Skip to main content
Log in

Evolution of clinical and translational advances in the management of pediatric arteriovenous malformations

  • Review
  • Published:
Child's Nervous System Aims and scope Submit manuscript

Abstract

Arteriovenous malformations (AVMs) represent one of the most challenging diagnoses in pediatric neurosurgery. Until recently, the majority of AVMs was only identified after hemorrhage and primarily treated with surgery. However, recent advances in a wide range of fields—imaging, surgery, interventional radiology, radiation therapy, and molecular biology—have profoundly advanced the understanding and therapy of these complex lesions. Here we review the progress made in pediatric AVMs with a specific focus on innovations relevant to clinical care.

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.

Similar content being viewed by others

References

  1. Luessenhop AJ, Spence WT (1960) Artificial embolization of cerebral arteries. Report of use in a case of arteriovenous malformation. J Am Med Assoc 172:1153–1155. (In eng). https://doi.org/10.1001/jama.1960.63020110001009

  2. Gross BA, Scott RM, Smith ER (2014) Management of brain arteriovenous malformations. Lancet 383(9929):1635. https://doi.org/10.1016/S0140-6736(14)60785-6

    Article  PubMed  Google Scholar 

  3. Lin N, Smith ER, Scott RM, Orbach DB (2015) Safety of neuroangiography and embolization in children: complication analysis of 697 consecutive procedures in 394 patients. J Neurosurg Pediatr 16(4):432–438. https://doi.org/10.3171/2015.2.PEDS14431

    Article  PubMed  Google Scholar 

  4. Ravindra VM, Karsy M, Lanpher A et al (2019) A national analysis of 9655 pediatric cerebrovascular malformations: effect of hospital volume on outcomes. J Neurosurg Pediatr 1–10. https://doi.org/10.3171/2019.5.PEDS19155

  5. Cassano R, Perri P, Esposito A et al (2023) Expanded polytetrafluoroethylene membranes for vascular stent coating: manufacturing, biomedical and surgical applications, innovations and case reports. Membranes (Basel) 13(2) (In eng). https://doi.org/10.3390/membranes13020240

  6. 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(4):445–451. (In eng). https://doi.org/10.1177/1591019916641316

  7. Flores BC, See AP, Weiner GM, Jankowitz BT, Ducruet AF, Albuquerque FC (2018) Use of the Apollo detachable-tip microcatheter for endovascular embolization of arteriovenous malformations and arteriovenous fistulas. J Neurosurg 130(3):963–971. (In eng). https://doi.org/10.3171/2017.9.Jns17397

  8. Maimon S, Strauss I, Frolov V, Margalit N, Ram Z (2010) Brain arteriovenous malformation treatment using a combination of Onyx and a new detachable tip microcatheter, SONIC: short-term results. AJNR Am J Neuroradiol 31(5):947–954. (In eng). https://doi.org/10.3174/ajnr.A1959

  9. Killer-Oberpfalzer M, Chapot R, Orion D, Barr JD, Cabiri O, Berenstein A (2022) Clinical experience with the Bendit steerable microcatheter: a new paradigm for endovascular treatment. J Neurointerv Surg (In eng). https://doi.org/10.1136/jnis-2022-019096

  10. Vollherbst DF, Chapot R, Bendszus M, Möhlenbruch MA (2022) Glue, Onyx, Squid or PHIL? Liquid embolic agents for the embolization of cerebral arteriovenous malformations and dural arteriovenous fistulas. Clin Neuroradiol 32(1):25–38. (In eng). https://doi.org/10.1007/s00062-021-01066-6

  11. Konya D, Yildirim O, Kurtkaya O et al (2005) Testing the angiogenic potential of cerebrovascular malformations by use of a rat cornea model: usefulness and novel assessment of changes over time. Neurosurgery 56(6):1339–1345; discussion 1345–1346. (In eng). https://doi.org/10.1227/01.neu.0000159886.08629.b7

  12. Buell TJ, Ding D, Starke RM, Webster Crowley R, Liu KC (2014) Embolization-induced angiogenesis in cerebral arteriovenous malformations. J Clin Neurosci 21(11):1866–1871. (In eng). https://doi.org/10.1016/j.jocn.2014.04.010

  13. Mamalui-Hunter M, Jiang T, Rich KM, Derdeyn CP, Drzymala RE (2011) Effect of liquid embolic agents on Gamma Knife surgery dosimetry for arteriovenous malformations. Clinical article. J Neurosurg 115(2):364–370. (In eng). https://doi.org/10.3171/2011.3.Jns10717

  14. Halbach VV, Higashida RT, Yang P, Barnwell S, Wilson CB, Hieshima GB (1988) Preoperative balloon occlusion of arteriovenous malformations. Neurosurgery 22(2):301–308. (In eng). https://doi.org/10.1227/00006123-198802000-00004

  15. Deveikis JP, Manz HJ, Luessenhop AJ et al (1994) A clinical and neuropathologic study of silk suture as an embolic agent for brain arteriovenous malformations. AJNR Am J Neuroradiol 15(2):263–271 (In eng)

    CAS  PubMed  PubMed Central  Google Scholar 

  16. Song JK, Eskridge JM, Chung EC et al (2000) Preoperative embolization of cerebral arteriovenous malformations with silk sutures: analysis and clinical correlation of complications revealed on computerized tomography scanning. J Neurosurg 92(6):955–960. https://doi.org/10.3171/jns.2000.92.6.0955. (In eng)

    Article  CAS  PubMed  Google Scholar 

  17. Ding D, Sheehan JP, Starke RM et al (2015) Embolization of cerebral arteriovenous malformations with silk suture particles prior to stereotactic radiosurgery. J Clin Neurosci 22(10):1643–1649. https://doi.org/10.1016/j.jocn.2015.03.046. (In eng)

    Article  PubMed  Google Scholar 

  18. Sorimachi T, Koike T, Takeuchi S et al (1999) Embolization of cerebral arteriovenous malformations achieved with polyvinyl alcohol particles: angiographic reappearance and complications. AJNR Am J Neuroradiol 20(7):1323–1328 (In eng)

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Hamada JI, Kai Y, Mizuno T et al (2004) A nonadhesive liquid embolic agent of ethylene vinyl alcohol copolymer and ethanol mixture for cerebral arteriovenous malformations. Clinical experience. Interv Neuroradio 10 Suppl 1(Suppl 1):135–142. (In eng). https://doi.org/10.1177/15910199040100s123

  20. U.S. Dept. of Health and Human Services PHS, Food and Drug Administration (1995) Target Therapeutics. Detachable Platinum Coil (Gugliemi Detachable Coil, GDC) 510(k) Premarket Notification. https://www.accessdata.fda.gov/scripts/cdrh/cfdocs/cfpmn/pmn.cfm?ID=K951256

  21. Park KY, Kim JW, Kim BM et al (2019) Coil-protected technique for liquid embolization in neurovascular malformations. Korean J Radiol 20(8):1285–1292. (In eng). https://doi.org/10.3348/kjr.2019.0127

  22. Gao X, Liang G, Li Z et al (2014) Transarterial coil-augmented Onyx embolization for brain arteriovenous malformation. Technique and experience in 22 consecutive patients. Interv Neuroradiol 20(1):83–90. (In eng). https://doi.org/10.15274/inr-2014-10012

  23. Berenstein A, Fifi J (2018) Study of PHIL® embolic system in the treatment of intracranial dural arteriovenous fistulas in the pediatric population. 11/5/2018 ed: U.S. National Library of Medicine, ClinicalTrials.gov

  24. 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(6):1492–1497. (In eng). https://doi.org/10.3171/2015.2.Jns131368

  25. Behzadi F, Heiferman DM, Wozniak A et al (2022) Comparison of transarterial n-BCA and Onyx embolization of brain arteriovenous malformations: a single-center 18-year retrospective analysis. J Cerebrovasc Endovasc Neurosurg 24(2):144–153. (In eng). https://doi.org/10.7461/jcen.2022.E2021.12.003

  26. Velat GJ, Reavey-Cantwell JF, Sistrom C et al (2008) Comparison of N-butyl cyanoacrylate and onyx for the embolization of intracranial arteriovenous malformations: analysis of fluoroscopy and procedure times. Neurosurgery 63(1 Suppl 1):ONS73–8; discussion ONS78–80. (In eng). https://doi.org/10.1227/01.neu.0000335015.83616.12

  27. Lv X, Wu Z, Jiang C et al (2011) Complication risk of endovascular embolization for cerebral arteriovenous malformation. Eur J Radiol 80(3):776–779. (In eng). https://doi.org/10.1016/j.ejrad.2010.09.024

  28. Yakes WF, Krauth L, Ecklund J et al (1997) Ethanol endovascular management of brain arteriovenous malformations: initial results. Neurosurgery 40(6):1145–1152; discussion 1152–1154. (In eng). https://doi.org/10.1097/00006123-199706000-00005

  29. Settecase F, Hetts SW, Nicholson AD et al (2016) Superselective intra-arterial ethanol sclerotherapy of feeding artery and nidal aneurysms in ruptured cerebral arteriovenous malformations. AJNR Am J Neuroradiol 37(4):692–697. (In eng). https://doi.org/10.3174/ajnr.A4584

  30. Yakes WF (2004) Endovascular management of high-flow arteriovenous malformations. Semin Intervent Radiol 21(1):49–58. (In eng). https://doi.org/10.1055/s-2004-831405

  31. Berthelsen B, Löfgren J, Svendsen P (1990) Embolization of cerebral arteriovenous malformations with bucrylate. Experience in a first series of 29 patients. Acta Radiol 31(1):13–21. (In eng)

  32. Brothers MF, Kaufmann JC, Fox AJ, Deveikis JP (1989) n-Butyl 2-cyanoacrylate–substitute for IBCA in interventional neuroradiology: histopathologic and polymerization time studies. AJNR Am J Neuroradiol 10(4):777–786 (In eng)

    CAS  PubMed  PubMed Central  Google Scholar 

  33. Fournier D, Terbrugge K, Rodesch G, Lasjaunias P (1990) Revascularization of brain arteriovenous malformations after embolization with bucrylate. Neuroradiology 32(6):497–501. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=2287379

  34. Debrun GM, Aletich V, Ausman JI, Charbel F, Dujovny M (1997) Embolization of the nidus of brain arteriovenous malformations with n-butyl cyanoacrylate. Neurosurgery 40(1):112–120; discussion 120–121. (In eng)

  35. U.S. Dept. of Health and Human Services PHS, Food and Drug Administration (2000) Medos International SARL. Trufill n-butyl Cyanoacrylate Liquid Embolic System 510(k) Premarket Notification. https://www.accessdata.fda.gov/scripts/cdrh/cfdocs/cfpma/pma.cfm?id=p990040

  36. Gounis MJ, Lieber BB, Wakhloo AK, Siekmann R, Hopkins LN (2002) Effect of glacial acetic acid and ethiodized oil concentration on embolization with N-butyl 2-cyanoacrylate: an in vivo investigation. AJNR Am J Neuroradiol 23(6):938–944 (In eng)

    PubMed  PubMed Central  Google Scholar 

  37. Moore C, Murphy K, Gailloud P (2006) Improved distal distribution of n-butyl cyanoacrylate glue by simultaneous injection of dextrose 5% through the guiding catheter: technical note. Neuroradiology 48(5):327–332. (In eng). https://doi.org/10.1007/s00234-006-0059-2

  38. Taki W, Yonekawa Y, Iwata H, Uno A, Yamashita K, Amemiya H (1990) A new liquid material for embolization of arteriovenous malformations. AJNR Am J Neuroradiol 11(1):163–168 (In eng)

    CAS  PubMed  PubMed Central  Google Scholar 

  39. Katsaridis V, Papagiannaki C, Aimar E (2008) Curative embolization of cerebral arteriovenous malformations (AVMs) with Onyx in 101 patients. Neuroradiology 50(7):589–597. (In eng). https://doi.org/10.1007/s00234-008-0382-x

  40. Mounayer C, Hammami N, Piotin M et al (2007) Nidal embolization of brain arteriovenous malformations using Onyx in 94 patients. AJNR Am J Neuroradiol 28(3):518–523 (In eng)

    CAS  PubMed  PubMed Central  Google Scholar 

  41. U.S. Dept. of Health and Human Services PHS, Food and Drug Administration (2005) EV3 Neurovascular. Onyx Liquid Embolic System. 510(k) Premarket Notification. (https://www.accessdata.fda.gov/scripts/cdrh/cfdocs/cfpma/pma.cfm?id=P030004)

  42. Loh Y, Duckwiler GR (2010) A prospective, multicenter, randomized trial of the Onyx liquid embolic system and N-butyl cyanoacrylate embolization of cerebral arteriovenous malformations. Clinical article. J Neurosurg 113(4):733–741. (In eng). https://doi.org/10.3171/2010.3.Jns09370

  43. Siekmann R (2005) Basics and Principles in the Application of Onyx LD Liquid Embolic System in the Endovascular Treatment of Cerebral Arteriovenous Malformations. Interv Neuroradiol 11(Suppl 1):131–140. (In eng). https://doi.org/10.1177/15910199050110s117

  44. Signorelli F, Gory B, Pelissou-Guyotat I et al (2014) Ruptured brain arteriovenous malformations associated with aneurysms: safety and efficacy of selective embolization in the acute phase of hemorrhage. Neuroradiology 56(9):763–769. (In eng). https://doi.org/10.1007/s00234-014-1395-2

  45. 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(7):1299–1304. (In eng). https://doi.org/10.3174/ajnr.A2947

  46. De Leacy R, Ansari SA, Schirmer CM et al (2022) Endovascular treatment in the multimodality management of brain arteriovenous malformations: report of the Society of NeuroInterventional Surgery Standards and Guidelines Committee. J Neurointerv Surg 14(11):1118–1124. (In eng). https://doi.org/10.1136/neurintsurg-2021-018632

  47. Subat YW, Dasenbrock HH, Gross BA et al (2019) Periprocedural intracranial hemorrhage after embolization of cerebral arteriovenous malformations: a meta-analysis. J Neurosurg 1–11. (In eng). https://doi.org/10.3171/2019.5.Jns183204

  48. Paramasivam S, Niimi Y, Fifi J, Berenstein A (2013) Onyx embolization using dual-lumen balloon catheter: initial experience and technical note. J Neuroradiol 40(4):294–302. (In eng). https://doi.org/10.1016/j.neurad.2013.08.001

  49. Iosif C, Almeida Filho JA, Gilbert CE et al (2022) Selective arterial temporary flow arrest with balloons during transvenous embolization for the treatment of brain arteriovenous malformations: a feasibility study with MRI-monitored adverse events. J Neurointerv Surg 14(12):1234–1238. (In eng). https://doi.org/10.1136/neurintsurg-2021-018097

  50. Chapot R, Stracke P, Velasco A et al (2014) The pressure cooker technique for the treatment of brain AVMs. J Neuroradiol 41(1):87–91. (In eng). https://doi.org/10.1016/j.neurad.2013.10.001

  51. De Sousa JMB, Iosif C, Sganzerla LZ et al (2020) Selection of patients for treatment of brain arteriovenous malformations by the transvenous approach: relationship with venous anatomy and risk of hemorrhagic complications. AJNR Am J Neuroradiol 41(12):2311–2316. (In eng). https://doi.org/10.3174/ajnr.A6810

  52. Iosif C, Mendes GA, Saleme S et al (2015) Endovascular transvenous cure for ruptured brain arteriovenous malformations in complex cases with high Spetzler-Martin grades. J Neurosurg 122(5):1229–1238. (In eng). https://doi.org/10.3171/2014.9.Jns141714

  53. Koyanagi M, Mosimann PJ, Nordmeyer H et al (2021) The transvenous retrograde pressure cooker technique for the curative embolization of high-grade brain arteriovenous malformations. J Neurointerv Surg 13(7):637–641. (In eng). https://doi.org/10.1136/neurintsurg-2020-016566

  54. Groff MW, Adams DC, Kahn RA, Kumbar UM, Yang BY, Bederson JB (1999) Adenosine-induced transient asystole for management of a basilar artery aneurysm. Case report. J Neurosurg 91(4):687–690. (In eng). https://doi.org/10.3171/jns.1999.91.4.0687

  55. Pile-Spellman J, Young WL, Joshi S et al (1999) Adenosine-induced cardiac pause for endovascular embolization of cerebral arteriovenous malformations: technical case report. Neurosurgery 44(4):881–886; discussion 886–887. (In eng). https://doi.org/10.1097/00006123-199904000-00117

  56. Ghorbani M, Griessenauer CJ, Wipplinger C et al (2021) Adenosine-induced transient circulatory arrest in transvenous embolization of cerebral arteriovenous malformations. Neuroradiol J 34(5):509–516. (In eng). https://doi.org/10.1177/1971400921998972

  57. Rangel-Castilla L, Shallwani H, Siddiqui AH (2019) Transvenous embolization of thalamic arteriovenous malformation under transient cardiac standstill. Neurosurg Focus 46(Suppl_1):V10. (In eng). https://doi.org/10.3171/2019.1.FocusVid.18416

  58. Jagadeesan BD, Grande AW, Tummala RP (2018) Safety and feasibility of balloon-assisted embolization with Onyx of brain arteriovenous malformations revisited: personal experience with the scepter XC balloon microcatheter. Interv Neurol 7(6):439–444. (In eng). https://doi.org/10.1159/000490579

  59. Manzoor MU, Almulhim IA, Alrashed AA, Althubait S, Alturki AY, Al-Qahtani SM (2023) Initial experience with Scepter Mini dual lumen balloon for embolization of cerebrovascular diseases. Journal of cerebrovascular and endovascular neurosurgery. https://doi.org/10.7461/jcen.2023.E2022.10.004

    Article  PubMed  PubMed Central  Google Scholar 

  60. Weinstock P, Prabhu SP, Flynn K, Orbach DB, Smith E (2015) Optimizing cerebrovascular surgical and endovascular procedures in children via personalized 3D printing. J Neurosurg Pediatr 1–6. https://doi.org/10.3171/2015.3.PEDS14677

  61. Gross BA, Storey A, Orbach DB, Scott RM, Smith ER (2015) Microsurgical treatment of arteriovenous malformations in pediatric patients: the Boston Children’s Hospital experience. J Neurosurg Pediatr 15(1):71–77. https://doi.org/10.3171/2014.9.PEDS146

    Article  PubMed  Google Scholar 

  62. Lin N, Smith ER, Scott RM, Orbach DB (2015) Safety of neuroangiography and embolization in children: complication analysis of 697 consecutive procedures in 394 patients. J Neurosurg Pediatr 1–7. https://doi.org/10.3171/2015.2.PEDS14431

  63. Pertuiset B, Ancri D, Kinuta Y et al (1991) Classification of supratentorial arteriovenous malformations. A score system for evaluation of operability and surgical strategy based on an analysis of 66 cases. Acta Neurochir (Wien) 110(1–2):6–16. https://doi.org/10.1007/BF01402041

  64. Spetzler RF, Martin NA (1986) A proposed grading system for arteriovenous malformations. J Neurosurg 65(4):476–483. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=3760956

  65. Hamilton MG, Spetzler RF (1994) The prospective application of a grading system for arteriovenous malformations. Neurosurgery 34(1):2–6; discussion 6–7. (http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=8121564)

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

    Article  PubMed  Google Scholar 

  67. Lawton MT (2003) Spetzler-Martin Grade III arteriovenous malformations: surgical results and a modification of the grading scale. Neurosurgery 52(4):740–748; discussion 748–749. (In eng). https://doi.org/10.1227/01.neu.0000053220.02268.9c

  68. 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(4):702–713; discussion 713. (In eng). https://doi.org/10.1227/01.Neu.0000367555.16733.E1

  69. 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(4):642–648. (In eng). https://doi.org/10.3171/jns.2005.103.4.0642

  70. Pollock BE (2013) Development and testing of a radiosurgery-based arteriovenous malformation grading system. Prog Neurol Surg 27:58–66. https://doi.org/10.1159/000341620

    Article  PubMed  Google Scholar 

  71. Pollock BE, Flickinger JC (2008) Modification of the radiosurgery-based arteriovenous malformation grading system. Neurosurgery 63(2):239–243; discussion 243. https://doi.org/10.1227/01.NEU.0000315861.24920.92

  72. Wegner RE, Oysul K, Pollock BE et al (2011) A modified radiosurgery-based arteriovenous malformation grading scale and its correlation with outcomes. Int J Radiat Oncol Biol Phys 79(4):1147–1150. (In eng). https://doi.org/10.1016/j.ijrobp.2009.12.056

  73. 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(4):981–987. https://doi.org/10.3171/2013.5.JNS1311

    Article  PubMed  Google Scholar 

  74. Gupta R, Adeeb N, Moore JM et al (2016) Validity assessment of grading scales predicting complications from embolization of cerebral arteriovenous malformations. Clin Neurol Neurosurg 151:102–107. (In eng). https://doi.org/10.1016/j.clineuro.2016.10.019

  75. Jin H, Jiang Y, Ge H et al (2017) Comparison of grading scales regarding perioperative complications and clinical outcomes of brain arteriovenous malformations after endovascular therapy-multicenter study. World neurosurgery 106:394–401. (In eng). https://doi.org/10.1016/j.wneu.2017.07.020

  76. Pulli B, Stapleton CJ, Walcott BP et al (2019) Comparison of predictive grading systems for procedural risk in endovascular treatment of brain arteriovenous malformations: analysis of 104 consecutive patients. J Neurosurg 1–9. (In eng). https://doi.org/10.3171/2019.4.Jns19266

  77. 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(2):117–120 (In eng)

    PubMed  PubMed Central  Google Scholar 

  78. 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. (In eng). https://doi.org/10.4103/2152-7806.148847

  79. Lopes DK, Moftakhar R, Straus D, Munich SA, Chaus F, Kaszuba MC (2016) Arteriovenous malformation embocure score: AVMES. J Neurointerv Surg 8(7):685–691. (In eng). https://doi.org/10.1136/neurintsurg-2015-011779

  80. Feghali J, Yang W, Xu R et al (2019) R(2)eD AVM Score. Stroke J Cereb Circ 50(7):1703–1710. (In eng). https://doi.org/10.1161/strokeaha.119.025054

  81. Rangwala SD, Albanese JS, Slingerland AL et al (2023) External validation of the R2eD AVM scoring system to assess rupture risk in pediatric AVM patients. J Neurosurg Pediatr 31(5):469–475. https://doi.org/10.3171/2023.1.PEDS22310

    Article  PubMed  Google Scholar 

  82. Chen Y, Han H, Meng X et al (2023) Development and validation of a scoring system for hemorrhage risk in brain arteriovenous malformations. JAMA Netw Open 6(3):e231070. (In eng). https://doi.org/10.1001/jamanetworkopen.2023.1070

  83. Stapf C, Mast H, Sciacca RR et al (2006) Predictors of hemorrhage in patients with untreated brain arteriovenous malformation. Neurology 66(9):1350–1355. (In eng). https://doi.org/10.1212/01.wnl.0000210524.68507.87

  84. Ter Brugge K, Lasjaunias P, Chiu M, Flodmark O, Chuang S, Burrows P (1986) Pediatric surgical neuroangiography. A multicentre approach. Acta Radiol Suppl 369:692–693. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=2980598

  85. Humphreys RP, Hoffman HJ, Drake JM, Rutka JT (1996) Choices in the 1990s for the management of pediatric cerebral arteriovenous malformations. Pediatr Neurosurg 25(6):277–285. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=9348147

  86. Hoh BL, Chapman PH, Loeffler JS, Carter BS, Ogilvy CS (2002) Results of multimodality treatment for 141 patients with brain arteriovenous malformations and seizures: factors associated with seizure incidence and seizure outcomes. Neurosurgery 51(2):303–309; discussion 309–311. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=12182768

  87. Lee BB, Do YS, Yakes W, Kim DI, Mattassi R, Hyon WS (2004) Management of arteriovenous malformations: a multidisciplinary approach. J Vasc Surg 39(3):590–600. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=14981454

  88. Raygor K PR, Rutledge C et al (2022) Socioeconomic factors associated with pediatric moyamoya disease hospitalizations: a nationwide cross-sectional study. J Neurosurg Pediatr. In press

  89. Vinchon M, Toubol A, Karnoub MA, Aboukais R, Leclerc X, Reyns N (2023) Unruptured cerebral arteriovenous malformation in children: outcome in treated and untreated patients. Neurochirurgie 69(3):101440. https://doi.org/10.1016/j.neuchi.2023.101440

  90. Montaser A, Smith ER (2021) Intracranial vascular abnormalities in children. Pediatr Clin North Am 68(4):825–843. https://doi.org/10.1016/j.pcl.2021.04.010

    Article  PubMed  Google Scholar 

  91. Fullerton HJ, Achrol AS, Johnston SC et al (2005) Long-term hemorrhage risk in children versus adults with brain arteriovenous malformations. Stroke; a journal of cerebral circulation 36(10):2099–2104. https://doi.org/10.1161/01.STR.0000181746.77149.2b

    Article  Google Scholar 

  92. Chowdhury SS, See AP, Eriksson LP et al (2022) Closing the gap in pediatric hemorrhagic stroke: a systematic review. Semin Pediatr Neurol 43:101001. https://doi.org/10.1016/j.spen.2022.101001

  93. Ciochon UM, Bindslev JBB, Hoei-Hansen CE et al (2022) Causes and risk factors of pediatric spontaneous intracranial hemorrhage-a systematic review. Diagnostics (Basel) 12(6). https://doi.org/10.3390/diagnostics12061459

  94. Ferriero DM, Fullerton HJ, Bernard TJ et al (2019) Management of stroke in neonates and children: a scientific statement from the American Heart Association/American Stroke Association. Stroke; a journal of cerebral circulation 50(3):e51–e96. https://doi.org/10.1161/STR.0000000000000183

    Article  Google Scholar 

  95. Sanchez-Mejia RO, Chennupati SK, Gupta N, Fullerton H, Young WL, Lawton MT (2006) Superior outcomes in children compared with adults after microsurgical resection of brain arteriovenous malformations. J Neurosurg 105(2 Suppl):82–87. https://doi.org/10.3171/ped.2006.105.2.82

    Article  PubMed  Google Scholar 

  96. Mohr JP, Parides MK, Stapf C et al (2014) Medical management with or without interventional therapy for unruptured brain arteriovenous malformations (ARUBA): a multicentre, non-blinded, randomised trial. Lancet 383(9917):614–621. https://doi.org/10.1016/S0140-6736(13)62302-8

    Article  CAS  PubMed  Google Scholar 

  97. Pinkiewicz M, Pinkiewicz M, Walecki J, Zawadzki M (2022) State of the art in the role of endovascular embolization in the management of brain arteriovenous malformations-a systematic review. J Clin Med 11(23). https://doi.org/10.3390/jcm11237208

  98. Ravindra VM, Bollo RJ, Eli IM et al (2019) A study of pediatric cerebral arteriovenous malformations: clinical presentation, radiological features, and long-term functional and educational outcomes with predictors of sustained neurological deficits. J Neurosurg Pediatr 24(1):1–8. https://doi.org/10.3171/2019.2.PEDS18731

    Article  PubMed  Google Scholar 

  99. Burke RM, Chen CJ, Ding D et al (2021) Effect of prior embolization on outcomes after stereotactic radiosurgery for pediatric brain arteriovenous malformations: an international multicenter study. Neurosurgery 89(4):672–679. https://doi.org/10.1093/neuros/nyab245

    Article  PubMed  Google Scholar 

  100. De Leacy R, Ansari SA, Schirmer CM et al (2022) Endovascular treatment in the multimodality management of brain arteriovenous malformations: report of the Society of NeuroInterventional Surgery Standards and Guidelines Committee. J Neurointerv Surg 14(11):1118–1124. https://doi.org/10.1136/neurintsurg-2021-018632

    Article  PubMed  Google Scholar 

  101. Rodriguez-Calienes A, Vivanco-Suarez J, Borjas-Calderon NF et al (2023) Curative embolization of ruptured pediatric cerebral arteriovenous malformations. Clin Neurol Neurosurg 227:107663. https://doi.org/10.1016/j.clineuro.2023.107663

  102. Razavi SAS, Mirbolouk MH, Gorji R et al (2022) Endovascular treatment as the first-line approach for cure of low-grade brain arteriovenous malformation. Neurosurg Focus 53(1):E8. https://doi.org/10.3171/2022.4.FOCUS22122

    Article  PubMed  Google Scholar 

  103. Hak JF, Boulouis G, Kerleroux B et al (2022) Pediatric brain arteriovenous malformation recurrence: a cohort study, systematic review and meta-analysis. J Neurointerv Surg 14(6):611–617. https://doi.org/10.1136/neurintsurg-2021-017777

    Article  PubMed  Google Scholar 

  104. Lindqvist M, Karlsson B, Guo WY, Kihlstrom L, Lippitz B, Yamamoto M (2000) Angiographic long-term follow-up data for arteriovenous malformations previously proven to be obliterated after gamma knife radiosurgery. Neurosurgery 46(4):803–808; discussion 809–810. http://www.ncbi.nlm.nih.gov/pubmed/10764252

  105. Winkler EA, Lu A, Morshed RA et al (2020) Bringing high-grade arteriovenous malformations under control: clinical outcomes following multimodality treatment in children. J Neurosurg Pediatr 26(1):82–91. https://doi.org/10.3171/2020.1.PEDS19487

    Article  PubMed  Google Scholar 

  106. Yamamoto M, Akabane A, Matsumaru Y, Higuchi Y, Kasuya H, Urakawa Y (2012) Long-term follow-up results of intentional 2-stage Gamma Knife surgery with an interval of at least 3 years for arteriovenous malformations larger than 10 cm(3). J Neurosurg 117(Suppl):126–134. https://doi.org/10.3171/2012.6.GKS12757

    Article  PubMed  Google Scholar 

  107. Seymour ZA, Sneed PK, Gupta N et al (2016) Volume-staged radiosurgery for large arteriovenous malformations: an evolving paradigm. J Neurosurg 124(1):163–174. https://doi.org/10.3171/2014.12.JNS141308

    Article  PubMed  Google Scholar 

  108. Nicolato A, Longhi M, Tommasi N et al (2015) Leksell Gamma Knife for pediatric and adolescent cerebral arteriovenous malformations: results of 100 cases followed up for at least 36 months. J Neurosurg Pediatr 16(6):736–747. https://doi.org/10.3171/2015.4.PEDS158

    Article  PubMed  Google Scholar 

  109. Thiex R, Mulliken JB, Revencu N et al (2010) A novel association between RASA1 mutations and spinal arteriovenous anomalies. AJNR Am J Neuroradiol 31(4):775–779. (In eng). https://doi.org/10.3174/ajnr.A1907

  110. Lasjaunias P (1997) Vascular Diseases in Neonates. Springer Verlag, Infants and Children

    Book  Google Scholar 

  111. Faughnan ME, Palda VA, Garcia-Tsao G et al (2011) International guidelines for the diagnosis and management of hereditary haemorrhagic telangiectasia. J Med Genet 48(2):73–87. https://doi.org/10.1136/jmg.2009.069013

    Article  CAS  PubMed  Google Scholar 

  112. Latino GA, Al-Saleh S, Carpenter S, Ratjen F (2014) The diagnostic yield of rescreening for arteriovenous malformations in children with hereditary hemorrhagic telangiectasia. J Pediatr 165(1):197–199. https://doi.org/10.1016/j.jpeds.2014.03.040

    Article  PubMed  Google Scholar 

  113. Shovlin CL, Guttmacher AE, Buscarini E et al (2000) Diagnostic criteria for hereditary hemorrhagic telangiectasia (Rendu-Osler-Weber syndrome). Am J Med Genet 91(1):66–67. https://www.ncbi.nlm.nih.gov/pubmed/10751092

  114. Starke RM, Ding D, Kano H et al (2017) International multicenter cohort study of pediatric brain arteriovenous malformations. Part 2: Outcomes after stereotactic radiosurgery. J Neurosurg Pediatr 19(2):136–148. https://doi.org/10.3171/2016.9.PEDS16284

  115. Borcek AO, Emmez H, Akkan KM et al (2014) Gamma Knife radiosurgery for arteriovenous malformations in pediatric patients. Childs Nerv Syst 30(9):1485–1492. https://doi.org/10.1007/s00381-014-2469-5

    Article  PubMed  Google Scholar 

  116. Potts MB, Jahangiri A, Jen M et al (2014) Deep arteriovenous malformations in the basal ganglia, thalamus, and insula: multimodality management, patient selection, and results. World neurosurgery 82(3–4):386–394. https://doi.org/10.1016/j.wneu.2014.03.033

    Article  PubMed  PubMed Central  Google Scholar 

  117. Blauwblomme T, Bourgeois M, Meyer P et al (2014) Long-term outcome of 106 consecutive pediatric ruptured brain arteriovenous malformations after combined treatment. Stroke; a journal of cerebral circulation 45(6):1664–1671. https://doi.org/10.1161/STROKEAHA.113.004292

    Article  Google Scholar 

  118. Reitz M, von Spreckelsen N, Vettorazzi E et al (2016) Angioarchitectural risk factors for hemorrhage and clinical long-term outcome in pediatric patients with cerebral arteriovenous malformations. World neurosurgery 89:540–551. https://doi.org/10.1016/j.wneu.2016.02.050

    Article  PubMed  Google Scholar 

  119. Patibandla MR, Ding D, Xu Z, Sheehan JP (2017) Stereotactic radiosurgery for pediatric high-grade brain arteriovenous malformations: our experience and review of literature. World neurosurgery 102:613–622. https://doi.org/10.1016/j.wneu.2017.03.064

    Article  PubMed  Google Scholar 

  120. Aboukais R, Vinchon M, Quidet M, Bourgeois P, Leclerc X, Lejeune JP (2017) Reappearance of arteriovenous malformations after complete resection of ruptured arteriovenous malformations: true recurrence or false-negative early postoperative imaging result? J Neurosurg 126(4):1088–1093. https://doi.org/10.3171/2016.3.JNS152846

    Article  PubMed  Google Scholar 

  121. Morgenstern PF, Hoffman CE, Kocharian G, Singh R, Stieg PE, Souweidane MM (2015) Postoperative imaging for detection of recurrent arteriovenous malformations in children. J Neurosurg Pediatr 1–7. https://doi.org/10.3171/2015.6.PEDS14708

  122. Lang SS, Beslow LA, Bailey RL et al (2012) Follow-up imaging to detect recurrence of surgically treated pediatric arteriovenous malformations. J Neurosurg Pediatr 9(5):497–504. https://doi.org/10.3171/2012.1.PEDS11453

    Article  PubMed  PubMed Central  Google Scholar 

  123. Graffeo CS, Bhandarkar AR, Carlstrom LP et al (2023) That which is unseen: 3D printing for pediatric cerebrovascular education. Childs Nerv Syst. https://doi.org/10.1007/s00381-023-05987-0

    Article  PubMed  Google Scholar 

  124. Fehnel KP, Penn DL, Duggins-Warf M et al (2020) Dysregulation of the EphrinB2-EphB4 ratio in pediatric cerebral arteriovenous malformations is associated with endothelial cell dysfunction in vitro and functions as a novel noninvasive biomarker in patients. Exp Mol Med 52(4):658–671. https://doi.org/10.1038/s12276-020-0414-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Goss JA, Huang AY, Smith E et al (2019) Somatic mutations in intracranial arteriovenous malformations. PLoS One 14(12):e0226852. https://doi.org/10.1371/journal.pone.0226852

  126. Fish JE, Flores-Suarez CP, Boudreau E et al (2020) Somatic gain of KRAS function in the endothelium is sufficient to cause vascular malformations that Require MEK but not PI3K Signaling. Circ Res. https://doi.org/10.1161/CIRCRESAHA.119.316500

    Article  PubMed  PubMed Central  Google Scholar 

  127. Kahle KT, Duran D, Smith ER (2023) Increasing precision in the management of pediatric neurosurgical cerebrovascular diseases with molecular genetics. J Neurosurg Pediatr 31(3):228–237. https://doi.org/10.3171/2022.12.PEDS22332

    Article  PubMed  Google Scholar 

  128. Zeng X, Hunt A, Jin SC, Duran D, Gaillard J, Kahle KT (2019) EphrinB2-EphB4-RASA1 signaling in human cerebrovascular development and disease. Trends Mol Med 25(4):265–286. https://doi.org/10.1016/j.molmed.2019.01.009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Copelan A, Drocton G, Caton MT et al (2020) Brain arteriovenous malformation recurrence after apparent microsurgical cure: increased risk in children who present with arteriovenous malformation rupture. Stroke; a journal of cerebral circulation 51(10):2990–2996. https://doi.org/10.1161/STROKEAHA.120.030135

    Article  CAS  Google Scholar 

  130. Sesen J, Driscoll J, Moses-Gardner A, Orbach DB, Zurakowski D, Smith ER (2021) Non-invasive urinary biomarkers in moyamoya disease. Front Neurol 12:661952. https://doi.org/10.3389/fneur.2021.661952

  131. Baxter PA, Su JM, Onar-Thomas A et al (2020) A phase I/II study of veliparib (ABT-888) with radiation and temozolomide in newly diagnosed diffuse pontine glioma: a Pediatric Brain Tumor Consortium study. Neuro Oncol 22(6):875–885. https://doi.org/10.1093/neuonc/noaa016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  132. Smith ER, Zurakowski D, Saad A, Scott RM, Moses MA (2008) Urinary biomarkers predict brain tumor presence and response to therapy. Clin Cancer Res 14(8):2378–2386. (In eng). https://doi.org/10.1158/1078-0432.Ccr-07-1253

  133. Smith ER, Manfredi M, Scott RM, Black PM, Moses MA (2007) A recurrent craniopharyngioma illustrates the potential usefulness of urinary matrix metalloproteinases as noninvasive biomarkers: case report. Neurosurgery 60(6):E1148–9; discussion E1149. (In eng). http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=17538362

Download references

Author information

Authors and Affiliations

Authors

Contributions

ERS and APS wrote the manuscript and reviewed it together.

Corresponding author

Correspondence to Edward R. Smith.

Ethics declarations

Conflict of interests

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

See, A.P., Smith, E.R. Evolution of clinical and translational advances in the management of pediatric arteriovenous malformations. Childs Nerv Syst 39, 2807–2818 (2023). https://doi.org/10.1007/s00381-023-06077-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00381-023-06077-x

Keywords

Navigation