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Benefits from Exclusion Treatment of Unruptured Brain Arteriovenous Malformations on Epilepsy in Adults

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Abstract

Purpose

In approximately 30% of the patients, brain arteriovenous malformations (bAVMs) are revealed by seizures, which may alter the patients’ quality of life. Our objective was to evaluate the benefits of exclusion treatment (radiosurgery, embolization and/or surgery) on posttherapeutic epilepsy in bAVM patients without intracranial hemorrhage prior to treatment.

Methods

Our retrospective observational single-center study included all consecutive adult patients with an unruptured bAVM and epilepsy, treated at our institution from 1995 to 2019 and who were followed for at least 1 year. Data on angioarchitectural characteristics of bAVMs, on epilepsy and posttreatment modified Rankin Scale (mRS) were collected. The primary endpoint was a seizure-free status (defined as Engel class IA) after exclusion treatment versus conservative management.

Results

In this study one hundred and one consecutive adult patients with bAVMs, epilepsy and without bAVM rupture before any treatment were included; 21 (21%) in the conservative management group vs. 80 (79%) in the exclusion treatment group. After exclusion treatment, 55% of the patients from the group were Engel IA after treatment vs. 10% of the conservative management group (odds ratio [OR] 11.37, 95% confidence interval [CI] 2.48–107.24, p < 0.001).

Conclusion

Our results suggest that exclusion treatment in unruptured bAVMs with epilepsy is associated with a higher seizure-free rate in comparison with conservative management. Data from randomized controlled studies are necessary to confirm these findings.

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Abbreviations

AED:

Antiepileptic drug

bAVM:

Brain arteriovenous malformations

DSA:

Digital subtraction angiography

EVE:

Endovascular embolization

mRS:

modified Rankin Scale

SRS:

Stereotaxic radiosurgery

TCGS:

Tonic-clonic generalized seizures

References

  1. ApSimon HT, Reef H, Phadke RV, Popovic EA. A population-based study of brain arteriovenous malformation: long-term treatment outcomes. Stroke. 2002;33:2794–800.

    Article  CAS  PubMed  Google Scholar 

  2. Al-Shahi R, Bhattacharya JJ, Currie DG, Papanastassiou V, Ritchie V, Roberts RC, Sellar RJ, Warlow CP; Scottish Intracranial Vascular Malformation Study Collaborators. Prospective, population-based detection of intracranial vascular malformations in adults: the Scottish Intracranial Vascular Malformation Study (SIVMS). Stroke. 2003;34:1163–9.

    Article  PubMed  Google Scholar 

  3. Al-Shahi R, Warlow C. A systematic review of the frequency and prognosis of arteriovenous malformations of the brain in adults. Brain. 2001;124:1900–26.

    Article  CAS  Google Scholar 

  4. Kim H, Su H, Weinsheimer S, Pawlikowska L, Young WL. Brain arteriovenous malformation pathogenesis: a response-to-injury paradigm. Acta Neurochir Suppl. 2011;111:83–92.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Hofmeister C, Stapf C, Hartmann A, Sciacca RR, Mansmann U, terBrugge K, Lasjaunias P, Mohr JP, Mast H, Meisel J. Demographic, morphological, and clinical characteristics of 1289 patients with brain arteriovenous malformation. Stroke. 2000;31:1307–10.

    Article  CAS  PubMed  Google Scholar 

  6. Crawford PM, West CR, Shaw MD, Chadwick DW. Cerebral arteriovenous malformations and epilepsy: factors in the development of epilepsy. Epilepsia. 1986;27:270–5.

    Article  CAS  PubMed  Google Scholar 

  7. Kraemer DL, Awad IA. Vascular malformations and epilepsy: clinical considerations and basic mechanisms. Epilepsia. 1994;35 Suppl 6:S30–43.

    Article  PubMed  Google Scholar 

  8. Fierstra J, Conklin J, Krings T, Slessarev M, Han JS, Fisher JA, Terbrugge K, Wallace MC, Tymianski M, Mikulis DJ. Impaired peri-nidal cerebrovascular reserve in seizure patients with brain arteriovenous malformations. Brain. 2011;134:100–9.

    Article  Google Scholar 

  9. McCormick W. Pathology of vascular malformations of the brain. In: Wilson C, Stein B, editors. Intracranial arter malform. Baltimore: Williams & Wilkins; 1984. pp. 44–63.

    Google Scholar 

  10. Bishop M, Allen CA. The impact of epilepsy on quality of life: a qualitative analysis. Epilepsy Behav. 2003;4:226–33.

    Article  PubMed  Google Scholar 

  11. Trinka E, Bauer G, Oberaigner W, Ndayisaba JP, Seppi K, Granbichler CA. Cause-specific mortality among patients with epilepsy: results from a 30-year cohort study. Epilepsia. 2013;54:495–501.

    Article  PubMed  Google Scholar 

  12. Josephson CB, Sauro K, Wiebe S, Clement F, Jette N. Medical vs. invasive therapy in AVM-related epilepsy: Systematic review and meta-analysis. Neurology. 2016;86:64–71.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Englot DJ, Young WL, Han SJ, McCulloch CE, Chang EF, Lawton MT. Seizure predictors and control after microsurgical resection of supratentorial arteriovenous malformations in 440 patients. Neurosurgery. 2012;71:572–80; discussion 580.

    Article  PubMed  Google Scholar 

  14. Korosue. Complications of complete surgical resection of AVMs of the brain. In: Barrow DL, editor. Intracranial vasc malform. Park Ridge: American Association of Neurological Surgeons; 1990. pp. 157–68.

    Google Scholar 

  15. Ditty BJ, Omar NB, Foreman PM, Miller JH, Kicielinski KP, Fisher WS 3rd, Harrigan MR. Seizure outcomes after stereotactic radiosurgery for the treatment of cerebral arteriovenous malformations. J Neurosurg. 2017;126:845–51.

    Article  PubMed  Google Scholar 

  16. Thorpe ML, Cordato DJ, Morgan MK, Herkes GK. Postoperative seizure outcome in a series of 114 patients with supratentorial arteriovenous malformations. J Clin Neurosci. 2000;7:107–11.

    Article  CAS  PubMed  Google Scholar 

  17. Heikkinen ER, Konnov B, Melnikov L, Yalynych N, Zubkov YuN, Garmashov YuA, Pak VA. Relief of epilepsy by radiosurgery of cerebral arteriovenous malformations. Stereotact Funct Neurosurg. 1989;53:157–66.

    Article  CAS  PubMed  Google Scholar 

  18. Schäuble B, Cascino GD, Pollock BE, Gorman DA, Weigand S, Cohen-Gadol AA, McClelland RL. Seizure outcomes after stereotactic radiosurgery for cerebral arteriovenous malformations. Neurology. 2004;63:683–7.

    Article  PubMed  Google Scholar 

  19. Ferlisi M, Zanoni T, Moretto G, Pasqualin A. Seizures and Brain Arterovenous Malformation: A Surgical Series. Acta Neurochir Suppl. 2016;123:147–51.

    Article  CAS  PubMed  Google Scholar 

  20. de Los Reyes K, Patel A, Doshi A, Egorova N, Panov F, Bederson JB, Frontera JA. Seizures after Onyx embolization for the treatment of cerebral arteriovenous malformation. Interv Neuroradiol. 2011;17:331–8.

    Article  Google Scholar 

  21. Josephson CB, Bhattacharya JJ, Counsell CE, Papanastassiou V, Ritchie V, Roberts R, Sellar R, Warlow CP, Al-Shahi Salman R; Scottish Audit of Intracranial Vascular Malformations (SAIVMs) steering committee and collaborators. Seizure risk with AVM treatment or conservative management: prospective, population-based study. Neurology. 2012;79:500–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Murphy MJ. Long-term follow-up of seizures associated with cerebral arteriovenous malformations. Results of therapy. Arch Neurol. 1985;42:477–9.

    Article  CAS  PubMed  Google Scholar 

  23. Mohr JP, Parides MK, Stapf C, Moquete E, Moy CS, Overbey JR, Al-Shahi Salman R, Vicaut E, Young WL, Houdart E, Cordonnier C, Stefani MA, Hartmann A, von Kummer R, Biondi A, Berkefeld J, Klijn CJ, Harkness K, Libman R, Barreau X, Moskowitz AJ; international ARUBA investigators. Medical management with or without interventional therapy for unruptured brain arteriovenous malformations (ARUBA): a multicentre, non-blinded, randomised trial. Lancet. 2014;383:614–21.

    Article  CAS  PubMed  Google Scholar 

  24. Vandenbroucke JP, von Elm E, Altman DG, Gøtzsche PC, Mulrow CD, Pocock SJ, Poole C, Schlesselman JJ, Egger M; STROBE Initiative. Strengthening the Reporting of Observational Studies in Epidemiology (STROBE): explanation and elaboration. Epidemiology. 2007;18:805–35.

    Article  PubMed  Google Scholar 

  25. Spetzler RF, Martin NA. A proposed grading system for arteriovenous malformations. J Neurosurg. 1986;65:476–83.

    Article  CAS  PubMed  Google Scholar 

  26. Rankin J. Cerebral vascular accidents in patients over the age of 60. II. Prognosis. Scott Med J. 1957;2:200–15.

    Article  CAS  PubMed  Google Scholar 

  27. Bonita R, Beaglehole R. Recovery of motor function after stroke. Stroke. 1988;19:1497–500.

    Article  CAS  PubMed  Google Scholar 

  28. Fisher RS, Cross JH, D’Souza C, French JA, Haut SR, Higurashi N, Hirsch E, Jansen FE, Lagae L, Moshé SL, Peltola J, Roulet Perez E, Scheffer IE, Schulze-Bonhage A, Somerville E, Sperling M, Yacubian EM, Zuberi SM. Instruction manual for the ILAE 2017 operational classification of seizure types. Epilepsia. 2017;58:531–42.

    Article  PubMed  Google Scholar 

  29. Jr Engel J, Van Ness P, Rasmussen T, Ojemann L. Outcome with respect to epileptic seizures. In: Jr Engel J, editor. Surg treat epilepsies. 2nd ed. New York: Raven Press; 1993. pp. 609–21.

    Google Scholar 

  30. Ding D, Quigg M, Starke RM, Yen CP, Przybylowski CJ, Dodson BK, Sheehan JP. Cerebral Arteriovenous Malformations and Epilepsy, Part 2: Predictors of Seizure Outcomes Following Radiosurgery. World Neurosurg. 2015;84:653–62.

    Article  PubMed  Google Scholar 

  31. Ironside N, Chen CJ, Ding D, Ilyas A, Kumar JS, Buell TJ, Taylor D, Lee CC, Sheehan JP. Seizure Outcomes After Radiosurgery for Cerebral Arteriovenous Malformations: An Updated Systematic Review and Meta-Analysis. World Neurosurg. 2018;120:550–62.e3.

    Article  PubMed  Google Scholar 

  32. Baranoski JF, Grant RA, Hirsch LJ, Visintainer P, Gerrard JL, Günel M, Matouk CC, Spencer DD, Bulsara KR. Seizure control for intracranial arteriovenous malformations is directly related to treatment modality: a meta-analysis. J Neurointerv Surg. 2014;6:684–90.

    Article  PubMed  Google Scholar 

  33. Chen CJ, Chivukula S, Ding D, Starke RM, Lee CC, Yen CP, Xu Z, Sheehan JP. Seizure outcomes following radiosurgery for cerebral arteriovenous malformations. Neurosurg Focus. 2014;37:E17.

    Article  PubMed  Google Scholar 

  34. Zhang B, Feng X, Peng F, Wang L, Guo EK, Zhang Y, Liu P, Wu Z, Liu A. Seizure predictors and outcome after Onyx embolization in patients with brain arteriovenous malformations. Interv Neuroradiol. 2019;25:124–31.

    Article  PubMed  Google Scholar 

  35. Hoh BL, Chapman PH, Loeffler JS, Carter BS, Ogilvy CS. Results of multimodality treatment for 141 patients with brain arteriovenous malformations and seizures: factors associated with seizure incidence and seizure outcomes. Neurosurgery. 2002;51:303–9; discussion 309–11.

    Article  PubMed  Google Scholar 

  36. Yang SY, Kim DG, Chung HT, Paek SH. Radiosurgery for unruptured cerebral arteriovenous malformations: long-term seizure outcome. Neurology. 2012;78:1292–8.

    Article  PubMed  Google Scholar 

  37. Eisenschenk S, Gilmore RL, Friedman WA, Henchey RA. The effect of LINAC stereotactic radiosurgery on epilepsy associated with arteriovenous malformations. Stereotact Funct Neurosurg. 1998;71:51–61.

    Article  CAS  PubMed  Google Scholar 

  38. Kurita H, Kawamoto S, Suzuki I, Sasaki T, Tago M, Terahara A, Kirino T. Control of epilepsy associated with cerebral arteriovenous malformations after radiosurgery. J Neurol Neurosurg Psychiatry. 1998;65:648–55.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Rossi GF, Scerrati M, Roselli R. Epileptogenic cerebral low-grade tumors: effect of interstitial stereotactic irradiation on seizures. Appl Neurophysiol. 1985;48:127–32.

    CAS  PubMed  Google Scholar 

  40. Tolliver JM, Pellmar TC. Ionizing radiation alters neuronal excitability in hippocampal slices of the guinea pig. Radiat Res. 1987;112:555–63.

    Article  CAS  PubMed  Google Scholar 

  41. Arnaout OM, Gross BA, Eddleman CS, Bendok BR, Getch CC, Batjer HH. Posterior fossa arteriovenous malformations. Neurosurg Focus. 2009;26:E12.

    Article  PubMed  Google Scholar 

  42. Niranjan A, Kashkoush A, Kano H, Monaco EA, Flickinger JC, Lunsford LD. Seizure control after radiosurgery for cerebral arteriovenous malformations: a 25-year experience. J Neurosurg. 2018;131:1763–72.

    Article  PubMed  Google Scholar 

  43. Hyun SJ, Kong DS, Lee JI, Kim JS, Hong SC. Cerebral arteriovenous malformations and seizures: differential impact on the time to seizure-free state according to the treatment modalities. Acta Neurochir (Wien). 2012;154:1003–10.

    Article  PubMed  Google Scholar 

  44. Fisher RS, Acevedo C, Arzimanoglou A, Bogacz A, Cross JH, Elger CE, Engel J Jr, Forsgren L, French JA, Glynn M, Hesdorffer DC, Lee BI, Mathern GW, Moshé SL, Perucca E, Scheffer IE, Tomson T, Watanabe M, Wiebe S. ILAE official report: a practical clinical definition of epilepsy. Epilepsia. 2014;55:475–82.

    Article  PubMed  Google Scholar 

  45. Ledezma CJ, Hoh BL, Carter BS, Pryor JC, Putman CM, Ogilvy CS. Complications of cerebral arteriovenous malformation embolization: multivariate analysis of predictive factors. Neurosurgery. 2006;58:602–11; discussion 602–11.

    Article  PubMed  Google Scholar 

  46. Sato K, Matsumoto Y, Tominaga T, Satow T, Iihara K, Sakai N; Japanese Registry of Neuroendovascular Therapy Investigators. Complications of Endovascular Treatments for Brain Arteriovenous Malformations: A Nationwide Surveillance. AJNR Am J Neuroradiol. 2020;41:669–75.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Correspondence to Frédéric Clarençon.

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Conflict of interest

R. Capocci, M. Bustuchina Vlaicu, E. Shotar, B. Mathon, M. Delaitre, K. Premat, M. Talaat, A. Talbi, A.-L. Boch, S. Lenck, A. Carpentier and V. Degos report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper. The manuscript is not supported by industry. N.A. Sourour is consultant for Medtronic, Balt Extrusion, Microvention. F. Clarençon reports conflict of interest with Medtronic, Guerbet, Balt Extrusion, Penumbra (payment for readings; non-related to the study), Codman Neurovascular and Microvention (core laboratory; non-related to the study).

Ethical standards

The data were anonymized and retrospectively collected. This retrospective study was performed after consultation with the institutional ethics committee and in accordance with national legal requirements. The study was approved by the local ethics committee and validated by the National Commission of Informatics and Liberty.

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Availability of Data and Material

Data collected for the study are available and include individual participant data that underlie the results reported in this article, after de-identification (tables). The availability will begin 9 months and end 36 months following article publication (proposals may be submitted up to 36 months following article publication). The data access will be given to investigators whose proposed use of the data has been approved by an independent review committee (“learned intermediary”) identified for this purpose, exclusively for individual participant data meta-analysis, upon request directed to the corresponding author; to gain access, data requestors will need to sign a data access agreement.

The authors Michaela Bustuchina Vlaicu and Eimad Shotar contributed equally to the manuscript.

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Capocci, R., Bustuchina Vlaicu, M., Shotar, E. et al. Benefits from Exclusion Treatment of Unruptured Brain Arteriovenous Malformations on Epilepsy in Adults. Clin Neuroradiol 32, 749–760 (2022). https://doi.org/10.1007/s00062-021-01119-w

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