Integration of functional neuronavigation and intraoperative MRI in surgery for drug-resistant extratemporal epilepsy close to eloquent brain areas.

OBJECT The authors performed a retrospective study to assess the impact of functional neuronavigation and intraoperative MRI (iMRI) on surgery of extratemporal epileptogenic lesions on postsurgical morbidity and seizure control. METHODS Twenty-five patients (14 females and 11 males) underwent extratemporal resections for drug-resistant epilepsy close to speech/motor brain areas or adjacent to white matter tracts. The mean age at surgery was 34 years (range 12-67 years). The preoperative mean disease duration was 13.2 years. To avoid awake craniotomy, cortical motor-sensory representation was mapped during preoperative evaluation in 14 patients and speech representation was mapped in 15 patients using functional MRI. In addition, visualization of the pyramidal tract was performed in 11 patients, of the arcuate fascicle in 7 patients, and of the visual tract in 6 patients using diffusion tensor imaging. The mean minimum distance of tailored resection between the eloquent brain areas was 5.6 mm. During surgery, blood oxygen level-dependent imaging and diffusion tensor imaging data were integrated into neuronavigation and displayed through the operating microscope. The postoperative mean follow-up was 44.2 months. RESULTS In 20% of these patients, further intraoperative resection was performed because of intraoperatively documented residual lesions according to iMRI findings. At the end of resection, the final iMRI scans confirmed achievement of total resection of the putative epileptogenic lesion in all patients. Postoperatively, transient complications and permanent complications were observed in 20% and 12% of patients, respectively. Favorable postoperative seizure control (Engel Classes I and II) was achieved in 84% and seizure freedom in 72% of these consecutive surgical patients. CONCLUSIONS By using functional neuronavigation and iMRI for treatment of epileptogenic brain lesions, the authors achieved a maximum extent of resection despite the lesions' proximity to eloquent brain cortex and fiber tracts in all cases. The authors' results underline possible benefits of this technique leading to a favorable seizure outcome with acceptable neurological deficit rates in difficult-to-treat extratemporal epilepsy.

[1]  Maria Thom,et al.  The clinicopathologic spectrum of focal cortical dysplasias: A consensus classification proposed by an ad hoc Task Force of the ILAE Diagnostic Methods Commission 1 , 2011, Epilepsia.

[2]  Daniel M. Branco,et al.  Integrated image‐ and function‐guided surgery in eloquent cortex: a technique report , 2006, The international journal of medical robotics + computer assisted surgery : MRCAS.

[3]  J. Britton,et al.  Long-term outcome of epilepsy surgery among 399 patients with nonlesional seizure foci including mesial temporal lobe sclerosis. , 2006, Journal of neurosurgery.

[4]  A. Ebner,et al.  OUTCOME OF EXTRATEMPORAL EPILEPSY SURGERY EXPERIENCE OF A SINGLE CENTER , 2008, Neurosurgery.

[5]  D. Cho,et al.  Application of neuronavigator coupled with an operative microscope and electrocorticography in epilepsy surgery. , 2005, Surgical neurology.

[6]  J. Rutka,et al.  Corpus callosotomy in children with intractable epilepsy using frameless stereotactic neuronavigation: 12-year experience at the Hospital for Sick Children in Toronto. , 2008, Neurosurgical focus.

[7]  K. M. Oliveira,et al.  Outcome of fully awake craniotomy for lesions near the eloquent cortex: analysis of a prospective surgical series of 79 supratentorial primary brain tumors with long follow-up , 2009, Acta Neurochirurgica.

[8]  W. Bingaman,et al.  Surgical pathologic findings of extratemporal-based intractable epilepsy: a study of 133 consecutive resections. , 2000, Archives of pathology & laboratory medicine.

[9]  R. L. Kutsy,et al.  Focal extratemporal epilepsy: clinical features, EEG patterns, and surgical approach , 1999, Journal of the Neurological Sciences.

[10]  Amir Reza Tahamtan,et al.  Evaluation of preoperative high magnetic field motor functional MRI (3 Tesla) in glioma patients by navigated electrocortical stimulation and postoperative outcome , 2005, Journal of Neurology, Neurosurgery & Psychiatry.

[11]  G. Jackson,et al.  Long‐term seizure outcome and risk factors for recurrence after extratemporal epilepsy surgery , 2012, Epilepsia.

[12]  Jerome Engel,et al.  Outcome with respect to epileptic seizures. , 1993 .

[13]  J. Girvin,et al.  Epilepsy surgery involving the sensory-motor cortex. , 2006, Brain : a journal of neurology.

[14]  C. Elger,et al.  Insular lesionectomy for refractory epilepsy: management and outcome. , 2008, Brain : a journal of neurology.

[15]  A. Mahapatra,et al.  Awake craniotomy versus surgery under general anesthesia for resection of intrinsic lesions of eloquent cortex—A prospective randomised study , 2007, Clinical Neurology and Neurosurgery.

[16]  K. Radhakrishnan,et al.  Selection of ideal candidates for extratemporal resective epilepsy surgery in a country with limited resources , 2010, Epileptic disorders : international epilepsy journal with videotape.

[17]  O Ganslandt,et al.  Localisation of the sensorimotor cortex during surgery for brain tumours: feasibility and waveform patterns of somatosensory evoked potentials , 2002, Journal of neurology, neurosurgery, and psychiatry.

[18]  Mark Richardson,et al.  Current themes in neuroimaging of epilepsy: Brain networks, dynamic phenomena, and clinical relevance , 2010, Clinical Neurophysiology.

[19]  G. Ojemann,et al.  Interictal, unifocal spikes in refractory extratemporal epilepsy predict ictal origin and postsurgical outcome , 2000, Clinical Neurophysiology.

[20]  A. Cukiert,et al.  Results of Surgery in Patients with Refractory Extratemporal Epilepsy with Normal or Nonlocalizing Magnetic Resonance Findings Investigated with Subdural Grids , 2001, Epilepsia.

[21]  Volker Seifert,et al.  Intraoperative MRI guidance and extent of resection in glioma surgery: a randomised, controlled trial. , 2011, The Lancet. Oncology.

[22]  D W Roberts,et al.  Medically Intractable, Localization‐related Epilepsy with Normal MRI: Presurgical Evaluation and Surgical Outcome in 43 Patients , 2001, Epilepsia.

[23]  Christopher Nimsky,et al.  Intraoperative visualization of the pyramidal tract by diffusion-tensor-imaging-based fiber tracking , 2006, NeuroImage.

[24]  C. Matula,et al.  Frameless stereotactic lesion contour-guided surgery using a computer-navigated microscope. , 1998, Surgical neurology.

[25]  Dong Wang,et al.  Intraoperative MRI with integrated functional neuronavigation-guided resection of supratentorial cavernous malformations in eloquent brain areas , 2011, Journal of Clinical Neuroscience.

[26]  H. Urbach,et al.  Surgical treatment of parietal lobe epilepsy. , 2009, Journal of neurosurgery.

[27]  Extratemporal resective surgery for epilepsy. , 1993, Neurosurgery clinics of North America.

[28]  S. Roper Surgical treatment of the extratemporal epilepsies , 2009, Epilepsia.

[29]  Samuel Wiebe,et al.  Surgical outcomes in lesional and non-lesional epilepsy: A systematic review and meta-analysis , 2010, Epilepsy Research.

[30]  Walter A Hall,et al.  Intraoperative MR‐guided neurosurgery , 2008, Journal of magnetic resonance imaging : JMRI.

[31]  M. Brodie,et al.  Definition of drug resistant epilepsy: Consensus proposal by the ad hoc Task Force of the ILAE Commission on Therapeutic Strategies , 2011 .

[32]  M. Bernstein,et al.  Prospective study of awake craniotomy used routinely and nonselectively for supratentorial tumors. , 2007, Journal of neurosurgery.

[33]  Garnette R Sutherland,et al.  Optimizing Epilepsy Surgery with Intraoperative MR Imaging , 2002, Epilepsia.

[34]  Robert Jech,et al.  Validity of primary motor area localization with fMRI versus electric cortical stimulation: A comparative study , 2009, Acta Neurochirurgica.

[35]  Christopher Nimsky,et al.  Intraoperative MRI and functional mapping. , 2011, Acta neurochirurgica. Supplement.

[36]  G. Sutherland,et al.  Epilepsy surgery with intraoperative MRI at 1.5 T. , 2005, Neurosurgery clinics of North America.

[37]  Mahinda Yogarajah,et al.  Diffusion tensor imaging tractography to visualize the relationship of the optic radiation to epileptogenic lesions prior to neurosurgery , 2011, Epilepsia.

[38]  W. Hall,et al.  Functional Magnetic Resonance Imaging-Guided Brain Tumor Resection , 2008, Topics in Magnetic Resonance Imaging (TMRI).

[39]  C. Nimsky,et al.  Multimodal navigation integrated with imaging. , 2011, Acta neurochirurgica. Supplement.

[40]  Christopher Nimsky,et al.  Combining fMRI and MEG increases the reliability of presurgical language localization: A clinical study on the difference between and congruence of both modalities , 2006, NeuroImage.

[41]  C. Sarkar,et al.  Successful selection of patients with intractable extratemporal epilepsy using non-invasive investigations , 2003, Seizure.

[42]  W T Blume,et al.  A randomized, controlled trial of surgery for temporal-lobe epilepsy. , 2001, The New England journal of medicine.

[43]  Christopher Nimsky,et al.  Visualization of the pyramidal tract in glioma surgery by integrating diffusion tensor imaging in functional neuronavigation. , 2005 .

[44]  Christopher Nimsky,et al.  Quantification of Glioma Removal by Intraoperative High-Field Magnetic Resonance Imaging: An Update , 2011, Neurosurgery.

[45]  Catherine Zahn,et al.  Practice parameter: Temporal lobe and localized neocortical resections for epilepsy , 2003, Neurology.

[46]  G. Sutherland,et al.  Application of intraoperative high-field magnetic resonance imaging in pediatric neurosurgery. , 2009, Journal of neurosurgery. Pediatrics.

[47]  Ashesh D. Mehta,et al.  Clinical utility of functional magnetic resonance imaging for brain mapping in epilepsy surgery , 2010, Epilepsy Research.

[48]  Samuel Wiebe,et al.  Long-term seizure outcomes following epilepsy surgery: a systematic review and meta-analysis. , 2005, Brain : a journal of neurology.

[49]  C. Elger,et al.  Surgical Treatment of Extratemporal Epilepsy: Clinical, Radiologic, and Histopathologic Findings in 60 Patients , 1996, Epilepsia.

[50]  J. S. Duncan,et al.  MR tractography predicts visual field defects following temporal lobe resection , 2005, Neurology.

[51]  Christopher Nimsky,et al.  Prediction of visual field deficits by diffusion tensor imaging in temporal lobe epilepsy surgery , 2009, NeuroImage.