Skip to main content
Top
Published in: Acta Neurochirurgica 4/2016

01-04-2016 | Clinical Article - Brain Tumors

Intraoperative 3D contrast-enhanced ultrasound (CEUS): a prospective study of 50 patients with brain tumours

Authors: Felix Arlt, Claire Chalopin, Andrea Müns, Jürgen Meixensberger, Dirk Lindner

Published in: Acta Neurochirurgica | Issue 4/2016

Login to get access

Abstract

Background

Reliable intraoperative resection control during surgery of malignant brain tumours is associated with the longer overall survival of patients. B-mode ultrasound (BUS) is a familiar intraoperative imaging application in neurosurgical procedures and supplies excellent image quality. However, due to resection-induced artefacts, its ability to distinguish between tumour borders, oedema, surrounding tissue and tumour remnants is sometimes limited. In experienced hands, this “bright rim effect” could be reduced. However, it should be determined, if contrast-enhanced ultrasound can improve this situation by providing high-quality imaging during the resection. The aim of this clinical study was to examine contrast-enhanced and three-dimensional reconstructed ultrasound (3D CEUS) in brain tumour surgery regarding the uptake of contrast agent pre- and post-tumour resection, imaging quality and in comparison with postoperative magnetic resonance imaging in different tumour entities.

Methods

Fifty patients, suffering from various brain tumours intra-axial and extra-axial, who had all undergone surgery with the support of neuronavigation in our neurosurgical department, were included in the study. Their median age was 56 years (range, 28–79). Ultrasound imaging was performed before the Dura was opened and for resection control at the end of tumour resection as defined by the neurosurgeon. A high-end ultrasound (US) device (Toshiba Aplio XG®) with linear and sector probes for B-mode and CEUS was used. Navigation and 3D reconstruction were performed with a LOCALITE SonoNavigator® and the images were transferred digitally (DVI) to the navigation system. The contrast agent consists of echoic micro-bubbles showing tumour vascularisation. The ultrasound images were compared with the corresponding postoperative MR data in order to determine the accuracy and imaging quality of the tumours and tumour remnants after resection.

Results

Different types of tumours were investigated. High, dynamic contrast agent uptake was observed in 19 of 21 patients (90 %) suffering from glioblastoma, while in 2 patients uptake was low and insufficient. In 52.4 % of glioblastoma and grade III astrocytoma patients CEUS led to an improved delineation in comparison to BUS and showed a high-resolution imaging quality of the tumour margins and tumour boarders. Grade II and grade III astrocytoma (n = 6) as well as metastasis (n = 18) also showed high contrast agent uptake, which led in 50 % to an improved imaging quality. In 5 of these 17 patients, intraoperative CEUS for resection control showed tumour remnants, leading to further tumour resection. Patients treated with CEUS showed no increased neurological deficits after tumour resection. No pharmacological side-effects occurred.

Conclusions

Three-dimensional CEUS is a reliable intraoperative imaging modality and could improve imaging quality. Ninety percent of the high-grade gliomas (HGG, glioblastoma and astrocytoma grade III) showed high contrast uptake with an improved imaging quality in more than 50 %. Gross total resection and incomplete resection of glioblastoma were adequately highlighted by 3D CEUS intraoperatively. The application of US contrast agent could be a helpful imaging tool, especially for resection control in glioblastoma surgery.
Literature
1.
go back to reference Coburger J, König RW, Scheuerle A, Engelke J, Hlavac M, Thal DR, Wirtz CR (2014) Navigated high frequency ultrasound: description of technique and clinical comparison with conventional intracranial ultrasound. World Surg 82:366–75 Coburger J, König RW, Scheuerle A, Engelke J, Hlavac M, Thal DR, Wirtz CR (2014) Navigated high frequency ultrasound: description of technique and clinical comparison with conventional intracranial ultrasound. World Surg 82:366–75
2.
go back to reference Lindner D, Trantakis C, Arnold S, Schmitgen A, Schneider J, Meixensberger J (2005) Neuronavigation based on intraoperative 3D-ultrasound during tumor resection. Proceedings of computer assisted radiology and surgery. CARS. 815–820 Lindner D, Trantakis C, Arnold S, Schmitgen A, Schneider J, Meixensberger J (2005) Neuronavigation based on intraoperative 3D-ultrasound during tumor resection. Proceedings of computer assisted radiology and surgery. CARS. 815–820
3.
go back to reference Selbekk T, Jakola AS, Solheim O (2013) Ultrasound imaging in neurosurgery: approaches to minimize surgically induced image artefacts for improved resection control. Acta Neurochir (Wein) 155:973–980CrossRef Selbekk T, Jakola AS, Solheim O (2013) Ultrasound imaging in neurosurgery: approaches to minimize surgically induced image artefacts for improved resection control. Acta Neurochir (Wein) 155:973–980CrossRef
4.
go back to reference Unsgaard G, Gronningsaeter A, Ommedal S, Nagelhus Hernes TA (2002) Brain operations guided by real-time two-dimensional ultrasound: new possibilities as a result of improved image quality. Neurosurgery 51:402–412PubMed Unsgaard G, Gronningsaeter A, Ommedal S, Nagelhus Hernes TA (2002) Brain operations guided by real-time two-dimensional ultrasound: new possibilities as a result of improved image quality. Neurosurgery 51:402–412PubMed
5.
go back to reference Willems PW, Taphoorn MJB, Burger H, van der Sprenkel JWB, Tulleken CAF (2006) Effectiveness of neuronavigation in resecting solitary intracerebral contrast-enhancing tumors: a randomized controlled trial. J Neurosurg 104:360–368CrossRefPubMed Willems PW, Taphoorn MJB, Burger H, van der Sprenkel JWB, Tulleken CAF (2006) Effectiveness of neuronavigation in resecting solitary intracerebral contrast-enhancing tumors: a randomized controlled trial. J Neurosurg 104:360–368CrossRefPubMed
6.
go back to reference Unsgaard G, Ommedal S, Muller T, Gronningsaeter A, Nagelhus Hernes TA (2002) Neuronavigation by intraoperative three-dimensional ultrasound: initial experience during brain tumor resection. Neurosurgery 50:804–812CrossRefPubMed Unsgaard G, Ommedal S, Muller T, Gronningsaeter A, Nagelhus Hernes TA (2002) Neuronavigation by intraoperative three-dimensional ultrasound: initial experience during brain tumor resection. Neurosurgery 50:804–812CrossRefPubMed
7.
go back to reference Busse H, Schmitgen A, Trantakis C, Schober R, Kahn T, Moche M (2006) Advanced approach for intraoperative MRI guidance and potential benefit for neurosurgical applications. J Magn Reson Imaging 24:140–151CrossRefPubMed Busse H, Schmitgen A, Trantakis C, Schober R, Kahn T, Moche M (2006) Advanced approach for intraoperative MRI guidance and potential benefit for neurosurgical applications. J Magn Reson Imaging 24:140–151CrossRefPubMed
8.
go back to reference Chalopin C, Krissian K, Meixensberger J, Müns A, Arlt F, Lindner D (2013) Evaluation of a semi-automatic segmentation algorithm in 3D intraoperative ultrasound brain angiography. Biomed Tech 58:293–30CrossRef Chalopin C, Krissian K, Meixensberger J, Müns A, Arlt F, Lindner D (2013) Evaluation of a semi-automatic segmentation algorithm in 3D intraoperative ultrasound brain angiography. Biomed Tech 58:293–30CrossRef
9.
go back to reference Kaps M, Legemate DA, Ries F, Ackerstaff RG, Markus H, Pezzoll C, Llull JB, Spinazzi A (2001) SonoVue in transcranial Doppler investigations of the cerebral arteries. J Neuroimaging 11:261–7CrossRefPubMed Kaps M, Legemate DA, Ries F, Ackerstaff RG, Markus H, Pezzoll C, Llull JB, Spinazzi A (2001) SonoVue in transcranial Doppler investigations of the cerebral arteries. J Neuroimaging 11:261–7CrossRefPubMed
10.
go back to reference Mert A, Buehler K, Sutherland GR, Tomanek B, Widhalm G, Kasprian G, Knosp E, Wolfsberger S (2012) Brain tumor surgery with 3-dimensional surface navigation. Neurosurgery 71:286–94 Mert A, Buehler K, Sutherland GR, Tomanek B, Widhalm G, Kasprian G, Knosp E, Wolfsberger S (2012) Brain tumor surgery with 3-dimensional surface navigation. Neurosurgery 71:286–94
11.
go back to reference Müns A, Mühl C, Haase R, Möckel H, Chalopin C, Meixensberger J, Lindner D (2014) A neurosurgical phantom-based training system with ultrasound simulation. Acta Neurochir (Wein) 156:1237–43CrossRef Müns A, Mühl C, Haase R, Möckel H, Chalopin C, Meixensberger J, Lindner D (2014) A neurosurgical phantom-based training system with ultrasound simulation. Acta Neurochir (Wein) 156:1237–43CrossRef
12.
go back to reference Renovanz M, Hickmann AK, Henkel C, Nadji-Ohl M, Hopf NJ (2014) Navigated versus non-navigated intraoperative ultrasound: is there any impact on the extent of resection of high-grade gliomas? A retrospective clinical analysis. Neurol Surq A Centr Eur Neurosurq 75:224–30CrossRef Renovanz M, Hickmann AK, Henkel C, Nadji-Ohl M, Hopf NJ (2014) Navigated versus non-navigated intraoperative ultrasound: is there any impact on the extent of resection of high-grade gliomas? A retrospective clinical analysis. Neurol Surq A Centr Eur Neurosurq 75:224–30CrossRef
13.
go back to reference Trantakis C, Meixensberger J, Lindner D, Strauss G, Grunst G, Schmidtgen A, Arnold S (2002) Iterative neuronavigation using 3D ultrasound. A feasibility study. Neurol Res 24:666–670CrossRefPubMed Trantakis C, Meixensberger J, Lindner D, Strauss G, Grunst G, Schmidtgen A, Arnold S (2002) Iterative neuronavigation using 3D ultrasound. A feasibility study. Neurol Res 24:666–670CrossRefPubMed
14.
go back to reference Lindseth F, Kaspersen JH, Ommedal S (2003) Multimodal image fusion in ultrasound-based neuronavigation: improving overview and interpretation by integrating preoperative MRI with intraoperative 3D ultrasound. Comput Aided Surg 8:49–69CrossRefPubMed Lindseth F, Kaspersen JH, Ommedal S (2003) Multimodal image fusion in ultrasound-based neuronavigation: improving overview and interpretation by integrating preoperative MRI with intraoperative 3D ultrasound. Comput Aided Surg 8:49–69CrossRefPubMed
15.
go back to reference Reinertsen I, Lindseth F, Askeland C, Iversen DH, Unsgård G (2014) Intra-operative correction of brain-shift. Acta Neurochir (Wein) 156:1301–10CrossRef Reinertsen I, Lindseth F, Askeland C, Iversen DH, Unsgård G (2014) Intra-operative correction of brain-shift. Acta Neurochir (Wein) 156:1301–10CrossRef
16.
go back to reference Senft C, Bink A, Franz K, Vatter H, Gasser T, Seifert V (2011) Intraoperative MRI guidance and extent of resection in glioma surgery: a randomised, controlled trial. Lancet Oncol 12:997–1003CrossRefPubMed Senft C, Bink A, Franz K, Vatter H, Gasser T, Seifert V (2011) Intraoperative MRI guidance and extent of resection in glioma surgery: a randomised, controlled trial. Lancet Oncol 12:997–1003CrossRefPubMed
17.
go back to reference Prada F, Perin A, Martegani A (2014) Intraoperative contrast enhanced ultra-sound (iCEUS) for brain surgery. Neurosurgery 74:542–552CrossRefPubMed Prada F, Perin A, Martegani A (2014) Intraoperative contrast enhanced ultra-sound (iCEUS) for brain surgery. Neurosurgery 74:542–552CrossRefPubMed
18.
go back to reference Kate GL, van Dijk AC, van den Oord SC, Hussain B, Verhagen HJ, Sijbrands EJ, van der Steen AF, van der Lugt A, Schinkel AF (2013) Usefulness of contrast-enhanced ultrasound for detection of carotid plaque ulceration in patients with symptomatic carotid atherosclerosis. Am J Cardiol 112:292–8CrossRefPubMed Kate GL, van Dijk AC, van den Oord SC, Hussain B, Verhagen HJ, Sijbrands EJ, van der Steen AF, van der Lugt A, Schinkel AF (2013) Usefulness of contrast-enhanced ultrasound for detection of carotid plaque ulceration in patients with symptomatic carotid atherosclerosis. Am J Cardiol 112:292–8CrossRefPubMed
19.
go back to reference Nanda NC, Wistran DC, Karlsberg RP, Hack TC, Smith WB, Foley DA, Picard MH, Cotter B (2002) Multicenter evaluation of SonoVue for improved endocardial border delineation. Echocardiography 19:27–36CrossRefPubMed Nanda NC, Wistran DC, Karlsberg RP, Hack TC, Smith WB, Foley DA, Picard MH, Cotter B (2002) Multicenter evaluation of SonoVue for improved endocardial border delineation. Echocardiography 19:27–36CrossRefPubMed
20.
go back to reference Park KH, Kwon SH, Lee YS, Jeong SW, Jang JY, Lee SH, Kim SG, Cha SW, Kim YS, Cho YD, Kim HS, Kim BS, Kim YJ (2015) Predictive factors of contrast-enhanced ultrasonography for the response to transarterial chemoembolization in hepatocellular carcinoma. Clin Mol Hepatol 21:158–64CrossRefPubMedPubMedCentral Park KH, Kwon SH, Lee YS, Jeong SW, Jang JY, Lee SH, Kim SG, Cha SW, Kim YS, Cho YD, Kim HS, Kim BS, Kim YJ (2015) Predictive factors of contrast-enhanced ultrasonography for the response to transarterial chemoembolization in hepatocellular carcinoma. Clin Mol Hepatol 21:158–64CrossRefPubMedPubMedCentral
21.
go back to reference Bogdahn U, Fröhlich T, Becker G (1994) Vascularization of primary central nervous system tumors: detection with contrast-enhanced transcranial color-coded real-time sonography. Radiology 192:141–148CrossRefPubMed Bogdahn U, Fröhlich T, Becker G (1994) Vascularization of primary central nervous system tumors: detection with contrast-enhanced transcranial color-coded real-time sonography. Radiology 192:141–148CrossRefPubMed
22.
go back to reference Claudon M, Cosgrove D, Albrecht T (2008) Guidelines and good clinical practice recommendations for contrast enhanced ultrasound (CEUS)—update 2008. Ultraschall Med 29:28–44CrossRefPubMed Claudon M, Cosgrove D, Albrecht T (2008) Guidelines and good clinical practice recommendations for contrast enhanced ultrasound (CEUS)—update 2008. Ultraschall Med 29:28–44CrossRefPubMed
23.
go back to reference Engelhardt M, Hansen C, Eyding J (2007) Feasibility of contrast-enhanced sonography during resection of cerebral tumours: initial results of a prospective study. Ultrasound Med Biol 33:571–575CrossRefPubMed Engelhardt M, Hansen C, Eyding J (2007) Feasibility of contrast-enhanced sonography during resection of cerebral tumours: initial results of a prospective study. Ultrasound Med Biol 33:571–575CrossRefPubMed
24.
go back to reference He W, Jiang X-Q, Wang S (2008) Intraoperative contrast-enhanced ultrasound for brain tumors. Clin Imaging 32:419–424CrossRefPubMed He W, Jiang X-Q, Wang S (2008) Intraoperative contrast-enhanced ultrasound for brain tumors. Clin Imaging 32:419–424CrossRefPubMed
25.
go back to reference Prada F, Mattei L, DelBene M, Aiani L, Saini M (2014) Intraoperative cerebral glioma characterization with contrast enhanced ultrasound. Biomed Res Int. 484261 Prada F, Mattei L, DelBene M, Aiani L, Saini M (2014) Intraoperative cerebral glioma characterization with contrast enhanced ultrasound. Biomed Res Int. 484261
26.
go back to reference Quaia E (2011) Assessment of tissue perfusion by contrast-enhanced ultrasound. Eur Radiol 21:604–615CrossRefPubMed Quaia E (2011) Assessment of tissue perfusion by contrast-enhanced ultrasound. Eur Radiol 21:604–615CrossRefPubMed
27.
go back to reference Woydt M, Krone A, Becker G, Schmidt K, Roggendorf W, Roosen K (1996) Correlation of intra-operative ultrasound with histopathologic findings after tumour resection in supratentorial gliomas. A method to improve gross total tumour resection. Acta Neurochir (Wein) 138:1391–1398CrossRef Woydt M, Krone A, Becker G, Schmidt K, Roggendorf W, Roosen K (1996) Correlation of intra-operative ultrasound with histopathologic findings after tumour resection in supratentorial gliomas. A method to improve gross total tumour resection. Acta Neurochir (Wein) 138:1391–1398CrossRef
Metadata
Title
Intraoperative 3D contrast-enhanced ultrasound (CEUS): a prospective study of 50 patients with brain tumours
Authors
Felix Arlt
Claire Chalopin
Andrea Müns
Jürgen Meixensberger
Dirk Lindner
Publication date
01-04-2016
Publisher
Springer Vienna
Published in
Acta Neurochirurgica / Issue 4/2016
Print ISSN: 0001-6268
Electronic ISSN: 0942-0940
DOI
https://doi.org/10.1007/s00701-016-2738-z

Other articles of this Issue 4/2016

Acta Neurochirurgica 4/2016 Go to the issue