Abstract
Introduction
Aneurysmal subarachnoid hemorrhage constitutes a clinical entity associated with high mortality and morbidity. It is widely accepted that improper clip placement may have as a result of incomplete aneurysm occlusion and/or partial or complete obstruction of an adjacent vessel. Various modalities, including intraoperative or postoperative digital subtracting angiography, near-infrared indocyanine green angiography, micro-Doppler ultrasonography (MDU), and neurophysiological studies, have been utilized for verifying proper clip placement. The aim of our study was to review the role of MDU during aneurysmal surgery.
Methods
A literature search was performed using any possible combination of the following terms: “aneurysm,” “brain,” “cerebral,” “clip,” “clipping,” “clip malpositioning,” “clip repositioning,” “clip suboptimal positioning,” “Doppler,” “intracranial,” “microsurgery,” “micro-Doppler,” “residual neck,” “ultrasonography,” “ultrasound,” and “vessel occlusion”. Additionally, reference lists from the retrieved articles were reviewed for identifying any additional articles. Case reports and miniseries were excluded.
Results
A total of 19 series employing intraoperative MDU during aneurysmal microsurgery were retrieved. All studies demonstrated that MDU accuracy is extremely high. The highest reported false-positive rate of MDU was 2 %, while the false-negative rate was reported as high as 1.6 %. It has been demonstrated that the presence of subarachnoid hemorrhage, specific anatomic locations, and large size may predispose to improper clip placement. Intraoperative MDU’s technical limitations and weaknesses are adequately identified, in order to minimize the possibility of any misinterpretations.
Conclusion
Intraoperative MDU constitutes a safe, accurate, and low cost imaging modality for evaluating blood flow and for verifying proper clip placement during microsurgical clipping.
Similar content being viewed by others
References
Kassell NF, Torner JC, Jane JA, Haley EC Jr, Adams HP (1990) The international cooperative study on the timing of aneurysm surgery. Part 2: surgical results. J Neurosurg 73:37–47
Ljunggren B, Säveland H, Brandt L (1983) Causes of unfavorable outcome after early aneurysm operation. Neurosurgery 13:629–633
Molyneux A, Kerr R, Stratton I, Sandercock P, Clarke M, Shrimpton J, Holman R, International Subarachnoid Aneurysm Trial (ISAT) Collaborative Group (2002) International Subarachnoid Aneurysm Trial (ISAT) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomised trial. Lancet 360:1267–1274
Nanda A, Vannemreddy P (2003) Management of intracranial aneurysms: factors that influence clinical grade and surgical outcome. South Med J 96:259–263
David CA, Vishteh AG, Spetzler RF, Lemole M, Lawton MT, Partovi S (1999) Late angiographic follow-up review of surgically treated aneurysms. J Neurosurg 91:396–401
Fogelholm R, Hernesniemi J, Vapalahti M (1993) Impact of early surgery on outcome after aneurysmal subarachnoid hemorrhage. A population-based study. Stroke 24:1649–1654
Hernesniemi J, Vapalahti M, Niskanen M, Tapaninaho A, Kari A, Luukkonen M, Puranen M, Saari T, Rajpar M (1993) One-year outcome in early aneurysm surgery: a 14 year experience. Acta Neurochir (Wien) 122:1–10
Macdonald RL, Wallace MC, Kestle JR (1993) Role of angiography following aneurysm surgery. J Neurosurg 79:826–832
Meyer B, Urbach H, Schaller C, Baslam M, Nordblom J, Schramm J (2004) Immediate postoperative angiography after aneurysm clipping-implications for quality control and guidance of further management. Zentralbl Neurochir 65:49–56
Akdemir H, Oktem IS, Tucer B, Menkü A, Başaslan K, Günaldi O (2006) Intraoperative microvascular Doppler sonography in aneurysm surgery. Minim Invasive Neurosurg 49:312–316
Alexander TD, Macdonald RL, Weir B, Kowalczuk A (1996) Intraoperative angiography in cerebral aneurysm surgery: a prospective study of 100 craniotomies. Neurosurgery 39:10–17
Andrychowski J, Czernicki Z, Bogucki J, Mierzejewski M (1998) The usefulness of intraoperative high-frequency Doppler flowmetry in surgeries for intracranial aneurysms. Neurol Neurochir Pol 32:331–339
Bailes JE, Tantuwaya LS, Fukushima T, Schurman GW, Davis D (1997) Intraoperative microvascular Doppler sonography in aneurysm surgery. Neurosurgery 40:965–970
Chen SF, Kato Y, Oda J, Kumar A, Watabe T, Imizu S, Oguri D, Sano H, Hirose Y (2011) The application of intraoperative near-infrared indocyanine green videoangiography and analysis of fluorescence intensity in cerebrovascular surgery. Surg Neurol Int 2:42
Critchley GR, O’Neill KS, Bell BA (1998) Cerebral blood flow and tissue oxygenation monitoring during aneurysm surgery. Neurol Res 20(Suppl 1):S44–S47
Cui H, Wang Y, Yin Y, Wan J, Fei Z, Gao W, Jiang J (2011) Role of intraoperative microvascular Doppler in the microsurgical management of intracranial aneurysms. J Clin Ultrasound 39:27–31
Dehdashti AR, Thines L, Da Costa LB, terBrugge KG, Willinsky RA, Wallace MC, Tymianski M (2009) Intraoperative biplanar rotational angiography during neurovascular surgery. Technical note. J Neurosurg 111:188–192
Eliava ShSh, Shekhtman OD, Zolotukhin SP, Sazonov IA, Kheĭreddin AS (2006) Intraoperative contact Doppler ultrasonography in the surgery of cerebral aneurysm. Zh Vopr Neirokhir Im N N Burdenko Apr–Jun:42–7
Firsching R, Synowitz HJ, Hanebeck J (2000) Practicability of intraoperative microvascular Doppler sonography in aneurysm surgery. Minim Invasive Neurosurg 43:144–148
Fischer G, Stadie A, Oertel JM (2010) Near-infrared indocyanine green videoangiography versus microvascular Doppler sonography in aneurysm surgery. Acta Neurochir (Wien) 152:1519–1525
Friedman WA, Chadwick GM, Verhoeven FJ, Mahla M, Day AL (1991) Monitoring of somatosensory evoked potentials during surgery for middle cerebral artery aneurysms. Neurosurgery 29:83–88
Gaĭdar BV, Shcherbuk IuA, Parfenov VE, Svistov DV, Kandyba DV, Polezhaev AV (1998) The combined use of intraoperative video endoscopy and contact microvascular Dopplerography in the surgery of cerebral aneurysms. De Vries AJ Vestn Khir Im I I Grek 157:133–137
Gilsbach JM (1984) Microvascular intraoperative Doppler sonography. Ultraschall Med 5:246–254
Hecht N, Woitzik J, Dreier JP, Vajkoczy P (2009) Intraoperative monitoring of cerebral blood flow by laser speckle contrast analysis. Neurosurg Focus 27:E11
Heiroth HJ, Etminan N, Steiger HJ, Hänggi D (2011) Intraoperative Doppler and Duplex sonography in cerebral aneurysm surgery. Br J Neurosurg 25:586–590
Hölscher T, Rodriguez-Rodriguez J, Wilkening WG, Lasheras JC, U HS (2006) Intraoperative brain ultrasound: a new approach to study flow dynamics in intracranial aneurysms. Ultrasound Med Biol 32:1307–1313
Hölscher T, Postert T, Meves S, Thies T, Ermert H, Bogdahn U, Wilkening W (2002) Assessment of brain perfusion with echo contrast specific imaging modes and Optison. Acad Radiol Suppl 2:S386–S388
Imizu S, Kato Y, Sangli A, Oguri D, Sano H (2008) Assessment of incomplete clipping of aneurysms intraoperatively by a near-infrared indocyanine green-video angiography (Niicg-Va) integrated microscope. Minim Invasive Neurosurg 51:199–203
Kapsalaki EZ, Lee GP, Robinson JS 3rd, Grigorian AA, Fountas KN (2008) The role of intraoperative micro-Doppler ultrasound in verifying proper clip placement in intracranial aneurysm surgery. J Clin Neurosci 15:153–157
Katz JM, Gologorsky Y, Tsiouris AJ, Wells-Roth D, Mascitelli J, Gobin YP, Stieg PE, Riina HA (2006) Is routine intraoperative angiography in the surgical treatment of cerebral aneurysms justified? A consecutive series of 147 aneurysms. Neurosurgery 58:719–727
Klopfenstein JD, Spetzler RF, Kim LJ, Feiz-Erfan I, Han PP, Zabramski JM, Porter RW, Albuquerque FC, McDougall CG, Fiorella DJ (2004) Comparison of routine and selective use of intraoperative angiography during aneurysm surgery: a prospective assessment. J Neurosurg 100:230–235
Laborde G, Gilsbach J, Harders A (1988) The microvascular Doppler—an intraoperative tool for the treatment of large and giant aneurysms. Acta Neurochir Suppl (Wien) 42:75–80
Manninen PH, Patterson S, Lam AM, Gelb AW, Nantau WE (1994) Evoked potential monitoring during posterior fossa aneurysm surgery: a comparison of two modalities. Can J Anaesth 41:92–97
Marchese E, Albanese A, Denaro L, Vignati A, Fernandez E, Maira G (2005) Intraoperative microvascular Doppler in intracranial aneurysm surgery. Surg Neurol 63:336–342
Martin NA, Bentson J, Viñuela F, Hieshima G, Reicher M, Black K, Dion J, Becker D (1990) Intraoperative digital subtraction angiography and the surgical treatment of intracranial aneurysms and vascular malformations. J Neurosurg 73:526–533
Neuloh G, Schramm J (2004) Monitoring of motor evoked potentials compared with somatosensory evoked potentials and microvascular Doppler ultrasonography in cerebral aneurysm surgery. J Neurosurg 100:389–399
Raabe A, Beck J, Gerlach R, Zimmermann M, Seifert V (2003) Near-infrared indocyanine green video angiography: a new method for intraoperative assessment of vascular flow. Neurosurgery 52:132–139
Raabe A, Nakaji P, Beck J, Kim LJ, Hsu FP, Kamerman JD, Seifert V, Spetzler RF (2005) Prospective evaluation of surgical microscope-integrated intraoperative near-infrared indocyanine green videoangiography during aneurysm surgery. J Neurosurg 103:982–989
Raabe A, Spetzler RF (2008) Fluorescence angiography. J Neurosurg 108:429–430
Rauzzino MJ, Quinn CM, Fisher WS 3rd (1998) Angiography after aneurysm surgery: indications for “selective” angiography. Surg Neurol 49:32–40
Sanzenbacher KE (2005) Intraoperative monitoring during aneurysm surgery as a neuroprotective activity with reference to evoked potential and microvascular Doppler techniques. Ann N Y Acad Sci 1053:28–29
Shibata Y, Fujita S, Kawaguchi T, Hosoda K, Komatsu H, Tamaki N (2000) Use of microvascular Doppler sonography in aneurysm surgery on the anterior choroidal artery. Neurol Med Chir (Tokyo) 40:30–35
Stendel R, Pietilä T, Al Hassan AA, Schilling A, Brock M (2000) Intraoperative microvascular Doppler ultrasonography in cerebral aneurysm surgery. J Neurol Neurosurg Psychiatry 68:29–35
Tang G, Cawley CM, Dion JE, Barrow DL (2002) Intraoperative angiography during aneurysm surgery: a prospective evaluation of efficacy. J Neurosurg 96:993–999
Tong J, Wang S, Zhao YL, Zhao JZ (2007) Intraoperative microvascular Doppler ultrasonography monitoring in intracranial aneurysm surgery. Zhonghua Yi Xue Za Zhi 87:881–884
Unsgaard G, Rygh OM, Selbekk T, Müller TB, Kolstad F, Lindseth F, Hernes TA (2006) Intra-operative 3D ultrasound in neurosurgery. Acta Neurochir (Wien) 148:235–253
Wrobel CJ, Meltzer H, Lamond R, Alksne JF (1994) Intraoperative assessment of aneurysm clip placement by intravenous fluorescein angiography. Neurosurgery 35:970–973
Klein KU, Stadie A, Fukui K, Schramm P, Werner C, Oertel J, Engelhard K, Fischer G (2011) Measurement of cortical microcirculation during intracranial aneurysm surgery by combined laser-Doppler flowmetry and photo-spectrometry. Neurosurgery 69:391–398
O’Hara JA, Khan N, Hou H, Wilmo CM, Demidenko E, Dunn JF, Swartz HM (2004) Comparison of EPR oximetry and Eppendorf polarographic electrode assessments of rat brain PtO2. Physiol Meas 25:1413–1423
Shaw AD, Li Z, Thomas Z, Stevens CW (2002) Assessment of tissue oxygen tension: comparison of dynamic fluorescence quenching and polarographic electrode technique. Crit Care 6:76–80
Gagel B, Piroth M, Pinkawa M, Reinartz P, Zimny M, Kaiser HJ, Stanzel S, Asadpour B, Demirel C, Hamacher K, Coenen HH, Scholbach T, Maneschi P, DiMartino E, Eble MJ (2007) pO polarography, contrast enhanced color duplex sonography (CDS), [18F] fluoromisonidazole and [18F] fluorodeoxyglucose positron emission tomography: validated methods for the evaluation of therapy-relevant tumor oxygenation or only bricks in the puzzle of tumor hypoxia? BMC Cancer 7:113
Mazzeo AT, Di Pasquale R, Settineri N, Bottari G, Granata F, Faragò G, Pitrone A, Longo M, Santamaria L (2012) Usefulness and limits of near infrared spectroscopy monitoring during endovascular neuroradiologic procedures. Minerva Anestesiol 78:34–45
Uchino H, Nakamura T, Kuroda S, Houkin K, Murata JI, Saito H (2011) Intraoperative dual monitoring during carotid endarterectomy using motor evoked potential and near-infrared spectroscopy. World Neurosurg 2011. doi:10.1016/j.wneu.2011.10.039
Buravtcov DE, Vlasova IM, Saletsky AM (2008) Raman spectroscopy and fluorescence analysis in investigation of the protective action of ischemic preconditioning at ischemic insult by estimation of damage of low-density lipoprotein of blood. Photomed Laser Surg 26:181–187
Nornes H, Grip A, Wikeby P (1979) Intraoperative evaluation of cerebral hemodynamics using directional Doppler technique. Part 2: Saccular aneurysms. J Neurosurg 50:570–577
Woydt M, Greiner K, Perez J, Krone A, Roosen K (1997) Intraoperative color duplex sonography of basal arteries during aneurysm surgery. J Neuroimaging 7:203–207
Xu BN, Sun ZH, Romani R, Jiang JL, Wu C, Zhou DB, Yu XG, Hernesniemi J, Li BM (2010) Microsurgical management of large and giant paraclinoid aneurysms. World Neurosurgery 73:137–146
Miyazaki M, Kato K (1965) Measurement of cerebral blood flow by ultrasonic Doppler technique. Jpn Circ J 29:375–382
Aaslid R, Markwalder TM, Nornes H (1982) Noninvasive transcranial Doppler ultrasound recording of flow velocity in basal cerebral arteries. J Neurosurg 57:769–774
Gilsbach JM, Hassler WE (1984) Intraoperative Doppler and real time sonography in neurosurgery. Neurosurg Rev 7:199–208
Black KL, Rubin JM, Chandler WF, McGillicuddy JE (1998) Intraoperative color-flow Doppler imaging of AVM’s and aneurysms. J Neurosurg 68:635–639
Amin-Hanjani S, Meglio G, Gatto R, Bauer A, Charbel FT (2008) The utility of intraoperative blood flow measurement during aneurysm surgery using an ultrasonic perivascular flow probe. Neurosurgery 62:1346–1353
Lindseth F, Lovstakken L, Rygh OM, Tangen GA, Torp H, Unsgaard G (2009) Blood flow imaging: an angle-independent ultrasound modality for intraoperative assessment of flow dynamics in neurovascular surgery. Neurosurgery 65:149–157
Barrow DL, Boyer KL, Joseph GJ (1992) Intraoperative angiography in the management of neurovascular disorders. Neurosurgery 30:153–159
Drake CG, Allcock JM (1973) Postoperative angiography and the “slipped” clip. J Neurosurg 39:683–689
Proust F, Hannequin D, Langlois O, Freger P, Creissard P (1995) Causes of morbidity and mortality after ruptured aneurysm surgery in a series of 230 patients. The importance of control angiography. Stroke 26:1553–1557
Suzuki J, Kwak R, Katakura R (1980) Review of incompletely occluded surgically treated cerebral aneurysms. Surg Neurol 13:306–310
Karhunen PJ (1991) Neurosurgical vascular complications associated with aneurysm clips evaluated by postmortem angiography. Forensic Sci Int 51:13–22
Conflict of interest
We declare that we have no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Siasios, I., Kapsalaki, E.Z. & Fountas, K.N. The role of intraoperative micro-Doppler ultrasound in verifying proper clip placement in intracranial aneurysm surgery. Neuroradiology 54, 1109–1118 (2012). https://doi.org/10.1007/s00234-012-1023-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00234-012-1023-y