- Email: [email protected]
Intraoperative low-field MR imaging in neurosurgery—experience in 300 patients
International Congress Series 1230 (2001) 235–239
Intraoperative low-field MR imaging in neurosurgery—experience in 300 patients Ch. Nimskya,*, O. Ganslandta, J. Grallaa, B. Tomandlb, H. Koberc, P. Hastreiterc, M. Buchfeldera, R. Fahlbuscha a
Department of Neurosurgery, University Erlangen – Nuremberg, Schwabachanlage 6, 91054 Erlangen, Germany b Division of Neuroradiology, Department of Neurosurgery, University Erlangen – Nuremberg, Schwabachanlage 6, 91054 Erlangen, Germany c Neurocenter, Department of Neurosurgery, University Erlangen – Nuremberg, Schwabachanlage 6, 91054 Erlangen, Germany
Abstract Intraoperative magnetic resonance (MR) imaging was used to evaluate the extent of a resection, mainly in pituitary, brain tumor and epilepsy surgery. This paper summarizes some of our experience gained in 300 patients, which were investigated by intraoperative MR imaging. In addition to MR imaging, functional data from magnetoencephalography and functional magnetic resonance imaging, resulting in so-called functional neuronavigation, were visualized intraoperatively, when lesions near eloquent brain areas were operated on. Both methods could be integrated in our intraoperative setup with a new navigation microscope that could be used at the 5 Gauss line. The combination of both methods offers the possibility to perform more radical resections without additional morbidity. Intraoperative MR imaging serves as quality control to evaluate the extent of a resection, while functional neuronavigation prevents too extensive resections that could result in neurological deficits. D 2001 Elsevier Science B.V. All rights reserved. Keywords: Functional neuronavigation; Intraoperative magnetic resonance imaging; Resection control; Brain shift
*
Corresponding author. Tel.: +49-9131-853-3001; fax: +49-9131-853-4476. E-mail address: [email protected] (Ch. Nimsky).
0531-5131/01/$ – see front matter D 2001 Elsevier Science B.V. All rights reserved. PII: S 0 5 3 1 - 5 1 3 1 ( 0 1 ) 0 0 0 4 7 - 4
236
Ch. Nimsky et al. / International Congress Series 1230 (2001) 235–239
1. Purpose Intraoperative magnetic resonance (MR) imaging has so far been applied to 300 patients. This paper gives an overview of the experience we gained in the last 5 years, summarizing our main indications for intraoperative MR imaging.
2. Methods For intraoperative MR imaging, we used a 0.2 Tesla Magnetom Open scanner (Siemens, Erlangen, Germany), which was placed in a twin-operating theater [2,12]. Craniotomy procedures were performed in a conventional operating theater, because microscope-based neuronavigation using the MKM microscope (Zeiss, Oberkochen, Germany) was incompatible with the magnetic field. For intraoperative imaging, the patient was moved a 5-m distance into the scanner. Transsphenoidal surgery, catheter placements, and recently, craniotomy procedures as well, using a new navigation microscope (NC4, Zeiss) were performed in the fringe field of the scanner, the patient lying on the movable table of the MR scanner, the head near the 5 Gauss line. For imaging, the MR table slid into the center of the scanner in less than half a minute [11]. In glioma and epilepsy surgery, the extent of the resection was evaluated using a T1weighted 3-D-FLASH gradient echo sequence (FLASH, fast low angle shot; TE, 7.0 ms; TR, 16.1 ms; flip angle, 30°; slab, 168 mm; 112 slices; FOV, 250 mm; matrix, 256 256), which allowed multiplanar reformatting. These data could also be used for an intraoperative update of the neuronavigation system, if tumor remnants had to be localized. Additionally, in certain cases (e.g. in low-grade glioma) 2-dimensional T2-weighted and inversion recovery sequences were applied. MR contrast agent (20 ml Gadolinium – DTPA, intravenously), which was given just prior to scanning, was administered if the tumor showed enhancement in the preoperative images. For imaging of pituitary tumors in transsphenoidal surgery, coronal and sagittal T1-weighted spin echo sequences (slice thickness, 3 mm; TR, 340 ms; TE, 26 ms; FOV, 200 mm; matrix, 192 256) were measured. Optionally, a T2-weighted turbo-spin echo sequence (slice thickness, 3 mm; TR, 5700 ms; TE, 117 ms; FOV, 230 mm; matrix, 224 256) was applied. Anatomical microscope-based neuronavigation was established on the identical 3-DFLASH sequence. In tumors adjacent to eloquent brain areas, functional data from magnetoencephalography (MAGNES II, Biomagnetic Technologies, San Diego, USA) or functional MR imaging (1.5 Tesla Magnetom Symphony, Siemens) were integrated into the navigational setup [3,4,7 –9].
3. Results A total of 300 patients were investigated with intraoperative MR imaging. There were no complications due to intraoperative imaging. The complication rate, with respect to wound healing and rebleeding did not differ from the regular numbers in our department (1.2% of the glioma patients). Our main applications for intraoperative imaging were in:
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transsphenoidal surgery, glioma surgery, and epilepsy surgery, where the results are detailed below. Besides these main indications, intraoperative MR imaging was used for resection control in ventricular tumor surgery, other intra-axial brain lesions, and to control the placements of electrodes and catheters. 3.1. Transsphenoidal surgery 50 patients with large intra- and suprasellar, mainly hormonally inactive pituitary tumors (44 adenomas, six craniopharyngiomas) were operated by a transsphenoidal approach. In 72% of these 50 patients, intraoperative MR imaging allowed an ultra-early evaluation of tumor resection, which is normally only possible 2 – 3 months after surgery. A second look (n = 24) for suspected tumor remnants in the adenoma patients led to further resection in 15 patients (34%). However, there were some challenges of image artifacts caused by metal debris from drilling or by a blood accumulation in the resection cavity. Intraoperative MR imaging undoubtedly offered the option of a second look within the same surgical procedure if incomplete tumor resection was suspected. Thus, the rate of procedures during which complete tumor removal was being achieved could be improved. Furthermore, additional treatments for those with incomplete tumor removal could be planned in an early stage, namely, just after surgery. 3.2. Glioma surgery In 83 glioma patients, intraoperative MR imaging revealed incomplete tumor removal in 63%. In 21 patients, i.e. in 40% (21 out of 52) of the patients with incomplete resection, the resection was extended and further tumor resected based on the results of intraoperative MR scanning. This could increase the rate of gross total removal in the WHO grade I astrocytoma (n = 17), from 82% to 94%. In the grade II astrocytoma (n = 25), further tumor removal was performed in 12 patients. In seven of them, a finally complete removal could be achieved. Thus, the gross total removal rate in grade II astrocytomas increased from 24% to 52%. In the remaining five patients, despite further tumor removal, complete resection was not possible due to small tumor remnants infiltrating eloquent brain areas. In the high-grade astrocytomas, the extent of resection was enlarged in seven patients, resulting in an increased removal rate of 50% vs. 37% in the grade III, and 28% vs. 20% in the grade IV patients. In eight of the low-grade gliomas (WHO grade I and II), the resection could not be extended primarily, because eloquent brain areas were infiltrated. In the majority (23 out of 30) of the high-grade gliomas, where intraoperative imaging had depicted incomplete removal, it was the policy above all to avoid new neurological deficits. While it was sometimes difficult to depict the completeness of a resection in the T1weighted 3-D-FLASH-images, especially in the grade II gliomas, in all of these cases, the inversion recovery and dark fluid sequences were of supplementary value in the evaluation of tumor resection. On the other hand, application of contrast media in the high-grade gliomas often resulted in difficulties in image interpretation, due to contrast media leakage and spreading into the borderline of the resection cavity (in 14 out of the 41). The comparison with preoperative scans, which were measured in the same fashion,
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and which were displayed along the intraoperative images, provided valuable information for image interpretation. We used functional neuronavigation if the tumor was located near eloquent areas to preserve neurological function. With the combined usage of intraoperative MR imaging and functional neuronavigation, we encountered an aggravation of the neurological deficit in only one patient of this subgroup. Anatomical and functional neuronavigation were used as guides to identify relevant structures. Intraoperative MR imaging allowed a delineation of the extent of the resection, so that the combination of both, allowed the maximum possible resection with least neurological deficits, while taking incomplete tumor removal into account when eloquent brain areas were infiltrated. 3.3. Epilepsy surgery In 64 patients suffering from pharmaco-resistant epilepsy, intraoperative MR imaging was used to assess whether a resection or disconnection procedure was tailored to the individual needs of the patient, thus ideally meeting the treatment plan and enhancing the efficiency of the procedure. In the nonlesional cases (n = 32) the extent of the tailored temporal resection (n = 28) or callosotomy (n = 4) could be exactly documented. In the 29 lesional cases, complete resection was primarily proved in 23 patients. In three glioma patients, a lesion that extended into eloquent areas did not allow complete removal. A second look (n = 3) could increase the rate of total resection in the lesional cases from 79% to 90%. Increased knowledge of structure – function relationships, as partially defined by intraoperative imaging, may reduce the adverse neuropsychological sequels of epilepsy surgery in the future [1]. 3.4. Intraoperative image update In a series of 16 brain tumor patients, we used intraoperative MR imaging to perform an intraoperative update of the neuronavigation system. In all cases, updating of the neuronavigation system with the intraoperative MR data was successful. It led to reliable neuronavigation with high accuracy, the mean registration error of the update procedure was 1.1 mm. In all patients, the area suspicious for remaining tumor was reached and further tumor could be resected, resulting in complete tumor removal in 14 patients. In the remaining patients, an extension of the tumor into eloquent brain areas prevented a macroscopic complete excision. The update of a neuronavigation system with intraoperative MR images compensated for the effects of brain shift reliably [5,6,10,13].
4. Conclusion Up to our current experience, we consider indications of intraoperative MR imaging in the surgical treatment of gliomas, especially low-grade gliomas, ventricular tumors, epilepsy and complicated pituitary tumors. Furthermore, intraoperative MR imaging could be used to compensate for the effects of brain shift, if in complicated cases, tumor remnants were to be localized in the surgical field and ongoing neuronavigational
Ch. Nimsky et al. / International Congress Series 1230 (2001) 235–239
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guidance was needed. Intraoperative MR imaging allows a reliable evaluation of the extent of a resection. Tumor removal can be completed by a second look during the same surgical procedure, increasing the radicality. The integrated use of functional neuronavigation helps to lower the morbidity, especially in the surgery of tumors in eloquent brain areas.
References [1] M. Buchfelder, O. Ganslandt, R. Fahlbusch, C. Nimsky, Intraoperative magnetic resonance imaging in epilepsy surgery, J. Magn. Reson. Imaging 12 (2000) 547 – 555. [2] R. Fahlbusch, T. Heigl, W. Huk, R. Steinmeier, The role of endoscopy and intraoperative MRI in transsphenoidal pituitary surgery, in: v.K. Werder, R. Fahlbusch (Eds.), Pituitary Adenomas. From Basic Research to Diagnosis and Therapy, Elsevier, Amsterdam, 1996, pp. 237 – 241. [3] O. Ganslandt, R. Fahlbusch, C. Nimsky, H. Kober, M. Mo¨ller, R. Steinmeier, et al., Functional neuronavigation with magnetoencephalography: outcome in 50 patients with lesions around the motor cortex, J. Neurosurg. 91 (1) (1999) 73 – 79. [4] O. Ganslandt, R. Steinmeier, H. Kober, J. Vieth, J. Kassubek, J. Romsto¨ck, et al., Magnetic source imaging combined with image-guided frameless stereotaxy: a new method in surgery around the motor strip, Neurosurgery 41 (3) (1997) 621 – 628. [5] P. Hastreiter, C. Rezk-Salama, C. Nimsky, C. Lu¨rig, G. Greiner, T. Ertl, Registration techniques for the analysis of the brain shift in neurosurgery, Comput. Graphics 24 (3) (2000) 385 – 389. [6] C. Lu¨rig, P. Hastreiter, C. Nimsky, T. Ertl, Analysis and visualization of the brain shift phenomenon in neurosurgery, in: E. Gro¨ller, H. Lo¨ffelmann, W. Ribarsky (Eds.), Data Visualization ’99, Springer, Berlin, 1999, pp. 285 – 289. [7] H. Kober, P. Grummich, J. Vieth, Fit of the digitized head surface with the surface reconstructed from MRI tomography, in: C. Baumgartner (Ed.), Biomagnetism: Fundamental Research and Clinical Applications, Elsevier, Amsterdam, 1995, pp. 309 – 312. [8] M. Mo¨ller, H. Kober, O. Ganslandt, C. Nimsky, J. Vieth, R. Fahlbusch, Functional mapping of speech evoked brain activity by magnetoencephalography and its clinical application, Biomed. Tech. (Berl) 44 (1999) 159 – 161 (Suppl.). [9] C. Nimsky, O. Ganslandt, H. Kober, M. Mo¨ller, S. Ulmer, B. Tomandl, et al., Integration of functional magnetic resonance imaging supported by magnetoencephalography in functional neuronavigation, Neurosurgery 44 (1999) 1249 – 1256. [10] C. Nimsky, O. Ganslandt, S. Cerny, P. Hastreiter, G. Greiner, R. Fahlbusch, Quantification of, visualization of, and compensation for brain shift using intraoperative magnetic resonance imaging, Neurosurgery 47 (2000) 1070 – 1080. [11] C. Nimsky, O. Ganslandt, H. Kober, M. Buchfelder, R. Fahlbusch, Intraoperative magnetic resonance imaging combined with neuronavigation — a new concept, Neurosurgery 48 (5) (2001) (in press). [12] R. Steinmeier, R. Fahlbusch, O. Ganslandt, C. Nimsky, M. Buchfelder, M. Kaus, et al., Intraoperative magnetic resonance imaging with the magnetom open scanner: concepts, neurosurgical indications, and procedures. A preliminary report, Neurosurgery 43 (4) (1998) 739 – 748. [13] M. Wolf, T. Vogel, P. Weierich, H. Niemann, C. Nimsky, Automatic transfer of pre-operation fMRI markers into intra-operation MR-images for updating functional neuronavigation, in: K. Ikeuchi (Ed.), Proceedings of IAPR Workshop on Machine Vision Applications, MVA2000. Tokyo: University of Tokyo, 2000, pp. 405 – 408.
Intraoperative low-field MR imaging in neurosurgery—experience in 300 patients Ch. Nimskya,*, O. Ganslandta, J. Grallaa, B. Tomandlb, H. Koberc, P. Hastreiterc, M. Buchfeldera, R. Fahlbuscha a
Department of Neurosurgery, University Erlangen – Nuremberg, Schwabachanlage 6, 91054 Erlangen, Germany b Division of Neuroradiology, Department of Neurosurgery, University Erlangen – Nuremberg, Schwabachanlage 6, 91054 Erlangen, Germany c Neurocenter, Department of Neurosurgery, University Erlangen – Nuremberg, Schwabachanlage 6, 91054 Erlangen, Germany
Abstract Intraoperative magnetic resonance (MR) imaging was used to evaluate the extent of a resection, mainly in pituitary, brain tumor and epilepsy surgery. This paper summarizes some of our experience gained in 300 patients, which were investigated by intraoperative MR imaging. In addition to MR imaging, functional data from magnetoencephalography and functional magnetic resonance imaging, resulting in so-called functional neuronavigation, were visualized intraoperatively, when lesions near eloquent brain areas were operated on. Both methods could be integrated in our intraoperative setup with a new navigation microscope that could be used at the 5 Gauss line. The combination of both methods offers the possibility to perform more radical resections without additional morbidity. Intraoperative MR imaging serves as quality control to evaluate the extent of a resection, while functional neuronavigation prevents too extensive resections that could result in neurological deficits. D 2001 Elsevier Science B.V. All rights reserved. Keywords: Functional neuronavigation; Intraoperative magnetic resonance imaging; Resection control; Brain shift
*
Corresponding author. Tel.: +49-9131-853-3001; fax: +49-9131-853-4476. E-mail address: [email protected] (Ch. Nimsky).
0531-5131/01/$ – see front matter D 2001 Elsevier Science B.V. All rights reserved. PII: S 0 5 3 1 - 5 1 3 1 ( 0 1 ) 0 0 0 4 7 - 4
236
Ch. Nimsky et al. / International Congress Series 1230 (2001) 235–239
1. Purpose Intraoperative magnetic resonance (MR) imaging has so far been applied to 300 patients. This paper gives an overview of the experience we gained in the last 5 years, summarizing our main indications for intraoperative MR imaging.
2. Methods For intraoperative MR imaging, we used a 0.2 Tesla Magnetom Open scanner (Siemens, Erlangen, Germany), which was placed in a twin-operating theater [2,12]. Craniotomy procedures were performed in a conventional operating theater, because microscope-based neuronavigation using the MKM microscope (Zeiss, Oberkochen, Germany) was incompatible with the magnetic field. For intraoperative imaging, the patient was moved a 5-m distance into the scanner. Transsphenoidal surgery, catheter placements, and recently, craniotomy procedures as well, using a new navigation microscope (NC4, Zeiss) were performed in the fringe field of the scanner, the patient lying on the movable table of the MR scanner, the head near the 5 Gauss line. For imaging, the MR table slid into the center of the scanner in less than half a minute [11]. In glioma and epilepsy surgery, the extent of the resection was evaluated using a T1weighted 3-D-FLASH gradient echo sequence (FLASH, fast low angle shot; TE, 7.0 ms; TR, 16.1 ms; flip angle, 30°; slab, 168 mm; 112 slices; FOV, 250 mm; matrix, 256 256), which allowed multiplanar reformatting. These data could also be used for an intraoperative update of the neuronavigation system, if tumor remnants had to be localized. Additionally, in certain cases (e.g. in low-grade glioma) 2-dimensional T2-weighted and inversion recovery sequences were applied. MR contrast agent (20 ml Gadolinium – DTPA, intravenously), which was given just prior to scanning, was administered if the tumor showed enhancement in the preoperative images. For imaging of pituitary tumors in transsphenoidal surgery, coronal and sagittal T1-weighted spin echo sequences (slice thickness, 3 mm; TR, 340 ms; TE, 26 ms; FOV, 200 mm; matrix, 192 256) were measured. Optionally, a T2-weighted turbo-spin echo sequence (slice thickness, 3 mm; TR, 5700 ms; TE, 117 ms; FOV, 230 mm; matrix, 224 256) was applied. Anatomical microscope-based neuronavigation was established on the identical 3-DFLASH sequence. In tumors adjacent to eloquent brain areas, functional data from magnetoencephalography (MAGNES II, Biomagnetic Technologies, San Diego, USA) or functional MR imaging (1.5 Tesla Magnetom Symphony, Siemens) were integrated into the navigational setup [3,4,7 –9].
3. Results A total of 300 patients were investigated with intraoperative MR imaging. There were no complications due to intraoperative imaging. The complication rate, with respect to wound healing and rebleeding did not differ from the regular numbers in our department (1.2% of the glioma patients). Our main applications for intraoperative imaging were in:
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transsphenoidal surgery, glioma surgery, and epilepsy surgery, where the results are detailed below. Besides these main indications, intraoperative MR imaging was used for resection control in ventricular tumor surgery, other intra-axial brain lesions, and to control the placements of electrodes and catheters. 3.1. Transsphenoidal surgery 50 patients with large intra- and suprasellar, mainly hormonally inactive pituitary tumors (44 adenomas, six craniopharyngiomas) were operated by a transsphenoidal approach. In 72% of these 50 patients, intraoperative MR imaging allowed an ultra-early evaluation of tumor resection, which is normally only possible 2 – 3 months after surgery. A second look (n = 24) for suspected tumor remnants in the adenoma patients led to further resection in 15 patients (34%). However, there were some challenges of image artifacts caused by metal debris from drilling or by a blood accumulation in the resection cavity. Intraoperative MR imaging undoubtedly offered the option of a second look within the same surgical procedure if incomplete tumor resection was suspected. Thus, the rate of procedures during which complete tumor removal was being achieved could be improved. Furthermore, additional treatments for those with incomplete tumor removal could be planned in an early stage, namely, just after surgery. 3.2. Glioma surgery In 83 glioma patients, intraoperative MR imaging revealed incomplete tumor removal in 63%. In 21 patients, i.e. in 40% (21 out of 52) of the patients with incomplete resection, the resection was extended and further tumor resected based on the results of intraoperative MR scanning. This could increase the rate of gross total removal in the WHO grade I astrocytoma (n = 17), from 82% to 94%. In the grade II astrocytoma (n = 25), further tumor removal was performed in 12 patients. In seven of them, a finally complete removal could be achieved. Thus, the gross total removal rate in grade II astrocytomas increased from 24% to 52%. In the remaining five patients, despite further tumor removal, complete resection was not possible due to small tumor remnants infiltrating eloquent brain areas. In the high-grade astrocytomas, the extent of resection was enlarged in seven patients, resulting in an increased removal rate of 50% vs. 37% in the grade III, and 28% vs. 20% in the grade IV patients. In eight of the low-grade gliomas (WHO grade I and II), the resection could not be extended primarily, because eloquent brain areas were infiltrated. In the majority (23 out of 30) of the high-grade gliomas, where intraoperative imaging had depicted incomplete removal, it was the policy above all to avoid new neurological deficits. While it was sometimes difficult to depict the completeness of a resection in the T1weighted 3-D-FLASH-images, especially in the grade II gliomas, in all of these cases, the inversion recovery and dark fluid sequences were of supplementary value in the evaluation of tumor resection. On the other hand, application of contrast media in the high-grade gliomas often resulted in difficulties in image interpretation, due to contrast media leakage and spreading into the borderline of the resection cavity (in 14 out of the 41). The comparison with preoperative scans, which were measured in the same fashion,
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and which were displayed along the intraoperative images, provided valuable information for image interpretation. We used functional neuronavigation if the tumor was located near eloquent areas to preserve neurological function. With the combined usage of intraoperative MR imaging and functional neuronavigation, we encountered an aggravation of the neurological deficit in only one patient of this subgroup. Anatomical and functional neuronavigation were used as guides to identify relevant structures. Intraoperative MR imaging allowed a delineation of the extent of the resection, so that the combination of both, allowed the maximum possible resection with least neurological deficits, while taking incomplete tumor removal into account when eloquent brain areas were infiltrated. 3.3. Epilepsy surgery In 64 patients suffering from pharmaco-resistant epilepsy, intraoperative MR imaging was used to assess whether a resection or disconnection procedure was tailored to the individual needs of the patient, thus ideally meeting the treatment plan and enhancing the efficiency of the procedure. In the nonlesional cases (n = 32) the extent of the tailored temporal resection (n = 28) or callosotomy (n = 4) could be exactly documented. In the 29 lesional cases, complete resection was primarily proved in 23 patients. In three glioma patients, a lesion that extended into eloquent areas did not allow complete removal. A second look (n = 3) could increase the rate of total resection in the lesional cases from 79% to 90%. Increased knowledge of structure – function relationships, as partially defined by intraoperative imaging, may reduce the adverse neuropsychological sequels of epilepsy surgery in the future [1]. 3.4. Intraoperative image update In a series of 16 brain tumor patients, we used intraoperative MR imaging to perform an intraoperative update of the neuronavigation system. In all cases, updating of the neuronavigation system with the intraoperative MR data was successful. It led to reliable neuronavigation with high accuracy, the mean registration error of the update procedure was 1.1 mm. In all patients, the area suspicious for remaining tumor was reached and further tumor could be resected, resulting in complete tumor removal in 14 patients. In the remaining patients, an extension of the tumor into eloquent brain areas prevented a macroscopic complete excision. The update of a neuronavigation system with intraoperative MR images compensated for the effects of brain shift reliably [5,6,10,13].
4. Conclusion Up to our current experience, we consider indications of intraoperative MR imaging in the surgical treatment of gliomas, especially low-grade gliomas, ventricular tumors, epilepsy and complicated pituitary tumors. Furthermore, intraoperative MR imaging could be used to compensate for the effects of brain shift, if in complicated cases, tumor remnants were to be localized in the surgical field and ongoing neuronavigational
Ch. Nimsky et al. / International Congress Series 1230 (2001) 235–239
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guidance was needed. Intraoperative MR imaging allows a reliable evaluation of the extent of a resection. Tumor removal can be completed by a second look during the same surgical procedure, increasing the radicality. The integrated use of functional neuronavigation helps to lower the morbidity, especially in the surgery of tumors in eloquent brain areas.
References [1] M. Buchfelder, O. Ganslandt, R. Fahlbusch, C. Nimsky, Intraoperative magnetic resonance imaging in epilepsy surgery, J. Magn. Reson. Imaging 12 (2000) 547 – 555. [2] R. Fahlbusch, T. Heigl, W. Huk, R. Steinmeier, The role of endoscopy and intraoperative MRI in transsphenoidal pituitary surgery, in: v.K. Werder, R. Fahlbusch (Eds.), Pituitary Adenomas. From Basic Research to Diagnosis and Therapy, Elsevier, Amsterdam, 1996, pp. 237 – 241. [3] O. Ganslandt, R. Fahlbusch, C. Nimsky, H. Kober, M. Mo¨ller, R. Steinmeier, et al., Functional neuronavigation with magnetoencephalography: outcome in 50 patients with lesions around the motor cortex, J. Neurosurg. 91 (1) (1999) 73 – 79. [4] O. Ganslandt, R. Steinmeier, H. Kober, J. Vieth, J. Kassubek, J. Romsto¨ck, et al., Magnetic source imaging combined with image-guided frameless stereotaxy: a new method in surgery around the motor strip, Neurosurgery 41 (3) (1997) 621 – 628. [5] P. Hastreiter, C. Rezk-Salama, C. Nimsky, C. Lu¨rig, G. Greiner, T. Ertl, Registration techniques for the analysis of the brain shift in neurosurgery, Comput. Graphics 24 (3) (2000) 385 – 389. [6] C. Lu¨rig, P. Hastreiter, C. Nimsky, T. Ertl, Analysis and visualization of the brain shift phenomenon in neurosurgery, in: E. Gro¨ller, H. Lo¨ffelmann, W. Ribarsky (Eds.), Data Visualization ’99, Springer, Berlin, 1999, pp. 285 – 289. [7] H. Kober, P. Grummich, J. Vieth, Fit of the digitized head surface with the surface reconstructed from MRI tomography, in: C. Baumgartner (Ed.), Biomagnetism: Fundamental Research and Clinical Applications, Elsevier, Amsterdam, 1995, pp. 309 – 312. [8] M. Mo¨ller, H. Kober, O. Ganslandt, C. Nimsky, J. Vieth, R. Fahlbusch, Functional mapping of speech evoked brain activity by magnetoencephalography and its clinical application, Biomed. Tech. (Berl) 44 (1999) 159 – 161 (Suppl.). [9] C. Nimsky, O. Ganslandt, H. Kober, M. Mo¨ller, S. Ulmer, B. Tomandl, et al., Integration of functional magnetic resonance imaging supported by magnetoencephalography in functional neuronavigation, Neurosurgery 44 (1999) 1249 – 1256. [10] C. Nimsky, O. Ganslandt, S. Cerny, P. Hastreiter, G. Greiner, R. Fahlbusch, Quantification of, visualization of, and compensation for brain shift using intraoperative magnetic resonance imaging, Neurosurgery 47 (2000) 1070 – 1080. [11] C. Nimsky, O. Ganslandt, H. Kober, M. Buchfelder, R. Fahlbusch, Intraoperative magnetic resonance imaging combined with neuronavigation — a new concept, Neurosurgery 48 (5) (2001) (in press). [12] R. Steinmeier, R. Fahlbusch, O. Ganslandt, C. Nimsky, M. Buchfelder, M. Kaus, et al., Intraoperative magnetic resonance imaging with the magnetom open scanner: concepts, neurosurgical indications, and procedures. A preliminary report, Neurosurgery 43 (4) (1998) 739 – 748. [13] M. Wolf, T. Vogel, P. Weierich, H. Niemann, C. Nimsky, Automatic transfer of pre-operation fMRI markers into intra-operation MR-images for updating functional neuronavigation, in: K. Ikeuchi (Ed.), Proceedings of IAPR Workshop on Machine Vision Applications, MVA2000. Tokyo: University of Tokyo, 2000, pp. 405 – 408.