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Pathophysiology of Arteriovenous Anomaly-Related Hemorrhage

  • Jae H. Choi
  • John Pile-Spellman
Chapter
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.

References

  1. 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.CrossRefPubMedGoogle Scholar
  2. 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.CrossRefPubMedGoogle Scholar
  3. 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.CrossRefGoogle Scholar
  4. 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.CrossRefGoogle Scholar
  5. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  6. 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.CrossRefGoogle Scholar
  7. 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.CrossRefPubMedGoogle Scholar
  8. 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.CrossRefPubMedGoogle Scholar
  9. 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.CrossRefPubMedGoogle Scholar
  10. 10.
    Newton TH, Cronqvist S. Involvement of dural arteries in intracranial arteriovenous malformations. Radiology. 1969;93:1071–8.CrossRefPubMedGoogle Scholar
  11. 11.
    Choi JH, Mohr JP. Brain arteriovenous malformations in adults. Lancet Neurol. 2005;4:299–308.CrossRefPubMedGoogle Scholar
  12. 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.CrossRefPubMedGoogle Scholar
  13. 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.CrossRefPubMedGoogle Scholar
  14. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Gross BA, Ropper AE, Du R. Cerebral dural arteriovenous fistulas and aneurysms. Neurosurg Focus. 2012;32:E2.CrossRefPubMedGoogle Scholar
  16. 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.CrossRefPubMedGoogle Scholar
  17. 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.CrossRefPubMedGoogle Scholar
  18. 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. 19.
    Spetzler RF, Martin NA. A proposed grading system for arteriovenous malformations. J Neurosurg. 1986;65:476–83.CrossRefPubMedGoogle Scholar
  20. 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.CrossRefPubMedGoogle Scholar
  21. 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.CrossRefPubMedGoogle Scholar
  22. 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.PubMedGoogle Scholar
  23. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  24. 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.CrossRefPubMedGoogle Scholar
  25. 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.PubMedGoogle Scholar
  26. 26.
    Mast H, Mohr JP, Thompson JLP, et al. Transcranial doppler ultrasonography in cerebral arteriovenous malformations. Stroke. 1995;26:1024–7.CrossRefPubMedGoogle Scholar
  27. 27.
    Marks MP, Lane B, Steinberg GK, et al. Hemorrhage in intracerebral arteriovenous malformations: angiographic determinants. Radiology. 1990;176:807–13.CrossRefPubMedGoogle Scholar
  28. 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.CrossRefGoogle Scholar
  29. 29.
    Stapf C, Mast H, Sciacca RR, et al. Predictors of hemorrhage in patients with untreated brain arteriovenous malformation. Neurology. 2006;66:1350–5.CrossRefPubMedGoogle Scholar
  30. 30.
    Gross BA, Du R. Natural history of cerebral arteriovenous malformations: a meta-analysis. J Neurosurg. 2013;118:437–43.CrossRefPubMedGoogle Scholar
  31. 31.
    Derdeyn CP, Zipfel GJ, Albuquerque FC, et al. Management of brain arteriovenous malformations. Stroke. 2017;48:e200–24.CrossRefPubMedGoogle Scholar
  32. 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.CrossRefPubMedGoogle Scholar
  33. 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.CrossRefPubMedGoogle Scholar
  34. 34.
    Suh DC, Alvarez H, Bhattacharya JJ, et al. Intracranial hemorrhage within the first two years of life. Acta Neurochir. 2001;143:997–1004.CrossRefPubMedGoogle Scholar
  35. 35.
    Abdulrauf SI, Malik GM, Awad IA. Spontaneous angiographic obliteration of cerebral arteriovenous malformations. Neurosurgery. 1999;44:280–7.CrossRefPubMedGoogle Scholar
  36. 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. 37.
    Abdalla SA, Letarte M. Hereditary haemorrhagic telangiectasia: current views on genetics and mechanisms of disease. J Med Genet. 2006;43:97–110.CrossRefPubMedPubMedCentralGoogle Scholar
  38. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  39. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  40. 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.CrossRefPubMedGoogle Scholar
  41. 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. 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. 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.CrossRefPubMedGoogle Scholar
  44. 44.
    Gandhi D, Chen J, Pearl M, et al. Intracranial dural arteriovenous fistulas: classification, imaging findings, and treatment. AJNR. 2012;33:1007–13.CrossRefPubMedGoogle Scholar
  45. 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.CrossRefPubMedGoogle Scholar
  46. 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.CrossRefGoogle Scholar
  47. 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.CrossRefPubMedGoogle Scholar
  48. 48.
    Soderman M, Pavic L, Edner G, et al. Natural history of dural arteriovenous shunts. Stroke. 2008;39:1735–9.CrossRefPubMedGoogle Scholar
  49. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Izumi T, Miyachi S, Hattori K, et al. Thrombophilic abnormalities among patients with cranial dural arteriovenous fistulas. Neurosurgery. 2007;61:262–8.CrossRefPubMedGoogle Scholar
  51. 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.CrossRefGoogle Scholar
  52. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Chung SJ, Kim JS, Kim JC, et al. Intracranial dural arteriovenous fistulas: analysis of 60 patients. Cerebrovasc Dis. 2002;13:79–88.CrossRefPubMedGoogle Scholar
  54. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Nabors MW, Azzam CJ, Albanna FJ, et al. Delayed postoperative dural arteriovenous malformations: report of two cases. J Neurosurg. 1987;66:768–72.CrossRefPubMedGoogle Scholar
  56. 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.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Singapore 2018

Authors and Affiliations

  • Jae H. Choi
    • 1
    • 2
    • 3
  • John Pile-Spellman
    • 1
    • 3
  1. 1.Center for Unruptured Brain Aneurysms, Neurological Surgery, P.CLake SuccessUSA
  2. 2.Department of NeurologyState University of New York, Downstate Medical CenterBrooklynUSA
  3. 3.Hybernia Medical, LLCUniondaleUSA

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