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30-09-2023 | Stroke | Research

Comparison of Long-Term Outcomes in Ruptured Diffuse Brain Arteriovenous Malformations Between Interventional Therapy and Conservative Management

Authors: Changyu Lu, Heze Han, Li Ma, Ruinan Li, Zhipeng Li, Haibin Zhang, Kexin Yuan, Yukun Zhang, Anqi Li, Ke Wang, Yang Zhao, Weitao Jin, Dezhi Gao, Hengwei Jin, Xiangyu Meng, Debin Yan, Runting Li, Fa Lin, Qiang Hao, Hao Wang, Xun Ye, Shuai Kang, Jun Pu, Zhiyong Shi, Xiaofeng Chao, Zhengfeng Lin, Junlin Lu, Youxiang Li, Yuanli Zhao, Shibin Sun, Xiaolin Chen, Weiwei Chen, Yu Chen, Shuo Wang, on behalf of Registry of Multimodality Treatment for Brain Arteriovenous Malformation in Mainland China (MATCH)

Published in: Translational Stroke Research

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Abstract

Brain arteriovenous malformations (AVMs) with a diffuse nidus structure present a therapeutic challenge due to their complexity and elevated risk of hemorrhagic events. This study examines the long-term effectiveness of interventional therapy versus conservative management in reducing hemorrhagic stroke or death in patients with ruptured diffuse AVMs. The analysis was conducted based on a multi-institutional database in China. Patients were divided into two groups: conservative management and interventional therapy. Using propensity score matching, patients were compared for the primary outcome of hemorrhagic stroke or death and the secondary outcomes of disability and neurofunctional decline. Out of 4286 consecutive AVMs in the registry, 901 patients were eligible. After matching, 70 pairs of patients remained with a median follow-up of 4.0 years. The conservative management group showed a trend toward higher rates of the primary outcome compared to the interventional group (4.15 vs. 1.87 per 100 patient-years, P = 0.090). While not statistically significant, intervention reduced the risk of hemorrhagic stroke or death by 55% (HR, 0.45 [95% CI 0.18–1.14], P = 0.094). No significant differences were observed in secondary outcomes of disability (OR, 0.89 [95% CI 0.35–2.26], P = 0.813) and neurofunctional decline (OR, 0.65 [95% CI 0.26 –1.63], P = 0.355). Subgroup analysis revealed particular benefits in interventional therapy for AVMs with a supplemented S-M grade of II-VI (HR, 0.10 [95% CI 0.01–0.79], P = 0.029). This study suggests a trend toward lower long-term hemorrhagic risks with intervention when compared to conservative management in ruptured diffuse AVMs, especially within supplemented S-M grade II–VI subgroups. No evidence indicated that interventional approaches worsen neurofunctional outcomes.
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Literature
1.
go back to reference Solomon RA, Connolly ES. Arteriovenous malformations of the brain. N Engl J Med. 2017;376:1859–66.CrossRefPubMed Solomon RA, Connolly ES. Arteriovenous malformations of the brain. N Engl J Med. 2017;376:1859–66.CrossRefPubMed
2.
go back to reference Chin LS, Raffel C, Gonzalez-Gomez I, Giannotta SL, McComb JG. Diffuse arteriovenous malformations: a clinical, radiological, and pathological description. Neurosurgery. 1992;31:863–8 discussion 868-869.PubMed Chin LS, Raffel C, Gonzalez-Gomez I, Giannotta SL, McComb JG. Diffuse arteriovenous malformations: a clinical, radiological, and pathological description. Neurosurgery. 1992;31:863–8 discussion 868-869.PubMed
3.
go back to reference Spears J, Terbrugge KG, Moosavian M, Montanera W, Willinsky RA, Wallace MC, et al. A discriminative prediction model of neurological outcome for patients undergoing surgery of brain arteriovenous malformations. Stroke. 2006;37:1457–64.CrossRefPubMed Spears J, Terbrugge KG, Moosavian M, Montanera W, Willinsky RA, Wallace MC, et al. A discriminative prediction model of neurological outcome for patients undergoing surgery of brain arteriovenous malformations. Stroke. 2006;37:1457–64.CrossRefPubMed
4.
go back to reference Lawton MT, Kim H, McCulloch CE, Mikhak B, Young WL. A supplementary grading scale for selecting patients with brain arteriovenous malformations for surgery. Neurosurgery. 2010;66:702–13 discussion 713.CrossRefPubMed Lawton MT, Kim H, McCulloch CE, Mikhak B, Young WL. A supplementary grading scale for selecting patients with brain arteriovenous malformations for surgery. Neurosurgery. 2010;66:702–13 discussion 713.CrossRefPubMed
5.
go back to reference Jiao Y, Lin F, Wu J, Li H, Wang L, Jin Z, et al. A supplementary grading scale combining lesion-to-eloquence distance for predicting surgical outcomes of patients with brain arteriovenous malformations. J Neurosurg. 2018;128:530–40.CrossRefPubMed Jiao Y, Lin F, Wu J, Li H, Wang L, Jin Z, et al. A supplementary grading scale combining lesion-to-eloquence distance for predicting surgical outcomes of patients with brain arteriovenous malformations. J Neurosurg. 2018;128:530–40.CrossRefPubMed
6.
go back to reference Chen C-J, Ding D, Derdeyn CP, Lanzino G, Friedlander RM, Southerland AM, et al. Brain arteriovenous malformations: a review of natural history, pathobiology, and interventions. Neurology. 2020;95:917–27.CrossRefPubMed Chen C-J, Ding D, Derdeyn CP, Lanzino G, Friedlander RM, Southerland AM, et al. Brain arteriovenous malformations: a review of natural history, pathobiology, and interventions. Neurology. 2020;95:917–27.CrossRefPubMed
7.
go back to reference Kim H, Sidney S, McCulloch CE, Poon KYT, Singh V, Johnston SC, et al. Racial/Ethnic differences in longitudinal risk of intracranial hemorrhage in brain arteriovenous malformation patients. Stroke. 2007;38:2430–7.CrossRefPubMed Kim H, Sidney S, McCulloch CE, Poon KYT, Singh V, Johnston SC, et al. Racial/Ethnic differences in longitudinal risk of intracranial hemorrhage in brain arteriovenous malformation patients. Stroke. 2007;38:2430–7.CrossRefPubMed
8.
go back to reference Hernesniemi JA, Dashti R, Juvela S, Väärt K, Niemelä M, Laakso A. Natural history of brain arteriovenous malformations: a long-term follow-up study of risk of hemorrhage in 238 patients. Neurosurgery. 2008;63:823–9 discussion 829-831.CrossRefPubMed Hernesniemi JA, Dashti R, Juvela S, Väärt K, Niemelä M, Laakso A. Natural history of brain arteriovenous malformations: a long-term follow-up study of risk of hemorrhage in 238 patients. Neurosurgery. 2008;63:823–9 discussion 829-831.CrossRefPubMed
9.
go back to reference da Costa L, Wallace MC, Ter Brugge KG, O’Kelly C, Willinsky RA, Tymianski M. The natural history and predictive features of hemorrhage from brain arteriovenous malformations. Stroke. 2009;40:100–5.CrossRefPubMed da Costa L, Wallace MC, Ter Brugge KG, O’Kelly C, Willinsky RA, Tymianski M. The natural history and predictive features of hemorrhage from brain arteriovenous malformations. Stroke. 2009;40:100–5.CrossRefPubMed
10.
go back to reference Kim H, Al-Shahi Salman R, McCulloch CE, Stapf C, Young WL, MARS Coinvestigators. Untreated brain arteriovenous malformation: patient-level meta-analysis of hemorrhage predictors. Neurology. 2014;83:590–7.CrossRefPubMedPubMedCentral Kim H, Al-Shahi Salman R, McCulloch CE, Stapf C, Young WL, MARS Coinvestigators. Untreated brain arteriovenous malformation: patient-level meta-analysis of hemorrhage predictors. Neurology. 2014;83:590–7.CrossRefPubMedPubMedCentral
11.
go back to reference Pollock BE, Flickinger JC, Lunsford LD, Bissonette DJ, Kondziolka D. Factors that predict the bleeding risk of cerebral arteriovenous malformations. Stroke. 1996;27:1–6.CrossRefPubMed Pollock BE, Flickinger JC, Lunsford LD, Bissonette DJ, Kondziolka D. Factors that predict the bleeding risk of cerebral arteriovenous malformations. Stroke. 1996;27:1–6.CrossRefPubMed
12.
go back to reference Chen Y, Han H, Ma L, Li R, Li Z, Yan D, et al. Multimodality treatment for brain arteriovenous malformation in Mainland China: design, rationale, and baseline patient characteristics of a nationwide multicenter prospective registry. Chin Neurosurg J. 2022;8:33.CrossRefPubMedPubMedCentral Chen Y, Han H, Ma L, Li R, Li Z, Yan D, et al. Multimodality treatment for brain arteriovenous malformation in Mainland China: design, rationale, and baseline patient characteristics of a nationwide multicenter prospective registry. Chin Neurosurg J. 2022;8:33.CrossRefPubMedPubMedCentral
13.
go back to reference Chen Y, Han H, Jin H, Meng X, Ma L, Li R, et al. Association of embolization with long-term outcomes in brain arteriovenous malformations: a propensity score-matched analysis using nationwide multicenter prospective registry data. Int J Surg. 2023;109:1900–1909 Chen Y, Han H, Jin H, Meng X, Ma L, Li R, et al. Association of embolization with long-term outcomes in brain arteriovenous malformations: a propensity score-matched analysis using nationwide multicenter prospective registry data. Int J Surg. 2023;109:1900–1909
14.
go back to reference Chen Y, Han H, Meng X, Jin H, Gao D, Ma L, et al. Development and validation of a scoring system for hemorrhage risk in brain arteriovenous malformations. JAMA Netw Open. 2023;6: e231070.CrossRefPubMedPubMedCentral Chen Y, Han H, Meng X, Jin H, Gao D, Ma L, et al. Development and validation of a scoring system for hemorrhage risk in brain arteriovenous malformations. JAMA Netw Open. 2023;6: e231070.CrossRefPubMedPubMedCentral
15.
17.
go back to reference Psaty BM, Siscovick DS. Minimizing bias due to confounding by indication in comparative effectiveness research: the importance of restriction. JAMA. 2010;304:897–8.CrossRefPubMed Psaty BM, Siscovick DS. Minimizing bias due to confounding by indication in comparative effectiveness research: the importance of restriction. JAMA. 2010;304:897–8.CrossRefPubMed
18.
19.
go back to reference Du R, Keyoung HM, Dowd CF, Young WL, Lawton MT. The effects of diffuseness and deep perforating artery supply on outcomes after microsurgical resection of brain arteriovenous malformations. Neurosurgery. 2007;60:638–46 discussion 646-648.CrossRefPubMed Du R, Keyoung HM, Dowd CF, Young WL, Lawton MT. The effects of diffuseness and deep perforating artery supply on outcomes after microsurgical resection of brain arteriovenous malformations. Neurosurgery. 2007;60:638–46 discussion 646-648.CrossRefPubMed
20.
go back to reference Lang S-S, 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. 2012;9:497–504.CrossRefPubMedPubMedCentral Lang S-S, 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. 2012;9:497–504.CrossRefPubMedPubMedCentral
21.
go back to reference Ivanov AA, Alaraj A, Charbel FT, Aletich V, Amin-Hanjani S. Recurrence of cerebral arteriovenous malformations following resection in adults: does preoperative embolization increase the risk? Neurosurgery. 2016;78:562–71.CrossRefPubMed Ivanov AA, Alaraj A, Charbel FT, Aletich V, Amin-Hanjani S. Recurrence of cerebral arteriovenous malformations following resection in adults: does preoperative embolization increase the risk? Neurosurgery. 2016;78:562–71.CrossRefPubMed
22.
go back to reference Chang JH, Chang JW, Park YG, Chung SS. Factors related to complete occlusion of arteriovenous malformations after gamma knife radiosurgery. J Neurosurg. 2000;93:96–101.CrossRefPubMed Chang JH, Chang JW, Park YG, Chung SS. Factors related to complete occlusion of arteriovenous malformations after gamma knife radiosurgery. J Neurosurg. 2000;93:96–101.CrossRefPubMed
23.
go back to reference Zipfel GJ, Bradshaw P, Bova FJ, Friedman WA. Do the morphological characteristics of arteriovenous malformations affect the results of radiosurgery? J Neurosurg. 2004;101:393–401.CrossRefPubMed Zipfel GJ, Bradshaw P, Bova FJ, Friedman WA. Do the morphological characteristics of arteriovenous malformations affect the results of radiosurgery? J Neurosurg. 2004;101:393–401.CrossRefPubMed
24.
go back to reference Sato S, Kodama N, Sasaki T, Matsumoto M, Ishikawa T. Perinidal dilated capillary networks in cerebral arteriovenous malformations. Neurosurgery. 2004;54:163–8 discussion 168-170.CrossRefPubMed Sato S, Kodama N, Sasaki T, Matsumoto M, Ishikawa T. Perinidal dilated capillary networks in cerebral arteriovenous malformations. Neurosurgery. 2004;54:163–8 discussion 168-170.CrossRefPubMed
25.
go back to reference Kim H, Abla AA, Nelson J, McCulloch CE, Bervini D, Morgan MK, et al. Validation of the supplemented Spetzler-Martin grading system for brain arteriovenous malformations in a multicenter cohort of 1009 surgical patients. Neurosurgery. 2015;76:25–31 discussion 31-32; quiz 32–3.CrossRefPubMed Kim H, Abla AA, Nelson J, McCulloch CE, Bervini D, Morgan MK, et al. Validation of the supplemented Spetzler-Martin grading system for brain arteriovenous malformations in a multicenter cohort of 1009 surgical patients. Neurosurgery. 2015;76:25–31 discussion 31-32; quiz 32–3.CrossRefPubMed
26.
go back to reference Spetzler RF, Martin NA. A proposed grading system for arteriovenous malformations. J Neurosurg. 1986;65:476–83.CrossRefPubMed Spetzler RF, Martin NA. A proposed grading system for arteriovenous malformations. J Neurosurg. 1986;65:476–83.CrossRefPubMed
27.
go back to reference Yamada S, Takagi Y, Nozaki K, Kikuta K, Hashimoto N. Risk factors for subsequent hemorrhage in patients with cerebral arteriovenous malformations. J Neurosurg. 2007;107:965–72.CrossRefPubMed Yamada S, Takagi Y, Nozaki K, Kikuta K, Hashimoto N. Risk factors for subsequent hemorrhage in patients with cerebral arteriovenous malformations. J Neurosurg. 2007;107:965–72.CrossRefPubMed
28.
go back to reference Milatović B, Saponjski J, Huseinagić H, Moranjkić M, Milošević Medenica S, Marinković I, et al. Anatomy of the feeding arteries of the cerebral arteriovenous malformations. Folia Morphol (Warsz). 2018;77:656–69.PubMed Milatović B, Saponjski J, Huseinagić H, Moranjkić M, Milošević Medenica S, Marinković I, et al. Anatomy of the feeding arteries of the cerebral arteriovenous malformations. Folia Morphol (Warsz). 2018;77:656–69.PubMed
29.
go back to reference Al-Shahi R, Pal N, Lewis SC, Bhattacharya JJ, Sellar RJ, Warlow CP, et al. Observer agreement in the angiographic assessment of arteriovenous malformations of the brain. Stroke. 2002;33:1501–8.CrossRefPubMed Al-Shahi R, Pal N, Lewis SC, Bhattacharya JJ, Sellar RJ, Warlow CP, et al. Observer agreement in the angiographic assessment of arteriovenous malformations of the brain. Stroke. 2002;33:1501–8.CrossRefPubMed
30.
go back to reference Du R, Dowd CF, Johnston SC, Young WL, Lawton MT. Interobserver variability in grading of brain arteriovenous malformations using the Spetzler-Martin system. Neurosurgery. 2005;57:668–75 discussion 668-675.CrossRefPubMed Du R, Dowd CF, Johnston SC, Young WL, Lawton MT. Interobserver variability in grading of brain arteriovenous malformations using the Spetzler-Martin system. Neurosurgery. 2005;57:668–75 discussion 668-675.CrossRefPubMed
31.
go back to reference Frisoli FA, Lang S-S, Vossough A, Cahill AM, Heuer GG, Dahmoush HM, et al. Intrarater and interrater reliability of the pediatric arteriovenous malformation compactness score in children. J Neurosurg Pediatr. 2013;11:547–51.CrossRefPubMedPubMedCentral Frisoli FA, Lang S-S, Vossough A, Cahill AM, Heuer GG, Dahmoush HM, et al. Intrarater and interrater reliability of the pediatric arteriovenous malformation compactness score in children. J Neurosurg Pediatr. 2013;11:547–51.CrossRefPubMedPubMedCentral
32.
go back to reference Braileanu M, Yang W, Caplan JM, Lin L-M, Radvany MG, Tamargo RJ, et al. Interobserver agreement on arteriovenous malformation diffuseness using digital subtraction angiography. World Neurosurg. 2016;95:535-541.e3.CrossRefPubMed Braileanu M, Yang W, Caplan JM, Lin L-M, Radvany MG, Tamargo RJ, et al. Interobserver agreement on arteriovenous malformation diffuseness using digital subtraction angiography. World Neurosurg. 2016;95:535-541.e3.CrossRefPubMed
33.
go back to reference Jiao Y, Zhang J-Z, Zhao Q, Liu J-Q, Wu Z-Z, Li Y, et al. Machine learning-enabled determination of diffuseness of brain arteriovenous malformations from magnetic resonance angiography. Transl Stroke Res. 2021;13:939–948. Jiao Y, Zhang J-Z, Zhao Q, Liu J-Q, Wu Z-Z, Li Y, et al. Machine learning-enabled determination of diffuseness of brain arteriovenous malformations from magnetic resonance angiography. Transl Stroke Res. 2021;13:939–948.
34.
go back to reference Li M, Liu Q, Yang J, Jiang P, Yang Y, Zhang Y, et al. Metabolic disorder of extracellular matrix mediated by decorin upregulation is associated with brain arteriovenous malformation diffuseness. Front Aging Neurosci. 2020;12: 584839.CrossRefPubMedPubMedCentral Li M, Liu Q, Yang J, Jiang P, Yang Y, Zhang Y, et al. Metabolic disorder of extracellular matrix mediated by decorin upregulation is associated with brain arteriovenous malformation diffuseness. Front Aging Neurosci. 2020;12: 584839.CrossRefPubMedPubMedCentral
Metadata
Title
Comparison of Long-Term Outcomes in Ruptured Diffuse Brain Arteriovenous Malformations Between Interventional Therapy and Conservative Management
Authors
Changyu Lu
Heze Han
Li Ma
Ruinan Li
Zhipeng Li
Haibin Zhang
Kexin Yuan
Yukun Zhang
Anqi Li
Ke Wang
Yang Zhao
Weitao Jin
Dezhi Gao
Hengwei Jin
Xiangyu Meng
Debin Yan
Runting Li
Fa Lin
Qiang Hao
Hao Wang
Xun Ye
Shuai Kang
Jun Pu
Zhiyong Shi
Xiaofeng Chao
Zhengfeng Lin
Junlin Lu
Youxiang Li
Yuanli Zhao
Shibin Sun
Xiaolin Chen
Weiwei Chen
Yu Chen
Shuo Wang
on behalf of Registry of Multimodality Treatment for Brain Arteriovenous Malformation in Mainland China (MATCH)
Publication date
30-09-2023
Publisher
Springer US
Published in
Translational Stroke Research
Print ISSN: 1868-4483
Electronic ISSN: 1868-601X
DOI
https://doi.org/10.1007/s12975-023-01197-7