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

Clinical article

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  • 1 Departments of Neurosurgery,
  • | 3 Radiation Oncology,
  • | 4 Radiology, and
  • | 5 Neurology, Washington University School of Medicine, St. Louis, Missouri; and
  • | 2 Department of Neurosurgery, University of Texas Medical School at Houston, Texas
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Object

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.

Methods

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.

Results

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).

Conclusions

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.

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  • 1

    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
  • 2

    Chang JH, , Chang JW, , Park YG, & Chung SS: Factors related to complete occlusion of arteriovenous malformations after gamma knife radiosurgery. J Neurosurg 93:Suppl 3 96101, 2000

    • Search Google Scholar
    • Export Citation
  • 3

    Chang SD, , Marcellus ML, , Marks MP, , Levy RP, , Do HM, & Steinberg GK: Multimodality treatment of giant intracranial arteriovenous malformations. Neurosurgery 53:113, 2003

    • Search Google Scholar
    • Export Citation
  • 4

    Colombo F, , Pozza F, , Chierego G, , Casentini L, , De Luca G, & Francescon P: Linear accelerator radiosurgery of cerebral arteriovenous malformations: an update. Neurosurgery 34:1421, 1994

    • Search Google Scholar
    • Export Citation
  • 5

    Dawson RC III, , Tarr RW, , Hecht ST, , Jungreis CA, , Lunsford LD, & Coffey R, et al.: Treatment of arteriovenous malformations of the brain with combined embolization and stereotactic radiosurgery: results after 1 and 2 years. AJNR Am J Neuroradiol 11:857864, 1990

    • Search Google Scholar
    • Export Citation
  • 6

    Debrun GM, , Aletich V, , Ausman JI, , Charbel F, & Dujovny M: Embolization of the nidus of brain arteriovenous malformations with n-butyl cyanoacrylate. Neurosurgery 40:112121, 1997

    • Search Google Scholar
    • Export Citation
  • 7

    Ellis TL, , Friedman WA, , Bova FJ, , Kubilis PS, & Buatti JM: Analysis of treatment failure after radiosurgery for arteriovenous malformations. J Neurosurg 89:104110, 1998

    • Search Google Scholar
    • Export Citation
  • 8

    Fiorella D, , Albuquerque FC, , Woo HH, , McDougall CG, & Rasmussen PA: The role of neuroendovascular therapy for the treatment of brain arteriovenous malformations. Neurosurgery 59:5 Suppl 3 S163177, 2006

    • Search Google Scholar
    • Export Citation
  • 9

    Firlik AD, , Levy EI, , Kondziolka D, & Yonas H: Staged volume radiosurgery followed by microsurgical resection: a novel treatment for giant cerebral arteriovenous malformations: technical case report. Neurosurgery 43:12231228, 1998

    • Search Google Scholar
    • Export Citation
  • 10

    Flickinger JC: An integrated logistic formula for prediction of complications from radiosurgery. Int J Radiat Oncol Biol Phys 17:879885, 1989

    • Search Google Scholar
    • Export Citation
  • 11

    Flickinger JC, , Kondziolka D, , Lunsford LD, , Kassam A, , Phuong LK, & Liscak R, et al.: Development of a model to predict permanent symptomatic postradiosurgery injury for arteriovenous malformation patients. Int J Radiat Oncol Biol Phys 46:11431148, 2000

    • Search Google Scholar
    • Export Citation
  • 12

    Foote KD, , Friedman WA, , Ellis TL, , Bova FJ, , Buatti JM, & Meeks SL: Salvage retreatment after failure of radiosurgery in patients with arteriovenous malformations. J Neurosurg 98:337341, 2003

    • Search Google Scholar
    • Export Citation
  • 13

    Fox AJ, , Girvin JP, , Viñuela F, & Drake CG: Rolandic arteriovenous malformations: improvement in limb function by IBC embolization. AJNR Am J Neuroradiol 6:575582, 1985

    • Search Google Scholar
    • Export Citation
  • 14

    Fox AJ, , Pelz DM, & Lee DH: Arteriovenous malformations of the brain: recent results of endovascular therapy. Radiology 177:5157, 1990

  • 15

    Friedman WA: Radiosurgery for arteriovenous malformations. Clin Neurosurg 42:328347, 1995

  • 16

    Frizzel RT, & Fisher 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 37:10311040, 1995

    • Search Google Scholar
    • Export Citation
  • 17

    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 85:1928, 1996

    • Search Google Scholar
    • Export Citation
  • 18

    Guo WY, , Wikholm G, , Karlsson B, , Lindquist C, , Svendsen P, & Ericson K: Combined embolization and gamma knife radiosurgery for cerebral arteriovenous malformations. Acta Radiol 34:600606, 1993

    • Search Google Scholar
    • Export Citation
  • 19

    Hadjipanayis CG, , Levy EI, , Niranjan A, , Firlik AD, , Kondziolka D, & Flickinger JC, et al.: Stereotactic radiosurgery for motor cortex region arteriovenous malformations. Neurosurgery 48:7077, 2001

    • Search Google Scholar
    • Export Citation
  • 20

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

  • 21

    Hartmann A, , Pile-Spellman J, , Stapf C, , Sciacca RR, , Faulstich A, & Mohr JP, et al.: Risk of endovascular treatment of brain arteriovenous malformations. Stroke 33:18161820, 2002

    • Search Google Scholar
    • Export Citation
  • 22

    He HW, , Jiang CH, , Liu HB, , Li YX, , Zhang JB, & Wu ZX: Endovascular treatment of cerebral arteriovenous malformations with Onyx embolization. Chin Med J (Engl) 118:20412045, 2005

    • Search Google Scholar
    • Export Citation
  • 23

    Henkes H, , Nahser HC, , Berg-Dammer E, , Weber W, , Lange S, & Kühne D: Endovascular therapy of brain AVMs prior to radiosurgery. Neurol Res 20:479492, 1998

    • Search Google Scholar
    • Export Citation
  • 24

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

    • Search Google Scholar
    • Export Citation
  • 25

    Izawa M, , Hayashi M, , Chernov M, , Nakaya K, , Ochiai T, & Murata N, et al.: Long-term complications after gamma knife surgery for arteriovenous malformations. J Neurosurg 102:Suppl 3437, 2005

    • Search Google Scholar
    • Export Citation
  • 26

    Jayaraman MV, , Marcellus ML, , Hamilton S, , Do HM, , Campbell D, & Chang SD, et al.: Neurologic complications of arteriovenous malformation embolization using liquid embolic agents. AJNR Am J Neuroradiol 29:242246, 2008

    • Search Google Scholar
    • Export Citation
  • 27

    Karlsson B, , Jokura H, , Yamamoto M, , Söderman M, & Lax I: Is repeated radiosurgery an alternative to staged radiosurgery for very large brain arteriovenous malformations?. J Neurosurg 107:740744, 2007

    • Search Google Scholar
    • Export Citation
  • 28

    Karlsson B, , Lax I, & Söderman M: Can the probability for obliteration after radiosurgery for arteriovenous malformations be accurately predicted?. Int J Radiat Oncol Biol Phys 43:313319, 1999

    • Search Google Scholar
    • Export Citation
  • 29

    Karlsson B, , Lindquist C, & Steiner L: Prediction of obliteration after gamma knife surgery for cerebral arteriovenous malformations. Neurosurgery 40:425431, 1997

    • Search Google Scholar
    • Export Citation
  • 30

    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
  • 31

    Kusske JA, & Kelly WA: Embolization and reduction of the “steal” syndrome in cerebral arteriovenous malformations. J Neurosurg 40:313321, 1974

    • Search Google Scholar
    • Export Citation
  • 32

    Loy DN, , Rich KM, , Simpson J, , Dorward I, , Santanam L, & Derdeyn 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 26:5 E13, 2009

    • Search Google Scholar
    • Export Citation
  • 33

    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 54:573582, 1981

    • Search Google Scholar
    • Export Citation
  • 34

    Lundqvist C, , Wikholm G, & Svendsen P: Embolization of cerebral arteriovenous malformations: Part II—Aspects of complications and late outcome. Neurosurgery 39:460469, 1996

    • Search Google Scholar
    • Export Citation
  • 35

    Lunsford LD, , Kondziolka D, , Flickinger JC, , Bissonette DJ, , Jungreis CA, & Maitz AH, et al.: Stereotactic radiosurgery for arteriovenous malformations of the brain. J Neurosurg 75:512524, 1991

    • Search Google Scholar
    • Export Citation
  • 36

    Marks LB, & Spencer DP: The influence of volume on the tolerance of the brain to radiosurgery. J Neurosurg 75:177180, 1991

  • 37

    Mathis JA, , Barr JD, , Horton JA, , Jungreis CA, , Lunsford LD, & Kondziolka DS, et al.: The efficacy of particulate embolization combined with stereotactic radiosurgery for treatment of large arteriovenous malformations of the brain. AJNR Am J Neuroradiol 16:299306, 1995

    • Search Google Scholar
    • Export Citation
  • 38

    Miyachi S, , Negoro M, , Okamoto T, , Kobayashi T, , Kida Y, & Tanaka T, et al.: Embolisation of cerebral arteriovenous malformations to assure successful subsequent radiosurgery. J Clin Neurosci 7:Suppl 1 8285, 2000

    • Search Google Scholar
    • Export Citation
  • 39

    Miyawaki L, , Dowd C, , Wara W, , Goldsmith B, , Albright N, & Gutin P, et al.: Five year results of LINAC radiosurgery for arteriovenous malformations: outcome for large AVMS. Int J Radiat Oncol Biol Phys 44:10891106, 1999

    • Search Google Scholar
    • Export Citation
  • 40

    Mizoi K, , Jokura H, , Yoshimoto T, , Takahashi A, , Ezura M, & Kinouchi H, et al.: Multimodality treatment for large and critically located arteriovenous malformations. Neurol Med Chir (Tokyo) 38:Suppl 186192, 1998

    • Search Google Scholar
    • Export Citation
  • 41

    Mounayer C, , Hammami N, , Piotin M, , Spelle L, , Benndorf G, & Kessler I, et al.: Nidal embolization of brain arteriovenous malformations using Onyx in 94 patients. AJNR Am J Neuroradiol 28:518523, 2007

    • Search Google Scholar
    • Export Citation
  • 42

    Nataf F, , Merienne L, , Schlienger M, , Lefkopoulos D, , Meder JF, & Touboul E, et al.: Cerebral arteriovenous malformations treated by radiosurgery: a series of 705 cases. Neurochirurgie 47:268282, 2001

    • Search Google Scholar
    • Export Citation
  • 43

    Pan DH, , Guo WY, , Chung WY, , Shiau CY, , Chang YC, & Wang LW: Gamma knife radiosurgery as a single treatment modality for large cerebral arteriovenous malformations. J Neurosurg 93:Suppl 3 113119, 2000

    • Search Google Scholar
    • Export Citation
  • 44

    Panagiotopoulos V, , Gizewski E, , Asgari S, , Regel J, , Forsting M, & Wanke I: Embolization of ntracranial arteriovenous malformations with ethylene-vinyl alcohol copolymer (Onyx). AJNR Am J Neuroradiol 30:99106, 2008

    • Search Google Scholar
    • Export Citation
  • 45

    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
  • 46

    Pollock BE, , Kline RW, , Stafford SL, , Foote RL, & Schomberg PJ: The rationale and technique of staged-volume arteriovenous malformation radiosurgery. Int J Radiat Oncol Biol Phys 48:817824, 2000

    • Search Google Scholar
    • Export Citation
  • 47

    Schlienger M, , Atlan D, , Lefkopoulos D, , Merienne L, , Touboul E, & Missir O, et al.: Linac radiosurgery for cerebral arteriovenous malformations: results in 169 patients. Int J Radiat Oncol Biol Phys 46:11351142, 2000

    • Search Google Scholar
    • Export Citation
  • 48

    Sirin S, , Kondziolka D, , Niranjan A, , Flickinger JC, , Maitz AH, & Lunsford LD: Prospective staged volume radiosurgery for large arteriovenous malformations: indications and outcomes in otherwise untreatable patients. Neurosurgery 58:1727, 2006

    • Search Google Scholar
    • Export Citation
  • 49

    Sorimachi T, , Koike T, , Takeuchi S, , Minakawa T, , Abe H, & Nishimaki K, et al.: Embolization of cerebral arteriovenous malformations achieved with polyvinyl alcohol particles: angiographic reappearance and complications. AJNR Am J Neuroradiol 20:13231328, 1999

    • Search Google Scholar
    • Export Citation
  • 50

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

  • 51

    Steinberg GK, , Fabrikant JI, , Marks MP, , Levy RP, , Frankel KA, & Phillips MH, et al.: Stereotactic heavy-charged-particle Braggpeak radiation for intracranial arteriovenous malformations. N Engl J Med 323:96101, 1990

    • Search Google Scholar
    • Export Citation
  • 52

    Steinmeier R, , Schramm J, , Müller HG, & Fahlbusch R: Evaluation of prognostic factors in cerebral arteriovenous malformations. Neurosurgery 24:193200, 1989

    • Search Google Scholar
    • Export Citation
  • 53

    Taylor CL, , Dutton K, , Rappard G, , Pride GL, , Replogle R, & Purdy PD, et al.: Complications of preoperative embolization of cerebral arteriovenous malformations. J Neurosurg 100:810812, 2004

    • Search Google Scholar
    • Export Citation
  • 54

    van Rooij WJ, , Sluzewski M, & Beute GN: Brain AVM embolization with Onyx. AJNR Am J Neuroradiol 28:172178, 2007

  • 55

    Viñuela F, , Dion JE, , Duckwiler G, , Martin NA, , Lylyk P, & Fox A, et al.: Combined endovascular embolization and surgery in the management of cerebral arteriovenous malformations: experience with 101 cases. J Neurosurg 75:856864, 1991

    • Search Google Scholar
    • Export Citation
  • 56

    Weber W, , Kis B, , Siekmann R, , Jans P, , Laumer R, & Kühne D: Preoperative embolization of intracranial arteriovenous malformations with Onyx. Neurosurgery 61:244254, 2007

    • Search Google Scholar
    • Export Citation
  • 57

    Wikholm G, , Lundqvist C, & Svendsen P: The Göteborg cohort of embolized cerebral arteriovenous malformations: a 6-year follow-up. Neurosurgery 49:799806, 2001

    • Search Google Scholar
    • Export Citation

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