Acta Neurochirurgica

, Volume 159, Issue 8, pp 1479–1487 | Cite as

Early rebleeding of intracranial dural arteriovenous fistulas after an intracranial hemorrhage

  • Jai Ho Choi
  • Kyung Il Jo
  • Keon Ha Kim
  • Pyoung Jeon
  • Je Young Yeon
  • Jong Soo Kim
  • Seung Chyul Hong
Original Article - Vascular



The aim of this study was to evaluate the clinical and angiographic characteristics of dural arteriovenous fistulas (DAVF) presenting with intracranial hemorrhage (ICH), with a focus on early rebleeding according to the initial hemorrhage type.


The clinical and radiologic features of 21 dAVFs that presented with intracranial hemorrhage were retrospectively reviewed. The hemorrhage type was classified as pure intraparenchymal hemorrhage (pIPH) and subarachnoid or subdural hemorrhage with IPH (non-pIPH).


There were 13 patients with pIPH and 8 with non-pIPH. The median follow-up period was 30 months (range, 1–116 months), and the median interval from hemorrhage to treatment was 4 days (range, 0–72 days). Rebleeding occurred in 8 (38.1%) of 21 patients. Four (50%) of eight patients with non-pIPH suffered from early rebleeding within 3 days, while there was no early rebleeding in patients with pIPH. There was a significantly higher rate of early rebleeding in the non-pIPH group (p = 0.012). Angiographically, venous ectasia (p = 0.005) and direct cortical venous drainage (dCVD) (p = 0.008) showed a significantly higher proportion in the non-pIPH group than in the pIPH group.


DAVFs with ICH is likely to rebleed after the first hemorrhage. Thus, early treatment can be needed in all DAVFs with ICH. In addition, DAVFs that presenting with non-pIPH and containing venous ectasia or dCVD on initial angiography may have a higher risk of early rebleeding. Therefore, cautious attention and urgent treatment are necessary for these patients.


Dural arteriovenous fistula Intracranial hemorrhage Rebleeding Subarachnoid hemorrhage Subdural hemorrhage 


Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.



Ethical approval

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

Informed consent

Informed consent was obtained from all individual participants included in the study.


  1. 1.
    Borden JA, Wu JK, Shucart WA (1995) A proposed classification for spinal and cranial dural arteriovenous fistulous malformations and implications for treatment. J Neurosurg 82:166–179CrossRefPubMedGoogle Scholar
  2. 2.
    Brown RD Jr, Wiebers DO, Nichols DA (1994) Intracranial dural arteriovenous fistulae: angiographic predictors of intracranial hemorrhage and clinical outcome in nonsurgical patients. J Neurosurg 81:531–538CrossRefPubMedGoogle Scholar
  3. 3.
    Bulters DO, Mathad N, Culliford D, Millar J, Sparrow OC (2012) The natural history of cranial dural arteriovenous fistulae with cortical venous reflux—the significance of venous ectasia. Neurosurgery 70:312–318 discussion 318-319CrossRefPubMedGoogle Scholar
  4. 4.
    Cognard C, Casasco A, Toevi M, Houdart E, Chiras J, Merland JJ (1998) Dural arteriovenous fistulas as a cause of intracranial hypertension due to impairment of cranial venous outflow. J Neurol Neurosurg Psychiatry 65:308–316CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Cognard C, Gobin YP, Pierot L, Bailly AL, Houdart E, Casasco A, Chiras J, Merland JJ (1995) Cerebral dural arteriovenous fistulas: clinical and angiographic correlation with a revised classification of venous drainage. Radiology 194:671–680CrossRefPubMedGoogle Scholar
  6. 6.
    Daniels DJ, Vellimana AK, Zipfel GJ, Lanzino G (2013) Intracranial hemorrhage from dural arteriovenous fistulas: clinical features and outcome. Neurosurg Focus 34:E15CrossRefPubMedGoogle Scholar
  7. 7.
    Davies MA, TerBrugge K, Willinsky R, Coyne T, Saleh J, Wallace MC (1996) The validity of classification for the clinical presentation of intracranial dural arteriovenous fistulas. J Neurosurg 85:830–837CrossRefPubMedGoogle Scholar
  8. 8.
    Duffau H, Lopes M, Janosevic V, Sichez JP, Faillot T, Capelle L, Ismail M, Bitar A, Arthuis F, Fohanno D (1999) Early rebleeding from intracranial dural arteriovenous fistulas: report of 20 cases and review of the literature. J Neurosurg 90:78–84CrossRefPubMedGoogle Scholar
  9. 9.
    Duvernoy HM (1999) Vascularization of the cerebral cortex. Rev Neurol (Paris) 155:684–687Google Scholar
  10. 10.
    Duvernoy HM, Delon S, Vannson JL (1981) Cortical blood vessels of the human brain. Brain Res Bull 7:519–579CrossRefPubMedGoogle Scholar
  11. 11.
    Gandhi D, Chen J, Pearl M, Huang J, Gemmete JJ, Kathuria S (2012) Intracranial dural arteriovenous fistulas: classification, imaging findings, and treatment. AJNR Am J Neuroradiol 33:1007–1013CrossRefPubMedGoogle Scholar
  12. 12.
    Gross BA, Du R (2012) The natural history of cerebral dural arteriovenous fistulae. Neurosurgery 71:594–602 discussion 602-593CrossRefPubMedGoogle Scholar
  13. 13.
    Hassler W, Thron A, Grote EH (1989) Hemodynamics of spinal dural arteriovenous fistulas. An intraoperative study J Neurosurg 70:360–370PubMedGoogle Scholar
  14. 14.
    Jolink WM, van Dijk JM, van Asch CJ, de Kort GA, Algra A, Groen RJ, Rinkel GJ, Klijn CJ (2015) Outcome after intracranial haemorrhage from dural arteriovenous fistulae; a systematic review and case-series. J Neurol 262:2678–2683CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Piippo A, Laakso A, Seppa K, Rinne J, Jaaskelainen JE, Hernesniemi J, Niemela M (2013) Early and long-term excess mortality in 227 patients with intracranial dural arteriovenous fistulas. J Neurosurg 119:164–171CrossRefPubMedGoogle Scholar
  16. 16.
    Piippo A, Niemela M, van Popta J, Kangasniemi M, Rinne J, Jaaskelainen JE, Hernesniemi J (2013) Characteristics and long-term outcome of 251 patients with dural arteriovenous fistulas in a defined population. J Neurosurg 118:923–934CrossRefPubMedGoogle Scholar
  17. 17.
    Satomi J, Ghaibeh AA, Moriguchi H, Nagahiro S (2015) Predictability of the future development of aggressive behavior of cranial dural arteriovenous fistulas based on decision tree analysis. J Neurosurg 123:86–90CrossRefPubMedGoogle Scholar
  18. 18.
    Shin NY, Kwon YS, Ha SY, Kim BM, Kim DI, Kim DJ (2013) Venous angioarchitectural features of intracranial dural arteriovenous shunt and its relation to the clinical course. Neuroradiology 55:1119–1127CrossRefPubMedGoogle Scholar
  19. 19.
    Singh V, Smith WS, Lawton MT, Halbach VV, Young WL (2008) Risk factors for hemorrhagic presentation in patients with dural arteriovenous fistulae. Neurosurgery 62:628–635 discussion 628-635CrossRefPubMedGoogle Scholar
  20. 20.
    Soderman M, Pavic L, Edner G, Holmin S, Andersson T (2008) Natural history of dural arteriovenous shunts. Stroke 39:1735–1739CrossRefPubMedGoogle Scholar
  21. 21.
    Strom RG, Botros JA, Refai D, Moran CJ, Cross DT 3rd, Chicoine MR, Grubb RL Jr, Rich KM, Dacey RG Jr, Derdeyn CP, Zipfel GJ (2009) Cranial dural arteriovenous fistulae: asymptomatic cortical venous drainage portends less aggressive clinical course. Neurosurgery 64:241–247 discussion 247-248CrossRefPubMedGoogle Scholar
  22. 22.
    Willinsky R, Goyal M, terBrugge K, Montanera W (1999) Tortuous, engorged pial veins in intracranial dural arteriovenous fistulas: correlations with presentation, location, and MR findings in 122 patients. AJNR Am J Neuroradiol 20:1031–1036PubMedGoogle Scholar
  23. 23.
    Zhao LB, Suh DC, Lee DG, Kim SJ, Kim JK, Han S, Lee DH, Kim JS (2014) Association of pial venous reflux with hemorrhage or edema in dural arteriovenous fistula. Neurology 82:1897–1904CrossRefPubMedGoogle Scholar
  24. 24.
    Zipfel GJ, Shah MN, Refai D, Dacey RG Jr, Derdeyn CP (2009) Cranial dural arteriovenous fistulas: modification of angiographic classification scales based on new natural history data. Neurosurg Focus 26:E14CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Wien 2017

Authors and Affiliations

  • Jai Ho Choi
    • 1
  • Kyung Il Jo
    • 2
  • Keon Ha Kim
    • 3
  • Pyoung Jeon
    • 3
  • Je Young Yeon
    • 2
  • Jong Soo Kim
    • 2
  • Seung Chyul Hong
    • 2
  1. 1.Department of NeurosurgerySeoul St. Mary’s Hospital, The Catholic University of Korea College of MedicineSeoulSouth Korea
  2. 2.Department of Neurosurgery, Samsung Medical CenterSungkyunkwan University School of MedicineSeoulSouth Korea
  3. 3.Department of Radiology, Samsung Medical CenterSungkyunkwan University School of MedicineSeoulSouth Korea

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