Advertisement

Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Modern radiosurgical and endovascular classification schemes for brain arteriovenous malformations

Abstract

Stereotactic radiosurgery (SRS) and endovascular techniques are commonly used for treating brain arteriovenous malformations (bAVMs). They are usually used as ancillary techniques to microsurgery but may also be used as solitary treatment options. Careful patient selection requires a clear estimate of the treatment efficacy and complication rates for the individual patient. As such, classification schemes are an essential part of patient selection paradigm for each treatment modality. While the Spetzler-Martin grading system and its subsequent modifications are commonly used for microsurgical outcome prediction for bAVMs, the same system(s) may not be easily applicable to SRS and endovascular therapy. Several radiosurgical- and endovascular-based grading scales have been proposed for bAVMs. However, a comprehensive review of these systems including a discussion on their relative advantages and disadvantages is missing. This paper is dedicated to modern classification schemes designed for SRS and endovascular techniques.

This is a preview of subscription content, log in to check access.

References

  1. 1.

    Andrade-Souza YM, Zadeh G, Ramani M, Scora D, Tsao MN, Schwartz ML (2005) Testing the radiosurgery-based arteriovenous malformation score and the modified Spetzler-Martin grading system to predict radiosurgical outcome. J Neurosurg 103:642–648. https://doi.org/10.3171/jns.2005.103.4.0642

  2. 2.

    Andrade-Souza YM, Zadeh G, Scora D, Tsao MN, Schwartz ML (2005) Radiosurgery for basal ganglia, internal capsule, and thalamus arteriovenous malformation: clinical outcome. Neurosurgery 56:56–63 discussion 63-54

  3. 3.

    Bell DL, Leslie-Mazwi TM, Yoo AJ, Rabinov JD, Butler WE, Bell JE, Hirsch JA (2015) Application of a novel brain arteriovenous malformation endovascular grading scale for transarterial embolization. AJNR Am J Neuroradiol 36:1303–1309. https://doi.org/10.3174/ajnr.A4286

  4. 4.

    Bollet MA, Anxionnat R, Buchheit I, Bey P, Cordebar A, Jay N, Desandes E, Marchal C, Lapeyre M, Aletti P, Picard L (2004) Efficacy and morbidity of arc-therapy radiosurgery for cerebral arteriovenous malformations: a comparison with the natural history. Int J Radiat Oncol Biol Phys 58:1353–1363. https://doi.org/10.1016/j.ijrobp.2003.09.005

  5. 5.

    Cohen-Gadol AA, Pollock BE (2006) Radiosurgery for arteriovenous malformations in children. J Neurosurg 104:388–391. https://doi.org/10.3171/ped.2006.104.6.388

  6. 6.

    Cohen-Inbar O, Ding D, Sheehan JP (2016) Stereotactic radiosurgery for deep intracranial arteriovenous malformations, part 2: basal ganglia and thalamus arteriovenous malformations. J Clin Neurosci 24:37–42. https://doi.org/10.1016/j.jocn.2015.11.006

  7. 7.

    Consoli A, Renieri L, Nappini S, Limbucci N, Mangiafico S (2013) Endovascular treatment of deep hemorrhagic brain arteriovenous malformations with transvenous onyx embolization. AJNR Am J Neuroradiol 34:1805–1811. https://doi.org/10.3174/ajnr.A3497

  8. 8.

    Crowley RW, Ducruet AF, Kalani MY, Kim LJ, Albuquerque FC, McDougall CG (2015) Neurological morbidity and mortality associated with the endovascular treatment of cerebral arteriovenous malformations before and during the Onyx era. J Neurosurg 122:1492–1497. https://doi.org/10.3171/2015.2.JNS131368

  9. 9.

    Ding D, Yen CP, Starke RM, Xu Z, Sun X, Sheehan JP (2014) Radiosurgery for Spetzler-Martin grade III arteriovenous malformations. J Neurosurg 120:959–969. https://doi.org/10.3171/2013.12.JNS131041

  10. 10.

    Ding D, Yen CP, Xu Z, Starke RM, Sheehan JP (2014) Radiosurgery for low-grade intracranial arteriovenous malformations. J Neurosurg 121:457–467. https://doi.org/10.3171/2014.1.JNS131713

  11. 11.

    Dumont TM, Kan P, Snyder KV, Hopkins LN, Siddiqui AH, Levy EI (2015) A proposed grading system for endovascular treatment of cerebral arteriovenous malformations: Buffalo score. Surg Neurol Int 6:3. https://doi.org/10.4103/2152-7806.148847

  12. 12.

    Elsenousi A, Aletich VA, Alaraj A (2016) Neurological outcomes and cure rates of embolization of brain arteriovenous malformations with n-butyl cyanoacrylate or Onyx: a meta-analysis. J Neurointerv Surg 8:265–272. https://doi.org/10.1136/neurintsurg-2014-011427

  13. 13.

    Feliciano CE, de León-Berra R, Hernández-Gaitán MS, Rodríguez-Mercado R (2010) A proposal for a new arteriovenous malformation grading scale for neuroendovascular procedures and literature review. P R Health Sci J 29:117–120

  14. 14.

    Firlik AD, Levy EI, Kondziolka D, Yonas H (1998) Staged volume radiosurgery followed by microsurgical resection: a novel treatment for giant cerebral arteriovenous malformations: technical case report. Neurosurgery 43:1223–1228

  15. 15.

    Flickinger JC, Kondziolka D, Lunsford LD, Kassam A, Phuong LK, Liscak R, Pollock B (2000) Development of a model to predict permanent symptomatic postradiosurgery injury for arteriovenous malformation patients. Arteriovenous Malformation Radiosurgery Study Group. Int J Radiat Oncol Biol Phys 46:1143–1148

  16. 16.

    Flickinger JC, Kondziolka D, Lunsford LD, Pollock BE, Yamamoto M, Gorman DA, Schomberg PJ, Sneed P, Larson D, Smith V, McDermott MW, Miyawaki L, Chilton J, Morantz RA, Young B, Jokura H, Liscak R (1999) A multi-institutional analysis of complication outcomes after arteriovenous malformation radiosurgery. Int J Radiat Oncol Biol Phys 44:67–74

  17. 17.

    Flickinger JC, Pollock BE, Kondziolka D, Lunsford LD (1996) A dose-response analysis of arteriovenous malformation obliteration after radiosurgery. Int J Radiat Oncol Biol Phys 36:873–879

  18. 18.

    Fournier D, TerBrugge KG, Willinsky R, Lasjaunias P, Montanera W (1991) Endovascular treatment of intracerebral arteriovenous malformations: experience in 49 cases. J Neurosurg 75:228–233. https://doi.org/10.3171/jns.1991.75.2.0228

  19. 19.

    Friedman WA, Blatt DL, Bova FJ, Buatti JM, Mendenhall WM, Kubilis PS (1996) The risk of hemorrhage after radiosurgery for arteriovenous malformations. J Neurosurg 84:912–919. https://doi.org/10.3171/jns.1996.84.6.0912

  20. 20.

    Friedman WA, Bova FJ, Bollampally S, Bradshaw P (2003) Analysis of factors predictive of success or complications in arteriovenous malformation radiosurgery. Neurosurgery 52:296–307 discussion 307-298

  21. 21.

    Gobin YP, Laurent A, Merienne L, Schlienger M, Aymard A, Houdart E, Casasco A, Lefkopoulos D, George B, Merland JJ (1996) Treatment of brain arteriovenous malformations by embolization and radiosurgery. J Neurosurg 85:19–28. https://doi.org/10.3171/jns.1996.85.1.0019

  22. 22.

    Gupta R, Adeeb N, Moore JM, Motiei-Langroudi R, Griessenauer CJ, Patel AS, Ogilvy CS, Thomas AJ (2016) Validity assessment of grading scales predicting complications from embolization of cerebral arteriovenous malformations. Clin Neurol Neurosurg 151:102–107. https://doi.org/10.1016/j.clineuro.2016.10.019

  23. 23.

    Hartmann A, Mast H, Mohr JP, Pile-Spellman J, Connolly ES, Sciacca RR, Khaw A, Stapf C (2005) Determinants of staged endovascular and surgical treatment outcome of brain arteriovenous malformations. Stroke 36:2431–2435. https://doi.org/10.1161/01.STR.0000185723.98111.75

  24. 24.

    Hartmann A, Pile-Spellman J, Stapf C, Sciacca RR, Faulstich A, Mohr JP, Schumacher HC, Mast H (2002) Risk of endovascular treatment of brain arteriovenous malformations. Stroke 33:1816–1820

  25. 25.

    Hattangadi-Gluth JA, Chapman PH, Kim D, Niemierko A, Bussière MR, Stringham A, Daartz J, Ogilvy C, Loeffler JS, Shih HA (2014) Single-fraction proton beam stereotactic radiosurgery for cerebral arteriovenous malformations. Int J Radiat Oncol Biol Phys 89:338–346. https://doi.org/10.1016/j.ijrobp.2014.02.030

  26. 26.

    Haw CS, terBrugge K, Willinsky R, Tomlinson G (2006) Complications of embolization of arteriovenous malformations of the brain. J Neurosurg 104:226–232. https://doi.org/10.3171/jns.2006.104.2.226

  27. 27.

    Iosif C, Mendes GA, Saleme S, Ponomarjova S, Silveira EP, Caire F, Mounayer C (2015) Endovascular transvenous cure for ruptured brain arteriovenous malformations in complex cases with high Spetzler-Martin grades. J Neurosurg 122:1229–1238. https://doi.org/10.3171/2014.9.JNS141714

  28. 28.

    Jin H, Jiang Y, Ge H, Luo J, Li C, Wu H, Li Y (2017) Comparison of grading scales regarding perioperative complications and clinical outcomes of brain arteriovenous malformations after endovascular therapy-multicenter study. World Neurosurg 106:394–401. https://doi.org/10.1016/j.wneu.2017.07.020

  29. 29.

    Jordan JA, Llibre JC, Vazquez F, Rodríguez RM (2014) Predictors of total obliteration in endovascular treatment of cerebral arteriovenous malformations. Neuroradiol J 27:108–114. https://doi.org/10.15274/NRJ-2014-10013

  30. 30.

    Karlsson B, Lax I, Söderman M (2001) Risk for hemorrhage during the 2-year latency period following gamma knife radiosurgery for arteriovenous malformations. Int J Radiat Oncol Biol Phys 49:1045–1051

  31. 31.

    Karlsson B, Lindquist C, Steiner L (1997) Prediction of obliteration after gamma knife surgery for cerebral arteriovenous malformations. Neurosurgery 40:425–430 discussion 430-421

  32. 32.

    Kim LJ, Albuquerque FC, Spetzler RF, McDougall CG (2006) Postembolization neurological deficits in cerebral arteriovenous malformations: stratification by arteriovenous malformation grade. Neurosurgery 59:53–59; discussion 53-59. https://doi.org/10.1227/01.NEU.0000219219.97287.91

  33. 33.

    Kjellberg RN, Hanamura T, Davis KR, Lyons SL, Adams RD (1983) Bragg-peak proton-beam therapy for arteriovenous malformations of the brain. N Engl J Med 309:269–274. https://doi.org/10.1056/NEJM198308043090503

  34. 34.

    Lawton MT, Kim H, McCulloch CE, Mikhak B, Young WL (2010) A supplementary grading scale for selecting patients with brain arteriovenous malformations for surgery. Neurosurgery 66:702–713; discussion 713. https://doi.org/10.1227/01.NEU.0000367555.16733.E1

  35. 35.

    Lax I, Karlsson B (1996) Prediction of complications in gamma knife radiosurgery of arteriovenous malformation. Acta Oncol 35:49–55

  36. 36.

    Ledezma CJ, Hoh BL, Carter BS, Pryor JC, Putman CM, Ogilvy CS (2006) Complications of cerebral arteriovenous malformation embolization: multivariate analysis of predictive factors. Neurosurgery 58:602–611; discussion 602-611. https://doi.org/10.1227/01.NEU.0000204103.91793.77

  37. 37.

    Liscák R, Vladyka V, Simonová G, Urgosík D, Novotný J, Janousková L, Vymazal J (2007) Arteriovenous malformations after Leksell gamma knife radiosurgery: rate of obliteration and complications. Neurosurgery 60:1005–1014; discussion 1015-1006. https://doi.org/10.1227/01.NEU.0000255474.60505.4A

  38. 38.

    Lopes DK, Moftakhar R, Straus D, Munich SA, Chaus F, Kaszuba MC (2016) Arteriovenous malformation embocure score: AVMES. J Neurointerv Surg 8:685–691. https://doi.org/10.1136/neurintsurg-2015-011779

  39. 39.

    Lunsford LD, Kondziolka D, Flickinger JC, Bissonette DJ, Jungreis CA, Maitz AH, Horton JA, Coffey RJ (1991) Stereotactic radiosurgery for arteriovenous malformations of the brain. J Neurosurg 75:512–524. https://doi.org/10.3171/jns.1991.75.4.0512

  40. 40.

    Maruyama K, Kondziolka D, Niranjan A, Flickinger JC, Lunsford LD (2004) Stereotactic radiosurgery for brainstem arteriovenous malformations: factors affecting outcome. J Neurosurg 100:407–413. https://doi.org/10.3171/jns.2004.100.3.0407

  41. 41.

    Mavroidis P, Theodorou K, Lefkopoulos D, Nataf F, Schlienger M, Karlsson B, Lax I, Kappas C, Lind BK, Brahme A (2002) Prediction of AVM obliteration after stereotactic radiotherapy using radiobiological modelling. Phys Med Biol 47:2471–2494

  42. 42.

    Meder JF, Oppenheim C, Blustajn J, Nataf F, Merienne L, Lefkoupolos D, Laurent A, Merland JJ, Schlienger M, Fredy D (1997) Cerebral arteriovenous malformations: the value of radiologic parameters in predicting response to radiosurgery. AJNR Am J Neuroradiol 18:1473–1483

  43. 43.

    Milker-Zabel S, Kopp-Schneider A, Wiesbauer H, Schlegel W, Huber P, Debus J, Zabel-du Bois A (2012) Proposal for a new prognostic score for linac-based radiosurgery in cerebral arteriovenous malformations. Int J Radiat Oncol Biol Phys 83:525–532. https://doi.org/10.1016/j.ijrobp.2011.07.008

  44. 44.

    Nataf F, Ghossoub M, Schlienger M, Moussa R, Meder JF, Roux FX (2004) Bleeding after radiosurgery for cerebral arteriovenous malformations. Neurosurgery 55:298–305 discussion 305-296

  45. 45.

    Ogilvy CS, Stieg PE, Awad I, Brown RD, Kondziolka D, Rosenwasser R, Young WL, Hademenos G, Special Writing Group of the Stroke Council AeSA (2001) AHA scientific statement: recommendations for the management of intracranial arteriovenous malformations: a statement for healthcare professionals from a special writing group of the Stroke Council, American Stroke Association. Stroke 32:1458–1471

  46. 46.

    Pollock B, Flickinger J, Lunsford L, Maitz A, Kondziolka D (1997) The Pittsburgh arteriovenous malformation radiosurgery (PAR) grading scale. In: Kondziolka D (ed) Radiosurgery, vol 2. Karger, Radiosurgery, Basel, pp 137–146

  47. 47.

    Pollock BE, Flickinger JC (2002) A proposed radiosurgery-based grading system for arteriovenous malformations. J Neurosurg 96:79–85. https://doi.org/10.3171/jns.2002.96.1.0079

  48. 48.

    Pollock BE, Flickinger JC (2008) Modification of the radiosurgery-based arteriovenous malformation grading system. Neurosurgery 63:239–243; discussion 243. https://doi.org/10.1227/01.NEU.0000315861.24920.92

  49. 49.

    Pollock BE, Flickinger JC, Lunsford LD, Bissonette DJ, Kondziolka D (1996) Hemorrhage risk after stereotactic radiosurgery of cerebral arteriovenous malformations. Neurosurgery 38:652–659 discussion 659-661

  50. 50.

    Pollock BE, Flickinger JC, Lunsford LD, Maitz A, Kondziolka D (1998) Factors associated with successful arteriovenous malformation radiosurgery. Neurosurgery 42:1239–1244 discussion 1244-1237

  51. 51.

    Pollock BE, Gorman DA, Brown PD (2004) Radiosurgery for arteriovenous malformations of the basal ganglia, thalamus, and brainstem. J Neurosurg 100:210–214. https://doi.org/10.3171/jns.2004.100.2.0210

  52. 52.

    Pollock BE, Gorman DA, Coffey RJ (2003) Patient outcomes after arteriovenous malformation radiosurgical management: results based on a 5- to 14-year follow-up study. Neurosurgery 52:1291–1296 discussion 1296-1297

  53. 53.

    Pollock BE, Kondziolka D, Lunsford LD, Bissonette D, Flickinger JC (1996) Repeat stereotactic radiosurgery of arteriovenous malformations: factors associated with incomplete obliteration. Neurosurgery 38:318–324

  54. 54.

    Pollock BE, Lunsford LD, Kondziolka D, Maitz A, Flickinger JC (1994) Patient outcomes after stereotactic radiosurgery for “operable” arteriovenous malformations. Neurosurgery 35:1–7 discussion 7-8

  55. 55.

    Pollock BE, Storlie CB, Link MJ, Stafford SL, Garces YI, Foote RL (2017) Comparative analysis of arteriovenous malformation grading scales in predicting outcomes after stereotactic radiosurgery. J Neurosurg 126:852–858. https://doi.org/10.3171/2015.11.JNS151300

  56. 56.

    Raffa SJ, Chi YY, Bova FJ, Friedman WA (2009) Validation of the radiosurgery-based arteriovenous malformation score in a large linear accelerator radiosurgery experience. J Neurosurg 111:832–839. https://doi.org/10.3171/2009.4.JNS081532

  57. 57.

    Robert T, Blanc R, Sylvestre P, Ciccio G, Smajda S, Botta D, Redjem H, Fahed R, Piotin M (2017) A proposed grading system to evaluate the endovascular curability of deep-seated arteriovenous malformations. J Neurol Sci 377:212–218. https://doi.org/10.1016/j.jns.2017.04.020

  58. 58.

    Schaller C, Schramm J (1997) Microsurgical results for small arteriovenous malformations accessible for radiosurgical or embolization treatment. Neurosurgery 40:664–672 discussion 672-664

  59. 59.

    Schwartz M, Sixel K, Young C, Kemeny A, Forster D, Walton L, Franssen E (1997) Prediction of obliteration of arteriovenous malformations after radiosurgery: the obliteration prediction index. Can J Neurol Sci 24:106–109

  60. 60.

    Seifert V, Stolke D, Mehdorn HM, Hoffmann B (1994) Clinical and radiological evaluation of long-term results of stereotactic proton beam radiosurgery in patients with cerebral arteriovenous malformations. J Neurosurg 81:683–689. https://doi.org/10.3171/jns.1994.81.5.0683

  61. 61.

    Sheikh B, Nakahara I, El-Naggar A, Nagata I, Kikuchi H (2000) A grading system for intracranial arteriovenous malformations applicable to endovascular procedures. Interv Neuroradiol 6(Suppl 1):139–142. https://doi.org/10.1177/15910199000060S120

  62. 62.

    Shin M, Maruyama K, Kurita H, Kawamoto S, Tago M, Terahara A, Morita A, Ueki K, Takakura K, Kirino T (2004) 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 101:18–24. https://doi.org/10.3171/jns.2004.101.1.0018

  63. 63.

    Silander H, Pellettieri L, Enblad P, Montelius A, Grusell E, Vallhagen-Dahlgren C, Isacsson U, Nyberg G, Moström U, Lilja A, Gál G, Blomquist E (2004) Fractionated, stereotactic proton beam treatment of cerebral arteriovenous malformations. Acta Neurol Scand 109:85–90

  64. 64.

    Spetzler RF, Martin NA (1986) A proposed grading system for arteriovenous malformations. J Neurosurg 65:476–483. https://doi.org/10.3171/jns.1986.65.4.0476

  65. 65.

    Spetzler RF, Ponce FA (2011) A 3-tier classification of cerebral arteriovenous malformations. Clinical article. J Neurosurg 114:842–849. https://doi.org/10.3171/2010.8.JNS10663

  66. 66.

    Starke RM, Komotar RJ, Hwang BY, Fischer LE, Otten ML, Merkow MB, Garrett MC, Isaacson SR, Connolly ES (2008) A comprehensive review of radiosurgery for cerebral arteriovenous malformations: outcomes, predictive factors, and grading scales. Stereotact Funct Neurosurg 86:191–199. https://doi.org/10.1159/000126945

  67. 67.

    Starke RM, Yen CP, Ding D, Sheehan JP (2013) A practical grading scale for predicting outcome after radiosurgery for arteriovenous malformations: analysis of 1012 treated patients. J Neurosurg 119:981–987. https://doi.org/10.3171/2013.5.JNS1311

  68. 68.

    Vernimmen FJ, Slabbert JP, Wilson JA, Fredericks S, Melvill R (2005) Stereotactic proton beam therapy for intracranial arteriovenous malformations. Int J Radiat Oncol Biol Phys 62:44–52. https://doi.org/10.1016/j.ijrobp.2004.09.008

  69. 69.

    Viñuela F, Duckwiler G, Guglielmi G (1995) Intravascular embolization of cerebral arteriovenous malformations. In: Maciunas R (ed) Endovascular Neurological Intervention. American Association of Neurological Surgeons, Park Ridge, pp 189–199

  70. 70.

    Wegner RE, Oysul K, Pollock BE, Sirin S, Kondziolka D, Niranjan A, Lunsford LD, Flickinger JC (2011) A modified radiosurgery-based arteriovenous malformation grading scale and its correlation with outcomes. Int J Radiat Oncol Biol Phys 79:1147–1150. https://doi.org/10.1016/j.ijrobp.2009.12.056

  71. 71.

    Willinsky R, Goyal M, Terbrugge K, Montanera W, Wallace MC, Tymianski M (2001) Embolisation of small (< 3 cm) brain arteriovenous malformations. Correlation of angiographic results to a proposed angioarchitecture grading system. Interv Neuroradiol 7:19–27. https://doi.org/10.1177/159101990100700102

  72. 72.

    Yamamoto M, Jimbo M, Hara M, Saito I, Mori K (1996) Gamma knife radiosurgery for arteriovenous malformations: long-term follow-up results focusing on complications occurring more than 5 years after irradiation. Neurosurgery 38:906–914

  73. 73.

    Yu SC, Chan MS, Lam JM, Tam PH, Poon WS (2004) Complete obliteration of intracranial arteriovenous malformation with endovascular cyanoacrylate embolization: initial success and rate of permanent cure. AJNR Am J Neuroradiol 25:1139–1143

  74. 74.

    Zabel-du Bois A, Milker-Zabel S, Huber P, Schlegel W, Debus J (2006) Pediatric cerebral arteriovenous malformations: the role of stereotactic linac-based radiosurgery. Int J Radiat Oncol Biol Phys 65:1206–1211. https://doi.org/10.1016/j.ijrobp.2006.01.041

  75. 75.

    Zabel-du Bois A, Milker-Zabel S, Huber P, Schlegel W, Debus J (2006) Stereotactic linac-based radiosurgery in the treatment of cerebral arteriovenous malformations located deep, involving corpus callosum, motor cortex, or brainstem. Int J Radiat Oncol Biol Phys 64:1044–1048. https://doi.org/10.1016/j.ijrobp.2005.09.024

Download references

Author information

Correspondence to Michael T. Lawton.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

Not applicable—our study did not require IRB approval as it did not involve any human/animal subjects.

Informed consent

Not applicable—our study did not involve any human individual subjects.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Tayebi Meybodi, A., Lawton, M.T. Modern radiosurgical and endovascular classification schemes for brain arteriovenous malformations. Neurosurg Rev 43, 49–58 (2020). https://doi.org/10.1007/s10143-018-0983-8

Download citation

Keywords

  • Radiosurgery
  • Embolization
  • Grading system
  • Outcome prediction
  • Pollock-Flickinger