J Korean Neurosurg Soc.  2024 May;67(3):289-298. 10.3340/jkns.2024.0027.

Management of Pediatric Intracranial Arteriovenous Malformations

Affiliations
  • 1Department of Neurosurgery, Boston Children’s Hospital, Harvard Medical School, Boston, MA, USA

Abstract

Pediatric intracranial arteriovenous malformations (AVMs) are challenging lesions managed by pediatric neurosurgeons. The high risk of hemorrhage and neurologic injury is compounded by the unique anatomy of each malformation that requires individualizing treatment options. This article reviews the current status of pediatric AVM epidemiology, pathophysiology and clinical care, with a specific focus on the rationale and methodology of surgical resection.

Keyword

Arteriovenous malformations; Pediatrics; Perioperative care; Stroke

Figure

  • Fig. 1. Use of an intraoperative ultrasound to help localize clot (red arrowhead on CT) and AVM nidus (blue arrowhead on CTA) in order to guide controlled decompression of the clot through a small dural opening in advance of a wider exposure. Using the Doppler flow settings can be particularly helpful to visualize AVM, especially when paired with CT/CTA studies. CT : computed tomography, AVM : arteriovenous malformation, CTA : computed tomography angiography.

  • Fig. 2. Angiographic correlation with intraoperative photograph highlighting conical shape of arteriovenous malformation, including both surface findings and surgical technique of working around the “cone” of the nidus, walling the margins off with cottonoids.

  • Fig. 3. Intraoperative microscope images demonstrating small tuft of arterial vessels near ependyma of ventricle at base of arteriovenous malformation (left image, blue arrowhead) with subsequent cauterization and division of these feeders (right image). In addition, this image also highlights the utility of having an assistant working under the microscope to improve visualization and minimize prolonged retraction on adjacent brain.


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Reference

References

1. Abla AA, Rutledge WC, Seymour ZA, Guo D, Kim H, Gupta N, et al. A treatment paradigm for high-grade brain arteriovenous malformations: volume-staged radiosurgical downgrading followed by microsurgical resection. J Neurosurg. 122:419–432. 2015.
Article
2. Aboukaïs R, Vinchon M, Quidet M, Bourgeois P, Leclerc X, Lejeune JP. Reappearance of arteriovenous malformations after complete resection of ruptured arteriovenous malformations: true recurrence or falsenegative early postoperative imaging result? J Neurosurg. 126:1088–1093. 2017.
Article
3. Adil MM, Qureshi AI, Beslow LA, Malik AA, Jordan LC. Factors associated with increased in-hospital mortality among children with intracerebral hemorrhage. J Child Neurol. 30:1024–1028. 2015.
Article
4. Al-Jarallah A, Al-Rifai MT, Riela AR, Roach ES. Nontraumatic brain hemorrhage in children: etiology and presentation. J Child Neurol. 15:284–289. 2000.
Article
5. Altschuler E, Lunsford LD, Kondziolka D, Wu A, Maitz AH, Sclabassi R, et al. Radiobiologic models for radiosurgery. Neurosurg Clin N Am. 3:61–77. 1992.
Article
6. Andrade-Souza YM, Zadeh G, Ramani M, Scora D, Tsao MN, Schwartz ML. Testing the radiosurgery-based arteriovenous malformation score and the modified Spetzler-Martin grading system to predict radiosurgical outcome. J Neurosurg. 103:642–648. 2005.
Article
7. Beslow LA, Licht DJ, Smith SE, Storm PB, Heuer GG, Zimmerman RA, et al. Predictors of outcome in childhood intracerebral hemorrhage: a prospective consecutive cohort study. Stroke. 41:313–318. 2010.
Article
8. Blauwblomme T, Bourgeois M, Meyer P, Puget S, Di Rocco F, Boddaert N, et al. Long-term outcome of 106 consecutive pediatric ruptured brain arteriovenous malformations after combined treatment. Stroke. 45:1664–1671. 2014.
Article
9. Boon LM, Mulliken JB, Vikkula M. RASA1: variable phenotype with capillary and arteriovenous malformations. Curr Opin Genet Dev. 15:265–269. 2005.
Article
10. Börcek AÖ, Emmez H, Akkan KM, Öcal Ö, Kurt G, Aykol S, et al. Gamma Knife radiosurgery for arteriovenous malformations in pediatric patients. Childs Nerv Syst. 30:1485–1492. 2014.
Article
11. Broderick J, Talbot GT, Prenger E, Leach A, Brott T. Stroke in children within a major metropolitan area: the surprising importance of intracerebral hemorrhage. J Child Neurol. 8:250–255. 1993.
Article
12. Brown RD Jr, Wiebers DO, Torner JC, O’Fallon WM. Incidence and prevalence of intracranial vascular malformations in Olmsted County, Minnesota, 1965 to 1992. Neurology. 46:949–952. 1996.
Article
13. Celli P, Ferrante L, Palma L, Cavedon G. Cerebral arteriovenous malformations in children. Clinical features and outcome of treatment in children and in adults. Surg Neurol. 22:43–49. 1984.
Article
14. D’Aliberti G, Talamonti G, Versari PP, Todaro C, Bizzozero L, Arena O, et al. Comparison of pediatric and adult cerebral arteriovenous malformations. J Neurosurg Sci. 41:331–336. 1997.
15. Dawson RC 3rd, Tarr RW, Hecht ST, Jungreis CA, Lunsford LD, Coffey R, et al. Treatment of arteriovenous malformations of the brain with combined embolization and stereotactic radiosurgery: results after 1 and 2 years. AJNR Am J Neuroradiol. 11:857–864. 1990.
16. Di Rocco C, Tamburrini G, Rollo M. Cerebral arteriovenous malformations in children. Acta Neurochir (Wien). 142:145–156. discussion 156-158. 2000.
Article
17. Ding D, Starke RM, Kano H, Mathieu D, Huang PP, Feliciano C, et al. International multicenter cohort study of pediatric brain arteriovenous malformations. Part 1: predictors of hemorrhagic presentation. J Neurosurg Pediatr. 19:127–135. 2017.
Article
18. Dumont TM, Kan P, Snyder KV, Hopkins LN, Siddiqui AH, Levy EI. A proposed grading system for endovascular treatment of cerebral arteriovenous malformations: Buffalo score. Surg Neurol Int. 6:3. 2015.
Article
19. Elhadi AM, Zabramski JM, Almefty KK, Mendes GA, Nakaji P, McDougall CG, et al. Spontaneous subarachnoid hemorrhage of unknown origin: hospital course and long-term clinical and angiographic follow-up. J Neurosurg. 122:663–670. 2015.
Article
20. Ellis MJ, Armstrong D, Dirks PB. Large vascular malformation in a child presenting with vascular steal phenomenon managed with pial synangiosis. J Neurosurg Pediatr. 7:15–21. 2011.
Article
21. Ellis MJ, Armstrong D, Vachhrajani S, Kulkarni AV, Dirks PB, Drake JM, et al. Angioarchitectural features associated with hemorrhagic presentation in pediatric cerebral arteriovenous malformations. J Neurointerv Surg. 5:191–195. 2013.
Article
22. Feliciano CE, de León-Berra R, Hernández-Gaitán MS, Rodríguez-Mercado R. A proposal for a new arteriovenous malformation grading scale for neuroendovascular procedures and literature review. P R Health Sci J. 29:117–120. 2010.
23. Ferriero DM, Fullerton HJ, Bernard TJ, Billinghurst L, Daniels SR, DeBaun MR, et al. Management of stroke in neonates and children: a scientific statement from the American Heart Association/American Stroke Association. Stroke. 50:e51–e96. 2019.
Article
24. Fullerton HJ, Achrol AS, Johnston SC, McCulloch CE, Higashida RT, Lawton MT, et al. Long-term hemorrhage risk in children versus adults with brain arteriovenous malformations. Stroke. 36:2099–2104. 2005.
Article
25. Gold JJ, Crawford JR. Acute hemiparesis in a child as a presenting symptom of hemispheric cerebral proliferative angiopathy. Case Rep Neurol Med. 2013:920859. 2013.
Article
26. Goss JA, Huang AY, Smith E, Konczyk DJ, Smits PJ, Sudduth CL, et al. Somatic mutations in intracranial arteriovenous malformations. PLoS One. 14:e0226852. 2019.
Article
27. Graf CJ, Perret GE, Torner JC. Bleeding from cerebral arteriovenous malformations as part of their natural history. J Neurosurg. 58:331–337. 1983.
Article
28. Gross BA, Scott RM, Smith ER. Management of brain arteriovenous malformations. Lancet. 383:1635. 2014.
Article
29. Gross BA, Storey A, Orbach DB, Scott RM, Smith ER. Microsurgical treatment of arteriovenous malformations in pediatric patients: the Boston Children’s Hospital experience. J Neurosurg Pediatr. 15:71–77. 2015.
Article
30. Gupta R, Adeeb N, Moore JM, Motiei-Langroudi R, Griessenauer CJ, Patel AS, et al. Validity assessment of grading scales predicting complications from embolization of cerebral arteriovenous malformations. Clin Neurol Neurosurg. 151:102–107. 2016.
Article
31. Hamilton MG, Spetzler RF. The prospective application of a grading system for arteriovenous malformations. Neurosurgery. 34:2–6. discussion 6-7. 1994.
Article
32. Heros RC, Korosue K, Diebold PM. Surgical excision of cerebral arteriovenous malformations: late results. Neurosurgery. 26:570–577. discussion 577-578. 1990.
Article
33. Hoh BL, Chapman PH, Loeffler JS, Carter BS, Ogilvy CS. Results of multimodality treatment for 141 patients with brain arteriovenous malformations and seizures: factors associated with seizure incidence and seizure outcomes. Neurosurgery. 51:303–309. discussion 309-311. 2002.
Article
34. Humphreys RP, Hoffman HJ, Drake JM, Rutka JT. Choices in the 1990s for the management of pediatric cerebral arteriovenous malformations. Pediatr Neurosurg. 25:277–285. 1996.
Article
35. Itoyama Y, Uemura S, Ushio Y, Kuratsu J, Nonaka N, Wada H, et al. Natural course of unoperated intracranial arteriovenous malformations: study of 50 cases. J Neurosurg. 71:805–809. 1989.
Article
36. Jessurun GA, Kamphuis DJ, van der Zande FH, Nossent JC. Cerebral arteriovenous malformations in The Netherlands Antilles. High prevalence of hereditary hemorrhagic telangiectasia-related single and multiple cerebral arteriovenous malformations. Clin Neurol Neurosurg. 95:193–198. 1993.
37. Jin H, Jiang Y, Ge H, Luo J, Li C, Wu H, et al. Comparison of grading scales regarding perioperative complications and clinical outcomes of brain arteriovenous malformations after endovascular therapy-multicenter study. World Neurosurg. 106:394–401. 2017.
Article
38. Jomin M, Lesoin F, Lozes G. Prognosis for arteriovenous malformations of the brain in adults based on 150 cases. Surg Neurol. 23:362–366. 1985.
Article
39. Jordan LC, Kleinman JT, Hillis AE. Intracerebral hemorrhage volume predicts poor neurologic outcome in children. Stroke. 40:1666–1671. 2009.
Article
40. Kader A, Goodrich JT, Sonstein WJ, Stein BM, Carmel PW, Michelsen WJ. Recurrent cerebral arteriovenous malformations after negative postoperative angiograms. J Neurosurg. 85:14–18. 1996.
Article
41. Kahl W, Kessel G, Schwarz M, Voth D. Arterio-venous malformations in childhood: clinical presentation, results after operative treatment and long-term follow-up. Neurosurg Rev. 12:165–171. 1989.
Article
42. Kahle KT, Duran D, Smith ER. Increasing precision in the management of pediatric neurosurgical cerebrovascular diseases with molecular genetics. J Neurosurg Pediatr. 31:228–237. 2023.
Article
43. Kiriş T, Sencer A, Sahinbaş M, Sencer S, Imer M, Izgi N. Surgical results in pediatric Spetzler-Martin grades I-III intracranial arteriovenous malformations. Childs Nerv Syst. 21:69–74. discussion 75-76. 2005.
Article
44. Lang SS, Beslow LA, Bailey RL, Vossough A, Ekstrom J, Heuer GG, et al. Follow-up imaging to detect recurrence of surgically treated pediatric arteriovenous malformations. J Neurosurg Pediatr. 9:497–504. 2012.
Article
45. Lasjaunias P : Vascular Diseases in Neonates, Infants and Children. Berlin : Springer Verlag, 1997.
46. Lasjaunias PL, Landrieu P, Rodesch G, Alvarez H, Ozanne A, Holmin S, et al. Cerebral proliferative angiopathy: clinical and angiographic description of an entity different from cerebral AVMs. Stroke. 39:878–885. 2008.
47. Lawton MT; UCSF Brain Arteriovenous Malformation Study Project. Spetzler-Martin grade III arteriovenous malformations: surgical results and a modification of the grading scale. Neurosurgery. 52:740–748. discussion 748-749. 2003.
Article
48. Lawton MT, Kim H, McCulloch CE, Mikhak B, Young WL. A supplementary grading scale for selecting patients with brain arteriovenous malformations for surgery. Neurosurgery. 66:702–713. discussion 713. 2010.
Article
49. Lee BB, Do YS, Yakes W, Kim DI, Mattassi R, Hyon WS. Management of arteriovenous malformations: a multidisciplinary approach. J Vasc Surg. 39:590–600. 2004.
Article
50. Lin N, Smith ER, Scott RM, Orbach DB. Safety of neuroangiography and embolization in children: complication analysis of 697 consecutive procedures in 394 patients. J Neurosurg Pediatr. 16:432–438. 2015.
Article
51. Liu J, Wang D, Lei C, Xiong Y, Yuan R, Hao Z, et al. Etiology, clinical characteristics and prognosis of spontaneous intracerebral hemorrhage in children: a prospective cohort study in China. J Neurol Sci. 358:367–370. 2015.
Article
52. Lopes DK, Moftakhar R, Straus D, Munich SA, Chaus F, Kaszuba MC. Arteriovenous malformation embocure score: AVMES. J Neurointerv Surg. 8:685–691. 2016.
Article
53. Maher CO, Scott RM. Linear vein-based arteriovenous malformations in children. J Neurosurg Pediatr. 4:12–16. 2009.
Article
54. Mohr JP, Parides MK, Stapf C, Moquete E, Moy CS, Overbey JR, et al. Medical management with or without interventional therapy for unruptured brain arteriovenous malformations (ARUBA): a multicentre, nonblinded, randomised trial. Lancet. 383:614–621. 2014.
Article
55. Morgan MK, Rochford AM, Tsahtsarlis A, Little N, Faulder KC. Surgical risks associated with the management of grade I and II brain arteriovenous malformations. Neurosurgery. 54:832–837. discussion 837-839. 2004.
Article
56. Morgenstern PF, Hoffman CE, Kocharian G, Singh R, Stieg PE, Souweidane MM. Postoperative imaging for detection of recurrent arteriovenous malformations in children. J Neurosurg Pediatr. 17:134–140. 2015.
Article
57. Newton TH, Cronqvist S. Involvement of dural arteries in intracranial arteriovenous malformations. Radiology. 93:1071–1078. 1969.
Article
58. Ogilvy CS, Stieg PE, Awad I, Brown RD Jr, Kondziolka D, Rosenwasser R, et al. 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. Circulation. 103:2644–2657. 2001.
Article
59. Olivecrona H, Riives J. Arteriovenous aneurysms of the brain, their diagnosis and treatment. Arch Neurol Psychiatry. 59:567–603. 1948.
60. Orbach DB, Stamoulis C, Strauss KJ, Manchester J, Smith ER, Scott RM, et al. Neurointerventions in children: radiation exposure and its import. AJNR Am J Neuroradiol. 35:650–656. 2014.
Article
61. Pollock BE. Development and testing of a radiosurgery-based arteriovenous malformation grading system. Prog Neurol Surg. 27:58–66. 2013.
Article
62. Pollock BE, Flickinger JC. A proposed radiosurgery-based grading system for arteriovenous malformations. J Neurosurg. 96:79–85. 2002.
Article
63. Pollock BE, Flickinger JC. Modification of the radiosurgery-based arteriovenous malformation grading system. Neurosurgery. 63:239–243. discussion 243. 2008.
Article
64. Pott M, Huber M, Assheuer J, Bewermeyer H. Comparison of MRI, CT and angiography in cerebral arteriovenous malformations. Bildgebung. 59:98–102. 1992.
65. Pulli B, Stapleton CJ, Walcott BP, Koch MJ, Raymond SB, Leslie-Mazwi TM, et al. Comparison of predictive grading systems for procedural risk in endovascular treatment of brain arteriovenous malformations: analysis of 104 consecutive patients. J Neurosurg. 133:342–350. 2019.
Article
66. Rangwala SD, Albanese JS, Slingerland AL, Papadakis JE, Weber DS, Smith ER, et al. External validation of the R2eD AVM scoring system to assess rupture risk in pediatric AVM patients. J Neurosurg Pediatr. 31:469–475. 2023.
Article
67. Ravindra VM, Karsy M, Lanpher A, Bollo RJ, Griauzde J, Scott RM, et al. A national analysis of 9655 pediatric cerebrovascular malformations: effect of hospital volume on outcomes. J Neurosurg Pediat. 24:397–406. 2019.
Article
68. Rieger J, Hosten N, Neumann K, Langer R, Molsen P, Lanksch WR, et al. Initial clinical experience with spiral CT and 3D arterial reconstruction in intracranial aneurysms and arteriovenous malformations. Neuroradiology. 38:245–251. 1996.
Article
69. See AP, Mohammaden MH, Rizko M, Stapleton CJ, Amin-Hanjani S, Charbel FT, et al. Morbidity and mortality associated with sequential flow reduction embolization technique of cerebral arteriovenous malformations using n-butyl cyanoacrylate. J Neurointerv Surg. 13:237–241. 2021.
Article
70. Seymour ZA, Sneed PK, Gupta N, Lawton MT, Molinaro AM, Young W, et al. Volume-staged radiosurgery for large arteriovenous malformations: an evolving paradigm. J Neurosurg. 124:163–174. 2016.
Article
71. Spetzler RF, Martin NA. A proposed grading system for arteriovenous malformations. J Neurosurg. 65:476–483. 1986.
Article
72. Spetzler RF, Ponce FA. A 3-tier classification of cerebral arteriovenous malformations. Clinical article. J Neurosurg. 114:842–849. 2011.
73. Starke RM, Ding D, Kano H, Mathieu D, Huang PP, Feliciano C, et al. International multicenter cohort study of pediatric brain arteriovenous malformations. Part 2: outcomes after stereotactic radiosurgery. J Neurosurg Pediatr. 19:136–148. 2017.
Article
74. Starke RM, Yen CP, Ding D, Sheehan JP. A practical grading scale for predicting outcome after radiosurgery for arteriovenous malformations: analysis of 1012 treated patients. J Neurosurg. 119:981–987. 2013.
Article
75. Tan CL, Li DT, Shen SB. Detection of brain vascular diseases with CT angiography. Hunan Yi Ke Da Xue Xue Bao. 26:460–462. 2001.
76. Ter Brugge K, Lasjaunias P, Chiu M, Flodmark O, Chuang S, Burrows P. Pediatric surgical neuroangiography. A multicentre approach. Acta Radiol Suppl. 369:692–693. 1986.
77. Thiex R, Mulliken JB, Revencu N, Boon LM, Burrows PE, Cordisco M, et al. A novel association between RASA1 mutations and spinal arteriovenous anomalies. AJNR Am J Neuroradiol. 31:775–779. 2010.
Article
78. Wegner RE, Oysul K, Pollock BE, Sirin S, Kondziolka D, Niranjan A, et al. A modified radiosurgery-based arteriovenous malformation grading scale and its correlation with outcomes. Int J Radiat Oncol Biol Phys. 79:1147–1150. 2011.
Article
79. Weinstock P, Prabhu SP, Flynn K, Orbach DB, Smith E. Optimizing cerebrovascular surgical and endovascular procedures in children via personalized 3D printing. J Neurosurg Pediatr. 16:584–589. 2015.
Article
80. Wilkins RH. Natural history of intracranial vascular malformations: a review. Neurosurgery. 16:421–430. 1985.
Article
81. Yeung R, Ahmad T, Aviv RI, de Tilly LN, Fox AJ, Symons SP. Comparison of CTA to DSA in determining the etiology of spontaneous ICH. Can J Neurol Sci. 36:176–180. 2009.
Article
82. Young WL, Pile-Spellman J. Anesthetic considerations for interventional neuroradiology. Anesthesiology. 80:427–456. 1994.
Article
83. Young WL, Pile-Spellman J, Prohovnik I, Kader A, Stein BM. Evidence for adaptive autoregulatory displacement in hypotensive cortical territories adjacent to arteriovenous malformations. Columbia University AVM study project. Neurosurgery. 34:601–610. discussion 610-611. 1994.
Article
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