Natural history and treatment of deep-seated brain arteriovenous malformations in pediatric patients

*Shahab Aldin SattariDepartment of Neurosurgery, Johns Hopkins University School of Medicine, Baltimore, Maryland

Search for other papers by *Shahab Aldin Sattari in
jns
Google Scholar
PubMed
Close
 MD
,
Wuyang YangDepartment of Neurosurgery, Johns Hopkins University School of Medicine, Baltimore, Maryland

Search for other papers by Wuyang Yang in
jns
Google Scholar
PubMed
Close
 MD
,
Risheng XuDepartment of Neurosurgery, Johns Hopkins University School of Medicine, Baltimore, Maryland

Search for other papers by Risheng Xu in
jns
Google Scholar
PubMed
Close
 MD, PhD
,
James FeghaliDepartment of Neurosurgery, Johns Hopkins University School of Medicine, Baltimore, Maryland

Search for other papers by James Feghali in
jns
Google Scholar
PubMed
Close
 MD
,
Rafael J. TamargoDepartment of Neurosurgery, Johns Hopkins University School of Medicine, Baltimore, Maryland

Search for other papers by Rafael J. Tamargo in
jns
Google Scholar
PubMed
Close
 MD
, and
Judy HuangDepartment of Neurosurgery, Johns Hopkins University School of Medicine, Baltimore, Maryland

Search for other papers by Judy Huang in
jns
Google Scholar
PubMed
Close
 MD
Restricted access

Purchase Now

USD  $45.00

JNS + Pediatrics - 1 year subscription bundle (Individuals Only)

USD  $525.00

JNS + Pediatrics + Spine - 1 year subscription bundle (Individuals Only)

USD  $624.00
USD  $45.00
USD  $525.00
USD  $624.00
Print or Print + Online Sign in

OBJECTIVE

Pediatric deep brain arteriovenous malformations (bAVMs) represent a unique management challenge given their higher cumulative risk of hemorrhage as well as a higher risk of treatment. Better understanding of hemorrhage risk in this patient population will lead to a better decision-making process for patient management.

METHODS

The authors retrospectively reviewed their institutional bAVM database from 1990 to 2019 and included patients younger than 21 years who had deep-seated bAVMs. They present the annual hemorrhage risk, during the natural history and after treatment, and functional outcomes.

RESULTS

Thirty-one pediatric patients were included in this study (13 males and 18 females) with a mean age of 11.8 (SD 4.4) years. The most frequent presenting symptoms were headache (54.8%), weakness (38.7%), and seizure (22.6%). The mean follow-up duration was 13.14 (SD 12.5) years, during which 7 (22.6%) AVMs were obliterated, 10 (32.3%) individuals experienced hemorrhage, and the modified Rankin Scale score worsened in 8 (25.8%) patients. The annual natural history risk of hemorrhage was 3.24% per patient, and the overall annual hemorrhage risk after treatment was 1.98% per patient. In particular, the risk was reduced to 0.64% per patient in the stereotactic radiosurgery (SRS) group. Non-White race showed a trend of higher rupture at presentation (OR 5 [95% CI 0.84–41.68], p = 0.09). Female sex was associated with higher odds (OR 13.076 [95% CI 1.424–333.591], p = 0.048) and SRS was associated with lower odds (OR 0.122 [95% CI 0.011–0.862], p = 0.049) of follow-up hemorrhage.

CONCLUSIONS

Given the substantial cumulative risk of lifelong hemorrhagic stroke in pediatric patients, timely definitive treatment is warranted. SRS may be beneficial when the risk-benefit profile is deemed acceptable.

ABBREVIATIONS

AVM = arteriovenous malformation; bAVM = brain AVM; mRS = modified Rankin Scale; SRS = stereotactic radiosurgery.
  • Collapse
  • Expand

Images from Chiang et al. (pp 595–601).

  • 1

    Friedlander RM. Clinical practice. Arteriovenous malformations of the brain. N Engl J Med. 2007;356(26):27042712.

  • 2

    Lawton MT, Rutledge WC, Kim H, et al. Brain arteriovenous malformations. Nat Rev Dis Primers. 2015;1:15008.

  • 3

    Garza-Mercado R, Cavazos E, Tamez-Montes D. Cerebral arteriovenous malformations in children and adolescents. Surg Neurol. 1987;27(2):131140.

  • 4

    Meyer-Heim AD, Boltshauser E. Spontaneous intracranial haemorrhage in children: aetiology, presentation and outcome. Brain Dev. 2003;25(6):416421.

  • 5

    Boulouis G, Stricker S, Benichi S, et al. Etiology of intracerebral hemorrhage in children: cohort study, systematic review, and meta-analysis. J Neurosurg Pediatr. 2021;27(3):357363.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    Buis DR, Dirven CMF, Lagerwaard FJ, et al. Radiosurgery of brain arteriovenous malformations in children. J Neurol. 2008;255(4):551560.

  • 7

    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. 2015;15(1):7177.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 8

    Kondziolka D, Humphreys RP, Hoffman HJ, Hendrick EB, Drake JM. Arteriovenous malformations of the brain in children: a forty year experience. Can J Neurol Sci. 1992;19(1):4045.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Yang W, Anderson-Keightly H, Westbroek EM, et al. Long-term hemorrhagic risk in pediatric patients with arteriovenous malformations. J Neurosurg Pediatr. 2016;18(3):329338.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    LoPresti MA, Giridharan N, Kan P, Lam S. Natural history of high-grade pediatric arteriovenous malformations: implications for management options. Childs Nerv Syst. 2020;36(9):20552061.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Darsaut TE, Guzman R, Marcellus ML, et al. Management of pediatric intracranial arteriovenous malformations: experience with multimodality therapy. Neurosurgery. 2011;69(3):540556.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Ding D, Starke RM, Kano H, et al. International multicenter cohort study of pediatric brain arteriovenous malformations. Part 1: Predictors of hemorrhagic presentation. J Neurosurg Pediatr. 2017;19(2):127135.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Ai X, Ye Z, Xu J, You C, Jiang Y. The factors associated with hemorrhagic presentation in children with untreated brain arteriovenous malformation: a meta-analysis. J Neurosurg Pediatr. 2018;23(3):343354.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Sasaki T, Kurita H, Saito I, et al. Arteriovenous malformations in the basal ganglia and thalamus: management and results in 101 cases. J Neurosurg. 1998;88(2):285292.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    Meling TR, Patet G. What is the best therapeutic approach to a pediatric patient with a deep-seated brain AVM?. Neurosurg Rev. 2019;42(2):409416.

  • 16

    Ellis MJ, Armstrong D, Vachhrajani S, et al. Angioarchitectural features associated with hemorrhagic presentation in pediatric cerebral arteriovenous malformations. J Neurointerv Surg. 2013;5(3):191195.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    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. 1984;22(1):4349.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18

    Kano H, Kondziolka D, Flickinger JC, et al. Stereotactic radiosurgery for arteriovenous malformations, part 2: management of pediatric patients. J Neurosurg Pediatr. 2012;9(1):110.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19

    Al-Shahi R, Warlow C. A systematic review of the frequency and prognosis of arteriovenous malformations of the brain in adults. Brain. 2001;124(Pt 10):19001926.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20

    Liu R, Zhan Y, Piao J, et al. Treatments of unruptured brain arteriovenous malformations: a systematic review and meta-analysis. Medicine (Baltimore). 2021;100(25):e26352.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21

    Oulasvirta E, Koroknay-Pál P, Hafez A, Elseoud AA, Lehto H, Laakso A. Characteristics and long-term outcome of 127 children with cerebral arteriovenous malformations. Neurosurgery. 2019;84(1):151159.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22

    Zheng T, Wang QJ, Liu YQ, et al. Clinical features and endovascular treatment of intracranial arteriovenous malformations in pediatric patients. Childs Nerv Syst. 2014;30(4):647653.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23

    Niazi TN, Klimo P Jr, Anderson RCE, Raffel C. Diagnosis and management of arteriovenous malformations in children. Neurosurg Clin N Am. 2010;21(3):443456.

  • 24

    El-Ghanem M, Kass-Hout T, Kass-Hout O, et al. Arteriovenous malformations in the pediatric population: review of the existing literature. Intervent Neurol. 2016;5(3-4):218225.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 25

    Ma L, Kim H, Chen XL, et al. Morbidity after hemorrhage in children with untreated brain arteriovenous malformation. Cerebrovasc Dis. 2017;43(5-6):231241.

  • 26

    Laakso A, Dashti R, Seppänen J, et al. Long-term excess mortality in 623 patients with brain arteriovenous malformations. Neurosurgery. 2008;63(2):244255.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27

    Smyth MD, Sneed PK, Ciricillo SF, et al. Stereotactic radiosurgery for pediatric intracranial arteriovenous malformations: the University of California at San Francisco experience. J Neurosurg. 2002;97(1):4855.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28

    Pan DHC, Kuo YH, Guo WY, et al. Gamma Knife surgery for cerebral arteriovenous malformations in children: a 13-year experience. J Neurosurg Pediatr. 2008;1(4):296304.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29

    Starke RM, Ding D, Kano H, et al. International multicenter cohort study of pediatric brain arteriovenous malformations. Part 2: Outcomes after stereotactic radiosurgery. J Neurosurg Pediatr. 2017;19(2):136148.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30

    Yen CP, Monteith SJ, Nguyen JH, Rainey J, Schlesinger DJ, Sheehan JP. Gamma Knife surgery for arteriovenous malformations in children. J Neurosurg Pediatr. 2010;6(5):426434.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31

    Sanchez-Mejia RO, Chennupati SK, Gupta N, Fullerton H, Young WL, Lawton MT. Superior outcomes in children compared with adults after microsurgical resection of brain arteriovenous malformations. J Neurosurg. 2006;105(2)(suppl):8287.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32

    Potts MB, Young WL, Lawton MT. Deep arteriovenous malformations in the basal ganglia, thalamus, and insula: microsurgical management, techniques, and results. Neurosurgery. 2013;73(3):417429.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33

    Blauwblomme T, Bourgeois M, Meyer P, et al. Long-term outcome of 106 consecutive pediatric ruptured brain arteriovenous malformations after combined treatment. Stroke. 2014;45(6):16641671.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 34

    Natarajan SK, Ghodke B, Britz GW, Born DE, Sekhar LN. Multimodality treatment of brain arteriovenous malformations with microsurgery after embolization with Onyx: single-center experience and technical nuances. Neurosurgery. 2008;62(6):12131226.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35

    Kocer N, Kandemirli SG, 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. 2019;61(2):195205.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 36

    Russell D, Peck T, Ding D, et al. Stereotactic radiosurgery alone or combined with embolization for brain arteriovenous malformations: a systematic review and meta-analysis. J Neurosurg. 2018;128(5):13381348.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 37

    Xu F, Zhong J, Ray A, Manjila S, Bambakidis NC. Stereotactic radiosurgery with and without embolization for intracranial arteriovenous malformations: a systematic review and meta-analysis. Neurosurg Focus. 2014;37(3):E16.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 38

    Kleinerman RA. Cancer risks following diagnostic and therapeutic radiation exposure in children. Pediatr Radiol. 2006;36(2 Suppl):121125.

  • 39

    Kim H, Sidney S, McCulloch CE, et al. Racial/Ethnic differences in longitudinal risk of intracranial hemorrhage in brain arteriovenous malformation patients. Stroke. 2007;38(9):24302437.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 40

    Feghali J, Yang W, Xu R, et al. R2eD AVM Score. Stroke. 2019;50(7):17031710.

  • 41

    Potts MB, Jahangiri A, Jen M, et al. Deep arteriovenous malformations in the basal ganglia, thalamus, and insula: multimodality management, patient selection, and results. World Neurosurg. 2014;82(3-4):386394.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 42

    Colli A, Pagliaro L, Duca P. The ethical problem of randomization. Intern Emerg Med. 2014;9(7):799804.

Metrics

All Time Past Year Past 30 Days
Abstract Views 1159 1159 43
Full Text Views 241 241 15
PDF Downloads 218 218 20
EPUB Downloads 0 0 0