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Association between draining vein diameters and intracranial arteriovenous malformation hemorrhage: a multicentric retrospective study

  • Interventional Neuroradiology
  • Published:
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Abstract

Purpose

Intracranial arteriovenous malformations (AVMs) cause hemorrhage, and the role of draining vein diameters in rupture risk is controversial. The aims of the present study were to investigate the variables related with intracranial AVM rupture and to examine the association of draining vein diameters and AVM hemorrhage.

Methods

Two hundred three patients were included in this study, of which 117 (57%) had unruptured AVMs, and 86 (43%) had ruptured AVMs.

Results

In an adjusted (multivariate) analysis, the variables significantly associated with AVM hemorrhagic presentation were age (OR per year increase 0.97, 95%CI 0.95–0.99, p = 0.007), a deep nidus compared with superficial nidus (OR 3.21, 95%CI 1.13–9.06, p = 0.028), the nidus diameter (OR per each mm increase 0.95, 95%CI 0.92–0.97, p < 0.001), a single draining vein compared with multiple draining veins (OR 2.14, 95%CI 1.02–4.50, p = 0.044), the draining vein diameter (OR per mm increase 1.52, 95%CI 1.26–1.83, p < 0.001), and a draining vein diameter ≥ 5 mm compared with < 5 mm (OR 5.80, 95%CI 2.70–12.47, p < 0.001).

Conclusion

In this study, after adjusted analysis, the variables associated with intracranial AVM hemorrhagic presentation were a young age, a small nidus diameter, a deeply located nidus, a single draining vein, and large draining vein diameters. A draining vein diameter cutoff ≥ 5 mm was positively associated with the risk of AVM rupture. A large and prospective study is now necessary to confirm if draining vein diameter is a risk factor for AVM hemorrhage.

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References

  1. Lawton MT, Rutledge WC, Kim H, Stapf C, Whitehead KJ, Li DY, Krings T, ter Brugge K, Kondziolka D, Morgan MK, Moon K, Spetzler RF (2015) Brain arteriovenous malformations. Nat Rev Dis Primers 1:15008

    Article  Google Scholar 

  2. Derdeyn CP, Zipfel GJ, Albuquerque FC, Cooke DL, Feldmann E, Sheehan JP, Torner JC American Heart Association Stroke Council(2017) Management of brain arteriovenous malformations: a scientific statement for healthcare professionals from the American Heart Association/American Stroke Association. Stroke 48:e200–e224

    PubMed  Google Scholar 

  3. Graf CJ, Perret GE, Torner JC (1983) Bleeding from cerebral arteriovenous malformations as part of their natural history. J Neurosurg 58:331–337

    Article  CAS  Google Scholar 

  4. Miyasaka Y, Yada K, Ohwada T, Kitahara T, Kurata A, Irikura K (1992) An analysis of the venous drainage system as a factor in hemorrhage from arteriovenous malformations. J Neurosurg 76:239–243

    Article  CAS  Google Scholar 

  5. 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

    PubMed  CAS  Google Scholar 

  6. Brown RD Jr, Wiebers DO, Forbes GS (1990) Unruptured intracranial aneurysms and arteriovenous malformations: frequency of intracranial hemorrhage and relationship of lesions. J Neurosurg 73:859–863

    Article  Google Scholar 

  7. Ding D, Starke RM, Kano H, Mathieu D, Huang PP, Feliciano C, Rodriguez-Mercado R, Almodovar L, Grills IS, Silva D, Abbassy M, Missios S, Kondziolka D, Barnett GH, Dade Lunsford L, Sheehan JP (2017) International multicenter cohort study of pediatric brain arteriovenous malformations. Part 1: predictors of hemorrhagic presentation. J Neurosurg Pediatr 19:127–135

    Article  Google Scholar 

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

    Article  Google Scholar 

  9. Goldberg J, Raabe A, Bervini D (2018) Natural history of brain arteriovenous malformations: systematic review. J Neurosurg Sci 62:437–443

    PubMed  Google Scholar 

  10. Kim H, Al-Shahi Salman R, McCulloch CE, Stapf C, Young WL, MARS Coinvestigators (2014) Untreated brain arteriovenous malformation: patient-level meta-analysis of hemorrhage predictors. Neurology 83:590–597

    Article  Google Scholar 

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

    Article  Google Scholar 

  12. Hernesniemi JA, Dashti R, Juvela S, Väärt K, Niemelä M, Laakso A (2008) Natural history of brain arteriovenous malformations: a long-term follow-up study of risk of hemorrhage in 238 patients. Neurosurgery 63:823–829 discussion 829-31

    Article  Google Scholar 

  13. Rutledge WC, Ko NU, Lawton MT, Kim H (2014) Hemorrhage rates and risk factors in the natural history course of brain arteriovenous malformations. Transl Stroke Res 5:538–542

    Article  Google Scholar 

  14. Rangel-Castilla L, Russin JJ, Martinez-Del-Campo E, Soriano-Baron H, Spetzler RF, Nakaji P (2014) Molecular and cellular biology of cerebral arteriovenous malformations: a review of current concepts and future trends in treatment. Neurosurg Focus 37(3):E1

    Article  Google Scholar 

  15. Alexander MD, Cooke DL, Nelson J, Guo DE, Dowd CF, Higashida RT, Halbach VV, Lawton MT, Kim H, Hetts SW (2015) Association between venous angioarchitectural features of sporadic brain arteriovenous malformations and intracranial hemorrhage. AJNR Am J Neuroradiol 36:949–952

    Article  CAS  Google Scholar 

  16. 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  Google Scholar 

  17. Mohr JP, Parides MK, Stapf C, Moquete E, Moy CS, Overbey JR, Al-Shahi Salman R, Vicaut E, Young WL, Houdart E, Cordonnier C, Stefani MA, Hartmann A, von Kummer R, Biondi A, Berkefeld J, Klijn CJ, Harkness K, Libman R, Barreau X, Moskowitz AJ, international ARUBA investigators (2014) Medical management with or without interventional therapy for unruptured brain arteriovenous malformations (ARUBA): a multicentre, non-blinded, randomised trial. Lancet 383(9917):614–621

    Article  CAS  Google Scholar 

  18. Al-Shahi Salman R, White PM, Counsell CE, du Plessis J, van Beijnum J, Josephson CB, Wilkinson T, Wedderburn CJ, Chandy Z, St George EJ, Sellar RJ, Warlow CP, Scottish Audit of Intracranial Vascular Malformations Collaborators (2014) Outcome after conservative management or intervention for unruptured brain arteriovenous malformations. JAMA 311:1661–1669

    Article  CAS  Google Scholar 

  19. Amin-Hanjani S (2014) ARUBA results are not applicable to all patients with arteriovenous malformation. Stroke 45:1539–1540

    Article  Google Scholar 

  20. Day AL, Dannenbaum M, Jung S (2014) A randomized trial of unruptured brain arteriovenous malformations trial: an editorial review. Stroke 45:3147–3148

    Article  Google Scholar 

  21. Al-Shahi Salman R, Counsell CE, White PM (2014) Conservative management vs intervention for unruptured brain arteriovenous malformations—reply. JAMA 312:1058–1059

    Article  Google Scholar 

  22. Zaidi HA, Russin JJ, Spetzler RF (2014) Conservative management vs intervention for unruptured brain arteriovenous malformations. JAMA 312:1058

    Article  Google Scholar 

  23. Mohr JP, Moskowitz AJ, Parides M, Stapf C, Young WL (2012) Hull down on the horizon: a randomized trial of unruptured brain arteriovenous malformations (ARUBA) trial. Stroke 43:1744–1745

    Article  CAS  Google Scholar 

  24. Cockroft KM, Jayaraman MV, Amin-Hanjani S, Derdeyn CP, McDougall CG, Wilson JA (2012) A perfect storm: how a randomized trial of unruptured brain arteriovenous malformations’ (ARUBA’s) trial design challenges notions of external validity. Stroke 43:1979–1981

    Article  Google Scholar 

  25. Weiner GM, Grandhi R, Friedlander RM (2014) Conservative management vs intervention for unruptured brain arteriovenous malformations. JAMA 312(10):1057–1058

    Article  Google Scholar 

  26. Crowley RW, Ducruet AF, McDougall CG, Albuquerque FC (2014) Endovascular advances for brain arteriovenous malformations. Neurosurgery 74(Suppl 1):S74–S82

    Article  Google Scholar 

  27. van Beijnum J, van der Worp HB, Buis DR, Al-Shahi Salman R, Kappelle LJ, Rinkel GJ, van der Sprenkel JW, Vandertop WP, Algra A, Klijn CJ (2011) Treatment of brain arteriovenous malformations: a systematic review and meta-analysis. JAMA 306(18):2011–2019

    Article  Google Scholar 

  28. Kalani MY, Albuquerque FC, Fiorella D, McDougall CG (2013) Endovascular treatment of cerebral arteriovenous malformations. Neuroimaging Clin N Am 23:605–624

    Article  Google Scholar 

  29. Davies PF, Remuzzi A, Gordon EJ, Dewey DF, Gimbrone MA (1986) Turbulent fluid shear stress induces vascular endothelial cell turnover in vitro. Proc Natl Acad Sci 83:2114–2117

    Article  CAS  Google Scholar 

  30. Davies PF, Dewey CF, Bussolari SR et al (1984) Influence of hemodynamic forces on vascular endothelial function: in vitro studies of shear stress and pinocytosis in bovine aortic cells. J Clin Invest 73:1121–1129

    Article  CAS  Google Scholar 

  31. Masuda H, Saito N, Kawamura K et al (1986) Flow loaded canine carotid artery. Pt I: a morphometric study of microfilament bundles in endothelial cells. Acta Pathol Japan 36:1833–1842

    CAS  Google Scholar 

  32. Masuda H, Saito N, Kawamura K et al (1987) Flow loaded canine carotid artery. Pt II: ultrastructural changes in the subendothelial layer. Acta Pathol Japan 37:239–251

    CAS  Google Scholar 

  33. Smith RL, Blick EF, Coalson J, Stein PD (1972) Thrombus production by turbulence. J Appl Physiol 32:261–264

    Article  CAS  Google Scholar 

  34. Hook O, Johanson C (1958) Intracranial arteriovenous aneurysms. A follow-up study with particular attention to their growth. Arch Neural Psychiat 80:39–54

    Article  CAS  Google Scholar 

  35. Waltimo O (1973) The change in size of intracranial arteriovenous malformations. J Neurol Sci 19:21–27

    Article  CAS  Google Scholar 

  36. 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 46:1997–1999

    Article  Google Scholar 

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Funding

No funding was received for this study.

Author information

Authors and Affiliations

  1. Division of Interventional Neuroradiology, Medical School of Ribeirão Preto, University of São Paulo, Avenida Bandeirantes, 3900, Monte Alegre, Ribeirão Preto, SP, 14048-090, Brazil

    Luís Henrique de Castro-Afonso, Salomão Faroj Chodraui-Filho, Guilherme Seizem Nakiri & Daniel Giansante Abud

  2. Division of Interventional Neuroradiology, Hospital das Clínicas de Passo Fundo, Passo Fundo, RS, Brazil

    José Ricardo Vanzim

  3. Division of Interventional Neuroradiology, Instituto neurovascular, Felício Rocho hospital, Mater Dei hospital, University of Minas gerais, Belo Horizonte, Brazil

    Felipe Padovani Trivelato, Marco Tulio Rezende & Alexandre Cordeiro Ulhôa

  4. Department of Interventional Neuroradiology, Centre Hospitalier et Universitaire Dupuytren, Limoges, France

    Luiz Gustavo de Abreu Mattos & Charbel Mounayer

  5. Division of Neurosurgery, Ribeirão Preto Medical School, University of São Paulo, Ribeirão Preto, SP, Brazil

    Benedicto Oscar Colli

Authors
  1. Luís Henrique de Castro-Afonso
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  2. José Ricardo Vanzim
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  3. Felipe Padovani Trivelato
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  4. Marco Tulio Rezende
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  5. Alexandre Cordeiro Ulhôa
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  10. Benedicto Oscar Colli
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  11. Daniel Giansante Abud
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Consortia

IntraCranial Arteriovenous RUpture riSk Study (ICARUSS) investigators

Corresponding author

Correspondence to Luís Henrique de Castro-Afonso.

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The authors declare that they have no conflict of interest.

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All procedures performed in the studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.

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The institutional review board waived the need for written informed consent from participants.

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de Castro-Afonso, L.H., Vanzim, J.R., Trivelato, F.P. et al. Association between draining vein diameters and intracranial arteriovenous malformation hemorrhage: a multicentric retrospective study. Neuroradiology 62, 1497–1505 (2020). https://doi.org/10.1007/s00234-020-02484-y

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  • DOI: https://doi.org/10.1007/s00234-020-02484-y

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