Stereotactic Radiosurgery With vs. Without Prior Embolization for Brain Arteriovenous Malformations: A Propensity Score Matching Analysis

Debin Yan, Yu Chen, Zhipeng Li, Haibin Zhang, Ruinan Li, Kexin Yuan, Heze Han, Xiangyu Meng, Hengwei Jin, Dezhi Gao, Youxiang Li, Shibin Sun, Ali Liu, Xiaolin Chen, Yuanli Zhao, Debin Yan, Yu Chen, Zhipeng Li, Haibin Zhang, Ruinan Li, Kexin Yuan, Heze Han, Xiangyu Meng, Hengwei Jin, Dezhi Gao, Youxiang Li, Shibin Sun, Ali Liu, Xiaolin Chen, Yuanli Zhao

Abstract

Objective: Whether partial embolization could facilitate the post-stereotactic radiosurgery (SRS) obliteration for brain arteriovenous malformations (bAVMs) remains controversial. We performed this study to compare the outcomes of SRS with and without prior embolization for bAVMs. Methods: We retrospectively reviewed the Beijing Tiantan AVMs prospective registration research database from September 2011 to October 2014. Patients were categorized into two groups, combined upfront embolization and SRS (Em+SRS group) and SRS alone (SRS group), and we performed a propensity score matching analysis based on pre-embolization baseline characteristics; the matched groups each comprised 76 patients. Results: The obliteration rate was similar between SRS and Em+SRS (44.7 vs. 31.6%; OR, 1.754; 95% CI, 0.905-3.401; p = 0.096). However, the SRS group was superior to the Em+SRS group in terms of cumulative obliteration rate at a follow-up of 5 years (HR,1.778; 95% CI, 1.017-3.110; p = 0.033). The secondary outcomes, including functional state, post-SRS hemorrhage, all-cause mortality, and edema or cyst formation were similar between the matched cohorts. In the ruptured subgroup, the SRS group could achieve higher obliteration rate than Em+SRS group (56.5 vs. 31.9%; OR, 2.773; 95% CI, 1.190-6.464; p = 0.018). The cumulative obliteration rate at 5 years was also higher in the SRS group (64.5 vs. 41.3%; HR, 2.012; 95% CI, 1.037-3.903; p = 0.038), and the secondary outcomes were also similar between the matched cohorts. Conclusion: Although there was no significant difference in the overall obliteration rate between the two strategies, this study suggested that pre-SRS embolization may have a negative effect on post-SRS obliteration. Furthermore, the obliteration rates of the SRS only strategy was significantly higher than that of the Em+SRS strategy in the ruptured cohort, while no such phenomenon was found in the unruptured cohort.

Keywords: brain arteriovenous malformation; hemorrhage; obliteration; partial embolization; stereotactic radiosurgery.

Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Copyright © 2021 Yan, Chen, Li, Zhang, Li, Yuan, Han, Meng, Jin, Gao, Li, Sun, Liu, Chen and Zhao.

Figures

Figure 1
Figure 1
Patient flowchart demonstrating patient selection and propensity score matching (PSM) process. AVM, arteriovenous malformation; SRS, stereotactic radiosurgery; Em+SRS, prior embolization to stereotactic radiosurgery.
Figure 2
Figure 2
Comparisons of cumulative incidence between SRS and Em+SRS. (A) AVM obliteration. (B) Survival. (C) Post-SRS hemorrhage. (D) Post-SRS complication. AVM, arteriovenous malformation; Em+SRS, embolization + stereotactic radiosurgery. p′-Value refers to the result of a 5-year follow-up.
Figure 3
Figure 3
Comparisons of cumulative incidence in ruptured subgroup between SRS and Em+SRS. (A) AVM obliteration. (C) Post-SRS hemorrhage. Comparisons of cumulative incidence in the unruptured subgroup between SRS and Em+SRS: (B) AVM obliteration. (D) Post-SRS hemorrhage. AVM, arteriovenous malformation; Em+SRS, embolization + stereotactic radiosurgery. p′-Value refers to the result of a 5-year follow-up.

References

    1. Russell D, Peck T, Ding D, Chen C, Taylor D, Starke R, et al. . Stereotactic radiosurgery alone or combined with embolization for brain arteriovenous malformations: a systematic review and meta-analysis. J Neurosurg. (2018) 128:1338–48. 10.3171/2016.11.Jns162382
    1. Daou B, Palmateer G, Thompson B, Maher C, Hayman J, Lam K, et al. . Stereotactic radiosurgery for brain arteriovenous malformations: evaluation of obliteration and review of associated predictors. J Stroke Cerebrovasc Dis. (2020) 29:104863. 10.1016/j.jstrokecerebrovasdis.2020.104863
    1. Knippen S, Putz F, Semrau S, Lambrecht U, Knippen A, Buchfelder M, et al. . Predictors for occlusion of cerebral AVMs following radiation therapy: radiation dose and prior embolization, but not Spetzler-Martin grade. Strahlenther OnkolOrgan Deutschen Rontgengesellschaft. (2017) 193:185–91. 10.1007/s00066-016-1056-y
    1. Kano H, Kondziolka D, Flickinger J, Yang H, Park K, Flannery T, et al. . Aneurysms increase the risk of rebleeding after stereotactic radiosurgery for hemorrhagic arteriovenous malformations. Stroke. (2012) 43:2586–91. 10.1161/STROKEAHA.112.664045
    1. Solomon R, Connolly E. Arteriovenous malformations of the brain. N Engl J Med. (2017) 376:1859–66. 10.1056/NEJMra1607407
    1. Joint Writing Group of the Technology Assessment Committee American Society of I, Therapeutic N, Joint Section on Cerebrovascular Neurosurgery a Section of the American Association of Neurological S, Congress of Neurological S, Section of S, the Section of Interventional Neurology of the American Academy of N et al. . Reporting terminology for brain arteriovenous malformation clinical and radiographic features for use in clinical trials. Stroke. (2001) 32:1430–42. 10.1161/01.STR.32.6.1430
    1. Divani AA, Majidi S, Luo X, Souslian FG, Zhang J, Abosch A, et al. . The ABCs of accurate volumetric measurement of cerebral hematoma. Stroke. (2011) 42:1569–74. 10.1161/STROKEAHA.110.607861
    1. Pollock BE, Flickinger JC, Lunsford LD, Maitz A, Kondziolka D. Factors associated with successful arteriovenous malformation radiosurgery. Neurosurgery. (1998) 42:1239–44; discussion 44–7. 10.1097/00006123-199806000-00020
    1. Spetzler RF, Martin NA. A proposed grading system for arteriovenous malformations. J Neurosurg. (1986) 65:476–83. 10.3171/jns.1986.65.4.0476
    1. 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. (2013) 119:981–7. 10.3171/2013.5.JNS1311
    1. Chen C, Ding D, Lee C, Kearns K, Pomeraniec I, Cifarelli C, et al. . Stereotactic radiosurgery with versus without embolization for brain arteriovenous malformations. Neurosurgery. (2021) 88:313–21. 10.1093/neuros/nyaa418
    1. Dalyai R, Theofanis T, Starke R, Chalouhi N, Ghobrial G, Jabbour P, et al. . Stereotactic radiosurgery with neoadjuvant embolization of larger arteriovenous malformations: an institutional experience. Biomed Res Int. (2014) 2014:306518. 10.1155/2014/306518
    1. Hodgson T, Kemeny A, Gholkar A, Deasy N. Embolization of residual fistula following stereotactic radiosurgery in cerebral arteriovenous malformations. AJNR. (2009) 30:109–10. 10.3174/ajnr.A1240
    1. Huo X, Jiang Y, Lv X, Yang H, Zhao Y, Li Y. Gamma Knife surgical treatment for partially embolized cerebral arteriovenous malformations. J Neurosurg. (2016) 124:767–76. 10.3171/2015.1.JNS142711
    1. Ding D, Sheehan J, Starke R, Durst C, Raper D, Conger J, et al. . Embolization of cerebral arteriovenous malformations with silk suture particles prior to stereotactic radiosurgery. J Clin Neurosci. (2015) 22:1643–9. 10.1016/j.jocn.2015.03.046
    1. Derdeyn C, Zipfel G, Albuquerque F, Cooke D, Feldmann E, Sheehan J, et al. . Management of brain arteriovenous malformations: a scientific statement for healthcare professionals from the American Heart Association/American Stroke Association. Stroke. (2017) 48:e200–24. 10.1161/STR.0000000000000134
    1. Peciu-Florianu I, Leroy HA, Drumez E, Dumot C, Aboukais R, Touzet G, et al. . Radiosurgery for unruptured brain arteriovenous malformations in the pre-ARUBA era: long-term obliteration rate, risk of hemorrhage and functional outcomes. Sci Rep. (2020) 10:21427. 10.1038/s41598-020-78547-0
    1. Meng X, He H, Liu P, Gao D, Chen Y, Sun S, et al. . Radiosurgery-based AVM scale is proposed for combined embolization and gamma knife surgery for brain arteriovenous malformations. Front Neurol. (2021) 12:647167. 10.3389/fneur.2021.647167
    1. Chen C, Kearns K, Ding D, Kano H, Mathieu D, Kondziolka D, et al. . Stereotactic radiosurgery for arteriovenous malformations of the basal ganglia and thalamus: an international multicenter study. J Neurosurg. (2019) 132:122–31. 10.3171/2018.8.JNS182106
    1. Shtraus N, Schifter D, Corn B, Maimon S, Alani S, Frolov V, et al. . Radiosurgical treatment planning of AVM following embolization with Onyx: possible dosage error in treatment planning can be averted. J Neurooncol. (2010) 98:271–6. 10.1007/s11060-010-0177-x
    1. Andrade-Souza Y, Ramani M, Beachey D, Scora D, Tsao M, Terbrugge K, et al. . Liquid embolisation material reduces the delivered radiation dose: a physical experiment. Acta Neurochirurgica. (2008) 150:161–4; discussion 4. 10.1007/s00701-007-1482-9
    1. Buell T, Ding D, Starke R, Webster Crowley R, Liu K. Embolization-induced angiogenesis in cerebral arteriovenous malformations. J Clin Neurosci. (2014) 21:1866–71. 10.1016/j.jocn.2014.04.010
    1. Akakin A, Ozkan A, Akgun E, Koc D, Konya D, Pamir M, et al. . Endovascular treatment increases but gamma knife radiosurgery decreases angiogenic activity of arteriovenous malformations: an in vivo experimental study using a rat cornea model. Neurosurgery. (2010) 66:121–9; discussion 9–30. 10.1227/01.NEU.0000363154.88768.34
    1. Gross B, Du R. Natural history of cerebral arteriovenous malformations: a meta-analysis. J Neurosurg. (2013) 118:437–43. 10.3171/2012.10.JNS121280
    1. Kim H, Al-Shahi Salman R, McCulloch C, Stapf C, Young W. Untreated brain arteriovenous malformation: patient-level meta-analysis of hemorrhage predictors. Neurology. (2014) 83:590–7. 10.1212/WNL.0000000000000688
    1. Kano H, Flickinger J, Tonetti D, Hsu A, Yang H, Flannery T, et al. . Estimating the risks of adverse radiation effects after gamma knife radiosurgery for arteriovenous malformations. Stroke. (2017) 48:84–90. 10.1161/STROKEAHA.116.014825
    1. Ilyas A, Chen C, Ding D, Buell T, Raper D, Lee C, et al. . Radiation-induced changes after stereotactic radiosurgery for brain arteriovenous malformations: a systematic review and meta-analysis. Neurosurgery. (2018) 83:365–76. 10.1093/neuros/nyx502
    1. Chen C, Lee C, Ding D, Tzeng S, Kearns K, Kano H, et al. . Stereotactic radiosurgery for unruptured versus ruptured pediatric brain arteriovenous malformations. Stroke. (2019) 50:2745–51. 10.1161/STROKEAHA.119.026211
    1. Shin M, Maruyama K, Kurita H, Kawamoto S, Tago M, Terahara A, et al. . Analysis of nidus obliteration rates after gamma knife surgery for arteriovenous malformations based on long-term follow-up data: the University of Tokyo experience. J Neurosurg. (2004) 101:18–24. 10.3171/jns.2004.101.1.0018
    1. Liew J, Yang W, Mashouf L, Li S, Caplan J, Tamargo R, et al. . Incidence of spontaneous obliteration in untreated brain arteriovenous malformations. Neurosurgery. (2020) 86:139–49. 10.1093/neuros/nyz047
    1. Szeifert G, Kemeny A, Timperley W, Forster D. The potential role of myofibroblasts in the obliteration of arteriovenous malformations after radiosurgery. Neurosurgery. (1997) 40:61–5; discussion 5–6. 10.1227/00006123-199701000-00013
    1. Burkhardt JK, Chen X, Winkler EA, Cooke DL, Kim H, Lawton MT. Delayed venous drainage in ruptured arteriovenous malformations based on quantitative color-coded digital subtraction angiography. World Neurosurg. (2017) 104:619–27. 10.1016/j.wneu.2017.04.120
    1. Chen X, Cooke DL, Saloner D, Nelson J, Su H, Lawton MT, et al. . Higher flow is present in unruptured arteriovenous malformations with silent intralesional microhemorrhages. Stroke. (2017) 48:2881–4. 10.1161/STROKEAHA.117.017785
    1. Lin TM, Yang HC, Lee CC, Wu HM, Hu YS, Luo CB, et al. . Stasis index from hemodynamic analysis using quantitative DSA correlates with hemorrhage of supratentorial arteriovenous malformation: a cross-sectional study. J Neurosurg. (2019) 132:1574–82. 10.3171/2019.1.JNS183386
    1. Hu YS, Lee CC, Wu HM, Yang HC, Lin TM, Luo CB, et al. . Stagnant venous outflow predicts brain arteriovenous malformation obliteration after gamma knife radiosurgery without prior intervention. Neurosurgery. (2020) 87:338–47. 10.1093/neuros/nyz507
    1. Rivera R, Sordo J, Echeverria D, Badilla L, Pinto C, Merino-Osorio C. Quantitative evaluation of arteriovenous malformation hemodynamic changes after endovascular treatment using parametric color coding: a case series study. Interv Neuroradiol. (2017) 23:650–5. 10.1177/1591019917721867

Source: PubMed

3
Se inscrever