International Congress Series 1259 (2004) 389 – 395
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The role of functional neuronavigation in the treatment of lesions in eloquent areas of the brain Jan Klener a,*, Dusan Urgosik b, Jaroslav Tintera c, Josef Vymazal d, Robert Jech e a b
Department of Neurosurgery, Na Homolce Hospital, Roentgenova 2, 150 30, Prague 5, Czech Republic Department of Functional and Stereotactic Neurosurgery, Hospital Na Homolce, Prague, Czech Republic c ZRIR IKEM, Praha, Hospital Na Homolce, Prague, Czech Republic d RDG Department, Hospital Na Homolce, Prague, Czech Republic e Department of Neurology 1.LF UK, Prague, Czech Republic Received 20 September 2003; received in revised form 6 October 2003; accepted 9 October 2003
Abstract. The aim of this paper is to evaluate reliability and the contribution of functional neuronavigation in the operative treatment of lesions located in functionally important areas. Functional neuronavigation consists of co-registration of preoperative functional data into the frameless neuronavigation system and their interactive employment during the neurosurgical procedure. Nineteen patients with neurosurgical targets located in or near the eloquent areas were operated on using functional magnetic resonance imaging (fMRI) and/or electrophysiological functional data intraoperatively. During surgery, all fMRI data were reliably displayed and in spatial correlation with electrophysiological data in patients where both modalities were used. After operation, the neurological deficit remained the same or improved in 17 patients, 1 patient suffered from temporary, and 1 from permanent, worsening of the neurodeficit. Functional neuronavigation is a safe and reliable method of intraoperative localization of the functional areas. This method is complementary to the electrophysiological methods and, in selected cases, could even substitute for them. D 2003 Elsevier B.V. All rights reserved. Keywords: Functional neuronavigation; Functional magnetic resonance imaging; Neuronavigation; Brain mapping
1. Introduction The goal of microneurosurgery of brain tumors and many other lesions is to achieve maximal resection while preserving or improving function. The radicalism of tumor resection correlates with the better survival of patients but in the vicinity of functionally important areas, the risk of new postoperative neurodeficit could be relatively high [1]. In these situations, the pre- and intraoperative information on functional areas is critical. * Corresponding author. Tel./fax: +42-257273091. E-mail address:
[email protected] (J. Klener). 0531-5131/ D 2003 Elsevier B.V. All rights reserved. doi:10.1016/S0531-5131(03)01710-2
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The electrophysiological methods, namely somatosensory-evoked potentials (SSEP) phase reversal and motor-evoked potentials (MEP) stimulation, are considered the gold standard in intraoperative brain mapping [2– 5]. Recently, new, noninvasive methods of preoperative brain mapping are available—functional magnetic resonance imaging (fMRI), magnetoencephalography (MEG) and positron emission tomography (PET) [6– 8]. Co-registration of preoperative functional data into frameless neuronavigation system enables easy preoperative planning and intraoperative, functional, information-directed navigation. Due to relative availability and excellent spatial resolution, fMRI-based functional neuronavigation seems to be a promising tool in contemporary neurosurgical practice [9– 25]. The aim of this paper is to evaluate reliability and the contribution of functional neuronavigation in the operative treatment of lesions located in functionally important areas. 2. Patients and methods A consecutive series of 19 patients with different lesions within or in direct contact with pre-central, post-central or dominant inferior frontal gyrus were studied. There were 11 men and 8 women in the group with different pathological entities: glioblastoma multiforme (6 ) anaplastic astrocytoma (1 ), fibrillary astrocytoma (5 ), mixed oligoastrocytoma (2 ), metastasis (1 ), meningeoma (1 ), and cavernoma (3 ). Twenty procedures were performed on 19 patients; in all of them the frameless neuronavigation system (Stealth Station, Sofamor Danek, Surgical Navigation Technologies, Broomfield) was used, in combination with fMRI (16 patients) and/or SSEP (6 patients) and/or MEP (6 patients). Postoperative functional status was evaluated using standard neurological examination by the independent neurologist. All fMRI measurements were performed using the blood oxygen level-dependent (BOLD) technique with a 1.5 T MRI scanner equipped with a gradient system (Siemens Vison 1.5 T) 1 to 7 days before surgery. Two stimulation paradigms were used: maximal frequency cross finger-tipping (or simple finger movement, where a lower extremity was stimulated), and a verbal fluency test, where the subject generates words that begin with the indicated letter. Image analysis was performed by using the Marki and SPM (Statistical Parametrical Mapping) programs with correlation coefficient, linear model and t-test, and threshold probability ( p = 0.05) correlated for the number of voxels. Data were superimposed with volume 3D data and were loaded into the navigation system in DICOM format. A surgical plan was then made considering the location of the pathological lesion and fMRI activation areas (Fig. 1). Intraoperative SSEP phase reversal measurements were performed using standard transdermal stimulation of n. medinaus at the wrist (rectangle stimulus, width 0.2 ms; rate 4 Hz, intensity 30– 40 mA) and registration by the cortical strip electrode. MEP was recorded using needle electrodes from the thenar muscles after cortical stimulation by the bipolar electrode (intensity 5– 12 mA, 1 ms pulses, rate 20– 50 Hz). After introduction of isoflurane endotracheal anesthesia, three pinhead fixations were applied and virtual image and surgical space were registered using eight standard anatomical points and surface merges. Several scalp points were checked to confirm
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Fig. 1. Surgical plan in left frontal cavernoma case. Safer but longer trajectory (white line) was used due to presence of fMRI-activated area (white voxels) in the cortex nearest to the lesion.
accuracy of the registration. Standard osteoplastic craniotomy was performed and the cerebral cortex exposed. Cortical projection of the tumor and/or the site of the planned corticotomy was identified by visual inspection and neuronavigation; spatial relationship
Fig. 2. Intraoperative snapshot during resection of pre-central fibrillary astrocytoma. Note position of the navigation probe (white cross) on the tumor border near the primary motor area (white voxels).
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Fig. 3. Intraoperative snapshot during resection of post-central glioblastoma. Note position of the navigation probe (white cross) on the tumor border near the primary motor area (white voxels).
to the fMRI-activated areas was established. Electrophysiological SSEP or MEP study was performed in selected patients. After evaluating all available data, the final trajectory was established. Resection was performed by the microsurgical technique, in tumor cases with the aid of an ultrasonic aspirator. After debulking the tumor, the tumor –brain interface was identified in the ‘‘safest’’ area, then the resection proceeded towards the part of the tumor in the vicinity of the functional cortex. Resection was stopped at the tumor border, at the edge of the fMRI-activated area or when an MEP stimulation response occurred (Figs. 2 and 3). After thorough hemostasis, the craniotomy was closed in standard fashion.
Fig. 4. Preoperative (left) and postoperative (right) MRI after gross total resection of pre-central fibrillary astrocytoma.
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3. Results During all surgical procedures the mean registration error was less then 1.5 mm, and both pathological lesions and fMRI-activated areas were reliably identified on the images displayed by the navigation system and accessible by the navigation probe. Location of the pathologic lesions corresponded exactly with neuronavigation, and the fMRI activation areas matched functional areas established by the electrophysiological methods whenever they were performed. In 3 patients with cavernoma and 1 with meningeoma, total removal was achieved; in 13 with neuroepithelial tumors, gross total resection was done; one tumor was resected subtotally, one in first stage, partially and in second stage, gross totally. Radicalism of the resection was examined by early postoperative MRI (Fig. 4). Immediately after operation, 17 patients exhibited improved neurological deficit or remained the same, 2 patients developed worse hemiparesis. Three months after surgery, one patient improved to preoperative level, one remained slightly worse progressing from mild to medium level right upper extremity weakness. One patient with glioblastoma (with postoperative neurological improvement) died of pulmonary embolism, and another patient with recurrent glioblastoma missed the 3-month follow-up. 4. Discussion Focusing on function instead of structure alone is one of the features of contemporary neurosurgery. Established electrophysiological methods of brain mapping (SSEP phase reversal and direct cortical stimulation) helped to prove the accuracy and reliability of new, noninvasive brain mapping methods, namely fMRI, PET and MEG [6– 8]. Incorporation of fMRI functional data into the neuronavigation system enables accurate, intraoperative localization of both pathological lesion and functional areas during surgery, and thus could contribute to better functional results of neurosurgical procedures in eloquent areas [9 – 25]. The main advantages consist of noninvasiveness, high spatial accuracy, minimal intraoperative time consumption, easy use and possibility of preoperative planning. Nonreal time information, brain shift and variability of fMRI activation maps due to different acquisition and post-processing parameters are limits of this method. Several publications dealt with the actual contribution of functional navigation to better surgical results, but small numbers of patients and different study designs prevent fundamental conclusions [9,11,14,15,23– 25]. New trends in this area utilize multimodality functional data and subcortical tract mapping techniques; intraoperative functional imaging will probably be the next step [10 – 12,16,17,20 – 23,26]. 5. Conclusions Functional neuronavigation is technologically demanding, but a noninvasive, easy to use and reliable method of intraoperative localization of functional areas, which enables tailoring neurosurgical procedures to the specific lesion – eloquent area relationship. Although our results and similar studies indicate positive contribution to the functional results of neurosurgical procedures in eloquent areas, a definite role in neurosurgical armamentarium has to be proved by further studies. We conclude that in lower risk
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procedures functional navigation could substitute for electrophysiological methods, but in complex cases the role of both methods is complementary. References [1] M. Ammirati, N. Vick, Y. Liao, I. Ciric, M. Mikhael, Effect of the extent of surgical resection on survival and quality of life in patients with supratentorial glioblastomas and anaplastic astrocytomas, Neurosurgery 21 (1987) 201 – 206. [2] C. Cedzich, M. Taniguchi, S. Schafer, J. Schramm, Somatosensory evoked potential phase reversal and direct motor cortex stimulation in and around the central region, Neurosurgery 38 (1996) 962 – 970. [3] G. McCarthy, T. Allison, D.D. Spencer, Localization of the face area of human sensimotor cortex by intracranial recording of somatosensory evoked potentials, J. Neurosurg. 79 (1993) 874 – 884. [4] T. Kombos, O. Suess, O. Cilkatekerlio, M. Brock, Monitoring of intraoperative evoked potentials to increase the safety of surgery in and around the motor cortex, J. Neurosurg. 95 (2001) 608 – 614. [5] H.H. Zhou, P.J. Kelly, Transcranial electrical motor evoked potential monitoring for brain tumor resection, Neurosurgery 48 (2001) 1075 – 1081. [6] C.R. Jack Jr., R.M. Thompson, R.K. Butts, F.W. Sharbrough, P.J. Kelly, D.P. Hanson, et al, Sensory motor cortex: correlation of presurgical mapping with functional MRI and invasive cortical mapping, Radiology 190 (1994) 85 – 92. [7] W.M. Mueller, F.Z. Yetkin, T.A. Hammeke, G.L. Morris III, S.J. Swanson, K. Reichert, et al, Functional magnetic resonance imaging mapping of the motor cortex in patients with cerebral tumors, Neurosurgery 39 (1996) 515 – 521. [8] A. Puce, R.T. Constable, M.L. Luby, G. McCarthy, A.C. Nobre, D.D. Spencer, Functional magnetic resonance imaging of the sensory and motor cortex: comparison with electrophysiological localization, J. Neurosurg. 83 (1995) 262 – 270. [9] M. Schulder, J.A. Maldjian, W.C. Liu, A.I. Holodny, A.T. Kalnin, I.K. Mun, et al, Functional image guided surgery of intracranial tumors located in or near the sensimotor cortex, J. Neurosurg. 89 (1998) 412 – 418. [10] P. Jannin, X. Morandi, O.J. Fleig, E. Le Rumeur, P. Toulouse, B. Gibaud, et al, Integration of sulcal and functional information for multimodal neuronavigation, J. Neurosurg. 96 (2002) 713 – 723. [11] O. Granslandt, R. Fahlbusch, C. Nimsky, H. Kober, M. Moller, R. Steinmeier, et al, Functional neuronavigation with magnetoencephalography: outcome in 50 patients with lesions around the motor cortex, J. Neurosurg. 91 (1999) 73 – 79. [12] Ch. Nimsky, O. Ganslandt, H. Kober, M. Buchfelder, R. Fahlbusch, Intraoperative magnetic resonance imaging combined with neuronavigation: a new concept, Neurosurgery 48 (2001) 1082 – 1091. [13] H. Liu, W.A. Hall, C.L. Truwit, The roles of functional MRI in MR-guided neurosurgery in a combined 1.5 tesla MR operating room, Acta Neurochir., Suppl. 85 (2003) 127 – 135. [14] I.D. Wilkinson, C.A.J. Romanowski, D.A. Jellinek, J. Morris, P.D. Griffiths, Motor functional MRI for preoperative and intraoperative neurosurgical guidance, Br. J. Radiol. 76 (2003) 98 – 103. [15] H. Gumprecht, G.K. Ebel, D.P. Auer, C.B. Lumanta, Neuronavigation and functional MRI for surgery in patients with lesion in eloquent brain areas, Minim. Invasive Neurosurg. 45 (2002) 151 – 153. [16] T. Krings, H. Foltys, M.H. Reinges, S. Kemeny, V. Rohde, U. Spetzger, et al, Navigated transcranial magnetic stimulation for presurgical planning-correlation with functional MRI, Minim. Invasive Neurosurg. 44 (2001) 234 – 239. [17] K. Kamada, K. Houkin, F. Takeuchi, N. Ischii, J. Ikeda, Y. Sawamura, et al, Visualization of the eloquent motor system by integration of MEG, functional and anisotropic diffusion-weighted MRI in functional neuronavigation, Surg. Neurol. 59 (2003) 353 – 362. [18] T. H.Krings, M.H. Reinges, R. Thiex, J.M. Gilsbach, A. Thron, Functional and diffusion-weighted magnetic resonance images of space-occupying lesions affecting the motor system: imaging the motor cortex and pyramidal tracts, J. Neurosurg. 95 (2001) 816 – 824. [19] W. F.Mo¨ller-Hartmann, T. Krongs, V.A. Coenen, L. Mayfrank, J. Wiedermann, H. Kra¨nzlein, et al, Preoperative assessment of motor cortex and pyramidal tracts in central cavernoma employing functional and diffusion-weighted magnetic resonance imaging, Surg. Neurol. 58 (2002) 302 – 308.
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[20] P. Sabbah, H. Foehrenbach, G. Dutertre, C. Nioche, O. FdeDreuille, N. Bellegou, et al, Multimodal anatomic, functional, and metabolic brain imaging for tumor resection, J. Clin. Imaging 26 (2002) 6 – 12. [21] V. Braun, S. Dempf, R. Tomczak, A. Wunderlich, H. Weller Rrichter, Multimodal cranial neuronavigation: direct integration of functional magnetic resonance imaging and positron emission tomography data, (technical note)Neurosurgery 48 (2001) 1178 – 1182. [22] J.D. McDonald, B.W. Chong, J.D. Lewine, G. Jones, R.B. Burr, P.R. McDonald, et al, Integration of preoperative and intraoperative functional brain mapping in a frameless stereotactic environment for lesions near eloquent cortex, (technical note)J. Neurosurg. 39 (1999) 515 – 521. [23] C. Nimsky, O. Ganslandt, H. Kober, M. Moller, S. Ulmer, B. Tomandl, et al, Integration of functional magnetic imaging supported by magnetoencephalography in functional neuronavigation, Neurosurgery 44 (1999) 1249 – 1256. [24] J. Klener, D. Urgosˇ´ık, J. Tinteˇra, Vyuzˇitı´ funkcˇnı´ magneticke´ resonance v neurochirurgii centra´lnı´ krajiny. Cˇa´st I. Obecne´ principy. Cˇs neurol neurochir, in press. [25] J. Klener, D. Urgosik, J. Tintera, J. Vymazal, R. Jech, Vyuzˇitı´ funkcˇnı´ magneticke´ resonance v neurochirurgii centra´lnı´ krajiny. Cˇa´st II. Funkcˇnı´ neuronavigace-vlastnı´ zkusˇenosti. Cˇs neurol neurochir, in press. [26] S.B. Sobottka, J. Bredow, B. Beuthien-Baumann, G. Reiss, G. Schackert, R. Steinmeier, Comparison of functional brain PET images and intraoperative brain mapping data using image-guided surgery, Comput. Aided Surg. 7 (2002) 317 – 325.