Skip to main content

Advertisement

Log in

Single-stage planning for total cure of grade III–V brain arteriovenous malformations by embolization alone or in combination with microsurgical resection

  • Interventional Neuroradiology
  • Published:
Neuroradiology Aims and scope Submit manuscript

Abstract

Purpose

There are no established guidelines for treatment of Spetzler–Martin grade III–V brain arteriovenous malformations (bAVMs). The purpose of this study is to report our institutional experience in total obliteration/eradication of grade III–V bAVMs by single-stage planning of embolization combined with microsurgical resection when necessary.

Methods

All patients harboring Spetzler–Martin (S–M) grade III–V bAVMs treated with single-stage planning between January 2006 and January 2018 were retrospectively reviewed. This treatment paradigm is applicable only to surgically accessible bAVMs and does not include deep-seated bAVMs. Indications for treatment, clinical presentation, imaging characteristics, and treatment outcomes were analyzed. Outcomes were assessed based on modified Rankin Scale.

Results

A total of 31 patients were identified. Seventeen patients (54.8%) presented with hemorrhage, 10 (32.3%) with seizures, 3 (9.7%) with headaches, and 1 (3.2%) with progressive neurological deficit. Based on S–M grading system, 25 patients (80.6%) harbored grade III bAVM, 5 patients had grade IV bAVMs (16.1%), and 1 patient (3.2%) had a grade V bAVM. There were no treatment-related complications in 24/31 (77.4%) patients. Of the total of seven patients with complications, four patients had clinical deterioration. The long-term (> 6-month), non-disabling morbidity (mRS ≤ 2) rate was 6.5%. The long-term, disabling morbidity rate was 3.2% with a mortality of 3.2%. Complete angiographic obliteration was achieved in 30/31 (96.8%) patients.

Conclusion

Single-stage treatment strategy can be considered as an alternative to multistage embolization prior to surgery in grade III–V bAVMs. In this study, a high rate of total obliteration with relatively low rates of permanent morbidity and mortality was achieved.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Choi JH, Mohr JP (2005) Brain arteriovenous malformations in adults. Lancet Neurol 4:299–308

    Article  PubMed  Google Scholar 

  2. Friedlander RM (2007) Clinical practice. Arteriovenous malformations of the brain. N Engl J Med 356:2704–2712

    Article  CAS  PubMed  Google Scholar 

  3. Derdeyn CP, Zipfel GJ, Albuquerque FC, Cooke DL, Feldmann E, Sheehan JP, Torner JC, American Heart Association Stroke Council (2017) Management of brain arteriovenous malformations: a scientific statement for healthcare professionals from the American Heart Association/American Stroke Association. Stroke 48:e200–e224

    PubMed  Google Scholar 

  4. Mast H, Mohr JP, Osipov A, Pile-Spellman J, Marshall RS, Lazar RM, Stein BM, Young WL (1995) ‘Steal’ is an unestablished mechanism for the clinical presentation of cerebral arteriovenous malformations. Stroke 26:1215–1220

    Article  CAS  PubMed  Google Scholar 

  5. Itoyama Y, Uemura S, Ushio Y, Kuratsu J, Nonaka N, Wada H, Sano Y, Fukumura A, Yoshida K, Yano T (1989) Natural course of unoperated intracranial arteriovenous malformations: study of 50 cases. J Neurosurg 71:805–809

    Article  CAS  PubMed  Google Scholar 

  6. Ondra SL, Troupp H, George ED, Schwab K (1990) The natural history of symptomatic arteriovenous malformations of the brain: a 24-year follow-up assessment. J Neurosurg 73:387–391

    Article  CAS  PubMed  Google Scholar 

  7. Gross BA, Du R (2013) Natural history of cerebral arteriovenous malformations: a meta-analysis. J Neurosurg 118:437–443

    Article  PubMed  Google Scholar 

  8. Hernesniemi JA, Dashti R, Juvela S, Vaart K, Niemela M, Laakso A (2008) Natural history of brain arteriovenous malformations: a long-term follow-up study of risk of hemorrhage in 238 patients. Neurosurgery 63:823–829

    Article  PubMed  Google Scholar 

  9. Lv X, Wu Z, Jiang C, Yang X, Li Y, Sun Y, Zhang N (2011) Angioarchitectural characteristics of brain arteriovenous malformations with and without hemorrhage. World Neurosurg 76:95–99

    Article  PubMed  Google Scholar 

  10. Kim H, Al-Shahi Salman R, McCulloch CE, Stapf C, Young WL (2014) Untreated brain arteriovenous malformation: patient-level meta-analysis of hemorrhage predictors. Neurology 83:590–597

    Article  PubMed  PubMed Central  Google Scholar 

  11. Abad JM, Alvarez F, Manrique M, Garcia-Blazquez M (1983) Cerebral arteriovenous malformations. Comparative results of surgical vs conservative treatment in 112 cases. J Neurosurg Sci 27:203–210

    CAS  PubMed  Google Scholar 

  12. ApSimon HT, Reef H, Phadke RV, Popovic EA (2002) A population-based study of brain arteriovenous malformation: long-term treatment outcomes. Stroke 33:2794–2800

    Article  CAS  PubMed  Google Scholar 

  13. Crawford PM, West CR, Chadwick DW, Shaw MD (1986) Arteriovenous malformations of the brain: natural history in unoperated patients. J Neurol Neurosurg Psychiatry 49:1–10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Forster DM, Steiner L, Hakanson S (1972) Arteriovenous malformations of the brain. A long-term clinical study. J Neurosurg 37:562–570

    Article  CAS  PubMed  Google Scholar 

  15. 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 (2014) Medical management with or without interventional therapy for unruptured brain arteriovenous malformations (ARUBA): a multicentre, non-blinded, randomised trial. Lancet 383:614–621

    Article  CAS  PubMed  Google Scholar 

  16. Josephson CB, Leach JP, Duncan R, Roberts RC, Counsell CE, Al-Shahi Salman R (2011) Seizure risk from cavernous or arteriovenous malformations: prospective population-based study. Neurology 76:1548–1554

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Morgan MK, Davidson AS, Assaad NNA, Stoodley MA (2017) Critical review of brain AVM surgery, surgical results and natural history in 2017. Acta Neurochir 159:1457–1478

    Article  PubMed  Google Scholar 

  18. Saatci I, Geyik S, Yavuz K, Cekirge HS (2011) Endovascular treatment of brain arteriovenous malformations with prolonged intranidal Onyx injection technique: long-term results in 350 consecutive patients with completed endovascular treatment course. J Neurosurg 115:78–88

    Article  PubMed  Google Scholar 

  19. Xu F, Zhong J, Ray A, Manjila S, Bambakidis NC (2014) Stereotactic radiosurgery with and without embolization for intracranial arteriovenous malformations: a systematic review and meta-analysis. Neurosurg Focus 37:E16

    Article  PubMed  Google Scholar 

  20. Laakso A, Dashti R, Juvela S, Isarakul P, Niemela M, Hernesniemi J (2011) Risk of hemorrhage in patients with untreated Spetzler-Martin grade IV and V arteriovenous malformations: a long-term follow-up study in 63 patients. Neurosurgery 68:372–377

    Article  PubMed  Google Scholar 

  21. Han PP, Ponce FA, Spetzler RF (2003) Intention-to-treat analysis of Spetzler-Martin grades IV and V arteriovenous malformations: natural history and treatment paradigm. J Neurosurg 98:3–7

    Article  PubMed  Google Scholar 

  22. Spetzler RF, Ponce FA (2011) A 3-tier classification of cerebral arteriovenous malformations. Clin Artic J Neurosurg 114:842–849

    Article  Google Scholar 

  23. Kalani MY, Albuquerque FC, Fiorella D, McDougall CG (2013) Endovascular treatment of cerebral arteriovenous malformations. Neuroimaging Clin N Am 23:605–624

    Article  PubMed  Google Scholar 

  24. Lv X, Wu Z, Li Y, Yang X, Jiang C (2012) Hemorrhage risk after partial endovascular NBCA and ONYX embolization for brain arteriovenous malformation. Neurol Res 34:552–556

    Article  CAS  PubMed  Google Scholar 

  25. Laakso A, Dashti R, Seppanen J, Juvela S, Vaart K, Niemela M et al (2008) Long-term excess mortality in 623 patients with brain arteriovenous malformations. Neurosurgery 63:244–253

    Article  PubMed  Google Scholar 

  26. Spetzler RF, Martin NA (1986) A proposed grading system for arteriovenous malformations. J Neurosurg 65:476–483

    Article  CAS  PubMed  Google Scholar 

  27. 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

    Article  PubMed  PubMed Central  Google Scholar 

  28. Potts MB, Lau D, Abla AA, Kim H, Young WL, Lawton MT (2015) Current surgical results with low-grade brain arteriovenous malformations. J Neurosurg 122:912–920

    Article  PubMed  PubMed Central  Google Scholar 

  29. Theofanis T, Chalouhi N, Dalyai R, Starke RM, Jabbour P, Rosenwasser RH et al (2014) Microsurgery for cerebral arteriovenous malformations: postoperative outcomes and predictors of complications in 264 cases. Neurosurg Focus 37:E10

    Article  PubMed  Google Scholar 

  30. Teo MK, Young AM, St George EJ (2016) Comparative surgical outcome associated with the management of brain arteriovenous malformation in a regional neurosurgical centre. Br J Neurosurg 30:623–630

    Article  PubMed  Google Scholar 

  31. Korja M, Bervini D, Assaad N, Morgan MK (2014) Role of surgery in the management of brain arteriovenous malformations: prospective cohort study. Stroke 45:3549–3555

    Article  PubMed  Google Scholar 

  32. Lawton MT (2003) Spetzler-Martin Grade III arteriovenous malformations: surgical results and a modification of the grading scale. Neurosurgery 52:740–748

    Article  PubMed  Google Scholar 

  33. Pandey P, Marks MP, Harraher CD, Westbroek EM, Chang SD, Do HM, Levy RP, Dodd RL, Steinberg GK (2012) Multimodality management of Spetzler-Martin Grade III arteriovenous malformations. J Neurosurg 116:1279–1288

    Article  PubMed  Google Scholar 

  34. de Oliveira E, Tedeschi H, Raso J (1998) Comprehensive management of arteriovenous malformations. Neurol Res 20:673–683

    Article  PubMed  Google Scholar 

  35. Crowley RW, Ducruet AF, McDougall CG, Albuquerque FC (2014) Endovascular advances for brain arteriovenous malformations. Neurosurgery 74:S74–S82

    Article  PubMed  Google Scholar 

  36. Durst CR, Starke RM, Gaughen J, Evans AJ (2015) A method for complete angiographic obliteration of a brain arteriovenous malformation in a single session through a single pedicle. J Clin Neurosci 22:391–395

    Article  PubMed  Google Scholar 

  37. Spiotta AM, Miranpuri AS, Vargas J, Magarick J, Turner RD, Turk AS, Chaudry MI (2014) Balloon augmented Onyx embolization utilizing a dual lumen balloon catheter: utility in the treatment of a variety of head and neck lesions. J Neurointerv Surg 6:547–555

    Article  PubMed  Google Scholar 

  38. 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

    Article  PubMed  Google Scholar 

  39. Katsaridis V, Papagiannaki C, Aimar E (2008) Curative embolization of cerebral arteriovenous malformations (AVMs) with Onyx in 101 patients. Neuroradiology 50:589–597

    Article  PubMed  Google Scholar 

  40. Pierot L, Cognard C, Herbreteau D, Fransen H, van Rooij WJ, Boccardi E, Beltramello A, Sourour N, Kupcs K, Biondi A, Bonafé A, Reith W, Casasco A (2013) Endovascular treatment of brain arteriovenous malformations using a liquid embolic agent: results of a prospective, multicentre study (BRAVO). Eur Radiol 23:2838–2845

    Article  CAS  PubMed  Google Scholar 

  41. Richling B, Killer M, Al-Schameri AR, Ritter L, Agic R, Krenn M (2006) Therapy of brain arteriovenous malformations: multimodality treatment from a balanced standpoint. Neurosurgery 59:S148–S157

    PubMed  Google Scholar 

  42. Natarajan SK, Ghodke B, Britz GW, Born DE, Sekhar LN (2008) Multimodality treatment of brain arteriovenous malformations with microsurgery after embolization with onyx: single-center experience and technical nuances. Neurosurgery 62:1213–1225

    Article  PubMed  Google Scholar 

  43. Rodriguez-Boto G, Gutierrez-Gonzalez R, Gil A, Serna C, Lopez-Ibor L (2013) Combined staged therapy of complex arteriovenous malformations: initial experience. Acta Neurol Scand 127:260–267

    Article  CAS  PubMed  Google Scholar 

  44. Flores BC, Klinger DR, Rickert KL, Barnett SL, Welch BG, White JA et al (2014) Management of intracranial aneurysms associated with arteriovenous malformations. Neurosurg Focus 37:E11

    Article  PubMed  Google Scholar 

  45. Potts MB, Zumofen DW, Raz E, Nelson PK, Riina HA (2014) Curing arteriovenous malformations using embolization. Neurosurg Focus 37:E19

    Article  PubMed  Google Scholar 

  46. Mounayer C, Hammami N, Piotin M, Spelle L, Benndorf G, Kessler I, Moret J (2007) Nidal embolization of brain arteriovenous malformations using Onyx in 94 patients. AJNR Am J Neuroradiol 28:518–523

    CAS  PubMed  Google Scholar 

  47. Spetzler RF, Martin NA, Carter LP, Flom RA, Raudzens PA, Wilkinson E (1987) Surgical management of large AVM’s by staged embolization and operative excision. J Neurosurg 67:17–28

    Article  CAS  PubMed  Google Scholar 

  48. Fiorella D, Albuquerque FC, Woo HH, McDougall CG, Rasmussen PA (2006) The role of neuroendovascular therapy for the treatment of brain arteriovenous malformations. Neurosurgery 59:S163–S177

    PubMed  Google Scholar 

  49. 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

    Article  CAS  PubMed  Google Scholar 

  50. 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

    Article  CAS  PubMed  Google Scholar 

  51. Bradac O, Charvat F, Benes V (2013) Treatment for brain arteriovenous malformation in the 1998-2011 period and review of the literature. Acta Neurochir 155:199–209

    Article  PubMed  Google Scholar 

  52. Luksik AS, Law J, Yang W, Garzon-Muvdi T, Caplan JM, Colby G, Coon AL, Tamargo RJ, Huang J (2017) Assessing the role of preoperative embolization in the surgical management of cerebral arteriovenous malformations. World Neurosurg 104:430–441

    Article  PubMed  Google Scholar 

  53. Morgan MK, Sundt TM Jr (1989) The case against staged operative resection of cerebral arteriovenous malformations. Neurosurgery 25:429–435

    Article  CAS  PubMed  Google Scholar 

  54. Panagiotopoulos V, Gizewski E, Asgari S, Regel J, Forsting M, Wanke I (2009) Embolization of intracranial arteriovenous malformations with ethylene-vinyl alcohol copolymer (Onyx). AJNR Am J Neuroradiol 30:99–106

    Article  CAS  PubMed  Google Scholar 

  55. Xu F, Ni W, Liao Y, Gu Y, Xu B, Leng B, Song D (2011) Onyx embolization for the treatment of brain arteriovenous malformations. Acta Neurochir 153:869–878

    Article  PubMed  Google Scholar 

  56. van Rooij WJ, Jacobs S, Sluzewski M, van der Pol B, Beute GN, Sprengers ME (2012) Curative embolization of brain arteriovenous malformations with onyx: patient selection, embolization technique, and results. AJNR Am J Neuroradiol 33:1299–1304

    Article  PubMed  Google Scholar 

  57. Chang SD, Marcellus ML, Marks MP, Levy RP, Do HM, Steinberg GK (2007) Multimodality treatment of giant intracranial arteriovenous malformations. Neurosurgery 61:432–442

    PubMed  Google Scholar 

  58. Nerva JD, Mantovani A, Barber J, Kim LJ, Rockhill JK, Hallam DK, Ghodke BV, Sekhar LN (2015) Treatment outcomes of unruptured arteriovenous malformations with a subgroup analysis of ARUBA (A Randomized Trial of Unruptured Brain Arteriovenous Malformations)-eligible patients. Neurosurgery 76:563–570

    Article  PubMed  Google Scholar 

  59. Kocer N, Hanimoglu H, Batur S, Kandemirli SG, Kizilkilic O, Sanus Z, Oz B, Islak C, Kaynar MY (2016) Preliminary experience with precipitating hydrophobic injectable liquid in brain arteriovenous malformations. Diagn Interv Radiol 22:184–189

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Naci Kocer.

Ethics declarations

Funding

No funding was received for this study.

Conflict of Interest

NK consults and proctors for MicroVention, Inc and Medtronic, Inc. CI consults and proctors for Medtronic, Inc.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual participants included in the study. Additional informed consent was obtained from all individual participants for whom identifying information is included in this article.

Electronic supplementary material

Fig. 1

A 67-year-old male with progressive right hemiparesis, aphasia and swallowing difficulty due to extensive venous reflux from an unruptured left fronto-parietal grade V bAVM. The patient had initially presented with seizures 37 years back and had undergone unsuccessful microsurgical bAVM resection. The patient clinically deteriorated over the last 6 months. The patient was planned to undergo single combined embolization and surgical treatment. a-b) Coronal T2-weighted MRI (in the year 1996) shows a left parietal AVM with a corticoventricular nidus. Digital subtraction angiogram (in the year 1996) shows a mixed fistulous and plexiform nidus with perinidal angiogenesis and venous drainage into deep and superficial venous system. c-e) Cranial computed tomography (in the year 2013) shows a craniotomy defect with surgical metallic artifacts. There is effacement of left parietal sulci. T2W and T1W MRI show prominent posterior fossa veins and extensive deep white matter hyperintensities. An enlarged venous aneurysm is projecting into right lateral ventricle (arrow). f-g) DSA prior to embolization (in the year 2013) shows a progressively enlarged corticoventricular nidus involving almost the entire parietal and posterior frontal region with an enlarged venous aneurysm projecting into right lateral ventricle. h) Cerebral DSA in venous phase shows enlargement of posterior fossa veins with prolonged circulation time. i-m) The posterior, superior and inferior components of the nidus were embolized with Onyx® through multiple dural and pial arterial feeders (arrows). A small residual anterior component was spared intentionally to avoid post-embolization perinidal hemorrhage. Also note the venous stagnation of the entire hemispheric venous system. n-o) Immediately after surgical resection, control DSA anteroposterior and lateral projections show complete elimination of the bAVM. p-r) MRI brain at one-month follow up shows regressing post-operative changes with thrombosed intra-ventricular venous aneurysm. On the 3rd year follow-up, patient had only one episode of seizure but had no other fresh neurological deficit. His speech and swallowing improved, while his right hemiparesis persisted (JPG 1026 kb)

High resolution image (TIF 11087 kb)

Fig. 2

A 20-year-old female presented with seizures due to an unruptured right temporal grade III bAVM. a-c) Cerebral DSA shows a moderate 2.5x4cms sized bAVM supplied by enlarged temporal branches of right middle cerebral artery. The bAVM had a mixed fistulous and plexiform nidus located in cortical-subcortical region with a multiple venous drainage pattern. Note the 3x3cm sized venous aneurysm in the draining vein of Trolard. d-e) 3D roadmap with overlaying technology, thin section algorithm and automatic motion compensation were used for microcatheter navigation and final positioning (arrow indicates venous aneurysm). f-h) Post-embolization anteroposterior and lateral internal carotid artery angiograms depict complete obliteration of AVM nidus with no early venous drainage. However, there are multiple regions of perinidal vascular structures with stagnant flow. i-k Right temporal parenchymal hemorrhage is seen adjacent to embolized nidus with intraventricular hemorrhage in the immediate post-embolization non-contrast CT. The patient underwent surgical bAVM resection and hematoma evacuation. Post surgical CT shows hematoma evacuation and nidus resection. l-o) Immediate post-treatment DSA shows total elimination of the nidus and perinidal stagnant vessels. p-t) 6-month follow-up MRI and 12-month follow-up DSA show gliotic right temporal changes, normalization of the pial vessels with no recurrence of bAVM (PNG 2240 kb)

High resolution image (TIF 9661 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kocer, N., Kandemirli, S.G., Dashti, R. et al. Single-stage planning for total cure of grade III–V brain arteriovenous malformations by embolization alone or in combination with microsurgical resection. Neuroradiology 61, 195–205 (2019). https://doi.org/10.1007/s00234-018-2140-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00234-018-2140-z

Keywords

Navigation