Skip to main content


Log in

Vascular responses to abrupt blood flow change after bypass surgery for complex intracranial aneurysms

  • Original Article - Vascular Neurosurgery - Aneurysm
  • Published:
Acta Neurochirurgica Aims and scope Submit manuscript



Bypass surgery for complex intracranial aneurysms (IAs) results in drastic blood flow changes in intracranial arteries. The aim of the study was to elucidate how vessels adapt to blood flow changes after bypass surgery with phase-contrast magnetic resonance imaging (PC-MRI).


This is a prospective observational study to assess changes of the blood flow in intracranial arteries after bypass surgery for IAs. Flow rates and vessel diameters were measured with PC-MRI in 52 intracranial arteries of 7 healthy volunteers and 31 arteries of 8 IA patients who underwent bypass surgery. Wall shear stress (WSS) was calculated with the Hagen-Poiseuille formula. In 18 arteries of 5 patients, the same measurement was performed 1, 3, and 12 months after surgery.


PC-MRI showed a strong positive correlation between the flow rate and the third power of vessel diameter in both healthy volunteers (r = 0.82, P < 0.0001) and IA patients (r = 0.90, P < 0.0001), indicating the constant WSS. Of the 18 arteries in 5 patients, WSS increased in 7 arteries and decreased in 11 arteries immediately after surgery. In the WSS-increased group, WSS returned to the preoperative value in the third postoperative month. In the WSS-decreased group, WSS increased in the 12th month, but did not return to the preoperative level.


In a physiological state, WSS was constant in intracranial arteries. Changed WSS after bypass surgery tended to return to the preoperative value, suggesting that vessel diameter and flow rate might be controlled so that WSS remains constant.

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

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others



Intracranial aneurysm


Phase-contrast magnetic resonance imaging


Wall shear stress

EC-IC bypass:

Extracranial-intracranial bypass


Radial artery


Saphenous vein


Internal carotid artery


Middle cerebral artery


Superficial temporal artery


Superior cerebellar artery


Number of excitations


Velocity encoding


Field of view


Analysis of variance


Endothelial cell


Smooth muscle cell


  1. Baaj AA, Agazzi S, van Loveren H (2009) Graft selection in cerebral revascularization. Neurosurg Focus 26:E18

    Article  PubMed  Google Scholar 

  2. Bakker CJ, Hoogeveen RM, Viergever MA (1999) Construction of a protocol for measuring blood flow by two-dimensional phase-contrast MRA. J Magn Reson Imaging 9:119–127

    Article  PubMed  CAS  Google Scholar 

  3. Briganti F, Leone G, Marseglia M, Mariniello G, Caranci F, Brunetti A, Maiuri F (2015) Endovascular treatment of cerebral aneurysms using flow-diverter devices: a systematic review. Neuroradiol J 28:365–375

    Article  PubMed  PubMed Central  Google Scholar 

  4. Brockmann C, Gerigk L, Vajkoczy P, Groden C, Neumaier-Probst E (2012) Magnetic resonance imaging flow quantification of non-occlusive excimer laser-assisted EC-IC high-flow bypass in the treatment of complex intracranial aneurysms. Clin Neuroradiol 22:39–45

    Article  PubMed  CAS  Google Scholar 

  5. Cenzato M, Bortolotti C (2016) The role of extra and intracranial bypass in the treatment of complex aneurysms. J Neurosurg Sci

  6. Corson MA, James NL, Latta SE, Nerem RM, Berk BC, Harrison DG (1996) Phosphorylation of endothelial nitric oxide synthase in response to fluid shear stress. Circ Res 79:984–991

    Article  PubMed  CAS  Google Scholar 

  7. Davies PF (1995) Flow-mediated endothelial mechanotransduction. Physiol Rev 75:519–560

    Article  PubMed  CAS  Google Scholar 

  8. Enzmann DR, Ross MR, Marks MP, Pelc NJ (1994) Blood flow in major cerebral arteries measured by phase-contrast cine MR. AJNR Am J Neuroradiol 15:123–129

    PubMed  CAS  PubMed Central  Google Scholar 

  9. Evans AJ, Iwai F, Grist TA, Sostman HD, Hedlund LW, Spritzer CE, Negro-Vilar R, Beam CA, Pelc NJ (1993) Magnetic resonance imaging of blood flow with a phase subtraction technique. In vitro and in vivo validation. Investig Radiol 28:109–115

    Article  CAS  Google Scholar 

  10. Hendrikse J, van der Zwan A, Ramos LM, Tulleken CA, van der Grond J (2003) Hemodynamic compensation via an excimer laser-assisted, high-flow bypass before and after therapeutic occlusion of the internal carotid artery. Neurosurgery 53:858–863 discussion 863-855

    Article  PubMed  Google Scholar 

  11. Hoh BL, Putman CM, Budzik RF, Carter BS, Ogilvy CS (2001) Combined surgical and endovascular techniques of flow alteration to treat fusiform and complex wide-necked intracranial aneurysms that are unsuitable for clipping or coil embolization. J Neurosurg 95:24–35

    Article  PubMed  CAS  Google Scholar 

  12. Ishikawa T, Kamiyama H, Houkin K, Takahashi A, Iwasaki Y, Abe H (1995) Postsurgical observations of mean hemispheric cerebral blood flow with patients receiving high-flow EC-IC bypass using a radial artery graft (preliminary report, one-year observation of 10 hemispheres). Surg Neurol 43:500–506 discussion 506-509

    Article  PubMed  CAS  Google Scholar 

  13. Jafar JJ, Russell SM, Woo HH (2002) Treatment of giant intracranial aneurysms with saphenous vein extracranial-to-intracranial bypass grafting: indications, operative technique, and results in 29 patients. Neurosurgery 51:138–144 discussion 144-136

    Article  PubMed  Google Scholar 

  14. Kalani MY, Zabramski JM, Nakaji P, Spetzler RF (2013) Bypass and flow reduction for complex basilar and vertebrobasilar junction aneurysms. Neurosurgery 72:763–775 discussion 775-766

    Article  PubMed  Google Scholar 

  15. Kallmes DF, Hanel R, Lopes D, Boccardi E, Bonafe A, Cekirge S, Fiorella D, Jabbour P, Levy E, McDougall C, Siddiqui A, Szikora I, Woo H, Albuquerque F, Bozorgchami H, Dashti SR, Delgado Almandoz JE, Kelly ME, Turner R, Woodward BK, Brinjikji W, Lanzino G, Lylyk P (2015) International retrospective study of the pipeline embolization device: a multicenter aneurysm treatment study. AJNR Am J Neuroradiol 36:108–115

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  16. Kazumata K, Kamiyama H, Ishikawa T, Nakamura T, Terasaka S, Houkin K (2014) Impact of cervical internal carotid clamping and radial artery graft bypass on cortical arterial perfusion pressure during craniotomy. Neurosurg Rev 37:493–499 discussion 499-500

    Article  PubMed  Google Scholar 

  17. Lawton MT, Abla AA, Rutledge WC, Benet A, Zador Z, Rayz VL, Saloner D, Halbach VV (2016) Bypass surgery for the treatment of dolichoectatic basilar trunk aneurysms: a work in progress. Neurosurgery 79:83–99

    Article  PubMed  Google Scholar 

  18. Miyamoto S, Funaki T, Iihara K, Takahashi JC (2011) Successful obliteration and shrinkage of giant partially thrombosed basilar artery aneurysms through a tailored flow reduction strategy with bypass surgery. J Neurosurg 114:1028–1036

    Article  PubMed  Google Scholar 

  19. Morton RP, Moore AE, Barber J, Tariq F, Hare K, Ghodke B, Kim LJ, Sekhar LN (2014) Monitoring flow in extracranial-intracranial bypass grafts using duplex ultrasonography: a single-center experience in 80 grafts over 8 years. Neurosurgery 74:62–70

    Article  PubMed  Google Scholar 

  20. Murakami K, Shimizu H, Matsumoto Y, Tominaga T (2009) Acute ischemic complications after therapeutic parent artery occlusion with revascularization for complex internal carotid artery aneurysms. Surg Neurol 71:434–441 discussion 441

    Article  PubMed  Google Scholar 

  21. Peng SL, Su P, Wang FN, Cao Y, Zhang R, Lu H, Liu P (2015) Optimization of phase-contrast MRI for the quantification of whole-brain cerebral blood flow. J Magn Reson Imaging 42:1126–1133

    Article  PubMed  PubMed Central  Google Scholar 

  22. Pyke KE, Tschakovsky ME (2005) The relationship between shear stress and flow-mediated dilatation: implications for the assessment of endothelial function. J Physiol 568:357–369

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  23. Shav D, Gotlieb R, Zaretsky U, Elad D, Einav S (2014) Wall shear stress effects on endothelial-endothelial and endothelial-smooth muscle cell interactions in tissue engineered models of the vascular wall. PLoS One 9:e88304

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  24. Shimizu H, Matsumoto Y, Tominaga T (2010) Parent artery occlusion with bypass surgery for the treatment of internal carotid artery aneurysms: clinical and hemodynamic results. Clin Neurol Neurosurg 112:32–39

    Article  PubMed  Google Scholar 

  25. Sia SF, Davidson AS, Assaad NN, Stoodley M, Morgan MK (2011) Comparative patency between intracranial arterial pedicle and vein bypass surgery. Neurosurgery 69:308–314

    Article  PubMed  Google Scholar 

  26. Srichai MB, Lim RP, Wong S, Lee VS (2009) Cardiovascular applications of phase-contrast MRI. AJR Am J Roentgenol 192:662–675

    Article  PubMed  Google Scholar 

  27. Sughrue ME, Saloner D, Rayz VL, Lawton MT (2011) Giant intracranial aneurysms: evolution of management in a contemporary surgical series. Neurosurgery 69:1261–1270 discussion 1270-1261

    Article  PubMed  Google Scholar 

  28. Zarrinkoob L, Ambarki K, Wahlin A, Birgander R, Eklund A, Malm J (2015) Blood flow distribution in cerebral arteries. J Cereb Blood Flow Metab 35:648–654

    Article  PubMed  PubMed Central  Google Scholar 

Download references


The authors would like to thank Yoshifumi Hayashi M.D. and Hirotaka Yoshida M.D. at Kitahara International Hospital, Tokyo, Japan, for PC-MRI measurements of healthy volunteers.


This work was supported in part by Grants-in-aid for Scientific Research (grant numbers: 24592150 and 15H04952) from the Japan Society for the Promotion of Science and The Ministry of Education, Culture, Sports, Science, and Technology of Japan.

Author information

Authors and Affiliations


Corresponding author

Correspondence to Hiroharu Kataoka.

Ethics declarations

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. This study was approved by the Institutional Review Board at our institutes.

Informed consent

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

Additional information

This article is part of the Topical Collection on Vascular Neurosurgery – Aneurysm

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kataoka, H., Makino, Y., Takanishi, K. et al. Vascular responses to abrupt blood flow change after bypass surgery for complex intracranial aneurysms. Acta Neurochir 160, 1945–1953 (2018).

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: