Intraoperative Measurement of Arterial Blood Flow in Aneurysm Surgery

  • Alberto Pasqualin
  • Pietro Meneghelli
  • Angelo Musumeci
  • Alessandro Della Puppa
  • Giacomo Pavesi
  • Giampietro Pinna
  • Renato Scienza
Conference paper
Part of the Acta Neurochirurgica Supplement book series (NEUROCHIRURGICA, volume 129)


Intraoperative flowmetry (IF) has been recently introduced during cerebral aneurysm surgery in order to obtain a safer surgical exclusion of the aneurysm. This study evaluates the usefulness of IF during surgery for cerebral aneurysms and compares the results obtained in the joined surgical series of Verona and Padua to the more recent results obtained at the neurosurgical department of Verona.

In the first surgical series, between 2001 and 2010, a total of 312 patients were submitted to IF during surgery for cerebral aneurysm at the neurosurgical departments of Verona and Padua: 162 patients presented with subarachnoid hemorrhage (SAH) whereas 150 patients harbored unruptured aneurysms. In the second series, between 2011 and 2016, 112 patients were submitted to IF during surgery for cerebral aneurysm at the neurosurgical department of Verona; 24 patients were admitted for SAH, whereas 88 patients were operated on for unruptured aneurysms.

Comparison of the baseline values in the two surgical series and the baseline values between unruptured and ruptured aneurysms showed no statistical differences between the two clinical series. Analysis of flowmetry measurements showed three types of loco-regional flow derangements: hyperemia after temporary arterial occlusion, redistribution of flow in efferent vessels after clipping, and low flow in patients with SAH-related vasospasm.

IF provides real-time data about flow derangements caused by surgical clipping of cerebral aneurysm, thus enabling the surgeon to obtain a safer exclusion; furthermore, it permits the evaluation of other effects of clipping on the loco-regional blood flow. It is suggested that—in contribution with intraoperative neurophysiological monitoring—IF may now constitute the most reliable tool for increasing safety in aneurysm surgery.


Intraoperative flowmetry Cerebral aneurysm Clipping Surgery Temporary arterial occlusion (TAO) 


  1. 1.
    Origitano TC, Schwartz K, Anderson D, Azar-Kia B, Reichman OH. Optimal clip application and intraoperative angiography for intracranial aneurysms. Surg Neurol. 1999;51:117–24.CrossRefGoogle Scholar
  2. 2.
    Popadic A, Witzmann A, Amann T, Doringer W, Fleisch M, Hafel C, Hergan K, Langle M. The value of intraoperative angiography in surgery of intracranial aneurysms: a prospective study in 126 patients. Neuroradiology. 2001;43:466–71.CrossRefGoogle Scholar
  3. 3.
    Tang G, Cawley CM, Dion JE, Barrow DL. Intraoperative angiography during aneurysm surgery: a prospective evaluation of efficacy. J Neurosurg. 2002;96:993–9.CrossRefGoogle Scholar
  4. 4.
    Raabe A, Beck J, Gerlach R, Zimmermann M, Seifert V. Near-infrared indocyanine green video angiography: a new method for intraoperative assessment of vascular flow. Neurosurgery. 2003;52:132–9.PubMedGoogle Scholar
  5. 5.
    Raabe A, Nakaji P, Beck J, Kim LJ, Hsu FP, Kamerman JD, Seifert V, Spetzler RF. Prospective evaluation of surgical microscope-integrated intraoperative near-infrared indocyanine green videoangiography during aneurysm surgery. J Neurosurg. 2005;103:982–9.CrossRefGoogle Scholar
  6. 6.
    Marchese E, Albanese A, Denaro L, Vignati A, Fernandez E, Maira G. Intraoperative microvascular Doppler in intracranial aneurysm surgery. Surg Neurol. 2005;63:336–42.CrossRefGoogle Scholar
  7. 7.
    Stendel R, Pietila T, Al Hassan AA, Schilling A, Brock M. Intraoperative microvascular Doppler ultrasonography in cerebral aneurysm surgery. J Neurol Neurosurg Psychiatry. 2000;68:29–35.CrossRefGoogle Scholar
  8. 8.
    Charbel FT, Hoffman WE, Misra M, Ostergren L. Ultrasonic perivascular flow probe: technique and application in neurosurgery. Neurol Res. 1998;20:439–42.CrossRefGoogle Scholar
  9. 9.
    Hartman JC, Olszanski DA, Hullinger TG, Brunden MN. In vivo validation of a transit-time ultrasonic volume flow meter. J Pharmacol Toxicol Methods. 1994;31:153–60.CrossRefGoogle Scholar
  10. 10.
    Lundell A, Bergqvist D, Mattsson E, Nilsson B. Volume blood flow measurements with a transit time flowmeter: an in vivo and in vitro variability and validation study. Clin Physiol. 1993;13:547–57.CrossRefGoogle Scholar
  11. 11.
    Amin-Hanjani S, Meglio G, Gatto R, Bauer A, Charbel FT. The utility of intraoperative blood flow measurement during aneurysm surgery using an ultrasonic perivascular flow probe. Neurosurgery. 2006;58:ONS-305–12.CrossRefGoogle Scholar
  12. 12.
    Della Puppa A, Volpin F, Gioffre G, Rustemi O, Troncon I, Scienza R. Microsurgical clipping of intracranial aneurysms assisted by green indocyanine videoangiography (ICGV) and ultrasonic perivascular microflow probe measurement. Clin Neurol Neurosurg. 2014;116:35–40.CrossRefGoogle Scholar
  13. 13.
    Kirk HJ, Rao PJ, Seow K, Fuller J, Chandran N, Khurana VG. Intra-operative transit time flowmetry reduces the risk of ischemic neurological deficits in neurosurgery. Br J Neurosurg. 2009;23:40–7.CrossRefGoogle Scholar
  14. 14.
    Nakayama N, Kuroda S, Houkin K, Takikawa S, Abe H. Intraoperative measurement of arterial blood flow using a transit time flowmeter: monitoring of hemodynamic changes during cerebrovascular surgery. Acta Neurochir. 2001;143:17–24.CrossRefGoogle Scholar
  15. 15.
    Bailes JE, Tantuwaya LS, Fukushima T, Schurman GW, Davis D. Intraoperative microvascular Doppler sonography in aneurysm surgery. Neurosurgery. 1997;40:965–70.CrossRefGoogle Scholar
  16. 16.
    Fischer G, Stadie A, Oertel JM. Near-infrared indocyanine green videoangiography versus microvascular Doppler sonography in aneurysm surgery. Acta Neurochir. 2010;152:1519–25.CrossRefGoogle Scholar
  17. 17.
    Laborde G, Gilsbach J, Harders A. The microvascular Doppler—an intraoperative tool for the treatment of large and giant aneurysms. Acta Neurochir Suppl. 1988;42:75–80.PubMedGoogle Scholar
  18. 18.
    Siasios I, Kapsalaki EZ, Fountas KN. The role of intraoperative micro-Doppler ultrasound in verifying proper clip placement in intracranial aneurysm surgery. Neuroradiology. 2012;54:1109–18.CrossRefGoogle Scholar
  19. 19.
    Abla AA, Lawton MT. Indocyanine green angiography for cerebral aneurysm surgery: advantages, limitations, and neurosurgeon intuition. World Neurosurg. 2014;82:e585–6.CrossRefGoogle Scholar
  20. 20.
    Dashti R, Hernesniemi J. Intraoperative assessment of a quality of microneurosurgical clipping: role of indocyanine green videoangiography. World Neurosurg. 2014;82:e589–90.CrossRefGoogle Scholar
  21. 21.
    Della Puppa A, Rustemi O, Rossetto M, Gioffre G, Munari M, Charbel FT, Scienza R. The “squeezing maneuver” in microsurgical clipping of intracranial aneurysms assisted by indocyanine green videoangiography. Neurosurgery. 2014;10(Suppl 2):208–12.CrossRefGoogle Scholar
  22. 22.
    Lai LT, Morgan MK. Use of indocyanine green videoangiography during intracranial aneurysm surgery reduces the incidence of postoperative ischaemic complications. J Clin Neurosci. 2014;21:67–72.CrossRefGoogle Scholar
  23. 23.
    Lane B, Bohnstedt BN, Cohen-Gadol AA. A prospective comparative study of microscope-integrated intraoperative fluorescein and indocyanine videoangiography for clip ligation of complex cerebral aneurysms. J Neurosurg. 2015;122:618–26.CrossRefGoogle Scholar
  24. 24.
    Snyder LA, Spetzler RF. Current indications for indocyanine green angiography. World Neurosurg. 2011;76:405–6.CrossRefGoogle Scholar
  25. 25.
    de Oliveira JG, Beck J, Seifert V, Teixeira MJ, Raabe A. Assessment of flow in perforating arteries during intracranial aneurysm surgery using intraoperative near-infrared indocyanine green videoangiography. Neurosurgery. 2007;61:63–72.CrossRefGoogle Scholar
  26. 26.
    de Oliveira JG, Beck J, Seifert V, Teixeira MJ, Raabe A. Assessment of flow in perforating arteries during intracranial aneurysm surgery using intraoperative near-infrared indocyanine green videoangiography. Neurosurgery. 2008;62:1300–10.CrossRefGoogle Scholar
  27. 27.
    Irie T, Yoshitani K, Ohnishi Y, Shinzawa M, Miura N, Kusaka Y, Miyazaki S, Miyamoto S. The efficacy of motor-evoked potentials on cerebral aneurysm surgery and new-onset postoperative motor deficits. J Neurosurg Anesthesiol. 2010;22:247–51.CrossRefGoogle Scholar
  28. 28.
    Neuloh G, Pechstein U, Cedzich C, Schramm J. Motor evoked potential monitoring with supratentorial surgery. Neurosurgery. 2004;54:1061–70.CrossRefGoogle Scholar
  29. 29.
    Quinones-Hinojosa A, Alam M, Lyon R, Yingling CD, Lawton MT. Transcranial motor evoked potentials during basilar artery aneurysm surgery: technique application for 30 consecutive patients. Neurosurgery. 2004;54:916–24.CrossRefGoogle Scholar
  30. 30.
    Suzuki K, Kodama N, Sasaki T, Matsumoto M, Konno Y, Sakuma J, Oinuma M, Murakawa M. Intraoperative monitoring of blood flow insufficiency in the anterior choroidal artery during aneurysm surgery. J Neurosurg. 2003;98:507–14.CrossRefGoogle Scholar
  31. 31.
    Szelenyi A, Langer D, Kothbauer K, De Camargo AB, Flamm ES, Deletis V. Monitoring of muscle motor evoked potentials during cerebral aneurysm surgery: intraoperative changes and postoperative outcome. J Neurosurg. 2006;105:675–81.CrossRefGoogle Scholar
  32. 32.
    Yeon JY, Seo DW, Hong SC, Kim JS. Transcranial motor evoked potential monitoring during the surgical clipping of unruptured intracranial aneurysms. J Neurol Sci. 2010;293:29–34.CrossRefGoogle Scholar
  33. 33.
    Alexander TD, Macdonald RL, Weir B, Kowalczuk A. Intraoperative angiography in cerebral aneurysm surgery: a prospective study of 100 craniotomies. Neurosurgery. 1996;39:10–7.CrossRefGoogle Scholar
  34. 34.
    Chiang VL, Gailloud P, Murphy KJ, Rigamonti D, Tamargo RJ. Routine intraoperative angiography during aneurysm surgery. J Neurosurg. 2002;96:988–92.CrossRefGoogle Scholar
  35. 35.
    Klopfenstein JD, Spetzler RF, Kim LJ, Feiz-Erfan I, Han PP, Zabramski JM, Porter RW, Albuquerque FC, McDougall CG, Fiorella DJ. Comparison of routine and selective use of intraoperative angiography during aneurysm surgery: a prospective assessment. J Neurosurg. 2004;100:230–5.CrossRefGoogle Scholar
  36. 36.
    Morcos JJ. Editorial: indocyanine green videoangiography or intraoperative angiography? J Neurosurg. 2013;118:417–8.CrossRefGoogle Scholar
  37. 37.
    Holland NR. Subcortical strokes from intracranial aneurysm surgery: implications for intraoperative neuromonitoring. J Clin Neurophysiol. 1998;15:439–46.CrossRefGoogle Scholar
  38. 38.
    Kang D, Yao P, Wu Z, Yu L. Ischemia changes and tolerance ratio of evoked potential monitoring in intracranial aneurysm surgery. Clin Neurol Neurosurg. 2013;115:552–6.CrossRefGoogle Scholar
  39. 39.
    Mizoi K, Yoshimoto T. Permissible temporary occlusion time in aneurysm surgery as evaluated by evoked potential monitoring. Neurosurgery. 1993;33:434–40.PubMedGoogle Scholar
  40. 40.
    Mooij JJ, Buchthal A, Belopavlovic M. Somatosensory evoked potential monitoring of temporary middle cerebral artery occlusion during aneurysm operation. Neurosurgery. 1987;21:492–6.CrossRefGoogle Scholar
  41. 41.
    Wicks RT, Pradilla G, Raza SM, Hadelsberg U, Coon AL, Huang J, Tamargo RJ. Impact of changes in intraoperative somatosensory evoked potentials on stroke rates after clipping of intracranial aneurysms. Neurosurgery. 2012;70:1114–24.CrossRefGoogle Scholar
  42. 42.
    Ferch R, Pasqualin A, Pinna G, Chioffi F, Bricolo A. Temporary arterial occlusion in the repair of ruptured intracranial aneurysms: an analysis of risk factors for stroke. J Neurosurg. 2002;97:836–42.CrossRefGoogle Scholar
  43. 43.
    Ogilvy CS, Carter BS, Kaplan S, Rich C, Crowell RM. Temporary vessel occlusion for aneurysm surgery: risk factors for stroke in patients protected by induced hypothermia and hypertension and intravenous mannitol administration. J Neurosurg. 1996;84:785–91.CrossRefGoogle Scholar
  44. 44.
    Samson D, Batjer HH, Bowman G, Mootz L, Krippner WJ Jr, Meyer YJ, Allen BC. A clinical study of the parameters and effects of temporary arterial occlusion in the management of intracranial aneurysms. Neurosurgery. 1994;34:22–8.PubMedGoogle Scholar
  45. 45.
    Gruber A, Dorfer C, Standhardt H, Bavinzski G, Knosp E. Prospective comparison of intraoperative vascular monitoring technologies during cerebral aneurysm surgery. Neurosurgery. 2011;68:657–73.CrossRefGoogle Scholar
  46. 46.
    Raabe A, Seidel K. Prevention of ischemic complications during aneurysm surgery. J Neurosurg Sci. 2016;60:95–103.PubMedGoogle Scholar
  47. 47.
    Hossmann KA. Experimental models for the investigation of brain ischemia. Cardiovasc Res. 1998;39:106–20.CrossRefGoogle Scholar
  48. 48.
    Macfarlane R, Moskowitz MA, Tasdemiroglu E, Wei EP, Kontos HA. Postischemic cerebral blood flow and neuroeffector mechanisms. Blood Vessels. 1991;28:46–51.PubMedGoogle Scholar
  49. 49.
    Sundt TM Jr, Waltz AG. Cerebral ischemia and reactive hyperemia. Studies of cortical blood flow and microcirculation before, during, and after temporary occlusion of middle cerebral artery of squirrel monkeys. Circ Res. 1971;28:426–33.CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Alberto Pasqualin
    • 1
  • Pietro Meneghelli
    • 2
  • Angelo Musumeci
    • 2
  • Alessandro Della Puppa
    • 3
  • Giacomo Pavesi
    • 4
  • Giampietro Pinna
    • 2
  • Renato Scienza
    • 3
  1. 1.Section of Vascular Neurosurgery, Institute of Neurosurgery, Verona City and University HospitalVeronaItaly
  2. 2.Institute of Neurosurgery, Verona City and University HospitalVeronaItaly
  3. 3.Division of NeurosurgeryPadua City HospitalPadovaItaly
  4. 4.Division of NeurosurgeryBaggiovara HospitalModenaItaly

Personalised recommendations