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Published in: Acta Neurochirurgica 10/2008

01-10-2008 | Clinical Article

Comparison of navigated 3D ultrasound findings with histopathology in subsequent phases of glioblastoma resection

Authors: Ola Morten Rygh, Tormod Selbekk, Sverre Helge Torp, Stian Lydersen, Toril Anita Nagelhus Hernes, Geirmund Unsgaard

Published in: Acta Neurochirurgica | Issue 10/2008

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Abstract

Objective

The purpose of the study was to compare the ability of navigated 3D ultrasound to distinguish tumour and normal brain tissue at the tumour border zone in subsequent phases of resection.

Materials and methods

Biopsies were sampled in the tumour border zone as seen in the US images before and during surgery. After resection, biopsies were sampled in the resection cavity wall. Histopathology was compared with the surgeon’s image findings.

Results

Before resection, the tumour border was delineated by ultrasound with high specificity and sensitivity (both 95%). During resection, ultrasound had acceptable sensitivity (87%), but poor specificity (42%), due to biopsies falsely classified as tumour by the surgeon. After resection, sensitivity was poor (26%), due to tumour or infiltrated tissue in several biopsies deemed normal by ultrasound, but the specificity was acceptable (88%).

Conclusions

Our study shows that although glioblastomas are well delineated prior to resection, there seem to be overestimation of tumour tissue during resection. After resection tumour remnants and infiltrated brain tissue in the resection cavity wall may be undetected. We believe that the benefits of intraoperative ultrasound outweigh the shortcomings, but users of intraoperative ultrasound should keep the limitations shown in our study in mind.
Literature
1.
go back to reference Albert FK, Forsting M, Sartor K, Adams HP, Kunze S (1994) Early postoperative magnetic resonance imaging after resection of malignant glioma: objective evaluation of residual tumour and its influence on regrowth and prognosis. Neurosurgery 34:45–60 discussion 60–41PubMedCrossRef Albert FK, Forsting M, Sartor K, Adams HP, Kunze S (1994) Early postoperative magnetic resonance imaging after resection of malignant glioma: objective evaluation of residual tumour and its influence on regrowth and prognosis. Neurosurgery 34:45–60 discussion 60–41PubMedCrossRef
2.
go back to reference Burger PC, Heinz ER, Shibata T, Kleihues P (1988) Topographic anatomy and CT correlations in the untreated glioblastoma multiforme. J Neurosurg 68:698–704PubMed Burger PC, Heinz ER, Shibata T, Kleihues P (1988) Topographic anatomy and CT correlations in the untreated glioblastoma multiforme. J Neurosurg 68:698–704PubMed
3.
go back to reference Chacko AG, Kumar NKS, Chacko G, Athyal R, Rajshekhar V (2003) Intraoperative ultrasound in determining the extent of resection of parenchymal brain tumours—a comparative study with computed tomography and histopathology. Acta Neurochirurgica 145:743–748PubMedCrossRef Chacko AG, Kumar NKS, Chacko G, Athyal R, Rajshekhar V (2003) Intraoperative ultrasound in determining the extent of resection of parenchymal brain tumours—a comparative study with computed tomography and histopathology. Acta Neurochirurgica 145:743–748PubMedCrossRef
4.
go back to reference Croteau D, Scarpace L, Hearshen D, Gutierrez J, Fisher JL, Rock JP, Mikkelsen T (2001) Correlation between magnetic resonance spectroscopy imaging and image-guided biopsies: semiquantitative and qualitative histopathological analyses of patients with untreated glioma. Neurosurgery 49:823–829PubMedCrossRef Croteau D, Scarpace L, Hearshen D, Gutierrez J, Fisher JL, Rock JP, Mikkelsen T (2001) Correlation between magnetic resonance spectroscopy imaging and image-guided biopsies: semiquantitative and qualitative histopathological analyses of patients with untreated glioma. Neurosurgery 49:823–829PubMedCrossRef
5.
go back to reference Daumas-Duport C, Monsaigneon V, Blond S, Munari C, Musolino A, Chodkiewicz JP, Missir O (1987) Serial stereotactic biopsies and CT scan in gliomas: correlative study in 100 astrocytomas, oligo-astrocytomas and oligodendrocytomas. J Neurooncol 4:317–328PubMedCrossRef Daumas-Duport C, Monsaigneon V, Blond S, Munari C, Musolino A, Chodkiewicz JP, Missir O (1987) Serial stereotactic biopsies and CT scan in gliomas: correlative study in 100 astrocytomas, oligo-astrocytomas and oligodendrocytomas. J Neurooncol 4:317–328PubMedCrossRef
6.
go back to reference Ganslandt O, Stadlbauer A, Fahlbusch R, Kamada K, Buslei R, Blumcke I, Moser E, Nimsky C (2005) Proton magnetic resonance spectroscopic imaging integrated into image-guided surgery: correlation to standard magnetic resonance imaging and tumor cell density. Neurosurgery 56:291–298 discussion 291–298PubMedCrossRef Ganslandt O, Stadlbauer A, Fahlbusch R, Kamada K, Buslei R, Blumcke I, Moser E, Nimsky C (2005) Proton magnetic resonance spectroscopic imaging integrated into image-guided surgery: correlation to standard magnetic resonance imaging and tumor cell density. Neurosurgery 56:291–298 discussion 291–298PubMedCrossRef
7.
go back to reference Grønningsæter Å, Kleven A, Ommedal S, Årseth TE, Lie T, Lindseth F, Langø T, Unsgård G (2000) SonoWand, an ultrasound-based neuronavigation system. Neurosurgery 47:1373–1380PubMedCrossRef Grønningsæter Å, Kleven A, Ommedal S, Årseth TE, Lie T, Lindseth F, Langø T, Unsgård G (2000) SonoWand, an ultrasound-based neuronavigation system. Neurosurgery 47:1373–1380PubMedCrossRef
8.
go back to reference Hammoud MA, Ligon BL, elSouki R, Shi WM, Schomer DF, Sawaya R (1996) Use of intraoperative ultrasound for localizing tumors and determining the extent of resection: a comparative study with magnetic resonance imaging. J Neurosurg 84:737–741PubMed Hammoud MA, Ligon BL, elSouki R, Shi WM, Schomer DF, Sawaya R (1996) Use of intraoperative ultrasound for localizing tumors and determining the extent of resection: a comparative study with magnetic resonance imaging. J Neurosurg 84:737–741PubMed
9.
go back to reference Hirschberg H, Samset E, Hol PK, Tillung T, Lote K (2005) Impact of intraoperative MRI on the surgical results for high-grade gliomas. Minim Invasive Neurosurg 48:77–84PubMedCrossRef Hirschberg H, Samset E, Hol PK, Tillung T, Lote K (2005) Impact of intraoperative MRI on the surgical results for high-grade gliomas. Minim Invasive Neurosurg 48:77–84PubMedCrossRef
10.
go back to reference Iseki H, Muragaki Y, Nakamura R, Ozawa N, Taniguchi H, Hori T, Takakura K (2005) Intelligent operating theater using intraoperative open-MRI. Magn Reson Med Sci 4:129–136PubMedCrossRef Iseki H, Muragaki Y, Nakamura R, Ozawa N, Taniguchi H, Hori T, Takakura K (2005) Intelligent operating theater using intraoperative open-MRI. Magn Reson Med Sci 4:129–136PubMedCrossRef
11.
go back to reference Katisko JP, Koivukangas JP (2007) Optically neuronavigated ultrasonography in an intraoperative magnetic resonance imaging environment. Neurosurgery 60:373–380 discussion 380–371PubMedCrossRef Katisko JP, Koivukangas JP (2007) Optically neuronavigated ultrasonography in an intraoperative magnetic resonance imaging environment. Neurosurgery 60:373–380 discussion 380–371PubMedCrossRef
12.
go back to reference Kelly PJ, Daumas-Duport C, Scheithauer BW, Kall BA, Kispert DB (1987) Stereotactic histologic correlations of computed tomography- and magnetic resonance imaging-defined abnormalities in patients with glial neoplasms. Mayo Clin Proc 62:450–459PubMed Kelly PJ, Daumas-Duport C, Scheithauer BW, Kall BA, Kispert DB (1987) Stereotactic histologic correlations of computed tomography- and magnetic resonance imaging-defined abnormalities in patients with glial neoplasms. Mayo Clin Proc 62:450–459PubMed
13.
go back to reference Kleihues P, Cavenee WK (eds) (2000) Pathology and genetics of tumours of the nervous system: world health organization classification of tumours. IARC, Lyon Kleihues P, Cavenee WK (eds) (2000) Pathology and genetics of tumours of the nervous system: world health organization classification of tumours. IARC, Lyon
14.
go back to reference Knauth M, Aras N, Wirtz CR, Dorfler A, Engelhorn T, Sartor K (1999) Surgically induced intracranial contrast enhancement: potential source of diagnostic error in intraoperative MR imaging. AJNR Am J Neuroradiol 20:1547–1553PubMed Knauth M, Aras N, Wirtz CR, Dorfler A, Engelhorn T, Sartor K (1999) Surgically induced intracranial contrast enhancement: potential source of diagnostic error in intraoperative MR imaging. AJNR Am J Neuroradiol 20:1547–1553PubMed
15.
go back to reference Koivukangas J, Louhisalmi Y, Alakuijala J, Oikarinen J (1993) Ultrasound-controlled neuronavigator-guided brain surgery. J Neurosurg 79:36–42PubMed Koivukangas J, Louhisalmi Y, Alakuijala J, Oikarinen J (1993) Ultrasound-controlled neuronavigator-guided brain surgery. J Neurosurg 79:36–42PubMed
16.
go back to reference Kracht LW, Miletic H, Busch S, Jacobs AH, Voges J, Hoevels M, Klein JC, Herholz K, Heiss WD (2004) Delineation of brain tumor extent with [11C]l-methionine positron emission tomography: local comparison with stereotactic histopathology. Clin Cancer Res 10:7163–7170PubMedCrossRef Kracht LW, Miletic H, Busch S, Jacobs AH, Voges J, Hoevels M, Klein JC, Herholz K, Heiss WD (2004) Delineation of brain tumor extent with [11C]l-methionine positron emission tomography: local comparison with stereotactic histopathology. Clin Cancer Res 10:7163–7170PubMedCrossRef
17.
go back to reference Lacroix M, Abi-Said D, Fourney DR, Gokaslan ZL, Shi W, DeMonte F, Lang FF, McCutcheon IE, Hassenbusch SJ, Holland E, Hess K, Michael C, Miller D, Sawaya R (2001) A multivariate analysis of 416 patients with glioblastoma multiforme: prognosis, extent of resection, and survival. J Neurosurg 95:190–198PubMed Lacroix M, Abi-Said D, Fourney DR, Gokaslan ZL, Shi W, DeMonte F, Lang FF, McCutcheon IE, Hassenbusch SJ, Holland E, Hess K, Michael C, Miller D, Sawaya R (2001) A multivariate analysis of 416 patients with glioblastoma multiforme: prognosis, extent of resection, and survival. J Neurosurg 95:190–198PubMed
18.
go back to reference LeRoux PD, Winter TC, Berger MS, Mack LA, Wang K, Elliott JP (1994) A comparison between preoperative magnetic resonance and intraoperative ultrasound tumor volumes and margins. J Clin Ultrasound 22:29–36PubMedCrossRef LeRoux PD, Winter TC, Berger MS, Mack LA, Wang K, Elliott JP (1994) A comparison between preoperative magnetic resonance and intraoperative ultrasound tumor volumes and margins. J Clin Ultrasound 22:29–36PubMedCrossRef
19.
go back to reference Letteboer MM, Willems PW, Viergever MA, Niessen WJ (2005) Brain shift estimation in image-guided neurosurgery using 3-D ultrasound. IEEE Trans Biomed Eng 52:268–276PubMedCrossRef Letteboer MM, Willems PW, Viergever MA, Niessen WJ (2005) Brain shift estimation in image-guided neurosurgery using 3-D ultrasound. IEEE Trans Biomed Eng 52:268–276PubMedCrossRef
20.
go back to reference Lindner D, Trantakis C, Renner C, Arnold S, Schmitgen A, Schneider J, Meixensberger J (2006) Application of intraoperative 3D ultrasound during navigated tumor resection. Minim Invasive Neurosurg 49:197–202PubMedCrossRef Lindner D, Trantakis C, Renner C, Arnold S, Schmitgen A, Schneider J, Meixensberger J (2006) Application of intraoperative 3D ultrasound during navigated tumor resection. Minim Invasive Neurosurg 49:197–202PubMedCrossRef
21.
go back to reference Lindseth F, Lango T, Bang J, Nagelhus Hernes TA (2002) Accuracy evaluation of a 3D ultrasound-based neuronavigation system. Comput Aided Surg 7:197–222PubMed Lindseth F, Lango T, Bang J, Nagelhus Hernes TA (2002) Accuracy evaluation of a 3D ultrasound-based neuronavigation system. Comput Aided Surg 7:197–222PubMed
22.
go back to reference Lunsford LD, Martinez AJ, Latchaw RE (1986) Magnetic resonance imaging does not define tumor boundaries. Acta Radiol Suppl 369:154–156PubMed Lunsford LD, Martinez AJ, Latchaw RE (1986) Magnetic resonance imaging does not define tumor boundaries. Acta Radiol Suppl 369:154–156PubMed
23.
go back to reference McKnight TR, von dem Bussche MH, Vigneron DB, Lu Y, Berger MS, McDermott MW, Dillon WP, Graves EE, Pirzkall A, Nelson SJ (2002) Histopathological validation of a three-dimensional magnetic resonance spectroscopy index as a predictor of tumor presence. J Neurosurg 97:794–802PubMed McKnight TR, von dem Bussche MH, Vigneron DB, Lu Y, Berger MS, McDermott MW, Dillon WP, Graves EE, Pirzkall A, Nelson SJ (2002) Histopathological validation of a three-dimensional magnetic resonance spectroscopy index as a predictor of tumor presence. J Neurosurg 97:794–802PubMed
24.
go back to reference Nimsky C, Ganslandt O, Buchfelder M, Fahlbusch R (2006) Intraoperative visualization for resection of gliomas: the role of functional neuronavigation and intraoperative 1.5 T MRI. Neurol Res 28:482–487PubMedCrossRef Nimsky C, Ganslandt O, Buchfelder M, Fahlbusch R (2006) Intraoperative visualization for resection of gliomas: the role of functional neuronavigation and intraoperative 1.5 T MRI. Neurol Res 28:482–487PubMedCrossRef
25.
go back to reference Nimsky C, Ganslandt O, Cerny P, Hastreiter P, Greiner G, Fahlbush R (2000) Quantification of, visulaization of, and compensating for brain shift using intraoperative magnetic resonance imaging. Neurosurgery 47:1070–1080PubMedCrossRef Nimsky C, Ganslandt O, Cerny P, Hastreiter P, Greiner G, Fahlbush R (2000) Quantification of, visulaization of, and compensating for brain shift using intraoperative magnetic resonance imaging. Neurosurgery 47:1070–1080PubMedCrossRef
26.
go back to reference Nimsky C, Ganslandt O, Hastreiter P, Fahlbusch R (2001) Intraoperative compensation for brain shift. Surg Neurol 56:357–364 discussion 364–355PubMedCrossRef Nimsky C, Ganslandt O, Hastreiter P, Fahlbusch R (2001) Intraoperative compensation for brain shift. Surg Neurol 56:357–364 discussion 364–355PubMedCrossRef
27.
go back to reference Nimsky C, Ganslandt O, von Keller B, Romstock J, Fahlbusch R (2004) Intraoperative high-field-strength MR imaging: implementation and experience in 200 patients. Radiology 233:67–78PubMedCrossRef Nimsky C, Ganslandt O, von Keller B, Romstock J, Fahlbusch R (2004) Intraoperative high-field-strength MR imaging: implementation and experience in 200 patients. Radiology 233:67–78PubMedCrossRef
28.
go back to reference Price SJ, Jena R, Burnet NG, Hutchinson PJ, Dean AF, Pena A, Pickard JD, Carpenter TA, Gillard JH (2006) Improved delineation of glioma margins and regions of infiltration with the use of diffusion tensor imaging: an image-guided biopsy study. AJNR Am J Neuroradiol 27:1969–1974PubMed Price SJ, Jena R, Burnet NG, Hutchinson PJ, Dean AF, Pena A, Pickard JD, Carpenter TA, Gillard JH (2006) Improved delineation of glioma margins and regions of infiltration with the use of diffusion tensor imaging: an image-guided biopsy study. AJNR Am J Neuroradiol 27:1969–1974PubMed
29.
go back to reference Reinges MHT, Nguyen HH, Krings T, Hutter BO, Rohde V, Gilsbach JM (2004) Course of brain shift during microsurgical resection of supratentorial cerebral lesions: limits of conventional neuronavigation. Acta Neurochirurgica 146:369–377PubMedCrossRef Reinges MHT, Nguyen HH, Krings T, Hutter BO, Rohde V, Gilsbach JM (2004) Course of brain shift during microsurgical resection of supratentorial cerebral lesions: limits of conventional neuronavigation. Acta Neurochirurgica 146:369–377PubMedCrossRef
30.
go back to reference Rubin JM, Dohrmann GJ (1985) Efficacy of intraoperative US for evaluating intracranial masses. Radiology 157:509–511PubMed Rubin JM, Dohrmann GJ (1985) Efficacy of intraoperative US for evaluating intracranial masses. Radiology 157:509–511PubMed
31.
go back to reference Sergeeva O, Uhlemann F, Schackert G, Hergeth C, Morgenstern U, Steinmeier R (2006) Integration of intraoperative 3D-ultrasound in a commercial navigation system. Zentralbl Neurochir 67:197–203PubMedCrossRef Sergeeva O, Uhlemann F, Schackert G, Hergeth C, Morgenstern U, Steinmeier R (2006) Integration of intraoperative 3D-ultrasound in a commercial navigation system. Zentralbl Neurochir 67:197–203PubMedCrossRef
32.
go back to reference Stadlbauer A, Ganslandt O, Buslei R, Hammen T, Gruber S, Moser E, Buchfelder M, Salomonowitz E, Nimsky C (2006) Gliomas: histopathologic evaluation of changes in directionality and magnitude of water diffusion at diffusion-tensor MR imaging. Radiology 240:803–810PubMedCrossRef Stadlbauer A, Ganslandt O, Buslei R, Hammen T, Gruber S, Moser E, Buchfelder M, Salomonowitz E, Nimsky C (2006) Gliomas: histopathologic evaluation of changes in directionality and magnitude of water diffusion at diffusion-tensor MR imaging. Radiology 240:803–810PubMedCrossRef
33.
go back to reference Steinmeier R, Fahlbusch R, Ganslandt O, Nimsky C, Buchfelder M, Kaus M, Heigl T, Lenz G, Kuth R, Huk W (1998) Intraoperative magnetic resonance imaging with the magnetom open scanner: concepts, neurosurgical indications, and procedures: a preliminary report. Neurosurgery 43:739–747 discussion 747–738PubMedCrossRef Steinmeier R, Fahlbusch R, Ganslandt O, Nimsky C, Buchfelder M, Kaus M, Heigl T, Lenz G, Kuth R, Huk W (1998) Intraoperative magnetic resonance imaging with the magnetom open scanner: concepts, neurosurgical indications, and procedures: a preliminary report. Neurosurgery 43:739–747 discussion 747–738PubMedCrossRef
34.
go back to reference Sutherland GR, Kaibara T, Louw D, Hoult DI, Tomanek B, Saunders J (1999) A mobile high-field magnetic resonance system for neurosurgery. J Neurosurg 91:804–813PubMedCrossRef Sutherland GR, Kaibara T, Louw D, Hoult DI, Tomanek B, Saunders J (1999) A mobile high-field magnetic resonance system for neurosurgery. J Neurosurg 91:804–813PubMedCrossRef
35.
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 51:402–411 discussion 411–402PubMedCrossRef 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 51:402–411 discussion 411–402PubMedCrossRef
36.
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 50:804–812 discussion 812PubMedCrossRef 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 50:804–812 discussion 812PubMedCrossRef
37.
go back to reference Unsgaard G, Rygh OM, Selbekk T, Muller TB, Kolstad F, Lindseth F, Hernes TA (2006) Intra-operative 3D ultrasound in neurosurgery. Acta Neurochir (Wien) 148:235–253CrossRef Unsgaard G, Rygh OM, Selbekk T, Muller TB, Kolstad F, Lindseth F, Hernes TA (2006) Intra-operative 3D ultrasound in neurosurgery. Acta Neurochir (Wien) 148:235–253CrossRef
38.
go back to reference Unsgaard G, Selbekk T, Brostrup Muller T, Ommedal S, Torp SH, Myhr G, Bang J, Nagelhus Hernes TA (2005) Ability of navigated 3D ultrasound to delineate gliomas and metastases–comparison of image interpretations with histopathology. Acta Neurochir (Wien) 147:1259–1269 discussion 1269CrossRef Unsgaard G, Selbekk T, Brostrup Muller T, Ommedal S, Torp SH, Myhr G, Bang J, Nagelhus Hernes TA (2005) Ability of navigated 3D ultrasound to delineate gliomas and metastases–comparison of image interpretations with histopathology. Acta Neurochir (Wien) 147:1259–1269 discussion 1269CrossRef
39.
go back to reference Wirtz CR, Knauth M, Staubert A, Bonsanto MM, Sartor K, Kunze S, Tronnier VM (2000) Clinical evaluation and follow-up results for intraoperative magnetic resonance imaging in neurosurgery. Neurosurgery 46:1112–1120 discussion 1120–1112PubMedCrossRef Wirtz CR, Knauth M, Staubert A, Bonsanto MM, Sartor K, Kunze S, Tronnier VM (2000) Clinical evaluation and follow-up results for intraoperative magnetic resonance imaging in neurosurgery. Neurosurgery 46:1112–1120 discussion 1120–1112PubMedCrossRef
40.
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 (Wien) 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 (Wien) 138:1391–1398CrossRef
Metadata
Title
Comparison of navigated 3D ultrasound findings with histopathology in subsequent phases of glioblastoma resection
Authors
Ola Morten Rygh
Tormod Selbekk
Sverre Helge Torp
Stian Lydersen
Toril Anita Nagelhus Hernes
Geirmund Unsgaard
Publication date
01-10-2008
Publisher
Springer Vienna
Published in
Acta Neurochirurgica / Issue 10/2008
Print ISSN: 0001-6268
Electronic ISSN: 0942-0940
DOI
https://doi.org/10.1007/s00701-008-0017-3

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