Skip to main content
SpringerLink
Log in

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

  • Research
  • Published:
Translational Stroke Research Aims and scope Submit manuscript

An Author Correction to this article was published on 06 February 2024

This article has been updated

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Data Availability

All original data are available upon reasonable request to the corresponding authors.

Change history

References

  1. Solomon RA, Connolly ES. Arteriovenous malformations of the brain. N Engl J Med. 2017;376:1859–66.

    Article  PubMed  Google Scholar 

  2. 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  CAS  Google Scholar 

  3. 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.

    Article  PubMed  Google Scholar 

  4. 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.

    Article  PubMed  Google Scholar 

  5. 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.

    Article  PubMed  Google Scholar 

  6. 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.

    Article  PubMed  Google Scholar 

  7. 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.

    Article  PubMed  Google Scholar 

  8. 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.

    Article  PubMed  Google Scholar 

  9. 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.

    Article  PubMed  Google Scholar 

  10. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  11. 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.

    Article  PubMed  CAS  Google Scholar 

  12. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  13. 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. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Zhang Y, Chen Y, Han H, Ma L, Li R, Li Z, et al. Timing of microsurgical resection for ruptured brain arteriovenous malformations: a propensity score-matched analysis using prospective single-center registry data. J Neurosurg. 2023;1–8. https://doi.org/10.3171/2023.5.JNS222666

  16. Reporting terminology for brain arteriovenous malformation clinical and radiographic features for use in clinical trials. Stroke. 2001;32:1430–42. https://doi.org/10.1161/01.str.32.6.1430

  17. Psaty BM, Siscovick DS. Minimizing bias due to confounding by indication in comparative effectiveness research: the importance of restriction. JAMA. 2010;304:897–8.

    Article  PubMed  CAS  Google Scholar 

  18. Kyriacou DN, Lewis RJ. Confounding by indication in clinical research. JAMA. 2016;316:1818–9.

    Article  PubMed  Google Scholar 

  19. 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.

    Article  PubMed  Google Scholar 

  20. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  21. 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.

    Article  PubMed  Google Scholar 

  22. 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.

    Article  PubMed  Google Scholar 

  23. 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.

    Article  PubMed  Google Scholar 

  24. 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.

    Article  PubMed  Google Scholar 

  25. 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.

    Article  PubMed  Google Scholar 

  26. Spetzler RF, Martin NA. A proposed grading system for arteriovenous malformations. J Neurosurg. 1986;65:476–83.

    Article  PubMed  CAS  Google Scholar 

  27. 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.

    Article  PubMed  Google Scholar 

  28. 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  Google Scholar 

  29. 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.

    Article  PubMed  Google Scholar 

  30. 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.

    Article  PubMed  Google Scholar 

  31. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  32. 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.

    Article  PubMed  Google Scholar 

  33. 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. 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.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Acknowledgements

We thank all the staff for their contribution to this study and participant hospitals of the MATCH registry for their support.

Funding

This work was supported by the National Key Research and Development Program of China (grant no. 2021YFC2501101 and 2020YFC2004701 to Xiaolin Chen) and Natural Science Foundation of China (grant nos. 81771234 and 82071302 to Yuanli Zhao and 82202244 to Yu Chen).

Author information

Author notes

  1. Changyu Lu and Heze Han contributed equally to this manuscript.

Authors and Affiliations

  1. Department of Neurosurgery, Peking University International Hospital, Beijing, China

    Changyu Lu, Yukun Zhang, Yang Zhao & Weitao Jin

  2. Department of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, Beijing, China

    Heze Han, Li Ma, Ruinan Li, Zhipeng Li, Haibin Zhang, Kexin Yuan, Anqi Li, Ke Wang, Runting Li, Fa Lin, Qiang Hao, Hao Wang, Xun Ye, Shuai Kang, Yuanli Zhao, Xiaolin Chen, Yu Chen & Shuo Wang

  3. Beijing Neurosurgical Institute, Beijing Tiantan Hospital, Capital Medical University, Beijing, China

    Heze Han, Li Ma, Ruinan Li, Zhipeng Li, Haibin Zhang, Kexin Yuan, Anqi Li, Ke Wang, Runting Li, Fa Lin, Qiang Hao, Hao Wang, Xun Ye, Shuai Kang, Yuanli Zhao, Xiaolin Chen, Yu Chen & Shuo Wang

  4. China National Clinical Research Center for Neurological Diseases, Beijing, China

    Heze Han, Li Ma, Ruinan Li, Zhipeng Li, Haibin Zhang, Kexin Yuan, Anqi Li, Ke Wang, Runting Li, Fa Lin, Qiang Hao, Hao Wang, Xun Ye, Shuai Kang, Yuanli Zhao, Xiaolin Chen, Yu Chen & Shuo Wang

  5. Department of Gamma-Knife Center, Beijing Tiantan Hospital, Capital Medical University, Beijing, China

    Dezhi Gao & Shibin Sun

  6. Department of Interventional Neuroradiology, Beijing Tiantan Hospital, Capital Medical University, Beijing, China

    Hengwei Jin & Youxiang Li

  7. Department of Neurosurgery, The First Hospital of Hebei Medical University, Hebei Medical University, Shijiazhuang, China

    Xiangyu Meng

  8. Department of Neurosurgery, Shanxi Provincial People’s Hospital, Taiyuan, Shanxi, China

    Debin Yan

  9. First Department of Neurosurgery, The Second Affiliated Hospital of Kunming Medical University, Kunming, China

    Jun Pu

  10. Department of Neurosurgery, Nanjing Drum Tower Hospital, Affiliated to Nanjing University, Nanjing, Jiangsu, China

    Zhiyong Shi

  11. Department of Neurosurgery, The Second Affiliated Hospital of Xuzhou Medical University, Jiangsu, China

    Xiaofeng Chao

  12. Department of Neurosurgery, The First People’s Hospital of Qinzhou, Guangxi, China

    Zhengfeng Lin

  13. Department of Neurosurgery, West China Hospital, Sichuan University, Chengdu, Sichuan, China

    Junlin Lu

  14. Department of Neurosurgery, The First Affiliated Hospital of Anhui Medical University, Hefei, China

    Weiwei Chen

Authors
  1. Changyu Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Heze Han
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Li Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ruinan Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Zhipeng Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Haibin Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Kexin Yuan
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Yukun Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Anqi Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Ke Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Yang Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Weitao Jin
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Dezhi Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Hengwei Jin
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Xiangyu Meng
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Debin Yan
    View author publications

    You can also search for this author in PubMed Google Scholar

  17. Runting Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  18. Fa Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

  19. Qiang Hao
    View author publications

    You can also search for this author in PubMed Google Scholar

  20. Hao Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  21. Xun Ye
    View author publications

    You can also search for this author in PubMed Google Scholar

  22. Shuai Kang
    View author publications

    You can also search for this author in PubMed Google Scholar

  23. Jun Pu
    View author publications

    You can also search for this author in PubMed Google Scholar

  24. Zhiyong Shi
    View author publications

    You can also search for this author in PubMed Google Scholar

  25. Xiaofeng Chao
    View author publications

    You can also search for this author in PubMed Google Scholar

  26. Zhengfeng Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

  27. Junlin Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

  28. Youxiang Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  29. Yuanli Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  30. Shibin Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  31. Xiaolin Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  32. Weiwei Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  33. Yu Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  34. Shuo Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Consortia

on behalf of Registry of Multimodality Treatment for Brain Arteriovenous Malformation in Mainland China (MATCH)

Contributions

Study concept and design: C.L., H.H., S.W., Y.C., W.C., and X.C. Acquisition of data: C.L., H.H., Y.C., L.M., R.L., Z.L., H.Z., K.Y., A.L., Y.Z., K.W., H.J., X.M., D.Y., Y.Z., W.J., R.L., F.L., J.P., Z.S., X.C., Z.L., and J.L. Drafting of the manuscript: C.L. and H.H. Critical revision of the manuscript for important intellectual content: Y.C., Q.H., H.W., X.Y., S.K., D.G., S.S., Y.L., and Y.Z. Statistical analysis: H.H. and C.L. Study supervision and organization of the project: S.W., Y.C., W.C., and X.C. All authors commented on previous versions of the manuscript, and all authors read and approved the final manuscript.

Corresponding authors

Correspondence to Xiaolin Chen, Weiwei Chen, Yu Chen or Shuo Wang.

Ethics declarations

Ethics Approval

This study was approved by Institutional Research Ethics Committee of Beijing Tiantan Hospital (IRB approval number: KY 2020-003-01) and conducted under the guidance of the Declaration of Helsinki.

Consent for Publication

Not applicable.

Competing Interests

None declared.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

The original online version of this article was revised: It has come to our attention that affiliation address “Department of Neurosurgery, Peking University International Hospital, Peking University, Beijing, China” contains an error that needs rectification. The correct address should be “Department of Neurosurgery, Peking University International Hospital, Beijing, China” (i.e. removing the “Peking University”).

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 1185 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lu, C., Han, H., Ma, L. et al. Comparison of Long-Term Outcomes in Ruptured Diffuse Brain Arteriovenous Malformations Between Interventional Therapy and Conservative Management. Transl. Stroke Res. (2023). https://doi.org/10.1007/s12975-023-01197-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s12975-023-01197-7

Keywords

Search

Navigation