Skip to main content

Advertisement

SpringerLink
Log in

Association of nidus size and rupture in brain arteriovenous malformations: Insight from angioarchitecture and hemodynamics

  • Research
  • Published:
Neurosurgical Review Aims and scope Submit manuscript

Abstract

This study aims to investigate the correlation between AVM size and rupture by examining natural history, angioarchitecture characteristics, and quantitative hemodynamics. A retrospective review of 90 consecutive AVMs from the MATCH registry was conducted. Patients were categorized into small nidus (< 3 cm) and large nidus (≥ 3 cm) groups based on the Spetzler-Martin grading system. Natural history analysis used prospective cohort survival data, while imaging analysis examined angioarchitecture characteristics and quantitative hemodynamic parameters measured with QDSA. The small-nidus group had a significantly higher annualized rupture risk (2.3% vs. 1.0%; p = 0.011). Cross-sectional imaging revealed independent hemorrhagic risk factors, including small nidus (OR, 4.801; 95%CI, 1.280–18.008; p = 0.020) and draining vein stenosis (OR, 6.773; 95%CI, 1.179–38.911; p = 0.032). Hemodynamic analysis identified higher stasis index in the feeding artery (OR, 2.442; 95%CI, 1.074–5.550; p = 0.033), higher stasis index in the draining vein (OR, 11.812; 95%CI, 1.907–73.170; p = 0.008), and lower outflow gradient in the draining vein (OR, 1.658; 95%CI, 1.068–2.574; p = 0.024) as independent predictors of AVM rupture. The small nidus group also showed a higher likelihood of being associated with hemorrhagic risk factors. Small AVM nidus has a higher risk of rupture based on natural history, angioarchitecture, and hemodynamics.

Clinical Trial Registration-URL: http://www.clinicaltrials.gov. Unique identifier: NCT04572568.

Graphical Abstract

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
Fig. 4

Similar content being viewed by others

Data availability

The dataset analyzed and used to support the findings of this study are available from the corresponding author upon request.

References

  1. Joint Writing Group of the Technology Assessment Committee American Society of I, Therapeutic N, Joint Section on Cerebrovascular Neurosurgery a Section of the American Association of Neurological S et al (2001) Reporting terminology for brain arteriovenous malformation clinical and radiographic features for use in clinical trials. Stroke 32(6):1430–42. https://doi.org/10.1161/01.str.32.6.1430

    Article  Google Scholar 

  2. Al-Shahi R, Warlow C (2001) A systematic review of the frequency and prognosis of arteriovenous malformations of the brain in adults. Brain 124(Pt 10):1900–1926. https://doi.org/10.1093/brain/124.10.1900

    Article  CAS  PubMed  Google Scholar 

  3. Stapf C, Mast H, Sciacca RR et al (2006) Predictors of hemorrhage in patients with untreated brain arteriovenous malformation. Neurology 66(9):1350–1355. https://doi.org/10.1212/01.wnl.0000210524.68507.87

    Article  CAS  PubMed  Google Scholar 

  4. Tripathi M, Batish A, Mohindra S (2021) Gamma Knife Radiosurgery for Berry Aneurysms: Quo Vadis. J Neurosci Rural Pract 12(1):182–184. https://doi.org/10.1055/s-0040-1716795

    Article  PubMed  Google Scholar 

  5. Hernesniemi JA, Dashti R, Juvela S, Vaart K, Niemela M, Laakso A (2008) Natural history of brain arteriovenous malformations: a long-term follow-up study of risk of hemorrhage in 238 patients. Neurosurgery. 63(5):823–9. https://doi.org/10.1227/01.NEU.0000330401.82582.5E. (discussion 829-31)

    Article  PubMed  Google Scholar 

  6. Kim H, Al-Shahi Salman R, McCulloch CE, Stapf C, Young WL, Coinvestigators M (2014) Untreated brain arteriovenous malformation: patient-level meta-analysis of hemorrhage predictors. Neurology 83(7):590–597. https://doi.org/10.1212/WNL.0000000000000688

    Article  PubMed  PubMed Central  Google Scholar 

  7. Chen X, Cooke DL, Saloner D et al (2017) Higher Flow Is Present in Unruptured Arteriovenous Malformations With Silent Intralesional Microhemorrhages. Stroke 48(10):2881–2884. https://doi.org/10.1161/STROKEAHA.117.017785

    Article  PubMed  PubMed Central  Google Scholar 

  8. Spetzler RF, Hargraves RW, McCormick PW, Zabramski JM, Flom RA, Zimmerman RS (1992) Relationship of perfusion pressure and size to risk of hemorrhage from arteriovenous malformations. J Neurosurg 76(6):918–923. https://doi.org/10.3171/jns.1992.76.6.0918

    Article  CAS  PubMed  Google Scholar 

  9. Burkhardt JK, Chen X, Winkler EA et al (2018) Early Hemodynamic Changes Based on Initial Color-Coding Angiography as a Predictor for Developing Subsequent Symptomatic Vasospasm After Aneurysmal Subarachnoid Hemorrhage. World Neurosurg 109:e363–e373. https://doi.org/10.1016/j.wneu.2017.09.179

    Article  PubMed  Google Scholar 

  10. Chen Y, Ma L, Yang S et al (2020) Quantitative Angiographic Hemodynamic Evaluation After Revascularization Surgery for Moyamoya Disease. Transl Stroke Res 11(5):871–881. https://doi.org/10.1007/s12975-020-00781-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Lin TM, Yang HC, Lee CC et al (2019) Stasis index from hemodynamic analysis using quantitative DSA correlates with hemorrhage of supratentorial arteriovenous malformation: a cross-sectional study. J Neurosurg 132(5):1574–1582. https://doi.org/10.3171/2019.1.JNS183386

    Article  PubMed  Google Scholar 

  12. Burkhardt JK, Chen X, Winkler EA, Cooke DL, Kim H, Lawton MT (2017) Delayed Venous Drainage in Ruptured Arteriovenous Malformations Based on Quantitative Color-Coded Digital Subtraction Angiography. World Neurosurg 104:619–627. https://doi.org/10.1016/j.wneu.2017.04.120

    Article  PubMed  Google Scholar 

  13. Winkler EA, Birk H, Burkhardt JK et al (2018) Reductions in brain pericytes are associated with arteriovenous malformation vascular instability. J Neurosurg 129(6):1464–1474. https://doi.org/10.3171/2017.6.JNS17860

    Article  PubMed  PubMed Central  Google Scholar 

  14. Brunozzi D, Hussein AE, Shakur SF et al (2018) Contrast Time-Density Time on Digital Subtraction Angiography Correlates With Cerebral Arteriovenous Malformation Flow Measured by Quantitative Magnetic Resonance Angiography, Angioarchitecture, and Hemorrhage. Neurosurgery 83(2):210–216. https://doi.org/10.1093/neuros/nyx351

    Article  PubMed  Google Scholar 

  15. Chen Y, Chen P, Li R et al (2023) Rupture-related quantitative hemodynamics of the supratentorial arteriovenous malformation nidus. J Neurosurg 138(3):740–749. https://doi.org/10.3171/2022.6.JNS212818

    Article  PubMed  Google Scholar 

  16. Lin CJ, Chen KK, Hu YS, Yang HC, Lin CF, Chang FC (2022) Quantified Flow and Angioarchitecture Show Similar Associations with Hemorrhagic Presentation of Brain Arteriovenous Malformations. J Neuroradiol 1. https://doi.org/10.1016/j.neurad.2022.01.061

  17. Chen Y, Han H, Ma L, et al (2022) Multimodality treatment for brain arteriovenous malformation in Mainland China: design, rationale, and baseline patient characteristics of a nationwide multicenter prospective registry. Chi Neurosurg J 8(1) https://doi.org/10.1186/s41016-022-00296-y

  18. Chen Y, Han H, Jin H, et al (2023) 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 25. https://doi.org/10.1097/JS9.0000000000000341

  19. Chen Y, Han H, Meng X et al (2023) Development and Validation of a Scoring System for Hemorrhage Risk in Brain Arteriovenous Malformations. JAMA Network Open 6(3):e231070. https://doi.org/10.1001/jamanetworkopen.2023.1070

    Article  PubMed  PubMed Central  Google Scholar 

  20. Chen Y, Yan D, Li Z et al (2021) Long-Term Outcomes of Elderly Brain Arteriovenous Malformations After Different Management Modalities: A Multicenter Retrospective Study. Front Aging Neurosci 13:609588. https://doi.org/10.3389/fnagi.2021.609588

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Todaka T, Hamada J, Kai Y, Morioka M, Ushio Y (2003) Analysis of mean transit time of contrast medium in ruptured and unruptured arteriovenous malformations: a digital subtraction angiographic study. Stroke 34(10):2410–2414. https://doi.org/10.1161/01.STR.0000089924.43363.E3

    Article  PubMed  Google Scholar 

  22. Nikolaev SI, Vetiska S, Bonilla X et al (2018) Somatic Activating KRAS Mutations in Arteriovenous Malformations of the Brain. N Engl J Med 378(3):250–261. https://doi.org/10.1056/NEJMoa1709449

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Chen Y, Li R, Ma L, et al (2020) Long-term outcomes of brainstem arteriovenous malformations after different management modalities: a single-centre experience. Stroke Vasc Neurol 14. https://doi.org/10.1136/svn-2020-000407

  24. Deng Z, Chen Y, Ma L et al (2021) Long-term outcomes and prognostic predictors of 111 pediatric hemorrhagic cerebral arteriovenous malformations after microsurgical resection: a single-center experience. Neurosurg Rev 44(2):915–923. https://doi.org/10.1007/s10143-019-01210-4

    Article  PubMed  Google Scholar 

  25. Stefani MA, Porter PJ, terBrugge KG, Montanera W, Willinsky RA, Wallace MC (2002) Large and deep brain arteriovenous malformations are associated with risk of future hemorrhage. Stroke 33(5):1220–1224. https://doi.org/10.1161/01.str.0000013738.53113.33

    Article  PubMed  Google Scholar 

  26. Ai X, Ye Z, Xu J, You C, Jiang Y (2018) The factors associated with hemorrhagic presentation in children with untreated brain arteriovenous malformation: a meta-analysis. J Neurosurg Pediatr 23(3):343–354. https://doi.org/10.3171/2018.9.Peds18262

    Article  PubMed  Google Scholar 

  27. Feghali J, Yang W, Xu R et al (2019) R2eD AVM Score. Stroke 50(7):1703–1710. https://doi.org/10.1161/STROKEAHA.119.025054

    Article  PubMed  Google Scholar 

  28. Chen Y, Meng X, Ma L et al (2020) Contemporary management of brain arteriovenous malformations in mainland China: a web-based nationwide questionnaire survey. Chin Neurosurg J 6:26. https://doi.org/10.1186/s41016-020-00206-0

    Article  PubMed  PubMed Central  Google Scholar 

  29. Strother CM, Bender F, Deuerling-Zheng Y et al (2010) Parametric color coding of digital subtraction angiography. AJNR Am J Neuroradiol 31(5):919–924. https://doi.org/10.3174/ajnr.A2020

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Cheng P, Ma L, Shaligram S et al (2019) Effect of elevation of vascular endothelial growth factor level on exacerbation of hemorrhage in mouse brain arteriovenous malformation. J Neurosurg 132(5):1566–1573. https://doi.org/10.3171/2019.1.JNS183112

    Article  PubMed  PubMed Central  Google Scholar 

  31. Ye X, Wang L, Li M-t et al (2020) Hemodynamic changes in superficial arteriovenous malformation surgery measured by intraoperative ICG fluorescence videoangiography with FLOW 800 software. Chin Neurosurg J 6(1):29. https://doi.org/10.1186/s41016-020-00208-y

    Article  PubMed  PubMed Central  Google Scholar 

  32. Miyasaka Y, Kurata A, Tokiwa K, Tanaka R, Yada K, Ohwada T (Feb1994) Draining vein pressure increases and hemorrhage in patients with arteriovenous malformation. Stroke 25(2):504–507. https://doi.org/10.1161/01.str.25.2.504

    Article  CAS  PubMed  Google Scholar 

  33. Young WL, Kader A, Pile-Spellman J, Ornstein E, Stein BM (1994) Arteriovenous malformation draining vein physiology and determinants of transnidal pressure gradients The Columbia University AVM Study Project. Neurosurgery 35(3):389–95. https://doi.org/10.1227/00006123-199409000-00005. (discussion 395-6)

    Article  CAS  PubMed  Google Scholar 

  34. Yamada S, Takagi Y, Nozaki K, Kikuta K, Hashimoto N (2007) Risk factors for subsequent hemorrhage in patients with cerebral arteriovenous malformations. J Neurosurg 107(5):965–972. https://doi.org/10.3171/jns-07/11/0965

    Article  PubMed  Google Scholar 

  35. Shakur SF, Amin-Hanjani S, Mostafa H, Charbel FT, Alaraj A (2015) Hemodynamic Characteristics of Cerebral Arteriovenous Malformation Feeder Vessels With and Without Aneurysms. Stroke 46(7):1997–1999. https://doi.org/10.1161/STROKEAHA.115.009545

    Article  PubMed  Google Scholar 

  36. Shakur SF, Hussein AE, Amin-Hanjani S, Valyi-Nagy T, Charbel FT, Alaraj A (2017) Cerebral Arteriovenous Malformation Flow Is Associated With Venous Intimal Hyperplasia. Stroke 48(4):1088–1091. https://doi.org/10.1161/STROKEAHA.116.015666

    Article  PubMed  Google Scholar 

  37. Jin H, Lenck S, Krings T et al (2018) Interval angioarchitectural evolution of brain arteriovenous malformations following rupture. J Neurosurg 131(1):96–103. https://doi.org/10.3171/2018.2.JNS18128

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We thank the Cerebrovascular Surgery Study Project of Beijing Tiantan Hospital.

Funding

This study was supported by the National Key R&D Program (2021YFC2501101, and 2020YFC2004701 to Xiaolin Chen), and the Natural Science Foundation of China (81771234 and 82071302 to Yuanli Zhao; 82202244 to Yu Chen).

Author information

Authors and Affiliations

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

    Ruinan Li, Heze Han, Zhipeng Li, Xiaolin Chen, Yu Chen & Yuanli Zhao

  2. College of Energy and Power Engineering, Nanjing University of Aeronautics and Astronautics, Nanjing, China

    Pingting Chen

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

    Xiaolin Chen

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

    Yuanli Zhao

Authors
  1. Ruinan Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Pingting Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Heze Han
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zhipeng Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Xiaolin Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yu Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yuanli Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Ruinan Li and Pingting Chen. The first draft of the manuscript was written by Ruinan Li and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Yuanli Zhao.

Ethics declarations

Ethics approval

The Institutional Review Board of Beijing Tiantan Hospital approved this study (KY 2020–003-01).

Competing interests

The authors have no relevant financial or non-financial interests to disclose.

Additional information

Publisher's note

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

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 1149 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

Li, R., Chen, P., Han, H. et al. Association of nidus size and rupture in brain arteriovenous malformations: Insight from angioarchitecture and hemodynamics. Neurosurg Rev 46, 216 (2023). https://doi.org/10.1007/s10143-023-02113-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10143-023-02113-1

Keywords

Search

Navigation