Skip to main content
SpringerLink
Log in

Subsequent haemorrhage in children with untreated brain arteriovenous malformation: Higher risk with unbalanced inflow and outflow angioarchitecture

  • Paediatric
  • Published:
European Radiology Aims and scope Submit manuscript

Abstract

Objectives

Children with brain arteriovenous malformations (bAVMs) are at risk of life-threatening haemorrhage in their early lives. Our aim was to analyse various angioarchitectural features of bAVM to predict the risk of subsequent haemorrhage during follow-up in children.

Methods

We identified all consecutive children admitted to our institution for bAVMs between July 2009 and September 2015. Children with at least 1 month of treatment-free follow-up after diagnosis were included in further analysis. Annual rates of AVM rupture as well as several potential risk factors for subsequent haemorrhage were analysed using Kaplan-Meier analyses and Cox proportional hazards regression models.

Results

We identified 110 paediatric patients with a mean follow-up period of 2.1 years (range, 1 month–15.4 years). The average annual risk of haemorrhage from untreated AVMs was 4.3 % in children. No generalised venous ectasia in conjunction with fast arteriovenous shunt was predictive of subsequent haemorrhage (RR, 7.55; 95 % CI 1.96–29.06). The annual rupture risk was 11.1 % in bAVMs without generalised venous ectasia but with fast arteriovenous shunt.

Conclusions

bAVM angiographic features suggesting unbalanced inflow and outflow might be helpful to identify children at higher risk for future haemorrhage.

Key Points

• Haemorrhage risk stratification is important for children with untreated brain AVM.

• Angiographic features suggesting unbalanced inflow and outflow predict paediatric brain AVM haemorrhage.

• Identifying AVMs with high rupture risk help patient selection and tailoring treatment.

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

Similar content being viewed by others

Abbreviations

A-V:

Arteriovenous

bAVM:

Brain arteriovenous malformation

CI:

Confidence interval

CSF:

Cerebrospinal fluid

RR:

Relative risk

ICH:

Intracranial haemorrhage

OR:

Odds ratio

References

  1. Fullerton HJ, Achrol AS, Johnston SC et al (2005) Long-term hemorrhage risk in children versus adults with brain arteriovenous malformations. Stroke 36:2099–2104

    Article  PubMed  Google Scholar 

  2. Ellis MJ, Armstrong D, Vachhrajani S et al (2013) Angioarchitectural features associated with hemorrhagic presentation in pediatric cerebral arteriovenous malformations. J Neurointerv Surg 5:191–195

    Article  PubMed  Google Scholar 

  3. Kellner CP, McDowell MM, Phan MQ et al (2014) Number and location of draining veins in pediatric arteriovenous malformations: association with hemorrhage. J Neurosurg Pediatr 14:538–545

    Article  PubMed  Google Scholar 

  4. Friedlander RM (2007) Clinical practice. Arteriovenous malformations of the brain. N Engl J Med 356:2704–2712

    Article  CAS  PubMed  Google Scholar 

  5. ApSimon HT, Reef H, Phadke RV, Popovic EA (2002) A population-based study of brain arteriovenous malformation: long-term treatment outcomes. Stroke 33:2794–2800

    Article  CAS  PubMed  Google Scholar 

  6. Ma L, Huang Z, Chen XL et al (2015) Periventricular location as a risk factor for hemorrhage and severe clinical presentation in pediatric patients with untreated brain arteriovenous malformations. AJNR Am J Neuroradiol 36:1550–1557

    Article  CAS  PubMed  Google Scholar 

  7. Blauwblomme T, Bourgeois M, Meyer P et al (2014) Long-term outcome of 106 consecutive pediatric ruptured brain arteriovenous malformations after combined treatment. Stroke 45:1664–1671

    Article  PubMed  Google Scholar 

  8. Gross BA, Storey A, Orbach DB, Scott RM, Smith ER (2015) Microsurgical treatment of arteriovenous malformations in pediatric patients: the Boston Children's Hospital experience. J Neurosurg Pediatr 15:71–77

    Article  PubMed  Google Scholar 

  9. Lawton MT, Rutledge WC, Kim H et al (2015) Brain arteriovenous malformations. Nat Rev Dis Primers 1:15008

    Article  PubMed  Google Scholar 

  10. Gross BA, Du R (2013) Natural history of cerebral arteriovenous malformations: a meta-analysis. J Neurosurg 118:437–443

    Article  PubMed  Google Scholar 

  11. 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 83:590–597

    Article  PubMed  PubMed Central  Google Scholar 

  12. Duong DH, Young WL, Vang MC et al (1998) Feeding artery pressure and venous drainage pattern are primary determinants of hemorrhage from cerebral arteriovenous malformations. Stroke 29:1167–1176

    Article  CAS  PubMed  Google Scholar 

  13. Illies T, Forkert ND, Saering D et al (2012) Persistent hemodynamic changes in ruptured brain arteriovenous malformations. Stroke 43:2910–2915

    Article  PubMed  Google Scholar 

  14. Kader A, Young WL, Pile-Spellman J et al (1994) The influence of hemodynamic and anatomic factors on hemorrhage from cerebral arteriovenous malformations. Neurosurgery 34:801–807, discussion 807-808

    Article  CAS  PubMed  Google Scholar 

  15. 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 34:2410–2414

    Article  PubMed  Google Scholar 

  16. 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 32:1430–1442

    Article  Google Scholar 

  17. 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 33:1220–1224

    Article  PubMed  Google Scholar 

  18. Khaw AV, Mohr JP, Sciacca RR et al (2004) Association of infratentorial brain arteriovenous malformations with hemorrhage at initial presentation. Stroke 35:660–663

    Article  CAS  PubMed  Google Scholar 

  19. Taeshineetanakul P, Krings T, Geibprasert S et al (2012) Angioarchitecture determines obliteration rate after radiosurgery in brain arteriovenous malformations. Neurosurgery 71:1071–1078, discussion 1079

    Article  PubMed  Google Scholar 

  20. Shankar JJ, Menezes RJ, Pohlmann-Eden B, Wallace C, terBrugge K, Krings T (2013) Angioarchitecture of brain AVM determines the presentation with seizures: proposed scoring system. AJNR Am J Neuroradiol 34:1028–1034

    Article  CAS  PubMed  Google Scholar 

  21. Stapf C, Mohr JP, Pile-Spellman J et al (2002) Concurrent arterial aneurysms in brain arteriovenous malformations with haemorrhagic presentation. J Neurol Neurosurg Psychiatry 73:294–298

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Meyer-Heim AD, Boltshauser E (2003) Spontaneous intracranial haemorrhage in children: aetiology, presentation and outcome. Brain Dev 25:416–421

    Article  PubMed  Google Scholar 

  23. Choi JH, Mast H, Sciacca RR et al (2006) Clinical outcome after first and recurrent hemorrhage in patients with untreated brain arteriovenous malformation. Stroke 37:1243–1247

    Article  PubMed  Google Scholar 

  24. Stapf C, Mast H, Sciacca RR et al (2006) Predictors of hemorrhage in patients with untreated brain arteriovenous malformation. Neurology 66:1350–1355

    Article  CAS  PubMed  Google Scholar 

  25. Abecassis IJ, Xu DS, Batjer HH, Bendok BR (2014) Natural history of brain arteriovenous malformations: a systematic review. Neurosurg Focus 37, E7

    Article  PubMed  Google Scholar 

  26. Alexander MD, Cooke DL, Nelson J et al (2015) Association between venous angioarchitectural features of sporadic brain arteriovenous malformations and intracranial hemorrhage. AJNR Am J Neuroradiol 36:949–952

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Mansmann U, Meisel J, Brock M, Rodesch G, Alvarez H, Lasjaunias P (2000) Factors associated with intracranial hemorrhage in cases of cerebral arteriovenous malformation. Neurosurgery 46:272–279, discussion 279-281

    Article  CAS  PubMed  Google Scholar 

  28. Stefani MA, Porter PJ, terBrugge KG, Montanera W, Willinsky RA, Wallace MC (2002) Angioarchitectural factors present in brain arteriovenous malformations associated with hemorrhagic presentation. Stroke 33:920–924

    Article  PubMed  Google Scholar 

  29. Ionita CN, Garcia VL, Bednarek DR et al (2014) Effect of injection technique on temporal parametric imaging derived from digital subtraction angiography in patient specific phantoms. Proc SPIE Int Soc Opt Eng 9038:90380L

    PubMed  PubMed Central  Google Scholar 

  30. Harrigan MR, Deveikis JP (2009) Handbook of cerebrovascular disease and neurointerventional technique. Humana Press, Dordecht

    Book  Google Scholar 

  31. Rutledge WC, Abla AA, Nelson J, Halbach VV, Kim H, Lawton MT (2014) Treatment and outcomes of ARUBA-eligible patients with unruptured brain arteriovenous malformations at a single institution. Neurosurg Focus 37, E8

    Article  PubMed  PubMed Central  Google Scholar 

  32. van Beijnum J, van der Worp HB, Buis DR et al (2011) Treatment of brain arteriovenous malformations: a systematic review and meta-analysis. JAMA 306:2011–2019

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

The authors would like to thank Professor Helen Kim of the Center for Cerebrovascular Research, Department of Anesthesia and Perioperative Care, Department of Epidemiology and Biostatistics at the University of California San Francisco for her assistance with the statistical analysis and Professor Shuo Wang of the Department of Neurosurgery at Beijing Tiantan Hospital for supervision and administration of our study and Dr. Gu Wei-Bin of the Department of Neuroradiology at Beijing Tiantan Hospital for his assistance with the image preparation.

The scientific guarantor of this publication is Shuo Wang, Vice President of Department of Neurosurgery and Dean of Cerebrovascular Neurosurgery Section, Beijing Tiantan Hospital, Capital Medical University. The authors of this manuscript declare no relationships with any companies whose products or services may be related to the subject matter of the article. This project was supported by the Ministry of Science and Technology of China, National Key Technology Research and Development Program (2015BAI12B04, 2013BAI09B03, 2012CB720704); Beijing Institute for Brain Disorders grant (BIBD-PXM2013_014226_07_000084); National Natural Science Foundation of China (H0906 81271313 and H0906 81571110 to Y.L. Zhao); National Institutes of Health grant (R01 NS034949 to Y.L. Zhao); Health Industry Special Scientific Research Project (No. 201402019 to J. Ma); and China Scholarship Council (No. 201508110252 to L. Ma). Institutional Review Board approval was obtained. Written informed consent was obtained from all subjects (patients) in this study. None of the study subjects or cohorts have been previously reported. Methodology: retrospective, observational, performed at one institution.

Author information

Author notes

    Authors and Affiliations

    1. Department of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, No. 6 Tiantan Xili, Dongcheng District, Beijing, People’s Republic of China, 100050

      Li Ma, Xiao-Lin Chen, Yu Chen & Yuan-Li Zhao

    2. Center for Cerebrovascular Research, Department of Anesthesia and Perioperative Care, University of California San Francisco, San Francisco, CA, USA

      Li Ma & Xiao-Lin Chen

    3. China National Clinical Research Center for Neurological Diseases, Beijing, People’s Republic of China

      Li Ma, Xiao-Lin Chen, Yu Chen & Yuan-Li Zhao

    4. Department of Neuroradiology, Beijing Tiantan Hospital, Capital Medical University, No. 6 Tiantan Xili, Dongcheng District, Beijing, People’s Republic of China, 100050

      Chun-Xue Wu & Jun Ma

    5. Stroke Center, Beijing Institute for Brain Disorders, Beijing, People’s Republic of China

      Yuan-Li Zhao

    6. Beijing Key Laboratory of Translational Medicine for Cerebrovascular Disease, Beijing, People’s Republic of China

      Yuan-Li Zhao

    Authors
    1. Li Ma
      View author publications

      You can also search for this author in PubMed Google Scholar

    2. Xiao-Lin Chen
      View author publications

      You can also search for this author in PubMed Google Scholar

    3. Yu Chen
      View author publications

      You can also search for this author in PubMed Google Scholar

    4. Chun-Xue Wu
      View author publications

      You can also search for this author in PubMed Google Scholar

    5. Jun Ma
      View author publications

      You can also search for this author in PubMed Google Scholar

    6. Yuan-Li Zhao
      View author publications

      You can also search for this author in PubMed Google Scholar

    Corresponding authors

    Correspondence to Jun Ma or Yuan-Li Zhao.

    Additional information

    Jun Ma and Yuan-Li Zhao contributed equally to this work as senior authors.

    Electronic supplementary material

    Below is the link to the electronic supplementary material.

    ESM 1

    (DOCX 1094 kb)

    Rights and permissions

    Reprints and permissions

    About this article

    Check for updates. Verify currency and authenticity via CrossMark

    Cite this article

    Ma, L., Chen, XL., Chen, Y. et al. Subsequent haemorrhage in children with untreated brain arteriovenous malformation: Higher risk with unbalanced inflow and outflow angioarchitecture. Eur Radiol 27, 2868–2876 (2017). https://doi.org/10.1007/s00330-016-4645-3

    Download citation

    • Received:

    • Revised:

    • Accepted:

    • Published:

    • Issue Date:

    • DOI: https://doi.org/10.1007/s00330-016-4645-3

    Keywords

    Search

    Navigation