Endovascular Treatment of Brain Arteriovenous Malformations in Pediatric Patients: A Single Center Experience and Review of the Literature

Abstract

Background Brain arteriovenous malformations (bAVMs) are abnormal vascular connections with direct arteriovenous shunts, generally symptomatic in the adult life. However, a small number of bAVMs may manifest in pediatric patients, with higher bleeding risk and mortality rates when compared to adults. The purpose of this study is to review our experience with endovascular treatment of bAVMs in pediatric patients.

Methods This is a retrospective analysis of all bAVMs in pediatric patients (0–18 years) who underwent diagnostic digital subtraction angiography (DSA) at our institution from January 2010 to June 2021.

Results Twenty-six patients met the inclusion criteria, of which 12 underwent endovascular treatment. Treated patients had a mean age of 10.25 years and 58% were females. Complete angiographic exclusion was achieved in five (42%) patients with endovascular treatment. Five patients with residual bAVM after embolization needed adjuvant therapy with surgery (n = 3) or stereotactic radiosurgery (SRS; n = 2). Two patients are still undergoing embolization sessions. Procedure-related complications occurred in two patients (17%) and included small vessel perforation and an occipital ischemic stroke. Two patients showed bAVM recurrence on follow-up (17%) and subsequently underwent SRS (n = 1) or surgery (n = 1), both resulting in complete bAVM exclusion. All patients had a modified Rankin scale (mRS) score of 0 to 2 on follow-up.

Conclusion Our experience supports the effectiveness and safety of endovascular treatment of bAVM in selected pediatric patients. A multidisciplinary approach combining surgery and SRS is warranted to achieve higher complete bAVM obliteration rates. Long-term follow-up is important as these lesions may show recurrence over time, especially in the pediatric population.

Keywords

pediatric brain arteriovenous malformations - intracranial hemorrhage - endovascular embolization

Publication History

Received: 12 October 2022

Accepted: 13 March 2023

Article published online:
26 July 2023

• References

• 1 Niazi TN, Klimo Jr P, Anderson RCE, Raffel C. Diagnosis and management of arteriovenous malformations in children. Neurosurg Clin N Am 2010; 21 (03) 443-456
• 2 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 (04) 647-653
• 3 Toma AK, Davagnanam I, Ganesan V, Brew S. Cerebral arteriovenous shunts in children. Neuroimaging Clin N Am 2013; 23 (04) 757-770
• 4 LoPresti MA, Ravindra VM, Pyarali M. et al. Pediatric intracranial arteriovenous malformations: a single-center experience. J Neurosurg Pediatr 2020; 25 (01) 151-158
• 5 Hofmeister C, Stapf C, Hartmann A. et al. Demographic, morphological, and clinical characteristics of 1289 patients with brain arteriovenous malformation. Stroke 2000; 31 (06) 1307-1310
• 6 Di Rocco C, Tamburrini G, Rollo M. Cerebral arteriovenous malformations in children. Acta Neurochir (Wien) 2000; 142 (02) 145-156 , discussion 156–158
• 7 de Castro-Afonso LH, Nakiri GS, Oliveira RS. et al. Curative embolization of pediatric intracranial arteriovenous malformations using onyx: the role of new embolization techniques on patient outcomes. Neuroradiology 2016; 58 (06) 585-594
• 8 Meyer-Heim AD, Boltshauser E. Spontaneous intracranial haemorrhage in children: aetiology, presentation and outcome. Brain Dev 2003; 25 (06) 416-421
• 9 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): 218-225
• 10 Renieri L, Limbucci N, Consoli A. et al. Transvenous embolization: a report of 4 pediatric cases. J Neurosurg Pediatr 2015; 15 (04) 445-450
• 11 Rodriguez-Calienes A, Bustamante-Paytan D, Camacho K, Mayoria-Vargas A, Saal-Zapata G, Rodriguez-Varela R. Early outcomes and complications of endovascular treatment of cerebral arteriovenous malformations in pediatric patients. Pediatr Neurosurg 2021; 56 (02) 116-124
• 12 Niimi Y. Endovascular treatment of pediatric intracranial arteriovenous shunt. Pediatr Int 2017; 59 (03) 247-257
• 13 Spetzler RF, Ponce FA. A 3-tier classification of cerebral arteriovenous malformations. Clinical article. J Neurosurg 2011; 114 (03) 842-849
• 14 Bigi S, Fischer U, Wehrli E. et al. Acute ischemic stroke in children versus young adults. Ann Neurol 2011; 70 (02) 245-254
• 15 Mohr JP, Parides MK, Stapf C. et al; international ARUBA investigators. Medical management with or without interventional therapy for unruptured brain arteriovenous malformations (ARUBA): a multicentre, non-blinded, randomised trial. Lancet 2014; 383 (9917): 614-621
• 16 Mohr JP, Overbey JR, Hartmann A. et al; ARUBA co-investigators. Medical management with interventional therapy versus medical management alone for unruptured brain arteriovenous malformations (ARUBA): final follow-up of a multicentre, non-blinded, randomised controlled trial. Lancet Neurol 2020; 19 (07) 573-581
• 17 Potts MB, Zumofen DW, Raz E, Nelson PK, Riina HA. Curing arteriovenous malformations using embolization. Neurosurg Focus 2014; 37 (03) E19
• 18 Darsaut TE, Guzman R, Marcellus ML. et al. Management of pediatric intracranial arteriovenous malformations: experience with multimodality therapy. Neurosurgery 2011; 69 (03) 540-556 , discussion 556
• 19 Baharvahdat H, Blanc R, Fahed R. et al. Endovascular treatment for low-grade (Spetzler-Martin I-II) brain arteriovenous malformations. AJNR Am J Neuroradiol 2019; 40 (04) 668-672
• 20 Iosif C, de Lucena AF, Abreu-Mattos LG. et al. Curative endovascular treatment for low-grade Spetzler-Martin brain arteriovenous malformations: a single-center prospective study. J Neurointerv Surg 2019; 11 (07) 699-705
• 21 Razavi SAS, Mirbolouk MH, Gorji R. et al. Endovascular treatment as the first-line approach for cure of low-grade brain arteriovenous malformation. Neurosurg Focus 2022; 53 (01) E8
• 22 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 2007; 61 (1, Suppl):discussion 422–424 417-422
• 23 Daou BJ, Palmateer G, Thompson BG. et al. Stereotactic radiosurgery for brain arteriovenous malformations: evaluation of obliteration and review of associated predictors. J Stroke Cerebrovasc Dis 2020; 29 (08) 104863
• 24 Copelan A, Drocton G, Caton MT. et al; UCSF Center For Cerebrovascular Research and UCSF Pediatric Brain Center. Brain arteriovenous malformation recurrence after apparent microsurgical cure: increased risk in children who present with arteriovenous malformation rupture. Stroke 2020; 51 (10) 2990-2996
• 25 Sorenson TJ, Brinjikji W, Bortolotti C, Kaufmann G, Lanzino G. Recurrent brain arteriovenous malformations (AVMs): a systematic review. World Neurosurg 2018; 116: e856-e866
• 26 Sonstein WJ, Kader A, Michelsen WJ, Llena JF, Hirano A, Casper D. Expression of vascular endothelial growth factor in pediatric and adult cerebral arteriovenous malformations: an immunocytochemical study. J Neurosurg 1996; 85 (05) 838-845
• 27 Ashour R, Aziz-Sultan MA, Soltanolkotabi M. et al. Safety and efficacy of onyx embolization for pediatric cranial and spinal vascular lesions and tumors. Neurosurgery 2012; 71 (04) 773-784
• 28 Sato K, Matsumoto Y, Tominaga T, Satow T, Iihara K, Sakai N. Japanese Registry of Neuroendovascular Therapy Investigators. Complications of endovascular treatments for brain arteriovenous malformations: a nationwide surveillance. AJNR Am J Neuroradiol 2020; 41 (04) 669-675
• 29 Berenstein A, Ortiz R, Niimi Y. et al. Endovascular management of arteriovenous malformations and other intracranial arteriovenous shunts in neonates, infants, and children. Childs Nerv Syst 2010; 26 (10) 1345-1358
• 30 Skjøth-Rasmussen J, Obbekjær T, Birkeland P, Hauerberg J, Juhler M. Multimodality treatment approach in children with cerebral arteriovenous malformation: a survey in the Danish population. Childs Nerv Syst 2012; 28 (04) 587-592
• 31 Soltanolkotabi M, Schoeneman SE, Alden TD. et al. Onyx embolization of intracranial arteriovenous malformations in pediatric patients. J Neurosurg Pediatr 2013; 11 (04) 431-437
• 32 Umansky D, Corn BW, Strauss I. et al. Combined treatment approach to cerebral arteriovenous malformation in pediatric patients: stereotactic radiosurgery to partially Onyx-embolized AVM. Childs Nerv Syst 2018; 34 (11) 2269-2274
• 33 Al-Smadi AS, Ansari SA, Shokuhfar T. et al. Safety and outcome of combined endovascular and surgical management of low grade cerebral arteriovenous malformations in children compared to surgery alone. Eur J Radiol 2019; 116: 8-13
• 34 Winkler EA, Lu A, Morshed RA. et al. Bringing high-grade arteriovenous malformations under control: clinical outcomes following multimodality treatment in children. J Neurosurg Pediatr 2020; 26 (01) 82-91
• 35 Alias Q, Boulouis G, Blauwblomme T. et al. First line onyx embolization in ruptured pediatric arteriovenous malformations: safety and efficacy. Clin Neuroradiol 2021; 31 (01) 155-163
• 36 Rodriguez-Calienes A, Bustamante-Paytan D, Camacho-Caballero K, Mayoria-Vargas A, Rodríguez-Varela R, Saal-Zapata G. Single-center experience with endovascular treatment of cerebral arteriovenous malformations with intent to cure in pediatric patients. Childs Nerv Syst 2022; 38 (02) 343-351