Angiographic Intervention in Hemorrhagic Stroke

  • Chae Wook Huh
  • Duk Ho Gho
  • Sung-Chul Jin
Part of the Stroke Revisited book series (STROREV)


Angiographic intervention has an important role in the management of hemorrhagic stroke. Conventional cerebral angiography is the gold standard for the diagnosis of various vascular lesions that cause hemorrhagic stroke. With recent advancements in imaging techniques and endovascular devices, angiographic intervention in the treatment of hemorrhagic stroke has progressed as an alternative to surgery for inaccessible intracranial lesions or inoperable patients. In particular, the International Subarachnoid Aneurysm Trial (ISAT) established endovascular treatment as a feasible modality for the treatment of patients with aneurysmal subarachnoid hemorrhage (SAH). Various endovascular techniques, including conventional simple coil embolization, balloon-assisted coil embolization, stent-assisted coil embolization, and flow diversion, have been performed to prevent fatal rebleeding by blocking the aneurysm from the circulating blood flow. These techniques also provide useful treatment options for vascular lesions, such as dural arteriovenous fistula (dAVF) and arteriovenous malformation (AVM) that are another cause of hemorrhagic stroke. Hemorrhagic stroke requires urgent treatment to prevent fatal complications, and appropriate endovascular treatment options should be selected according to the anatomical configurations of the underlying vascular lesion.


  1. 1.
    Molyneux A, Kerr R, Stratton I, et al. International subarachnoid aneurysm trial (ISAT) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomised trial. Lancet. 2002;360:1267–74.CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Mcdougall CG, Spetzler RF, Zabramski JM, et al. The barrow ruptured aneurysm trial. J Neurosurg. 2012;116:135–44.CrossRefPubMedGoogle Scholar
  3. 3.
    Rouchaud A, Brinjikji W, Cloft HJ, et al. Endovascular treatment of ruptured blister-like aneurysms: a systematic review and meta-analysis with focus on deconstructive versus reconstructive and flow-diverter treatments. AJNR Am J Neuroradiol. 2015;36:2331–9.CrossRefPubMedGoogle Scholar
  4. 4.
    Pierot L. Flow diverter stents in the treatment of intracranial aneurysms: where are we? J Neuroradiol. 2011;38:40–6.CrossRefPubMedGoogle Scholar
  5. 5.
    Kallmes DF, Ding YH, Dai D, et al. A new endoluminal, flow-disrupting device for treatment of saccular aneurysms. Stroke. 2007;38:2346–52.CrossRefPubMedGoogle Scholar
  6. 6.
    Mendes GA, Silveira EP, Caire F, et al. Endovascular management of deep arteriovenous malformations: single institution experience in 22 consecutive patients. Neurosurgery. 2016;78:34–41.CrossRefPubMedGoogle Scholar
  7. 7.
    Raymond J, Roy D. Safety and efficacy of endovascular treatment of acutely ruptured aneurysms. Neurosurgery. 1997;41:1235–45. discussion 1245-1236CrossRefPubMedGoogle Scholar
  8. 8.
    Sluzewski M, Bosch JA, Van Rooij WJ, et al. Rupture of intracranial aneurysms during treatment with Guglielmi detachable coils: incidence, outcome, and risk factors. J Neurosurg. 2001;94:238–40.CrossRefPubMedGoogle Scholar
  9. 9.
    Janssen H, Berlis A, Lutz J, et al. State of practice: endovascular treatment of acute aneurysmal SAH in Germany. AJNR Am J Neuroradiol. 2017;38:1574–9.CrossRefPubMedGoogle Scholar
  10. 10.
    Molyneux AJ, Kerr RS, Yu LM, et al. International subarachnoid aneurysm trial (ISAT) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomised comparison of effects on survival, dependency, seizures, rebleeding, subgroups, and aneurysm occlusion. Lancet. 2005;366:809–17.CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Sadato A, Adachi K, Hayakawa M, et al. Effects of anatomic characteristics of aneurysms on packing density in endovascular coil embolization: analysis of a single center's experience. Neurosurg Rev. 2016;39:109–14. discussion 114CrossRefPubMedGoogle Scholar
  12. 12.
    Kwon OK, Kim SH, Oh CW, et al. Embolization of wide-necked aneurysms with using three or more microcatheters. Acta Neurochir. 2006;148:1139–45. discussion 1145CrossRefPubMedGoogle Scholar
  13. 13.
    Baxter BW, Rosso D, Lownie SP. Double microcatheter technique for detachable coil treatment of large, wide-necked intracranial aneurysms. AJNR Am J Neuroradiol. 1998;19:1176–8.PubMedGoogle Scholar
  14. 14.
    Moret J, Cognard C, Weill A, et al. Reconstruction technic in the treatment of wide-neck intracranial aneurysms. Long-term angiographic and clinical results. Apropos of 56 cases. J Neuroradiol. 1997;24:30–44.PubMedGoogle Scholar
  15. 15.
    Kurre W, Berkefeld J. Materials and techniques for coiling of cerebral aneurysms: how much scientific evidence do we have? Neuroradiology. 2008;50:909–27.CrossRefPubMedGoogle Scholar
  16. 16.
    Cai K, Zhang Y, Shen L, et al. Comparison of stent-assisted coiling and balloon-assisted coiling in the treatment of ruptured wide-necked intracranial aneurysms in the acute period. World Neurosurg. 2016;96:316–21.CrossRefPubMedGoogle Scholar
  17. 17.
    Chalouhi N, Jabbour P, Tjoumakaris S, et al. Single-center experience with balloon-assisted coil embolization of intracranial aneurysms: safety, efficacy and indications. Clin Neurol Neurosurg. 2013;115:607–13.CrossRefPubMedGoogle Scholar
  18. 18.
    Ross IB, Dhillon GS. Balloon assistance as a routine adjunct to the endovascular treatment of cerebral aneurysms. Surg Neurol. 2006;66:593–601. discussion 601-592CrossRefPubMedGoogle Scholar
  19. 19.
    Sluzewski M, Van Rooij WJ, Beute GN, et al. Balloon-assisted coil embolization of intracranial aneurysms: incidence, complications, and angiography results. J Neurosurg. 2006;105:396–9.CrossRefPubMedGoogle Scholar
  20. 20.
    Akpek S, Arat A, Morsi H, et al. Self-expandable stent-assisted coiling of wide-necked intracranial aneurysms: a single-center experience. AJNR Am J Neuroradiol. 2005;26:1223–31.PubMedGoogle Scholar
  21. 21.
    Muto M, Giurazza F, Ambrosanio G, et al. Stent-assisted coiling in ruptured cerebral aneurysms: multi-center experience in acute phase. Radiol Med. 2017;122:43–52.CrossRefPubMedGoogle Scholar
  22. 22.
    Kim M, Levy EI, Meng H, et al. Quantification of hemodynamic changes induced by virtual placement of multiple stents across a wide-necked basilar trunk aneurysm. Neurosurgery. 2007;61:1305–12. discussion 1312-1303CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Vanninen R, Manninen H, Ronkainen A. Broad-based intracranial aneurysms: thrombosis induced by stent placement. AJNR Am J Neuroradiol. 2003;24:263–6.PubMedGoogle Scholar
  24. 24.
    Bendok BR, Parkinson RJ, Hage ZA, et al. The effect of vascular reconstruction device-assisted coiling on packing density, effective neck coverage, and angiographic outcome: an in vitro study. Neurosurgery. 2007;61:835–40. discussion 840-831CrossRefPubMedGoogle Scholar
  25. 25.
    Kadkhodayan Y, Rhodes N, Blackburn S, et al. Comparison of Enterprise with Neuroform stent-assisted coiling of intracranial aneurysms. AJR Am J Roentgenol. 2013;200:872–8.CrossRefPubMedGoogle Scholar
  26. 26.
    Higashida RT, Halbach VV, Dowd CF, et al. Initial clinical experience with a new self-expanding nitinol stent for the treatment of intracranial cerebral aneurysms: the Cordis Enterprise stent. AJNR Am J Neuroradiol. 2005;26:1751–6.PubMedGoogle Scholar
  27. 27.
    Pearl M, Gregg L, Gailloud P. Endovascular treatment of aneurysmal subarachnoid hemorrhage. Neurosurg Clin N Am. 2010;21:271–80.CrossRefPubMedGoogle Scholar
  28. 28.
    Rong-Bo Q, Hua J, Kai W, et al. Stent-jail technique in endovascular treatment of wide-necked aneurysm. Turk Neurosurg. 2013;23:179–82.PubMedGoogle Scholar
  29. 29.
    Natarajan SK, Shallwani H, Fennell VS, et al. Flow diversion after aneurysmal subarachnoid hemorrhage. Neurosurg Clin N Am. 2017;28:375–88.CrossRefPubMedGoogle Scholar
  30. 30.
    Makoyeva A, Bing F, Darsaut TE, et al. The varying porosity of braided self-expanding stents and flow diverters: an experimental study. AJNR Am J Neuroradiol. 2013;34:596–602.CrossRefPubMedGoogle Scholar
  31. 31.
    Fiorella D, Hsu D, Woo HH, et al. Very late thrombosis of a pipeline embolization device construct: case report. Neurosurgery. 2010;67:onsE313–4. discussion onsE314PubMedGoogle Scholar
  32. 32.
    Sadasivan C, Cesar L, Seong J, et al. An original flow diversion device for the treatment of intracranial aneurysms: evaluation in the rabbit elastase-induced model. Stroke. 2009;40:952–8.CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Vinuela F, Fox AJ, Debrun GM, et al. Spontaneous carotid-cavernous fistulas: clinical, radiological, and therapeutic considerations. Experience with 20 cases. J Neurosurg. 1984;60:976–84.CrossRefPubMedGoogle Scholar
  34. 34.
    Newton TH, Cronqvist S. Involvement of dural arteries in intracranial arteriovenous malformations. Radiology. 1969;93:1071–8.CrossRefPubMedGoogle Scholar
  35. 35.
    Lasjaunias PBA. Surgical neuroangiography: endovascular treatment of craniofacial lesions. Berlin: Springer; 1987.Google Scholar
  36. 36.
    Cognard C, Gobin YP, Pierot 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
  37. 37.
    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
  38. 38.
    Friedman JA, Pollock BE, Nichols DA, et al. Results of combined stereotactic radiosurgery and transarterial embolization for dural arteriovenous fistulas of the transverse and sigmoid sinuses. J Neurosurg. 2001;94:886–91.CrossRefPubMedGoogle Scholar
  39. 39.
    Bertalanffy A, Dietrich W, Kitz K, et al. Treatment of dural arteriovenous fistulae (dAVF's) at the superior sagittal sinus (SSS) using embolisation combined with micro- or radiosurgery. Minim Invasive Neurosurg. 2001;44:205–10.CrossRefPubMedGoogle Scholar
  40. 40.
    Luo CB, Teng MM, Chang FC, et al. Transorbital direct puncture of the posterior cavernous sinus through the internal carotid artery for embolization of isolated cavernous sinus dural arteriovenous fistula. J Neurointerv Surg. 2013;5:e1.CrossRefPubMedGoogle Scholar
  41. 41.
    Luo CB, Chang FC, Wu HM, et al. Transcranial embolization of a transverse-sigmoid sinus dural arteriovenous fistula carried out through a decompressive craniectomy. Acta Neurochir. 2007;149:197–200. discussion 200CrossRefPubMedGoogle Scholar
  42. 42.
    Houdart E, Saint-Maurice JP, Chapot R, et al. Transcranial approach for venous embolization of dural arteriovenous fistulas. J Neurosurg. 2002;97:280–6.CrossRefPubMedGoogle Scholar
  43. 43.
    Rabinov JD, Yoo AJ, Ogilvy CS, et al. ONYX versus n-BCA for embolization of cranial dural arteriovenous fistulas. J Neurointerv Surg. 2013;5:306–10.CrossRefPubMedGoogle Scholar
  44. 44.
    Kim DJ, Willinsky RA, Krings T, et al. Intracranial dural arteriovenous shunts: transarterial glue embolization--experience in 115 consecutive patients. Radiology. 2011;258:554–61.CrossRefPubMedGoogle Scholar
  45. 45.
    Nelson PK, Russell SM, Woo HH, et al. Use of a wedged microcatheter for curative transarterial embolization of complex intracranial dural arteriovenous fistulas: indications, endovascular technique, and outcome in 21 patients. J Neurosurg. 2003;98:498–506.CrossRefPubMedGoogle Scholar
  46. 46.
    Maimon S, Nossek E, Strauss I, et al. Transarterial treatment with Onyx of intracranial dural arteriovenous fistula with cortical drainage in 17 patients. AJNR Am J Neuroradiol. 2011;32:2180–4.CrossRefPubMedGoogle Scholar
  47. 47.
    Cognard C, Januel AC, Silva NA Jr, et al. Endovascular treatment of intracranial dural arteriovenous fistulas with cortical venous drainage: new management using Onyx. AJNR Am J Neuroradiol. 2008;29:235–41.CrossRefPubMedGoogle Scholar
  48. 48.
    Lamin S, Chew HS, Chavda S, et al. Embolization of intracranial Dural arteriovenous fistulas using PHIL liquid embolic agent in 26 patients: a multicenter study. AJNR Am J Neuroradiol. 2017;38:127–31.CrossRefPubMedGoogle Scholar
  49. 49.
    Brown RD Jr, 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 country, Minnesota. J Neurosurg. 1996;85:29–32.CrossRefPubMedGoogle Scholar
  50. 50.
    Hofmeister C, Stapf C, Hartmann A, et al. Demographic, morphological, and clinical characteristics of 1289 patients with brain arteriovenous malformation. Stroke. 2000;31:1307–10.CrossRefPubMedGoogle Scholar
  51. 51.
    Ondra SL, Troupp H, George ED, et al. The natural history of symptomatic arteriovenous malformations of the brain: a 24-year follow-up assessment. J Neurosurg. 1990;73:387–91.CrossRefPubMedGoogle Scholar
  52. 52.
    Fleetwood IG, Steinberg GK. Arteriovenous malformations. Lancet. 2002;359:863–73.CrossRefPubMedGoogle Scholar
  53. 53.
    Kim EJ, Halim AX, Dowd CF, et al. The relationship of coexisting extranidal aneurysms to intracranial hemorrhage in patients harboring brain arteriovenous malformations. Neurosurgery. 2004;54:1349–57. discussion 1357-1348CrossRefPubMedGoogle Scholar
  54. 54.
    Redekop G, Terbrugge K, Montanera W, et al. Arterial aneurysms associated with cerebral arteriovenous malformations: classification, incidence, and risk of hemorrhage. J Neurosurg. 1998;89:539–46.CrossRefPubMedGoogle Scholar
  55. 55.
    Graf CJ, Perret GE, Torner JC. Bleeding from cerebral arteriovenous malformations as part of their natural history. J Neurosurg. 1983;58:331–7.CrossRefPubMedGoogle Scholar
  56. 56.
    Perret G NH. Arteriovenous malformations: an analysis of 545 cases of cranio-cerebral arteriovenous malformations and fistulae reported to the cooperative study. In: Sahs A, Perret G, Locksley H, Nishioka H, eds. Intracranial Aneurysms and Subarachnoid Hemorrhage: A Cooperative Study. JB Lippincott, Philadelphia; 1969.Google Scholar
  57. 57.
    Jafar JJ, Davis AJ, Berenstein A, et al. The effect of embolization with N-butyl cyanoacrylate prior to surgical resection of cerebral arteriovenous malformations. J Neurosurg. 1993;78:60–9.CrossRefPubMedGoogle Scholar
  58. 58.
    Strozyk D, Nogueira RG, Lavine SD. Endovascular treatment of intracranial arteriovenous malformation. Neurosurg Clin N Am. 2009;20:399–418.CrossRefPubMedGoogle Scholar
  59. 59.
    Izawa M, Chernov M, Hayashi M, et al. Combined management of intracranial arteriovenous malformations with embolization and gamma knife radiosurgery: comparative evaluation of the long-term results. Surg Neurol. 2009;71:43–52. discussion 52-43CrossRefPubMedGoogle Scholar
  60. 60.
    Yashar P, Amar AP, Giannotta SL, et al. Cerebral arteriovenous malformations: issues of the interplay between stereotactic radiosurgery and endovascular surgical therapy. World Neurosurg. 2011;75:638–47.CrossRefPubMedGoogle Scholar
  61. 61.
    Siddiqui AH, Chen PR, Rosenwasser RH. Endovascular therapy: indications, complications, and outcome. Informa Healthcare, New York; 2007.Google Scholar
  62. 62.
    Crowley RW, Ducruet AF, Mcdougall CG, et al. Endovascular advances for brain arteriovenous malformations. Neurosurgery. 2014;74(Suppl 1):S74–82.CrossRefPubMedGoogle Scholar
  63. 63.
    Heros RC. Embolization of arteriovenous malformations. J Neurosurg. 2004;100:807–9. discussion 809CrossRefPubMedGoogle Scholar
  64. 64.
    Han PP, Ponce FA, Spetzler RF. Intention-to-treat analysis of Spetzler-Martin grades IV and V arteriovenous malformations: natural history and treatment paradigm. J Neurosurg. 2003;98:3–7.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Singapore 2018

Authors and Affiliations

  • Chae Wook Huh
    • 1
  • Duk Ho Gho
    • 2
  • Sung-Chul Jin
    • 1
  1. 1.Department of NeurosurgeryInje University Haeundae Paik HospitalBusanSouth Korea
  2. 2.Department of NeurosurgerySeodaegu HospitalBusanSouth Korea

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