Skip to main content

Pathophysiology of Arteriovenous Anomaly-Related Hemorrhage

  • 1656 Accesses

Part of the Stroke Revisited book series (STROREV)

Abstract

Although uncommon, brain arteriovenous malformations (AVM) and dural arteriovenous fistula (DAVF, also known as dural AVM) are two important causes for intracranial hemorrhage. Characteristic of these intracranial vascular malformations is the direct connections between artery and vein, so-called AV shunts, where capillaries are missing. Brain AVMs have a nidus, a complex tangled bundle of abnormal vessels, between feeding artery and draining vein. The angioarchitecture of brain AVMs may be complex with multiple feeding arteries, occupation of a large space within the cerebral or cerebellar hemisphere, flow-related and intranidal aneurysms, connection to ventricular system, and superficial and deep draining veins. DAVFs are located along the dura with one or multiple feeders mostly from the meningeal arteries and may drain directly into a venous sinus or via cortical and leptomeningeal veins. DAVFs do not form a nidus. Brain AVMs are considered congenital lesions, whereas trauma, thrombosis, and atherosclerosis are known mechanisms for DAVFs. However, most DAVFs are idiopathic. Clinical factors and anatomical and angioarchitectural features of these lesions have been identified that are related to intracranial hemorrhage. Intranidal and venous hypertension, inflammation, angiogenesis, and genetic factors are thought to be important mechanisms in the pathogenesis of these rare lesions.

Keywords

These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   79.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   99.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   139.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  1. Al-Shahi R, Bhattacharya JJ, Currie DG, et al. Population-based detection of intracranial vascular malformations in adults; the Scottish intracranial vascular malformation study (SIVMS). Stroke. 2003;34:1163–9.

    Article  PubMed  Google Scholar 

  2. Brown RD, Wiebers DO, Torner JC, et al. Frequency of intracranial hemorrhage as a presenting symptom and subtype analysis: a population-based study of intracranial vascular malformations in Olmsted County, Minnesota. J Neurosurg. 1996;85:29–32.

    Article  PubMed  Google Scholar 

  3. Stapf C, Mohr JP, Hartmann A, et al. Arteriovenous malformations and other vascular anomalies. In: Mohr JP, editor. Stroke: pathophysiology, diagnosis, and management, 5th edn. Philadelphia: Elsevier; 2011. p. 616–42.

    Chapter  Google Scholar 

  4. Stapf C, Mast H, Sciacca RR, et al. The New York Islands AVM study design, study progress, and initial results. Stroke. 2003;34:29–33.

    Article  Google Scholar 

  5. Kim H, Al-Shahi Salman R, McCulloch CE, et al. Untreated brain arteriovenous malformation patient-level meta-analysis of hemorrhage predictors. Neurology. 2014;83:590–7.

    Article  PubMed  PubMed Central  Google Scholar 

  6. Mohr JP, Parides MK, Stapf C, et al. Medical management with or without interventional therapy for unruptured brain arteriovenous malformations (ARUBA): a multicentre, non-blinded, randomised trial. Lancet. 2014;9917:614–21.

    Article  Google Scholar 

  7. Davies MA, Ter Brugge K, Willinsky R, et al. The natural history and management of intracranial dural arteriovenous fistulae. Part 2: aggressive lesions. Interv Neuroradiol. 1997;3:303–11.

    Article  CAS  PubMed  Google Scholar 

  8. Shin NY, Kwon YS, Ha SY, et al. Venous angioarchitectural features of intracranial dural arteriovenous shunt and its relation to the clinical course. Neuroradiology. 2013;55:1119–27.

    Article  PubMed  Google Scholar 

  9. van Dijk JM, terBrugge KG, Willinsky RA, et al. Clinical course of cranial dural arteriovenous fistulas with long-term persistent cortical venous reflux. Stroke. 2002;33:1233–6.

    Article  PubMed  Google Scholar 

  10. Newton TH, Cronqvist S. Involvement of dural arteries in intracranial arteriovenous malformations. Radiology. 1969;93:1071–8.

    Article  CAS  PubMed  Google Scholar 

  11. Choi JH, Mohr JP. Brain arteriovenous malformations in adults. Lancet Neurol. 2005;4:299–308.

    Article  PubMed  Google Scholar 

  12. Borden JA, Wu JK, Shucart WA. A proposed classification for spinal and cranial dural arteriovenous malformations and implications for treatment. J Neurosurg. 1995;82:166–79.

    Article  CAS  PubMed  Google Scholar 

  13. Brown RD, Flemming KD, Meyer FB, et al. Natural history, evaluation, and management of intracranial vascular malformations. Mayo Clin Proc. 2005;80:269–81.

    Article  PubMed  Google Scholar 

  14. Stapf C, Mohr JP, Pile-Spellman J, et al. Concurrent arterial aneurysms in brain arteriovenous malformations with haemorrhagic presentation. J Neurol Neurosurg Psychiatry. 2002;73:294–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Gross BA, Ropper AE, Du R. Cerebral dural arteriovenous fistulas and aneurysms. Neurosurg Focus. 2012;32:E2.

    Article  PubMed  Google Scholar 

  16. Choi JH, Mast H, Sciacca RR, et al. Clinical outcome after first and recurrent hemorrhage in patients with untreated brain arteriovenous malformation. Stroke. 2006;37:1243–7.

    Article  PubMed  Google Scholar 

  17. van Beijnum J, Lovelock CE, Cordonnier C, et al. Outcome after spontaneous and arteriovenous malformation-related intracerebral haemorrhage: population-based studies. Brain. 2009;132:537–43.

    Article  PubMed  Google Scholar 

  18. Gross BA, Albuquerque FC, McDougall CG, et al. A multi-institutional analysis of the untreated course of cerebral dural arteriovenous fistulas. J Neurosurg. 2017:15:1–6.

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  20. Marshall RS, Hacein-Bey L, Young WL, et al. Functional reorganization induced by endovascular embolization of a cerebral AVM. Hum Brain Mapp. 1996;4:168–73.

    Article  CAS  PubMed  Google Scholar 

  21. Meyer B, Schaller C, Frenkel C, et al. Distributions of local oxygen saturation and its response to changes of mean arterial blood pressure in the cerebral cortex adjacent to arteriovenous malformations. Stroke. 1999;30:2623–30.

    Article  CAS  PubMed  Google Scholar 

  22. Young WL, Pile-Spellman J, Prohovnik I, et al. Evidence for adaptive autoregulatory displacement in hypotensive cortical territories adjacent to arteriovenous malformations. Neurosurgery. 1994;34:601–10.

    PubMed  CAS  Google Scholar 

  23. Choi JH, Mast H, Hartmann A, et al. Clinical and morphological determinants of focal neurological deficits in patients with unruptured brain arteriovenous malformation. J Neurol Sci. 2009;287:126–30.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Burchiel KJ, Clarke H, Ojemann GA, et al. Use of stimulation mapping and corticography in the excision of arteriovenous malformations in sensorimotor and language-related neocortex. Neurosurgery. 1989;24:322–7.

    Article  CAS  PubMed  Google Scholar 

  25. Alkadhi H, Kollias SS, Crelier GR, et al. Plasticity of the human motor cortex in patients with arteriovenous malformations: a functional MRI study. AJNR. 2000;21:1423–33.

    PubMed  CAS  PubMed Central  Google Scholar 

  26. Mast H, Mohr JP, Thompson JLP, et al. Transcranial doppler ultrasonography in cerebral arteriovenous malformations. Stroke. 1995;26:1024–7.

    Article  CAS  PubMed  Google Scholar 

  27. Marks MP, Lane B, Steinberg GK, et al. Hemorrhage in intracerebral arteriovenous malformations: angiographic determinants. Radiology. 1990;176:807–13.

    Article  CAS  PubMed  Google Scholar 

  28. Hoang Duong D, Young WL, Vang MC, et al. Feeding artery pressure and venous drainage pattern are primary determinants of hemorrhage from cerebral arteriovenous malformations. Stroke. 1998;29:1167–76.

    Article  Google Scholar 

  29. Stapf C, Mast H, Sciacca RR, et al. Predictors of hemorrhage in patients with untreated brain arteriovenous malformation. Neurology. 2006;66:1350–5.

    Article  CAS  PubMed  Google Scholar 

  30. Gross BA, Du R. Natural history of cerebral arteriovenous malformations: a meta-analysis. J Neurosurg. 2013;118:437–43.

    Article  PubMed  Google Scholar 

  31. Derdeyn CP, Zipfel GJ, Albuquerque FC, et al. Management of brain arteriovenous malformations. Stroke. 2017;48:e200–24.

    Article  PubMed  Google Scholar 

  32. Miyasaka Y, Yada K, Ohwada T, et al. An analysis of the venous drainage system as a factor in hemorrhage from arteriovenous malformations. J Neurosurg. 1992;76:239–43.

    Article  CAS  PubMed  Google Scholar 

  33. Vinuela F, Nombela L, Roach MR, et al. Stenotic and occlusive disease of the venous drainage system of deep brain AVMs. J Neurosurg. 1985;63:180–4.

    Article  CAS  PubMed  Google Scholar 

  34. Suh DC, Alvarez H, Bhattacharya JJ, et al. Intracranial hemorrhage within the first two years of life. Acta Neurochir. 2001;143:997–1004.

    Article  CAS  PubMed  Google Scholar 

  35. Abdulrauf SI, Malik GM, Awad IA. Spontaneous angiographic obliteration of cerebral arteriovenous malformations. Neurosurgery. 1999;44:280–7.

    Article  CAS  PubMed  Google Scholar 

  36. Kim H, Pawlikowska L, Young WL (2011) Genetics and vascular biology of brain vascular malformations. In: Mohr JP (ed) Stroke: Pathophysiology, diagnosis, and management, 5th edn. Elsevier, Philadelphia, 169–186.

    Google Scholar 

  37. Abdalla SA, Letarte M. Hereditary haemorrhagic telangiectasia: current views on genetics and mechanisms of disease. J Med Genet. 2006;43:97–110.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. McAllister KA, Grogg KM, Johnson DW, et al. Endoglin, a TGF-beta binding protein of endothelial cells, is the gene for hereditary haemorrhagic telangiectasia type 1. Nat Genet. 1994;8:345–51.

    Article  CAS  PubMed  Google Scholar 

  39. Johnson DW, Berg JN, Baldwin MA, et al. Mutations in the activin receptor-like kinase 1 gene in hereditary haemorrhagic telangiectasia type 2. Nat Genet. 1996;13:189–95.

    Article  CAS  PubMed  Google Scholar 

  40. Pawlikowska L, Tran MN, Achrol AS, et al. Polymorphisms in genes involved in inflammatory and angiogenic pathways and the risk of hemorrhagic presentation of brain arteriovenous malformations. Stroke. 2004;35:2294–300.

    Article  CAS  PubMed  Google Scholar 

  41. Achrol AS, Pawlikowska L, McCulloch CE et al (2006) Tumor necrosis factor-alpha-238G>A promoter polymorphism is associated with increased risk of new hemorrhage in the natural course of patients with brain arteriovenous malformations. Stroke 37:231–234.

    Google Scholar 

  42. Achrol AS, Kim H, Pawlikowska L et al (2007) Association of tumor necrosis factor-alpha-238G>A and Apolipoprotein E2 polymorphisms with intracranial hemorrhage after brain arteriovenous malformation treatment. Neurosurgery 61:731–739.

    Google Scholar 

  43. Zipfel GJ, Shah MN, Refal D, et al. Cranial dural arteriovenous fistulas: modification of angiographic classification scales based on new natural history data. Neurosurg Focus. 2009;26:E14.

    Article  PubMed  Google Scholar 

  44. Gandhi D, Chen J, Pearl M, et al. Intracranial dural arteriovenous fistulas: classification, imaging findings, and treatment. AJNR. 2012;33:1007–13.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Cognard C, Gobin YP, Pierrot L, et al. Cerebral dural arteriovenous fistulas: clinical and angiographic correlation with a revised classification of venous drainage. Radiology. 1995;194:671–80.

    Article  CAS  PubMed  Google Scholar 

  46. Djinjian R, Merland JJ. Meningeal arteriovenous fistulae. In: Djinjian R, editor. Super-selective arteriography of the external carotid artery. New York: Springer; 1978. p. 405–536.

    Chapter  Google Scholar 

  47. Borden JA, Wu JK, Shucart WA. A proposed classification for spinal and cranial dural arteriovenous fistulous malformations and implications for treatment. J Neurosurg. 1995;82:166–79.

    Article  CAS  PubMed  Google Scholar 

  48. Soderman M, Pavic L, Edner G, et al. Natural history of dural arteriovenous shunts. Stroke. 2008;39:1735–9.

    Article  PubMed  Google Scholar 

  49. Cognard C, Casasco A, Toevi M, et al. Dural arteriovenous fistulas as a cause of intracranial hypertension due to impairment of cranial venous outflow. J Neurol Neurosurg Psychiatry. 1998;65:308–31.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Izumi T, Miyachi S, Hattori K, et al. Thrombophilic abnormalities among patients with cranial dural arteriovenous fistulas. Neurosurgery. 2007;61:262–8.

    Article  PubMed  Google Scholar 

  51. Saito A, Takahashi N, Furuno Y, et al. Multiple isolated sinus dural arteriovenous fistulas associated with antithrombin iii deficiency-case report. Neurol Med Chir. 2008;48:455–9.

    Article  Google Scholar 

  52. Safavi-Abbasi S, Di Rocco F, Nakaji P, et al. Thrombophilia due to factor V and factor II mutations and formation of a dural arteriovenous fistula: case report and review of a rare entity. Skull Base. 2008;18:135–43.

    Article  PubMed  PubMed Central  Google Scholar 

  53. Chung SJ, Kim JS, Kim JC, et al. Intracranial dural arteriovenous fistulas: analysis of 60 patients. Cerebrovasc Dis. 2002;13:79–88.

    Article  PubMed  Google Scholar 

  54. Cooper CJ, Said S, Nunez A, et al. Dural arteriovenous fistula discovered in patient presenting with recent head trauma. Am J Case Rep. 2013;14:444–8.

    Article  PubMed  PubMed Central  Google Scholar 

  55. Nabors MW, Azzam CJ, Albanna FJ, et al. Delayed postoperative dural arteriovenous malformations: report of two cases. J Neurosurg. 1987;66:768–72.

    Article  CAS  PubMed  Google Scholar 

  56. Kojima T, Miyachi S, Sahara Y, et al. The relationship between venous hypertension and expression of vascular endothelial growth factor: hemodynamic and immunohistochemical examinations in a rat venous hypertension model. Surg Neurol. 2007;68:277–84.

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer Science+Business Media Singapore

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Choi, J.H., Pile-Spellman, J. (2018). Pathophysiology of Arteriovenous Anomaly-Related Hemorrhage. In: Lee, SH. (eds) Stroke Revisited: Hemorrhagic Stroke. Stroke Revisited. Springer, Singapore. https://doi.org/10.1007/978-981-10-1427-7_5

Download citation

  • DOI: https://doi.org/10.1007/978-981-10-1427-7_5

  • Published:

  • Publisher Name: Springer, Singapore

  • Print ISBN: 978-981-10-1426-0

  • Online ISBN: 978-981-10-1427-7

  • eBook Packages: MedicineMedicine (R0)

Publish with us

Policies and ethics