Search Google Scholar
    • Export Citation
  • 12

    Hamilton MG, & Spetzler RF: The prospective application of a grading system for arteriovenous malformations. Neurosurgery 34:27, 1994

  • 13

    Heros RC, , Korosue K, & Diebold PM: Surgical excision of cerebral arteriovenous malformations: late results. Neurosurgery 26:570578, 1990

    • Search Google Scholar
    • Export Citation
  • 14

    Kano H, , Lunsford LD, , Flickinger JC, , Yang HC, , Flannery TJ, & Awan NR, : Stereotactic radiosurgery for arteriovenous malformations, Part 1: management of Spetzler-Martin Grade I and II arteriovenous malformations. Clinical article. J Neurosurg 116:1120, 2012

    • Search Google Scholar
    • Export Citation
  • 15

    Karlsson B, , Lax I, & Söderman M: Risk for hemorrhage during the 2-year latency period following gamma knife radiosurgery for arteriovenous malformations. Int J Radiat Oncol Biol Phys 49:10451051, 2001

    • Search Google Scholar
    • Export Citation
  • 16

    Katsaridis V, , Papagiannaki C, & Aimar E: Curative embolization of cerebral arteriovenous malformations (AVMs) with Onyx in 101 patients. Neuroradiology 50:589597, 2008

    • Search Google Scholar
    • Export Citation
  • 17

    Kiliç K, , Konya D, , Kurtkaya O, , Sav A, , Pamir MN, & Kiliç T: Inhibition of angiogenesis induced by cerebral arteriovenous malformations using Gamma Knife irradiation. J Neurosurg 106:463469, 2007

    • Search Google Scholar
    • Export Citation
  • 18

    Langer DJ, , Lasner TM, , Hurst RW, , Flamm ES, , Zager EL, & King JT Jr: Hypertension, small size, and deep venous drainage are associated with risk of hemorrhagic presentation of cerebral arteriovenous malformations. Neurosurgery 42:481489, 1998

    • Search Google Scholar
    • Export Citation
  • 19

    Lawton MT, , Kim H, , McCulloch CE, , Mikhak B, & Young WL: A supplementary grading scale for selecting patients with brain arteriovenous malformations for surgery. Neurosurgery 66:702713, 2010

    • Search Google Scholar
    • Export Citation
  • 20

    Maruyama K, , Kawahara N, , Shin M, , Tago M, , Kishimoto J, & Kurita H, : The risk of hemorrhage after radiosurgery for cerebral arteriovenous malformations. N Engl J Med 352:146153, 2005

    • Search Google Scholar
    • Export Citation
  • 21

    Maruyama K, , Shin M, , Tago M, , Kishimoto J, , Morita A, & Kawahara N: Radiosurgery to reduce the risk of first hemorrhage from brain arteriovenous malformations. Neurosurgery 60:453459, 2007

    • Search Google Scholar
    • Export Citation
  • 22

    Mohr JP, , Moskowitz AJ, , Stapf C, , Hartmann A, , Lord K, & Marshall SM, : The ARUBA trial: current status, future hopes. Stroke 41:e537e540, 2010

    • Search Google Scholar
    • Export Citation
  • 23

    Morgan MK, , Rochford AM, , Tsahtsarlis A, , Little N, & Faulder KC: Surgical risks associated with the management of Grade I and II brain arteriovenous malformations. Neurosurgery 54:832839, 2004

    • Search Google Scholar
    • Export Citation
  • 24

    Nataf F, , Schlienger M, , Bayram M, , Ghossoub M, , George B, & Roux FX: Microsurgery or radiosurgery for cerebral arteriovenous malformations? A study of two paired series. Neurosurgery 61:3950, 2007

    • Search Google Scholar
    • Export Citation
  • 25

    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 62:12131226, 2008

    • Search Google Scholar
    • Export Citation
  • 26

    O'Laoire SA: Microsurgical treatment of arteriovenous malformations in critical areas of the brain. Br J Neurosurg 9:347360, 1995

  • 27

    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 73:387391, 1990

    • Search Google Scholar
    • Export Citation
  • 28

    Panagiotopoulos V, , Gizewski E, , Asgari S, , Regel J, , Forsting M, & Wanke I: Embolization of intracranial arteriovenous malformations with ethylene-vinyl alcohol copolymer (Onyx). AJNR Am J Neuroradiol 30:99106, 2009

    • Search Google Scholar
    • Export Citation
  • 29

    Pikus HJ, , Beach ML, & Harbaugh RE: Microsurgical treatment of arteriovenous malformations: analysis and comparison with stereotactic radiosurgery. J Neurosurg 88:641646, 1998

    • Search Google Scholar
    • Export Citation
  • 30

    Pollock BE, & Flickinger JC: Modification of the radiosurgery-based arteriovenous malformation grading system. Neurosurgery 63:239243, 2008

    • Search Google Scholar
    • Export Citation
  • 31

    Pollock BE, , Flickinger JC, , Lunsford LD, , Bissonette DJ, & Kondziolka D: Factors that predict the bleeding risk of cerebral arteriovenous malformations. Stroke 27:16, 1996

    • Search Google Scholar
    • Export Citation
  • 32

    Pollock BE, , Flickinger JC, , Lunsford LD, , Maitz A, & Kondziolka D: Factors associated with successful arteriovenous malformation radiosurgery. Neurosurgery 42:12391247, 1998

    • Search Google Scholar
    • Export Citation
  • 33

    Pollock BE, , Kondziolka D, , Flickinger JC, , Patel AK, , Bissonette DJ, & Lunsford LD: Magnetic resonance imaging: an accurate method to evaluate arteriovenous malformations after stereotactic radiosurgery. J Neurosurg 85:10441049, 1996

    • Search Google Scholar
    • Export Citation
  • 34

    Pollock BE, , Lunsford LD, , Kondziolka D, , Maitz A, & Flickinger JC: Patient outcomes after stereotactic radiosurgery for “operable” arteriovenous malformations. Neurosurgery 35:18, 1994

    • Search Google Scholar
    • Export Citation
  • 35

    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. Clinical article. J Neurosurg 115:7888, 2011

    • Search Google Scholar
    • Export Citation
  • 36

    Schaller C, & Schramm J: Microsurgical results for small arteriovenous malformations accessible for radiosurgical or embolization treatment. Neurosurgery 40:664674, 1997

    • Search Google Scholar
    • Export Citation
  • 37

    Schwyzer L, , Yen CP, , Evans A, , Zavoian S, & Steiner L: Long-term results of gamma knife surgery for partially embolized arteriovenous malformations. Neurosurgery 71:11391148, 2012

    • Search Google Scholar
    • Export Citation
  • 38

    Sisti MB, , Kader A, & Stein BM: Microsurgery for 67 intracranial arteriovenous malformations less than 3 cm in diameter. J Neurosurg 79:653660, 1993

    • Search Google Scholar
    • Export Citation
  • 39

    Spetzler RF, , Hargraves RW, , McCormick PW, , Zabramski JM, , Flom RA, & Zimmerman RS: Relationship of perfusion pressure and size to risk of hemorrhage from arteriovenous malformations. J Neurosurg 76:918923, 1992

    • Search Google Scholar
    • Export Citation
  • 40

    Spetzler RF, & Martin NA: A proposed grading system for arteriovenous malformations. J Neurosurg 65:476483, 1986

  • 41

    Stapf C, & Mohr JP: Unruptured brain arteriovenous malformations should be treated conservatively: yes. Stroke 38:33083309, 2007

  • 42

    Stapf C, , Mohr JP, , Choi JH, , Hartmann A, & Mast H: Invasive treatment of unruptured brain arteriovenous malformations is experimental therapy. Curr Opin Neurol 19:6368, 2006

    • Search Google Scholar
    • Export Citation
  • 43

    Starke RM, , Yen CP, , Ding D, & Sheehan JP: A practical grading scale for predicting outcome after radiosurgery for arteriovenous malformations: analysis of 1012 treated patients. Clinical article. J Neurosurg 119:981987, 2013

    • Search Google Scholar
    • Export Citation
  • 44

    Stefani MA, , Porter PJ, , terBrugge KG, , Montanera W, , Willinsky RA, & Wallace MC: Large and deep brain arteriovenous malformations are associated with risk of future hemorrhage. Stroke 33:12201224, 2002

    • Search Google Scholar
    • Export Citation
  • 45

    Steiner L, , Lindquist C, , Adler JR, , Torner JC, , Alves W, & Steiner M: Clinical outcome of radiosurgery for cerebral arteriovenous malformations. J Neurosurg 77:18, 1992

    • Search Google Scholar
    • Export Citation
  • 46

    Sure U, , Battenberg E, , Dempfle A, , Tirakotai W, , Bien S, & Bertalanffy H: Hypoxia-inducible factor and vascular endothelial growth factor are expressed more frequently in embolized than in nonembolized cerebral arteriovenous malformations. Neurosurgery 55:663670, 2004

    • Search Google Scholar
    • Export Citation
  • 47

    Takashima S, & Becker LE: Neuropathology of cerebral arteriovenous malformations in children. J Neurol Neurosurg Psychiatry 43:380385, 1980

    • Search Google Scholar
    • Export Citation
  • 48

    Valle RD, , Zenteno M, , Jaramillo J, , Lee A, & De Anda S: Definition of the key target volume in radiosurgical management of arteriovenous malformations: a new dynamic concept based on angiographic circulation time. J Neurosurg 109:Suppl 4150, 2008

    • Search Google Scholar
    • Export Citation
  • 49

    Wegner RE, , Oysul K, , Pollock BE, , Sirin S, , Kondziolka D, & Niranjan A, : A modified radiosurgery-based arteriovenous malformation grading scale and its correlation with outcomes. Int J Radiat Oncol Biol Phys 79:11471150, 2011

    • Search Google Scholar
    • Export Citation
  • 50

    Yen CP, , Sheehan JP, , Schwyzer L, & Schlesinger D: Hemorrhage risk of cerebral arteriovenous malformations before and during the latency period after GAMMA knife radiosurgery. Stroke 42:16911696, 2011

    • Search Google Scholar
    • Export Citation

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