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Targeted endovascular treatment for ruptured brain arteriovenous malformations

  • Kun Hou
  • Kan Xu
  • Xuan Chen
  • Tiefeng Ji
  • Yunbao Guo
  • Jinlu YuEmail author
Review
  • 35 Downloads

Abstract

Currently, endovascular treatment (EVT) is recommended for ruptured brain arteriovenous malformation (BAVM). When performing EVT for ruptured BAVM, curative complete embolization without complications is the ideal goal, but, more often than not, it is difficult, impossible, and dangerous. Therefore, EVT targeted toward ruptured focal weak structures plays a very important role. No previous study has comprehensively reviewed the use of targeted EVT for ruptured BAVMs. Therefore, the current paper reviews the available literature on this subject. In BAVM, the ruptured focal weak structures may include flow-related aneurysms, intranidal venous dilated structures, intranidal fistula, and venous varices or ectasia. These ruptured focal weak structures have direct and indirect imaging presentations. The indirect imaging presentations indicate various intracranial hemorrhages. In direct imaging presentations, digital subtraction angiography (DSA) has the highest degree resolution for showing ruptured focal weak structures. In addition, some magnetic resonance (MR) sequences can be useful to identify ruptured focal weak structures. Of all ruptured focal weak structures, flow-related aneurysms are considered the highest risk and require urgent occlusion. Other ruptured weak structures also need to undergo targeted EVT. After targeted EVT, a good prognosis can be obtained. Therefore, the use of targeted EVT for ruptured BAVM is promising.

Keywords

Ruptured brain arteriovenous malformation Targeted endovascular treatment Review 

Notes

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Informed consent

Informed consent was obtained from all individual participants included in the study.

References

  1. 1.
    Alexander MD, Cooke DL, Nelson J, Guo DE, Dowd CF, Higashida RT, Halbach VV, Lawton MT, Kim H, Hetts SW (2015) Association between venous angioarchitectural features of sporadic brain arteriovenous malformations and intracranial hemorrhage. AJNR Am J Neuroradiol 36:949–952.  https://doi.org/10.3174/ajnr.A4224 CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Alexander MD, Cooke DL, Hallam DK, Kim H, Hetts SW, Ghodke BV (2016) Less can be more: targeted embolization of aneurysms associated with arteriovenous malformations unsuitable for surgical resection. Interv Neuroradiol 22:445–451.  https://doi.org/10.1177/1591019916641316 CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Alexander MD, Hippe DS, Cooke DL, Hallam DK, Hetts SW, Kim H, Lawton MT, Sekhar LN, Kim LJ, Ghodke BV (2018) Targeted embolization of aneurysms associated with brain arteriovenous malformations at high risk for surgical resection: a case-control study. Neurosurgery 82:343–349.  https://doi.org/10.1093/neuros/nyx167 CrossRefPubMedGoogle Scholar
  4. 4.
    Aoun SG, Bendok BR, Batjer HH (2012) Acute management of ruptured arteriovenous malformations and dural arteriovenous fistulas. Neurosurg Clin N Am 23:87–103.  https://doi.org/10.1016/j.nec.2011.09.013 CrossRefPubMedGoogle Scholar
  5. 5.
    Asadi H, Kok HK, Looby S, Brennan P, O’Hare A, Thornton J (2016) Outcomes and complications after endovascular treatment of brain arteriovenous malformations: a prognostication attempt using artificial intelligence. World Neurosurg 96:562–569 e561.  https://doi.org/10.1016/j.wneu.2016.09.086 CrossRefPubMedGoogle Scholar
  6. 6.
    Baharvahdat H, Blanc R, Termechi R, Pistocchi S, Bartolini B, Redjem H, Piotin M (2014) Hemorrhagic complications after endovascular treatment of cerebral arteriovenous malformations. AJNR Am J Neuroradiol 35:978–983.  https://doi.org/10.3174/ajnr.A3906 CrossRefPubMedGoogle Scholar
  7. 7.
    Bhogal P, Lansley J, Wong K, Udani SD, Uff C, Wadley J, Kumar A, Matouk CC, Makalanda HL (2019) Vessel wall enhancement of a ruptured intra-nidal aneurysm in a brain arteriovenous malformation. Interv Neuroradiol 25:310–314.  https://doi.org/10.1177/1591019918824796 CrossRefPubMedGoogle Scholar
  8. 8.
    Biswas S, Chandran A, Radon M, Puthuran M, Bhojak M, Nahser HC, Das K (2015) Accuracy of four-dimensional CT angiography in detection and characterisation of arteriovenous malformations and dural arteriovenous fistulas. Neuroradiol J 28:376–384.  https://doi.org/10.1177/1971400915604526 CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Buell TJ, Ding D, Starke RM, Webster Crowley R, Liu KC (2014) Embolization-induced angiogenesis in cerebral arteriovenous malformations. J Clin Neurosci 21:1866–1871.  https://doi.org/10.1016/j.jocn.2014.04.010 CrossRefPubMedGoogle Scholar
  10. 10.
    Cagnazzo F, Brinjikji W, Lanzino G (2016) Arterial aneurysms associated with arteriovenous malformations of the brain: classification, incidence, risk of hemorrhage, and treatment-a systematic review. Acta Neurochir (Wien) 158:2095–2104.  https://doi.org/10.1007/s00701-016-2957-3 CrossRefGoogle Scholar
  11. 11.
    Chandran A, Radon M, Biswas S, Das K, Puthuran M, Nahser H (2016) Novel use of 4D-CTA in imaging of intranidal aneurysms in an acutely ruptured arteriovenous malformation: is this the way forward? J Neurointerv Surg 8:e36.  https://doi.org/10.1136/neurintsurg-2015-011784.rep CrossRefPubMedGoogle Scholar
  12. 12.
    Chang W, Wu Y, Johnson K, Loecher M, Wieben O, Edjlali M, Oppenheim C, Roca P, Hald J, Aagaard-Kienitz B, Niemann D, Mistretta C, Turski P (2015) Fast contrast-enhanced 4D MRA and 4D flow MRI using constrained reconstruction (HYPRFlow): potential applications for brain arteriovenous malformations. AJNR Am J Neuroradiol 36:1049–1055.  https://doi.org/10.3174/ajnr.A4245 CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Consoli A, Scarpini G, Rosi A, Renieri L, Chiarotti I, Vignoli C, Ciampa I, Nappini S, Limbucci N, Mangiafico S (2014) Endovascular treatment of unruptured and ruptured brain arteriovenous malformations with Onyx18: a monocentric series of 84 patients. J Neurointerv Surg 6:600–606.  https://doi.org/10.1136/neurintsurg-2013-010869 CrossRefPubMedGoogle Scholar
  14. 14.
    Cronqvist M, Wirestam R, Ramgren B, Brandt L, Romner B, Nilsson O, Saveland H, Holtas S, Larsson EM (2006) Endovascular treatment of intracerebral arteriovenous malformations: procedural safety, complications, and results evaluated by MR imaging, including diffusion and perfusion imaging. AJNR Am J Neuroradiol 27:162–176PubMedGoogle Scholar
  15. 15.
    D’Aliberti G, Talamonti G, Cenzato M, La Camera A, Debernardi A, Valvassori L, Mariangela P, Nichelatti M (2015) Arterial and venous aneurysms associated with arteriovenous malformations. World Neurosurg 83:188–196.  https://doi.org/10.1016/j.wneu.2014.05.037 CrossRefPubMedGoogle Scholar
  16. 16.
    de Castro-Afonso LH, Nakiri GS, Oliveira RS, Santos MV, Santos ACD, Machado HR, Abud DG (2016) Curative embolization of pediatric intracranial arteriovenous malformations using Onyx: the role of new embolization techniques on patient outcomes. Neuroradiology 58:585–594.  https://doi.org/10.1007/s00234-016-1666-1 CrossRefPubMedGoogle Scholar
  17. 17.
    Derdeyn CP, Zipfel GJ, Albuquerque FC, Cooke DL, Feldmann E, Sheehan JP, Torner JC, American Heart Association Stroke C (2017) Management of brain arteriovenous malformations: a scientific statement for healthcare professionals from the American Heart Association/American Stroke Association. Stroke 48:e200–e224.  https://doi.org/10.1161/STR.0000000000000134 CrossRefPubMedGoogle Scholar
  18. 18.
    Downer JJ, Cellerini M, Corkill RA, Lalloo S, Kuker W, Byrne JV (2011) Decision-making in the scheduling of endovascular treatment after brain arteriovenous malformation haemorrhage: a retrospective single centre study. Neuroradiol J 24:879–885.  https://doi.org/10.1177/197140091102400609 CrossRefPubMedGoogle Scholar
  19. 19.
    Eliava S, Dmitriev A, Shekhtman O, Yakovlev S, Kheireddin A, Pilipenko Y (2018) Treatment of brain arteriovenous malformations with hemodynamic aneurysms: a series of 131 consecutive cases. World Neurosurg 110:e917–e927.  https://doi.org/10.1016/j.wneu.2017.11.114 CrossRefPubMedGoogle Scholar
  20. 20.
    Fukaya R, Mizutani K, Fukuchi M, Fujii K (2017) Thrombosis of the draining vein causes intracranial haemorrhage in the natural history of brain arteriovenous malformation: case report. Br J Neurosurg:1–2.  https://doi.org/10.1080/02688697.2017.1318110 CrossRefGoogle Scholar
  21. 21.
    Gabrieli J, Clarencon F, Di Maria F, Fahed R, Boch AL, Degos V, Chiras J, Sourour NA (2015) Fatal rupture of a brain arteriovenous malformation flow-related aneurysm during microcatheter removal: a rare complication. J Neurosurg 122:929–932.  https://doi.org/10.3171/2014.11.JNS132515 CrossRefPubMedGoogle Scholar
  22. 22.
    Goldberg J, Raabe A, Bervini D (2018) Natural history of brain arteriovenous malformations: systematic review. J Neurosurg Sci 62:437–443.  https://doi.org/10.23736/S0390-5616.18.04452-1 CrossRefPubMedGoogle Scholar
  23. 23.
    Gupta V, Chugh M, Walia BS, Vaishya S, Jha AN (2008) Use of CT angiography for anatomic localization of arteriovenous malformation nidal components. AJNR Am J Neuroradiol 29:1837–1840.  https://doi.org/10.3174/ajnr.A1136 CrossRefPubMedGoogle Scholar
  24. 24.
    Hademenos GJ, Massoud TF (1996) Risk of intracranial arteriovenous malformation rupture due to venous drainage impairment. A theoretical analysis. Stroke 27:1072–1083CrossRefGoogle Scholar
  25. 25.
    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 CrossRefPubMedGoogle Scholar
  26. 26.
    Hodgson TJ, Kemeny AA, Gholkar A, Deasy N (2009) Embolization of residual fistula following stereotactic radiosurgery in cerebral arteriovenous malformations. AJNR Am J Neuroradiol 30:109–110.  https://doi.org/10.3174/ajnr.A1240 CrossRefPubMedGoogle Scholar
  27. 27.
    Hsu YH, Lee CW, Liu HM, Wang YH, Kuo MF (2015) Prioritized venous coiling facilitating endovascular treatment of brain arteriovenous malformations with a fistulous component. World Neurosurg 84:1857–1863.  https://doi.org/10.1016/j.wneu.2015.08.014 CrossRefPubMedGoogle Scholar
  28. 28.
    Komatsu K, Takagi Y, Ishii A, Kikuchi T, Yamao Y, Fushimi Y, Grinstead J, Ahn S, Miyamoto S (2018) Ruptured intranidal aneurysm of an arteriovenous malformation diagnosed by delay alternating with nutation for tailored excitation (DANTE)-prepared contrast-enhanced magnetic resonance imaging. Acta Neurochir (Wien). 160:2435–2438.  https://doi.org/10.1007/s00701-018-3713-7 CrossRefPubMedGoogle Scholar
  29. 29.
    Krings T, Hans FJ, Geibprasert S, Terbrugge K (2010) Partial “targeted” embolisation of brain arteriovenous malformations. Eur Radiol 20:2723–2731.  https://doi.org/10.1007/s00330-010-1834-3 CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Lang S, Golitz P, Struffert T, Rosch J, Rossler K, Kowarschik M, Strother C, Doerfler A (2017) 4D DSA for dynamic visualization of cerebral vasculature: a single-center experience in 26 cases. AJNR Am J Neuroradiol 38:1169–1176.  https://doi.org/10.3174/ajnr.A5161 CrossRefPubMedGoogle Scholar
  31. 31.
    Le Feuvre D, Taylor A (2007) Target embolization of AVMs: identification of sites and results of treatment. Interv Neuroradiol 13:389–394.  https://doi.org/10.1177/159101990701300411 CrossRefPubMedGoogle Scholar
  32. 32.
    Luo CB, Guo WY, Teng MM, Chang FC, Lin CJ, Wu HM, Chang CY, Chung WY (2013) Fistula components of brain arteriovenous malformations: angioarchitecture analysis and embolization prior to gamma-knife surgery. J Chin Med Assoc 76:277–281.  https://doi.org/10.1016/j.jcma.2013.01.011 CrossRefPubMedGoogle Scholar
  33. 33.
    Martinez JL, Macdonald RL (2015) Surgical strategies for acutely ruptured arteriovenous malformations. Front Neurol Neurosci 37:166–181.  https://doi.org/10.1159/000437121 CrossRefPubMedGoogle Scholar
  34. 34.
    Matsushige T, Shimonaga K, Mizoue T, Hosogai M, Hashimoto Y, Kaneko M, Ono C, Ishii D, Sakamoto S, Kurisu K (2019) Focal aneurysm wall enhancement on magnetic resonance imaging indicates intraluminal thrombus and the rupture point. World Neurosurg 127:e578–e584.  https://doi.org/10.1016/j.wneu.2019.03.209 CrossRefPubMedGoogle Scholar
  35. 35.
    Meisel HJ, Mansmann U, Alvarez H, Rodesch G, Brock M, Lasjaunias P (2002) Effect of partial targeted N-butyl-cyano-acrylate embolization in brain AVM. Acta Neurochir (Wien) 144:879–887; discussion 888.  https://doi.org/10.1007/s00701-002-0978-6 CrossRefGoogle Scholar
  36. 36.
    Mendoza-Elias N, Shakur SF, Charbel FT, Alaraj A (2018) Cerebral arteriovenous malformation draining vein stenosis is associated with atherosclerotic risk factors. J Neurointerv Surg 10:788–790.  https://doi.org/10.1136/neurintsurg-2017-013580 CrossRefPubMedGoogle Scholar
  37. 37.
    Mjoli N, Le Feuvre D, Taylor A (2011) Bleeding source identification and treatment in brain arteriovenous malformations. Interv Neuroradiol 17:323–330.  https://doi.org/10.1177/159101991101700307 CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    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 Ai (2014) Medical management with or without interventional therapy for unruptured brain arteriovenous malformations (ARUBA): a multicentre, non-blinded, randomised trial. Lancet 383:614–621.  https://doi.org/10.1016/S0140-6736(13)62302-8 CrossRefPubMedGoogle Scholar
  39. 39.
    Morgan MK, Guilfoyle M, Kirollos R, Heller GZ (2018) Remodeling of the feeding arterial system after surgery for resection of brain arteriovenous malformations: an observational study. Neurosurgery.  https://doi.org/10.1093/neuros/nyy007 CrossRefGoogle Scholar
  40. 40.
    Omodaka S, Endo H, Fujimura M, Niizuma K, Sato K, Matsumoto Y, Tominaga T (2015) High-grade cerebral arteriovenous malformation treated with targeted embolization of a ruptured site: wall enhancement of an intranidal aneurysm as a sign of ruptured site. Neurol Med Chir (Tokyo) 55:813–817.  https://doi.org/10.2176/nmc.cr.2015-0052 CrossRefGoogle Scholar
  41. 41.
    Peres CMA, Souza EC, Teixeira MJ, Figueiredo EG, Caldas J (2017) Impact of associated nidal lesions in outcome of brain arteriovenous malformations after radiosurgery with or without embolization. World Neurosurg 105:643–650.  https://doi.org/10.1016/j.wneu.2017.06.044 CrossRefPubMedGoogle Scholar
  42. 42.
    Platz J, Berkefeld J, Singer OC, Wolff R, Seifert V, Konczalla J, Guresir E (2014) Frequency, risk of hemorrhage and treatment considerations for cerebral arteriovenous malformations with associated aneurysms. Acta Neurochir (Wien) 156:2025–2034.  https://doi.org/10.1007/s00701-014-2225-3 CrossRefGoogle Scholar
  43. 43.
    Pollock GA, Shaibani A, Awad I, Batjer HH, Bendok BR (2011) Intraventricular hemorrhage secondary to intranidal aneurysm rupture-successful management by arteriovenous malformation embolization followed by intraventricular tissue plasminogen activator: case report. Neurosurgery 68:E581–E586; discussion E586.  https://doi.org/10.1227/NEU.0b013e31820208a6 CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Pritz MB (1994) Ruptured supratentorial arteriovenous malformations associated with venous aneurysms. Acta Neurochir (Wien) 128:150–162CrossRefGoogle Scholar
  45. 45.
    Rahme R, Farley CW, Zuccarello M, Ringer AJ, Khan U, Abruzzo TA (2011) Transarterial embolization of cerebral arteriovenous malformations: a durable treatment for venous side hemorrhage? Med Hypotheses 76:827–830.  https://doi.org/10.1016/j.mehy.2011.02.029 CrossRefPubMedGoogle Scholar
  46. 46.
    Rammos SK, Gardenghi B, Bortolotti C, Cloft HJ, Lanzino G (2016) Aneurysms associated with brain arteriovenous malformations. AJNR Am J Neuroradiol 37:1966–1971.  https://doi.org/10.3174/ajnr.A4869 CrossRefPubMedGoogle Scholar
  47. 47.
    Reynolds MR, Arias EJ, Chatterjee AR, Chicoine MR, Cross DT 3rd (2015) Acute rupture of a feeding artery aneurysm after embolization of a brain arteriovenous malformation. Interv Neuroradiol 21:613–619.  https://doi.org/10.1177/1591019915591740 CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Shakur SF, Hussein AE, Amin-Hanjani S, Valyi-Nagy T, Charbel FT, Alaraj A (2017) Cerebral arteriovenous malformation flow is associated with venous intimal hyperplasia. Stroke 48:1088–1091.  https://doi.org/10.1161/STROKEAHA.116.015666 CrossRefPubMedGoogle Scholar
  49. 49.
    Shakur SF, Brunozzi D, Ismail R, Pandey D, Charbel FT, Alaraj A (2018) Effect of age on cerebral arteriovenous malformation draining vein stenosis. World Neurosurg 113:e654–e658.  https://doi.org/10.1016/j.wneu.2018.02.116 CrossRefPubMedGoogle Scholar
  50. 50.
    Shotar E, Al Raaisi A, Lenck S, Premat K, Degos V, Mathon B, Clarencon F, Sourour NA (2019) Injection of N-butyl cyanoacrylate through a dual-lumen balloon for embolization of high-flow intranidal fistulas in brain arteriovenous malformations: technical note. Clin Neuroradiol.:1–7.  https://doi.org/10.1007/s00062-019-00780-6
  51. 51.
    Signorelli F, Gory B, Pelissou-Guyotat I, Guyotat J, Riva R, Dailler F, Turjman F (2014) Ruptured brain arteriovenous malformations associated with aneurysms: safety and efficacy of selective embolization in the acute phase of hemorrhage. Neuroradiology 56:763–769.  https://doi.org/10.1007/s00234-014-1395-2 CrossRefPubMedGoogle Scholar
  52. 52.
    Singh R, Gupta V, Ahuja C, Kumar A, Mukherjee KK, Khandelwal N (2018) Role of time-resolved-CTA in intracranial arteriovenous malformation evaluation at 128-slice CT in comparison with digital subtraction angiography. Neuroradiol J 31:235–243.  https://doi.org/10.1177/1971400917744403 CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Soize S, Bouquigny F, Kadziolka K, Portefaix C, Pierot L (2014) Value of 4D MR angiography at 3T compared with DSA for the follow-up of treated brain arteriovenous malformation. AJNR Am J Neuroradiol 35:1903–1909.  https://doi.org/10.3174/ajnr.A3982 CrossRefPubMedGoogle Scholar
  54. 54.
    Stapf C, Mohr JP, Pile-Spellman J, Sciacca RR, Hartmann A, Schumacher HC, Mast H (2002) Concurrent arterial aneurysms in brain arteriovenous malformations with haemorrhagic presentation. J Neurol Neurosurg Psychiatry 73:294–298CrossRefGoogle Scholar
  55. 55.
    Starke RM, Komotar RJ, Connolly ES (2013) A randomized trial of unruptured brain arteriovenous malformations. Neurosurgery 73:N13–N15.  https://doi.org/10.1227/01.neu.0000435114.33768.e3 CrossRefPubMedGoogle Scholar
  56. 56.
    Stemer AB, Bank WO, Armonda RA, Liu AH, Herzig DW, Bell RS (2013) Acute embolization of ruptured brain arteriovenous malformations. J Neurointerv Surg 5:196–200.  https://doi.org/10.1136/neurintsurg-2011-010214 CrossRefPubMedGoogle Scholar
  57. 57.
    Sun Y, Jin H, Li Y, Tian Z (2017) Target embolization of associated aneurysms in ruptured arteriovenous malformations. World Neurosurg 101:26–32.  https://doi.org/10.1016/j.wneu.2017.01.081 CrossRefPubMedGoogle Scholar
  58. 58.
    Todnem N, Ward A, Nahhas M, Vender J, Alleyne CH, Rahimi S (2018) A Retrospective cohort analysis of hemorrhagic AVMs treated with combination endovascular embolization and gamma-knife stereotactic radiosurgery. World Neurosurg.  https://doi.org/10.1016/j.wneu.2018.10.125 CrossRefGoogle Scholar
  59. 59.
    Tranvinh E, Heit JJ, Hacein-Bey L, Provenzale J, Wintermark M (2017) Contemporary imaging of cerebral arteriovenous malformations. AJR Am J Roentgenol 208:1320–1330.  https://doi.org/10.2214/AJR.16.17306 CrossRefPubMedGoogle Scholar
  60. 60.
    Tu J, Stoodley MA, Morgan MK, Storer KP (2006) Ultrastructure of perinidal capillaries in cerebral arteriovenous malformations. Neurosurgery 58:961–970; discussion 961-970.  https://doi.org/10.1227/01.NEU.0000210248.39504.B5 CrossRefPubMedGoogle Scholar
  61. 61.
    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.  https://doi.org/10.3174/ajnr.A2947 CrossRefPubMedGoogle Scholar
  62. 62.
    Wolf RL, Wang J, Detre JA, Zager EL, Hurst RW (2008) Arteriovenous shunt visualization in arteriovenous malformations with arterial spin-labeling MR imaging. AJNR Am J Neuroradiol 29:681–687.  https://doi.org/10.3174/ajnr.A0901 CrossRefPubMedGoogle Scholar
  63. 63.
    Yang W, Porras JL, Xu R, Braileanu M, Khalid S, Hung AL, Caplan JM, Garzon-Muvdi T, Rong X, Colby GP, Coon AL, Tamargo RJ, Huang J (2018) Comparison of hemorrhagic risk in intracranial arteriovenous malformations between conservative management and embolization as the single treatment modality. Neurosurgery 82:481–490.  https://doi.org/10.1093/neuros/nyx230 CrossRefPubMedGoogle Scholar
  64. 64.
    Yu JL, Yang S, Luo Q, Wang HL, Wang B, Qu YY, Xu K (2011) Endovascular treatment of intracranial ruptured aneurysms associated with arteriovenous malformations: a clinical analysis of 14 hemorrhagic cases. Interv Neuroradiol 17:78–86.  https://doi.org/10.1177/159101991101700113 CrossRefPubMedPubMedCentralGoogle Scholar
  65. 65.
    Yuki I, Kim RH, Duckwiler G, Jahan R, Tateshima S, Gonzalez N, Gorgulho A, Diaz JL, De Salles AA, Vinuela F (2010) Treatment of brain arteriovenous malformations with high-flow arteriovenous fistulas: risk and complications associated with endovascular embolization in multimodality treatment. Clinical article. J Neurosurg 113:715–722.  https://doi.org/10.3171/2009.9.JNS081588 CrossRefPubMedGoogle Scholar
  66. 66.
    Zacharia BE, Vaughan KA, Jacoby A, Hickman ZL, Bodmer D, Connolly ES Jr (2012) Management of ruptured brain arteriovenous malformations. Curr Atheroscler Rep 14:335–342.  https://doi.org/10.1007/s11883-012-0257-9 CrossRefPubMedGoogle Scholar
  67. 67.
    Zuurbier SM, Al-Shahi Salman R (2019) Interventions for treating brain arteriovenous malformations in adults. Cochrane Database Syst Rev 9:CD003436.  https://doi.org/10.1002/14651858.CD003436.pub4 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of NeurosurgeryThe First Hospital of Jilin UniversityChangchunChina
  2. 2.Department of RadiologyThe First Hospital of Jilin UniversityChangchunChina

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