Stereotactic radiosurgery for arteriovenous malformations of the basal ganglia and thalamus: an international multicenter study

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  • 1 Department of Neurological Surgery, University of Virginia Health System, Charlottesville, Virginia;
  • 2 Department of Neurosurgery, University of Louisville, Louisville, Kentucky;
  • 3 Department of Neurological Surgery, University of Pittsburgh, Pennsylvania;
  • 4 Division of Neurosurgery, Centre de recherché du CHUS, University of Sherbrooke, Quebec, Canada;
  • 5 Department of Neurosurgery, New York University Langone Medical Center, New York, New York;
  • 6 Section of Neurological Surgery, University of Puerto Rico, San Juan, Puerto Rico;
  • 7 Department of Radiation Oncology, Beaumont Health System, Royal Oak, Michigan; and
  • 8 Department of Neurosurgery, Cleveland Clinic Foundation, Cleveland, Ohio
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OBJECTIVE

Arteriovenous malformations (AVMs) of the basal ganglia (BG) and thalamus are associated with elevated risks of both hemorrhage if left untreated and neurological morbidity after resection. Therefore, stereotactic radiosurgery (SRS) has become a mainstay in the management of these lesions, although its safety and efficacy remain incompletely understood. The aim of this retrospective multicenter cohort study was to evaluate the outcomes of SRS for BG and thalamic AVMs and determine predictors of successful endpoints and adverse radiation effects.

METHODS

The authors retrospectively reviewed data on patients with BG or thalamic AVMs who had undergone SRS at eight institutions participating in the International Gamma Knife Research Foundation (IGKRF) from 1987 to 2014. Favorable outcome was defined as AVM obliteration, no post-SRS hemorrhage, and no permanently symptomatic radiation-induced changes (RICs). Multivariable models were developed to identify independent predictors of outcome.

RESULTS

The study cohort comprised 363 patients with BG or thalamic AVMs. The mean AVM volume and SRS margin dose were 3.8 cm3 and 20.7 Gy, respectively. The mean follow-up duration was 86.5 months. Favorable outcome was achieved in 58.5% of patients, including obliteration in 64.8%, with rates of post-SRS hemorrhage and permanent RIC in 11.3% and 5.6% of patients, respectively. Independent predictors of favorable outcome were no prior AVM embolization (p = 0.011), a higher margin dose (p = 0.008), and fewer isocenters (p = 0.044).

CONCLUSIONS

SRS is the preferred intervention for the majority of BG and thalamic AVMs. Patients with morphologically compact AVMs that have not been previously embolized are more likely to have a favorable outcome, which may be related to the use of a higher margin dose.

ABBREVIATIONS AVM = arteriovenous malformation; BG = basal ganglia; DSA = digital subtraction angiography; EBRT = external beam radiation therapy; IGKRF = International Gamma Knife Research Foundation; mRBAS = modified radiosurgery-based AVM score; RIC = radiation-induced change; SM = Spetzler-Martin; SRS = stereotactic radiosurgery; VRAS = Virginia Radiosurgery AVM Scale.

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Contributor Notes

Correspondence Ching-Jen Chen: University of Virginia Health System, Charlottesville, VA. chenjared@gmail.com.

INCLUDE WHEN CITING Published online January 11, 2019; DOI: 10.3171/2018.8.JNS182106.

Disclosures Dr. Grills reports stock ownership and serving on the board of directors for the Greater Michigan Gamma Knife, and she reports receiving through her institution research funding from Elekta, which is unrelated to this study. Dr. Lunsford reports stock ownership in Elekta AB and serving on the data safety monitoring board for Insightec.

  • 1

    Al-Shahi Salman R, White PM, Counsell CE, du Plessis J, van Beijnum J, Josephson CB, : Outcome after conservative management or intervention for unruptured brain arteriovenous malformations. JAMA 311:16611669, 2014

    • Search Google Scholar
    • Export Citation
  • 2

    Andrade-Souza YM, Ramani M, Beachey DJ, Scora D, Tsao MN, terBrugge K, : Liquid embolisation material reduces the delivered radiation dose: a physical experiment. Acta Neurochir (Wien) 150:161164, 2008

    • Search Google Scholar
    • Export Citation
  • 3

    Andrade-Souza YM, Ramani M, Scora D, Tsao MN, terBrugge K, Schwartz ML: Embolization before radiosurgery reduces the obliteration rate of arteriovenous malformations. Neurosurgery 60:443452, 2007

    • Search Google Scholar
    • Export Citation
  • 4

    Andrade-Souza YM, Zadeh G, Scora D, Tsao MN, Schwartz ML: Radiosurgery for basal ganglia, internal capsule, and thalamus arteriovenous malformation: clinical outcome. Neurosurgery 56:5664, 2005

    • Search Google Scholar
    • Export Citation
  • 5

    ApSimon HT, Reef H, Phadke RV, Popovic EA: A population-based study of brain arteriovenous malformation: long-term treatment outcomes. Stroke 33:27942800, 2002

    • Search Google Scholar
    • Export Citation
  • 6

    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
  • 7

    Buell TJ, Ding D, Starke RM, Webster Crowley R, Liu KC: Embolization-induced angiogenesis in cerebral arteriovenous malformations. J Clin Neurosci 21:18661871, 2014

    • Search Google Scholar
    • Export Citation
  • 8

    Chen CJ, Ding D, Wang TR, Buell TJ, Ilyas A, Ironside N, : Microsurgery versus stereotactic radiosurgery for brain arteriovenous malformations: a matched cohort study. Neurosurgery [epub ahead of print], 2018

    • Search Google Scholar
    • Export Citation
  • 9

    Cheng CH, Crowley RW, Yen CP, Schlesinger D, Shaffrey ME, Sheehan JP: Gamma Knife surgery for basal ganglia and thalamic arteriovenous malformations. J Neurosurg 116:899908, 2012

    • Search Google Scholar
    • Export Citation
  • 10

    Cohen-Inbar O, Ding D, Sheehan JP: Stereotactic radiosurgery for deep intracranial arteriovenous malformations, part 2: Basal ganglia and thalamus arteriovenous malformations. J Clin Neurosci 24:3742, 2016

    • Search Google Scholar
    • Export Citation
  • 11

    Ding D, Liu KC: Predictive capability of the Spetzler-Martin versus Supplementary Grading Scale for microsurgical outcomes of cerebellar arteriovenous malformations. J Cerebrovasc Endovasc Neurosurg 15:307310, 2013

    • Search Google Scholar
    • Export Citation
  • 12

    Ding D, Starke RM, Kano H, Lee JY, Mathieu D, Pierce J, : Stereotactic radiosurgery for Spetzler-Martin Grade III arteriovenous malformations: an international multicenter study. J Neurosurg 126:859871, 2017

    • Search Google Scholar
    • Export Citation
  • 13

    Ding D, Starke RM, Kano H, Lee JYK, Mathieu D, Pierce J, : Radiosurgery for unruptured brain arteriovenous malformations: an international multicenter retrospective cohort study. Neurosurgery 80:888898, 2017

    • Search Google Scholar
    • Export Citation
  • 14

    Ding D, Starke RM, Kano H, Mathieu D, Huang P, Kondziolka D, : Radiosurgery for cerebral arteriovenous malformations in A Randomized Trial of Unruptured Brain Arteriovenous Malformations (ARUBA)–eligible patients: a multicenter study. Stroke 47:342349, 2016

    • Search Google Scholar
    • Export Citation
  • 15

    Ding D, Starke RM, Sheehan JP: Radiosurgery for the management of cerebral arteriovenous malformations. Handb Clin Neurol 143:6983, 2017

    • Search Google Scholar
    • Export Citation
  • 16

    Fleetwood IG, Marcellus ML, Levy RP, Marks MP, Steinberg GK: Deep arteriovenous malformations of the basal ganglia and thalamus: natural history. J Neurosurg 98:747750, 2003

    • Search Google Scholar
    • Export Citation
  • 17

    Flickinger JC, Pollock BE, Kondziolka D, Lunsford LD: A dose-response analysis of arteriovenous malformation obliteration after radiosurgery. Int J Radiat Oncol Biol Phys 36:873879, 1996

    • Search Google Scholar
    • Export Citation
  • 18

    Gross BA, Duckworth EA, Getch CC, Bendok BR, Batjer HH: Challenging traditional beliefs: microsurgery for arteriovenous malformations of the basal ganglia and thalamus. Neurosurgery 63:393411, 2008

    • Search Google Scholar
    • Export Citation
  • 19

    Hartmann A, Mast H, Mohr JP, Koennecke HC, Osipov A, Pile-Spellman J, : Morbidity of intracranial hemorrhage in patients with cerebral arteriovenous malformation. Stroke 29:931934, 1998

    • Search Google Scholar
    • Export Citation
  • 20

    Hong CS, Peterson EC, Ding D, Sur S, Hasan D, Dumont AS, : Intervention for a randomized trial of unruptured brain arteriovenous malformations (ARUBA)–eligible patients: an evidence-based review. Clin Neurol Neurosurg 150:133138, 2016

    • Search Google Scholar
    • Export Citation
  • 21

    Kano H, Kondziolka D, Flickinger JC, Yang HC, Flannery TJ, Niranjan A, : Stereotactic radiosurgery for arteriovenous malformations, Part 4: management of basal ganglia and thalamus arteriovenous malformations. J Neurosurg 116:3343, 2012

    • Search Google Scholar
    • Export Citation
  • 22

    Koga T, Shin M, Maruyama K, Terahara A, Saito N: Long-term outcomes of stereotactic radiosurgery for arteriovenous malformations in the thalamus. Neurosurgery 67:398403, 2010

    • Search Google Scholar
    • Export Citation
  • 23

    Lawton MT, Hamilton MG, Spetzler RF: Multimodality treatment of deep arteriovenous malformations: thalamus, basal ganglia, and brain stem. Neurosurgery 37:2936, 1995

    • Search Google Scholar
    • Export Citation
  • 24

    Lee CC, Reardon MA, Ball BZ, Chen CJ, Yen CP, Xu Z, : The predictive value of magnetic resonance imaging in evaluating intracranial arteriovenous malformation obliteration after stereotactic radiosurgery. J Neurosurg 123:136144, 2015

    • Search Google Scholar
    • Export Citation
  • 25

    Mohr JP, Parides MK, Stapf C, Moquete E, Moy CS, Overbey JR, : Medical management with or without interventional therapy for unruptured brain arteriovenous malformations (ARUBA): a multicentre, non-blinded, randomised trial. Lancet 383:614621, 2014

    • Search Google Scholar
    • Export Citation
  • 26

    O’Connor TE, Friedman WA: Magnetic resonance imaging assessment of cerebral arteriovenous malformation obliteration after stereotactic radiosurgery. Neurosurgery 73:761766, 2013

    • Search Google Scholar
    • Export Citation
  • 27

    Oermann EK, Ding D, Yen CP, Starke RM, Bederson JB, Kondziolka D, : Effect of prior embolization on cerebral arteriovenous malformation radiosurgery outcomes: a case-control study. Neurosurgery 77:406417, 2015

    • Search Google Scholar
    • Export Citation
  • 28

    Oermann EK, Rubinsteyn A, Ding D, Mascitelli J, Starke RM, Bederson JB, : Using a machine learning approach to predict outcomes after radiosurgery for cerebral arteriovenous malformations. Sci Rep 6:21161, 2016

    • Search Google Scholar
    • Export Citation
  • 29

    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
  • 30

    Patibandla MR, Ding D, Kano H, Xu Z, Lee JYK, Mathieu D, : Stereotactic radiosurgery for Spetzler-Martin Grade IV and V arteriovenous malformations: an international multicenter study. J Neurosurg 129:498507, 2018

    • Search Google Scholar
    • Export Citation
  • 31

    Pollock BE, Gorman DA, Brown PD: Radiosurgery for arteriovenous malformations of the basal ganglia, thalamus, and brainstem. J Neurosurg 100:210214, 2004

    • Search Google Scholar
    • Export Citation
  • 32

    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
  • 33

    Rubin DB: Multiple Imputation for Nonresponse in Surveys. New York: Wiley, 1987

  • 34

    Russell D, Peck T, Ding D, Chen CJ, Taylor DG, Starke RM, : Stereotactic radiosurgery alone or combined with embolization for brain arteriovenous malformations: a systematic review and meta-analysis. J Neurosurg 128:13381348, 2018

    • Search Google Scholar
    • Export Citation
  • 35

    Sasaki T, Kurita H, Saito I, Kawamoto S, Nemoto S, Terahara A, : Arteriovenous malformations in the basal ganglia and thalamus: management and results in 101 cases. J Neurosurg 88:285292, 1998

    • Search Google Scholar
    • Export Citation
  • 36

    Shimizu T, Miyamoto A: Progesterone induces the expression of vascular endothelial growth factor (VEGF) 120 and Flk-1, its receptor, in bovine granulosa cells. Anim Reprod Sci 102:228237, 2007

    • Search Google Scholar
    • Export Citation
  • 37

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

  • 38

    Spetzler RF, Ponce FA: A 3-tier classification of cerebral arteriovenous malformations. Clinical article. J Neurosurg 114:842849, 2011

    • Search Google Scholar
    • Export Citation
  • 39

    Stapf C, Mast H, Sciacca RR, Choi JH, Khaw AV, Connolly ES, : Predictors of hemorrhage in patients with untreated brain arteriovenous malformation. Neurology 66:13501355, 2006

    • Search Google Scholar
    • Export Citation
  • 40

    Starke RM, Kano H, Ding D, Lee JY, Mathieu D, Whitesell J, : 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
  • 41

    Starke RM, Sheehan JP, Ding D, Liu KC, Kondziolka D, Crowley RW, : Conservative management or intervention for unruptured brain arteriovenous malformations. World Neurosurg 82:e668e669, 2014

    • Search Google Scholar
    • Export Citation
  • 42

    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. J Neurosurg 119:981987, 2013

    • Search Google Scholar
    • Export Citation
  • 43

    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
  • 44

    Tew JM Jr, Lewis AI, Reichert KW: Management strategies and surgical techniques for deep-seated supratentorial arteriovenous malformations. Neurosurgery 36:10651072, 1995

    • Search Google Scholar
    • Export Citation
  • 45

    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
  • 46

    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

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