Skip to main content
SpringerLink
Log in

Use of Cerebral Revascularization Techniques in the Endovascular Era. Is it Still a Useful Technique?

  • Surgery
  • Published:
SN Comprehensive Clinical Medicine Aims and scope Submit manuscript

Abstract

Cerebral revascularization (CR) was a revolutionary surgical technique first introduced by Professor Yasargil in 1967 in the treatment of cerebral ischemia’s case. In the following decades, its use was subjected to several modifications and implementations, to the point that its purpose has been expanded to other several cerebrovascular diseases. In the more recent years, its use was strongly reduced because of the advancement of the endovascular techniques, which have been showed to bring a significant number of benefits and avoid the most common surgical complications; not last, these endovascular techniques reduces in a significant way the recovery length and gives an effective treatment for those patients who were not suitable for traditional surgery. In this review, the authors search the literature to analyze the cases in which such techniques is still of use for the treatment of neurovascular diseases. CR is still a useful technique in the treatment of several pathologies, among which are moyamoya disease, complex intracranial aneurysms, and skull base tumors. A good neurosurgeon should be able to master both surgical and neurovascular approach. The teaching of CR seem to be even harder since the few cases suitable to this approaches are sometimes not enough to allow a resident or a young neurosurgeon to gain experience. CR remains an important tool in neurosurgeons’ armamentarium. In this review, authors analyze the role of the cerebral revascularization techniques in the contemporary era and study the pathologies for which it can be used, in particular, moyamoya disease, complex intracranial aneurysms, and skull base tumors.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

STA:

Superficial temporal artery

EC:

Extracranial

IC:

Intracranial

CR:

Cerebral revascularization

ICA:

Internal carotid artery

MCA:

Middle cerebral artery

TIA:

Transient ischemic attack

EDAS:

Encephalo-duro-arterio-synangiosis

GTR:

Gross total resection

STR:

Subtotal resection

References

  1. Yasargil MG, Yonekawa Y. Results of microsurgical extraintracranial arterial bypass in the treatment of cerebral ischemia. Neurosurgery. 1977;1:22–4. https://doi.org/10.1227/00006123-197707000-00005.

    Article  CAS  PubMed  Google Scholar 

  2. Vajkoczy P. Revival of extra-intracranial bypass surgery. Curr Opin Neurol. 2009;22:90–5. https://doi.org/10.1097/WCO.0b013e32832187f1.

    Article  PubMed  Google Scholar 

  3. Straus DC, Brito da Silva H, McGrath L, Levitt MR, Kim LJ, Ghodke BV, et al. Cerebral revascularization for aneurysms in the flow-diverter era. Neurosurgery. 2017 May 1;80(5):759–68. https://doi.org/10.1093/neuros/nyx064.

    Article  PubMed  Google Scholar 

  4. Zaed I, Lanzino G. Reader response: swallowing-induced displacement of the carotid artery as a risk of stroke: flip-flop phenomenon. Neurology. 2018 Mar 20;90(12):576. https://doi.org/10.1212/WNL.0000000000005156.

    Article  PubMed  Google Scholar 

  5. Failure of extracranial-intracranial arterial bypass to reduce the risk of ischemic stroke. Results of an international randomized trial. The EC/IC Bypass Study Group. N Engl J Med 313:1191–1200, 1985. https://doi.org/10.1056/NEJM198511073131904

  6. Powers WJ, Clarke WR, Grubb RL Jr, Videen TO, Adams HP Jr, Derdeyn CP. COSS investigators: extracranial-intracranial bypass surgery for stroke prevention in hemodynamic cerebral ischemia: the carotid occlusion surgery study randomized trial. JAMA. 2011;306:1983–92. https://doi.org/10.1001/jama.2011.1610.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Fluri F, Engelter S, Lyrer P. Extracranial-intracranial arterial bypass surgery for occlusive carotid artery disease. Cochrane Database Syst Rev. 2010 Feb 17;2:CD005953. https://doi.org/10.1002/14651858.CD005953.pub2.

    Article  Google Scholar 

  8. Extracranial to intracranial bypass and the prevention of stroke. Lancet 2:1401–1402, 1985. https://www.ncbi.nlm.nih.gov/pubmed/?term=Extracranial+to+intracranial+bypass+and+the+prevention+of+stroke+and+lancet

  9. The EC/IC Bypass Study group. The International Cooperative Study of Extracranial/Intracranial Arterial Anastomosis (EC/IC Bypass Study): methodology and entry characteristics. Stroke 16: 397–406, 1985. https://www.ncbi.nlm.nih.gov/pubmed/?term=The+EC%2FIC+Bypass+Study+group.+The+International+Cooperative+Study+of+Extracranial%2FIntracranial+Arterial+Anastomosis+(EC%2FIC+Bypass+Study)%3A+methodology+and+entry+characteristics.

  10. Awad IA, Spetzler RF. Extracranial-intracranial bypass surgery: a critical analysis in light of the international cooperative study. Neurosurgery. 1986;19:655–64. https://doi.org/10.1227/00006123-198610000-00028.

    Article  CAS  PubMed  Google Scholar 

  11. Lawton MT, Spetzler RF. Internal carotid artery sacrifice for radical resection of skull base tumors. Skull Base Surg. 1996;6:119–23 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1656574/.

    Article  CAS  Google Scholar 

  12. Ramanathan D, Temkin N, Kim LJ, Ghodke B, Sekhar LN. Cerebral bypasses for complex aneurysms and tumors: long-term results and graft management strategies. Neurosurgery. 2012;70:1442–57. https://doi.org/10.1227/NEU.0b013e31824c046f.

    Article  PubMed  Google Scholar 

  13. Sekhar LN, Natarajan SK, Ellenbogen RG, Ghodke B. Cerebral revascularization for ischemia, aneurysms, and cranial base tumors. Neurosurgery. 2008;62(Suppl 3):1373–410. https://doi.org/10.1227/01.neu.0000333803.97703.c6.

    Article  PubMed  Google Scholar 

  14. Abla AA, Gandhoke G, Clark JC, Oppenlander ME, Velat GJ, Zabramski JM, et al. Surgical outcomes for moyamoya angiopathy at barrow neurological institute with comparison of adult indirect encephaloduroarteriosynangiosis bypass, adult direct superficial temporal artery-to-middle cerebral artery bypass, and pediatric bypass: 154 revascularization surgeries in 140 affected hemispheres. Neurosurgery. 2013;73:430–9. https://doi.org/10.1227/NEU.0000000000000017.

    Article  PubMed  Google Scholar 

  15. Starke RM, Komotar RJ, Connolly ES. Optimal surgical treatment for moyamoya disease in adults: direct versus indirect bypass. Neurosurg Focus. 2009;26:E8. https://doi.org/10.3171/2009.01.FOCUS08309.

    Article  PubMed  Google Scholar 

  16. Hallemeier CL, Rich KM, Grubb RL Jr, et al. Clinical features and outcome in North American adults with moyamoya phenomenon. Stroke. 2006;37(6):1490–6. https://doi.org/10.1161/01.STR.0000221787.70503.ca.

    Article  PubMed  Google Scholar 

  17. Shirane R, Yoshida Y, Takahashi T, Yoshimoto T. Assessment of encephalo-galeomyo- synangiosis with dural pedicle insertion in childhood moyamoya disease: characteristics of cerebral blood flow and oxygen metabolism. Clin Neurol Neurosurg. 1997;99(suppl 2):S79–85 https://www.ncbi.nlm.nih.gov/pubmed/?term=Assessment+of+encephalo-galeomyo-+synangiosis+with+dural+pedicle+insertion+in+childhood+moyamoya+disease%3A+characteristics+of+cerebral+blood+flow+and+oxygen+metabolism.

    Article  Google Scholar 

  18. Drazin D, Calayag M, Gifford E, Dalfino J, Yamamoto J, Boulos AS. Endovascular treatment for moyamoya disease in a Caucasian twin with angioplasty and wingspan stent. Clin Neurol Neurosurg. 2009;111(10):913–7. https://doi.org/10.1016/j.clineuro.2009.08.012.

    Article  PubMed  Google Scholar 

  19. Santirso D, Oliva P, González M, Murias E, Vega P, Gil A, et al. Intracranial stent placement in a patient with moyamoya disease. J Neurol. 2012;259(1):170–1. https://doi.org/10.1007/s00415-011-6105-y.

    Article  PubMed  Google Scholar 

  20. Rodriguez GJ, Kirmani JF, Ezzeddine MA, Qureshi AI. Primary percutaneous transluminal angioplasty for early moyamoya disease. J Neuroimaging. 2007;17(1):48–53. https://doi.org/10.1111/j.1552-6569.2006.00075.x.

    Article  PubMed  Google Scholar 

  21. Khan N, Dodd R, Marks MP, Bell-Stephens T, Vavao J, Steinberg GK. Failure of primary percutaneous angioplasty and stenting in the prevention of ischemia in moyamoya angiopathy. Cerebrovasc Dis. 2011;31(2):147–53. https://doi.org/10.1159/000320253.

    Article  PubMed  Google Scholar 

  22. Spetzler RF, Roski RA, Kopaniky DR. Alternative superficial temporal artery to middle cerebral artery revascularization procedure. Neurosurgery. 1980;7(5):484–7. https://doi.org/10.1227/00006123-198011000-00012.

    Article  CAS  PubMed  Google Scholar 

  23. 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(9342):1267–74 https://www.ncbi.nlm.nih.gov/pubmed/12414200.

    Article  Google Scholar 

  24. Veeravagu A, Guzman R, Patil CG, Hou LC, Lee M, Steinberg GK. Moyamoya disease in pediatric patients: outcomes of neurosurgical interventions. Neurosurg Focus. 2008;24(2):E16. https://doi.org/10.3171/FOC/2008/24/2/E16.

    Article  PubMed  Google Scholar 

  25. Guzman R, Lee M, Achrol A, et al. Clinical outcome after 450 revascularization procedures for moyamoya disease: clinical article. J Neurosurg. 2009;111(5):927–35. https://doi.org/10.3171/2009.4.JNS081649.

    Article  PubMed  Google Scholar 

  26. Sakamoto T, Kawaguchi M, Kurehara K, Kitaguchi K, Furuya H, Karasawa J. Risk factors for neurologic deterioration after revascularization surgery in patients with moyamoya disease. Anesth Analg. 1997;85(5):1060–5 https://www.ncbi.nlm.nih.gov/pubmed/9356100.

    Article  CAS  Google Scholar 

  27. Ishikawa T, Houkin K, Kamiyama H, Abe H. Effects of surgical revascularization on outcome of patients with pediatric moyamoya disease. Stroke. 1997;28(6):1170–3 https://www.ncbi.nlm.nih.gov/pubmed/9183345.

    Article  CAS  Google Scholar 

  28. Narata AP, Yilmaz H, Schaller K, Lovblad KO, Pereira VM. Flow-diverting stent for ruptured intracranial dissecting aneurysm of vertebral artery. Neurosurgery. 2012;70(4):982–8. https://doi.org/10.1227/NEU.0b013e318236715e.

    Article  PubMed  Google Scholar 

  29. Kallmes DF, Ding YH, Dai D, Kadirvel R, Lewis DA, Cloft HJ. A new endoluminal, flow-disrupting device for treatment of saccular aneurysms. Stroke. 2007;38(8):2346–52. https://doi.org/10.1161/STROKEAHA.106.479576.

    Article  PubMed  Google Scholar 

  30. Becske T, Kallmes DF, Saatci I, et al. Pipeline for Uncoilable or failed aneurysms: results from a multicenter clinical trial. Radiology. 2013;267(3):858–68. https://doi.org/10.1148/radiol.13120099.

    Article  PubMed  Google Scholar 

  31. Parkinson RJ, Eddleman CS, Batjer HH, Bendok BR. Giant intracranial aneurysms: endovascular challenges. Neurosurgery. 2008;62(6 suppl 3):1336–45. https://doi.org/10.1227/01.neu.0000333798.67209.1f.

    Article  PubMed  Google Scholar 

  32. Peluso JP, van Rooij WJ, Sluzewski M, Beute GN. Coiling of basilar tip aneurysms: results in 154 consecutive patients with emphasis on recurrent haemorrhage and re-treatment during mid- and long-term follow-up. J Neurol Neurosurg Psychiatry. 2008;79(6):706–11. https://doi.org/10.1136/jnnp.2007.127480.

    Article  CAS  PubMed  Google Scholar 

  33. Jahromi BS, Mocco J, Bang JA, et al. Clinical and angiographic outcome after endovascular management of giant intracranial aneurysms. Neurosurgery. 2008;63(4):662–74. https://doi.org/10.1227/01.NEU.0000325497.79690.4C.

    Article  PubMed  Google Scholar 

  34. Fiorella D, Thiabolt L, Albuquerque FC, Deshmukh VR, McDougall CG, Rasmussen PA. Antiplatelet therapy in neuroendovascular therapeutics. Neurosurg Clin N Am. 2005;16(3):517–40, vi. https://doi.org/10.1016/j.nec.2005.03.003.

    Article  PubMed  Google Scholar 

  35. Polevaya NV, Kalani MY, Steinberg GK, Tse VC. The transition from Hunterian ligation to intracranial aneurysm clips: a historical perspective. Neurosurg Focus. 2006;20(6):E3 https://www.ncbi.nlm.nih.gov/pubmed/?term=The+transition+from+Hunterian+ligation+to+intracranial+aneurysm+clips%3A+a+historical+perspective.

    Article  Google Scholar 

  36. Torigai T, Mase M, Ohno T, et al. Usefulness of dual and fully automated measurements of cerebral blood flow during balloon occlusion test of the internal carotid artery. J Stroke Cerebrovasc Dis. 2013;22(3):197–204. https://doi.org/10.1016/j.jstrokecerebrovasdis.2011.07.015.

    Article  PubMed  Google Scholar 

  37. Jabbour P, Chalouhi N, Tjoumakaris S, et al. The pipeline embolization device: learning curve and predictors of complications and aneurysm obliteration. Neurosurgery. 2013;73(1):113–20. https://doi.org/10.1227/01.neu.0000429844.06955.39.

    Article  PubMed  Google Scholar 

  38. Kalani MY, Zabramski JM, Hu YC, Spetzler RF. Extracranial-intracranial bypass and vessel occlusion for the treatment of unclippable giant middle cerebral artery aneurysms. Neurosurgery. 2013;72(3):428–35. https://doi.org/10.1227/NEU.0b013e3182804381.

    Article  PubMed  Google Scholar 

  39. Kalani MYS, Rangel-Castilla L, Ramey W, Nakaji P, Albuquerque FC, McDougall CG, et al. Indications and results of direct cerebral revascularization in the modern era. World Neurosurg. 2015;83(3):345–50. https://doi.org/10.1016/j.wneu.2014.10.013.

    Article  PubMed  Google Scholar 

  40. Amin-Hanjani S, Alaraj A, Charbel FT. Flow replacement bypass for aneurysms: decision-making using intraoperative blood flow measurements. Acta Neurochir. 2010;152(6):1021–32. https://doi.org/10.1007/s00701-010-0635-4.

    Article  PubMed  Google Scholar 

  41. Kalani MY, Zabramski JM, Nakaji P, Spetzler RF. Bypass and flow reduction for complex basilar and vertebrobasilar junction aneurysms. Neurosurgery. 2013;72(5):763–75. https://doi.org/10.1227/NEU.0b013e3182870703.

    Article  PubMed  Google Scholar 

  42. Drake CG, Peerless SJ, Ferguson GG. Hunterian proximal arterial occlusion for giant aneurysms of the carotid circulation. J Neurosurg. 1994;81(5):656–65. https://doi.org/10.3171/jns.1994.81.5.0656.

    Article  CAS  PubMed  Google Scholar 

  43. Pfitzner J. Poiseuille and his law. Anaesthesia. 1976;31(2):273–5 https://www.ncbi.nlm.nih.gov/pubmed/779509.

    Article  CAS  Google Scholar 

  44. Kalani MY, Kalb S, Martirosyan NL, Lettieri SC, Spetzler RF, Porter RW, et al. Cerebral revascularization and carotid artery resection at the skull base for treatment of advanced head and neck malignancies. J Neurosurg. 2013;118:637–42. https://doi.org/10.3171/2012.9.JNS12332.

    Article  PubMed  Google Scholar 

  45. Sorenson TJ, Zaed I, Rangel-Castilla L, Lanzino G. Endovascular occlusion of epidural spinal dural arteriovenous fistula: 2-dimensional operative video. Oper Neurosurg (Hagerstown). 2018 Dec 1;15(6):726. https://doi.org/10.1093/ons/opy031.Noabstractavailable.

    Article  Google Scholar 

  46. Zaed I, Pinto MV, Mauermann ML, Lanzino G. Teaching NeuroImages: spinal cord syrinx secondary to a spinal dural arteriovenous fistula. Neurology. 2018;91(3):e295–6. https://doi.org/10.1212/WNL.0000000000005830 No abstract available.

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Humanitas University, Via Rita Levi Montalcini, Pieve Emanuele, Milan, Italy

    Ismail Zaed & Benedetta Tinterri

  2. Department of Neurosurgery, Humanitas University, Via Alessandro Manzoni, 56, 22089, Rozzano, Italy

    Ismail Zaed

  3. Department of Neurosurgery, International Neuroscience Institute, Hannover, Germany

    Mario Giordano

Authors
  1. Ismail Zaed
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Benedetta Tinterri
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mario Giordano
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ismail Zaed.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Ethical Approval and Informed Consent

The present study does not need any approval for the ethical committee, nor a signed Informed consent from patients.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

This article is part of the Topical Collection on Surgery

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zaed, I., Tinterri, B. & Giordano, M. Use of Cerebral Revascularization Techniques in the Endovascular Era. Is it Still a Useful Technique?. SN Compr. Clin. Med. 1, 952–957 (2019). https://doi.org/10.1007/s42399-019-00158-2

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s42399-019-00158-2

Keywords

Search

Navigation