Application of the Principles of Safe Hemodynamic Rearrangement to Reduce the Risk of Cerebral Arteriovenous Malformation Rupture during Curative Embolization using the Multimodal Approach

Abstract

Introduction

The grading system for arteriovenous malformations (AVMs) and the curative embolization principles for reducing the risks of AVM rupture caused by abrupt hemodynamic rearrangement have been modified using mathematical modeling methods. The objective of the study was to confirm the clinical effectiveness of these principles for reducing the rate of postoperative bleeding according to real-world data.

Methods

A retrospective study employing a pooled database involving 532 patients was performed for groups matched by demographic, anatomical, and clinical characteristics using the PSM method: the group of patients treated with adherence to all the embolization principles (Principles group, n = 92) and the control group of patients treated with violation of at least one principle (Control group, n = 46). Each patient underwent 1–9 embolization stages. If needed, radiosurgery or microsurgery was used at the final stage. The therapy outcomes were assessed according to the rate of achieving 100% AVM obliteration at follow-up angiography, as well as morbidity, mortality, and perioperative complication rate.

Results

Patients in the Principles group had much higher safety parameters after multimodal embolization therapy; the rate of postoperative bleeding episodes was 9 (9.78%) versus 11 (23.91%) in the Control group (p = 0.039). Radicality levels of AVM nidus obliteration at the control visit were comparable in groups (85 (93.41%) versus 42 (95.45%), respectively, p > 0.999), while the rate of neurologic deficit progression (worsening by at least 2 mRS points) in the principles group was significantly lower (5 (5.43%) versus 9 (19.57%), p = 0.015).

Conclusions

Endovascular embolization shows great potential as the main curative option for reducing the risk of postoperative bleeding due to changing the patient management strategy. Occluding a fistula (if it is present) at the first stage and reducing the degree of AVM obliteration per stage to 60% for large-sized malformations improve treatment safety without decreasing its radicality.

Resumo

Introdução

O sistema de classificação para malformações arteriovenosas (MAVs) e os princípios de embolização curativa para reduzir os riscos de ruptura de MAV causada por rearranjo hemodinâmico abrupto foram modificados utilizando métodos de modelagem matemática. O objetivo do estudo foi confirmar a eficácia clínica desses princípios na redução da taxa de sangramento pós-operatório, de acordo com dados do mundo real.

Métodos

Um estudo retrospectivo, utilizando um banco de dados agrupado, envolvendo 532 pacientes, foi realizado para grupos pareados por características demográficas, anatômicas e clínicas, utilizando o método PSM: o grupo de pacientes tratados com adesão a todos os princípios de embolização (grupo Princípios, n = 92) e o grupo controle, composto por pacientes tratados com violação de pelo menos um princípio (grupo Controle, n = 46). Cada paciente foi submetido a 1 a 9 estágios de embolização. Se necessário, radiocirurgia ou microcirurgia foram utilizadas no estágio final. Os desfechos da terapia foram avaliados de acordo com a taxa de obliteração de 100% da MAV na angiografia de acompanhamento, bem como a morbidade, a mortalidade e a taxa de complicações perioperatórias.

Resultados

Os pacientes do grupo Princípios apresentaram parâmetros de segurança muito mais elevados após a terapia de embolização multimodal; a taxa de episódios de sangramento pós-operatório foi de 9 (9,78%) versus 11 (23,91%) no grupo Controle (p = 0,039). Os níveis de radicalidade da obliteração do nicho da MAV na visita de controle foram comparáveis entre os grupos (85 (93,41%) versus 42 (95,45%), respectivamente, p > 0,999), enquanto a taxa de progressão do déficit neurológico (piora em pelo menos 2 pontos de mRS) no grupo Princípios foi significativamente menor (5 (5,43%) versus 9 (19,57%), p = 0,015).

Conclusões

A embolização endovascular apresenta grande potencial como principal opção curativa para reduzir o risco de sangramento pós-operatório devido à mudança na estratégia de manejo do paciente. A oclusão de uma fístula (se presente) no primeiro estágio e a redução do grau de obliteração da MAV por estágio para 60% em malformações de grande porte melhoram a segurança do tratamento sem diminuir sua radicalidade.

Keywords

AVM - brain arteriovenous malformation

Palavras-chave

MAV - malformação arteriovenosa cerebral

Publication History

Received: 15 November 2023

Accepted: 20 March 2025

Article published online:
16 July 2025

• References

• 1 Brosnan C, Amoo M, Javadpour M. Preoperative embolisation of brain arteriovenous malformations: a systematic review and meta-analysis. Neurosurg Rev 2022; 45 (03) 2051-2063 [Internet]
• 2 Nguyen AM, Nguyen HV, Tran TQ. Multimodality treatment of supratentorial arteriovenous malformations with microsurgery after embolization: A retrospective two-center study in Vietnam. Interdiscip Neurosurg Adv Tech Case Manag [Internet] 2021; 26: 101266
• 3 Franzetti G, Bonfanti M, Tanade C. et al. A Computational Framework for Pre-Interventional Planning of Peripheral Arteriovenous Malformations. Cardiovasc Eng Technol 2022; 13 (02) 234-246
• 4 Wang M, Jiao Y, Zeng C. et al. Chinese Cerebrovascular Neurosurgery Society and Chinese Interventional & Hybrid Operation Society, of Chinese Stroke Association Clinical Practice Guidelines for Management of Brain Arteriovenous Malformations in Eloquent Areas. Front Neurol 2021; 12 (June): 651663
• 5 Pezeshkpour P, Dmytriw AA, Phan K. et al. Treatment strategies and related outcomes for brain arteriovenous malformations in children: A systematic review and meta-analysis. AJR Am J Roentgenol 2020; 215 (02) 472-487
• 6 Jiang Z, Zhang X, Wan X. et al. Review Article Efficacy and Safety of Combined Endovascular Embolization and Stereotactic Radiosurgery for Patients with Intracranial Arteriovenous Malformations: A Systematic Review and Meta- Analysis. BioMed Res Int 2021; 202: 668
• 7 Africk BN, Heiferman DM, Wozniak AW. et al. Angioarchitectural features amongst patients with unruptured brain arteriovenous malformations presenting with headache: findings from a single center retrospective review of 76 patients. J Headache Pain 2021; 22 (01) 122
• 8 Vollherbst DF, Chapot R, Bendszus M, Möhlenbruch MA. Glue, Onyx, Squid or PHIL? Liquid Embolic Agents for the Embolization of Cerebral Arteriovenous Malformations and Dural Arteriovenous Fistulas. Clin Neuroradiol 2022; 32 (01) 25-38
• 9 Rana MM, Melancon MP. Emerging Polymer Materials in Trackable Endovascular Embolization and Cell Delivery: From Hype to Hope. Biomimetics (Basel) 2022; 7 (02) 77
• 10 Choudhri O, Ivan ME, Lawton MT. Transvenous Approach to Intracranial Arteriovenous Malformations: Challenging the Axioms of Arteriovenous Malformation Therapy?. Neurosurgery 2015; 77 (04) 644-651 , discussion 652
• 11 Jordan JA, Llibre JC, Vázquez F, Rodríguez R, Prince JA, Ugarte JC. Predictors of hemorrhagic complications from endovascular treatment of cerebral arteriovenous malformations. Interv Neuroradiol 2014; 20 (01) 74-82
• 12 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
• 13 Subat YW, Dasenbrock HH, Gross BA. et al. Periprocedural intracranial hemorrhage after embolization of cerebral arteriovenous malformations: a meta-analysis. J Neurosurg 2019; 133 (05) 1417-1427
• 14 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 2015; 6: 3
• 15 Fennell VS, Martirosyan NL, Atwal GS. et al. Hemodynamics Associated With Intracerebral Arteriovenous Malformations: The Effects of Treatment Modalities. Neurosurgery 2018; 83 (04) 611-621
• 16 Khe AK, Cherevko AA, Chupakhin AP, Krivoshapkin AL, Orlov KY, Panarin VA. Monitoring of hemodynamics of brain vessels. J Appl Mech Tech Phys 2017; 58 (05) 763-770
• 17 Madhugiri VS, Teo MKC, Westbroek EM. et al. Multimodal management of arteriovenous malformations of the basal ganglia and thalamus: factors affecting obliteration and outcome. J Neurosurg 2018; 131 (02) 410-419
• 18 Spetzler RF, Martin NA. A proposed grading system for arteriovenous malformations. 1986. J Neurosurg 2008; 108 (01) 186-193
• 19 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 2019; 23 (03) 343-354
• 20 Baharvahdat H, Blanc R, Termechi R. et al. Hemorrhagic complications after endovascular treatment of cerebral arteriovenous malformations. AJNR Am J Neuroradiol 2014; 35 (05) 978-983
• 21 Tayebi Meybodi A, Lawton MT. Modern radiosurgical and endovascular classification schemes for brain arteriovenous malformations. Neurosurg Rev 2020; 43 (01) 49-58
• 22 Hou K, Xu K, Chen X, Ji T, Guo Y, Yu J. Targeted endovascular treatment for ruptured brain arteriovenous malformations. Neurosurg Rev 2020; 43 (06) 1509-1518
• 23 Wang A, Mandigo GK, Feldstein NA. et al. Curative treatment for low-grade arteriovenous malformations. J Neurointerv Surg 2020; 12 (01) 48-54
• 24 Lu VM, Wahood W, Rinaldo L, Ahn ES, Daniels DJ. Long-term functional outcome after intervention for pediatric intracranial arteriovenous malformations: A systematic review and meta-analysis. Clin Neurol Neurosurg 2020; 191: 105707
• 25 Yang W, Wang JY, Caplan JM. et al. Microsurgery for cerebral arteriovenous malformations: postoperative outcomes and predictors of complications in 264 cases. Neurosurg Rev 2021; 13 (02) 1-7 [Internet]
• 26 Strauss I, Frolov V, Buchbut D, Gonen L, Maimon S. Critical appraisal of endovascular treatment of brain arteriovenous malformation using Onyx in a series of 92 consecutive patients. Acta Neurochir (Wien) 2013; 155 (04) 611-617
• 27 Zhang H, Liang S, Lv X. Radio-clinical grading system for transarterial AVM embolization: Tsinghua AVM grading system. Neurosci Informatics [Internet] 2021; 1 (03) 100021
• 28 Stein KP, Moenninghoff C, Kneist A, Sandalcioglu IE, Forsting M, Sure U. Transdural blood supply in cerebral arteriovenous malformations: A systematic evaluation of angioarchitecture. AJNR Am J Neuroradiol 2018; 39 (12) 2307-2312
• 29 Abecassis IJ, Nerva JD, Feroze A. et al. Multimodality Management of Spetzler-Martin Grade 3 Brain Arteriovenous Malformations with Subgroup Analysis. World Neurosurg 2017; 102: 263-274 [Internet]
• 30 Reitz M, von Spreckelsen N, Vettorazzi E. et al. Angioarchitectural Risk Factors for Hemorrhage and Clinical Long-Term Outcome in Pediatric Patients with Cerebral Arteriovenous Malformations. World Neurosurg 2016; 89: 540-551 [Internet]
• 31 Mosimann PJ, Chapot R. Contemporary endovascular techniques for the curative treatment of cerebral arteriovenous malformations and review of neurointerventional outcomes. J Neurosurg Sci 2018; 62 (04) 505-513
• 32 Platz J, Berkefeld J, Singer OC. et al. Frequency, risk of hemorrhage and treatment considerations for cerebral arteriovenous malformations with associated aneurysms. Acta Neurochir (Wien) 2014; 156 (11) 2025-2034
• 33 Jordan J, Llibre JC, Vazquez F. Predictors of neurological deficit after endovascular treatment of cerebral arteriovenous malformations and functional repercussions in prospective follow-up. Neuroradiol J 2014; 27 (06) 718-724
• 34 Derdeyn CP, Zipfel GJ, Albuquerque FC. et al; American Heart Association Stroke Council. Management of Brain Arteriovenous Malformations: A Scientific Statement for Healthcare Professionals From the American Heart Association/American Stroke Association. Stroke 2017; 48 (08) e200-e224