Preoperative magnetic source imaging for brain tumor surgery: a quantitative comparison with intraoperative sensory and motor mapping.

OBJECT The aim of this study was to compare quantitatively the methods of preoperative magnetic source (MS) imaging and intraoperative electrophysiological cortical mapping (ECM) in the localization of sensorimotor cortex in patients with intraaxial brain tumors. METHODS Preoperative magnetoencephalography (MEG) was performed while patients received painless tactile somatosensory stimulation of the lip, hand, and foot. The early somatosensory evoked field was modeled using a single equivalent current dipole approach to estimate the spatial source of the response. Three-dimensional magnetic resonance image volume data sets with fiducials were coregistered with the MEG recordings to form the MS image. These individualized functional brain maps were integrated into a neuronavigation system. Intraoperative mapping of somatosensory and/or motor cortex was performed and sites were compared. In two subgroups of patients we compared intraoperative somatosensory and motor stimulation sites with MS imaging-based somatosensory localizations. Mediolateral projection of the MS imaging source localizations to the cortical surface reduced systematic intermodality discrepancies. The distance between two corresponding points determined using MS imaging and ECM was 12.5 +/- 1.3 mm for somatosensory-somatosensory and 19 +/- 1.3 mm for somatosensory-motor comparisons. The observed 6.5 mm increase in site separation was systematically demonstrated in the anteroposterior direction, as expected from actual anatomy. In fact, intraoperative sites at which stimulation evoked the same patient response exhibited a spatial variation of 10.7 +/- 0.7 mm. CONCLUSIONS Preoperative MS imaging and intraoperative ECM show a favorable degree of quantitative correlation. Thus, MS imaging can be considered a valuable and accurate planning adjunct in the treatment of patients with intraaxial brain tumors.

[1]  Mitchel S. Berger,et al.  Intraoperative Cortical Mapping as a Guide to the Surgical Resection of Gliomas , 2004, Journal of Neuro-Oncology.

[2]  Mitchel S. Berger,et al.  Low grade gliomas: Functional mapping resection strategies, extent of resection, and outcome , 1997, Journal of Neuro-Oncology.

[3]  M M Bonsanto,et al.  Clinical evaluation and follow-up results for intraoperative magnetic resonance imaging in neurosurgery. , 2000, Neurosurgery.

[4]  M. Bernstein,et al.  Awake craniotomy with brain mapping as the routine surgical approach to treating patients with supratentorial intraaxial tumors: a prospective trial of 200 cases. , 1999, Journal of neurosurgery.

[5]  N. Barbaro,et al.  Correlation of functional magnetic source imaging with intraoperative cortical stimulation in neurosurgical patients. , 1995, Journal of image guided surgery.

[6]  I Berry,et al.  Cortical intraoperative stimulation in brain tumors as a tool to evaluate spatial data from motor functional MRI. , 1999, Investigative radiology.

[7]  R. Ilmoniemi,et al.  Selective localization of alpha brain activity with neuromagnetic measurements. , 1984, Electroencephalography and clinical neurophysiology.

[8]  C. Jack,et al.  Sensory motor cortex: correlation of presurgical mapping with functional MR imaging and invasive cortical mapping. , 1994, Radiology.

[9]  M. Berger,et al.  Rapid termination of intraoperative stimulation-evoked seizures with application of cold Ringer's lactate to the cortex. Technical note. , 1998, Journal of neurosurgery.

[10]  G. Ojemann,et al.  Cortical language localization in left, dominant hemisphere. An electrical stimulation mapping investigation in 117 patients. , 1989, Journal of neurosurgery.

[11]  H Weinberg,et al.  Electroencephalographic and magnetoencephalographic studies of motor function. , 1990, Advances in neurology.

[12]  H. Thaler,et al.  Morbidity and mortality of craniotomy for excision of supratentorial gliomas , 1988, Neurology.

[13]  Mitchel S. Berger,et al.  Brain Mapping Techniques to Maximize Resection, Safety, and Seizure Control in Children with Brain Tumors , 1989 .

[14]  P. Kelly,et al.  Grading of astrocytomas: A simple and reproducible method , 1988, Cancer.

[15]  R D Bucholz,et al.  Presurgical localization of functional cortex using magnetic source imaging. , 1995, Journal of neurosurgery.

[16]  R. Ilmoniemi,et al.  Magnetoencephalography-theory, instrumentation, and applications to noninvasive studies of the working human brain , 1993 .

[17]  C. Strauss,et al.  Magnetic source imaging combined with image-guided frameless stereotaxy: a new method in surgery around the motor strip. , 1997, Neurosurgery.

[18]  L. Kaufman,et al.  Latency of the neuromagnetic response of the human visual cortex , 1978, Vision Research.

[19]  F E Bloom,et al.  Intrasubject reliability and validity of somatosensory source localization using a large array biomagnetometer. , 1994, Electroencephalography and clinical neurophysiology.

[20]  H. Rowley,et al.  Magnetic source imaging as a tool for presurgical functional brain mapping. , 1997, Neurosurgery clinics of North America.

[21]  P. Black,et al.  Craniotomy Under Local Anesthesia and Monitored Conscious Sedation for the Resection of Tumors Involving Eloquent Cortex , 2000, Journal of Neuro-Oncology.

[22]  T A Yousry,et al.  Topography of the cortical motor hand area: prospective study with functional MR imaging and direct motor mapping at surgery. , 1995, Radiology.

[23]  J. Schramm,et al.  Somatosensory evoked potential phase reversal and direct motor cortex stimulation during surgery in and around the central region. , 1996, Neurosurgery.

[24]  B. O'neill,et al.  Awake craniotomy for aggressive resection of primary gliomas located in eloquent brain. , 2001, Mayo Clinic proceedings.

[25]  C. Woolsey,et al.  Localization in somatic sensory and motor areas of human cerebral cortex as determined by direct recording of evoked potentials and electrical stimulation. , 1979, Journal of neurosurgery.

[26]  F E Bloom,et al.  Noninvasive somatosensory homunculus mapping in humans by using a large-array biomagnetometer. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[27]  R. Hari,et al.  Functional Organization of the Human First and Second Somatosensory Cortices: a Neuromagnetic Study , 1993, The European journal of neuroscience.

[28]  O Salonen,et al.  Three‐dimensional integration of brain anatomy and function to facilitate intraoperative navigation around the sensorimotor strip , 2001, Human brain mapping.

[29]  T. Yoshimoto,et al.  Accuracy and Limitation of Functional Magnetic Resonance Imaging for Identification of the Central Sulcus: Comparison with Magnetoencephalography in Patients with Brain Tumors , 1999, NeuroImage.

[30]  R Steinmeier,et al.  Functional neuronavigation with magnetoencephalography: outcome in 50 patients with lesions around the motor cortex. , 1999, Neurosurgical focus.

[31]  M. Berger,et al.  Identification of motor pathways during tumor surgery facilitated by multichannel electromyographic recording. , 1999, Journal of neurosurgery.

[32]  A. Papanicolaou,et al.  Localization of language-specific cortex by using magnetic source imaging and electrical stimulation mapping. , 1999, Journal of neurosurgery.

[33]  Christopher Nimsky,et al.  Correlation of Sensorimotor Activation with Functional Magnetic Resonance Imaging and Magnetoencephalography in Presurgical Functional Imaging: A Spatial Analysis , 2001, NeuroImage.

[34]  F Isamat,et al.  Presurgical identification of the primary sensorimotor cortex by functional magnetic resonance imaging. , 1996, Journal of neurosurgery.

[35]  M. Berger,et al.  The effect of extent of resection on recurrence in patients with low grade cerebral hemisphere gliomas , 1994, Cancer.

[36]  W. Penfield,et al.  SOMATIC MOTOR AND SENSORY REPRESENTATION IN THE CEREBRAL CORTEX OF MAN AS STUDIED BY ELECTRICAL STIMULATION , 1937 .

[37]  David F. Sobel,et al.  Noninvasive presurgical neuromagnetic mapping of somatosensory cortex. , 1993, Neurosurgery.

[38]  A. Nakamura,et al.  Somatosensory Homunculus as Drawn by MEG , 1998, NeuroImage.

[39]  R. Llinás,et al.  The interactive use of magnetoencephalography in stereotactic image-guided neurosurgery. , 1996, Neurosurgery.

[40]  Shinya Kuriki,et al.  Functional neurosurgical simulation with brain surface magnetic resonance images and magnetoencephalography. , 1993, Neurosurgery.

[41]  R. Llinás,et al.  Magnetoencephalographic mapping: basic of a new functional risk profile in the selection of patients with cortical brain lesions. , 1997, Neurosurgery.

[42]  G McCarthy,et al.  Comparative localization of auditory comprehension by using functional magnetic resonance imaging and cortical stimulation. , 1999, Journal of neurosurgery.

[43]  W. Harkness,et al.  Postimaging brain distortion: magnitude, correlates, and impact on neuronavigation. , 1998, Journal of neurosurgery.

[44]  J. Sarvas Basic mathematical and electromagnetic concepts of the biomagnetic inverse problem. , 1987, Physics in medicine and biology.

[45]  M Brock,et al.  Monitoring of intraoperative motor evoked potentials to increase the safety of surgery in and around the motor cortex. , 2001, Journal of neurosurgery.

[46]  S S Kollias,et al.  Intraoperative validation of functional magnetic resonance imaging and cortical reorganization patterns in patients with brain tumors involving the primary motor cortex. , 1999, Journal of neurosurgery.

[47]  R. Llinás,et al.  Somatosensory cortical plasticity in adult humans revealed by magnetoencephalography. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[48]  J. Maldjian,et al.  Functional image-guided surgery of intracranial tumors located in or near the sensorimotor cortex. , 1998, Journal of neurosurgery.

[49]  J. Tsuruda,et al.  Integration of preoperative and intraoperative functional brain mapping in a frameless stereotactic environment for lesions near eloquent cortex. Technical note. , 1999, Journal of neurosurgery.

[50]  M. Berger,et al.  Low-grade hemispheric gliomas in adults: a critical review of extent of resection as a factor influencing outcome. , 2001, Journal of neurosurgery.

[51]  P Ferrari,et al.  Functional Activity within Brain Tumors: A Magnetic Source Imaging Study , 2001, Neurosurgery.

[52]  C. Lumenta,et al.  BrainLab VectorVision Neuronavigation System: technology and clinical experiences in 131 cases. , 1999, Neurosurgery.

[53]  M. Mikhael,et al.  Effect of the extent of surgical resection on survival and quality of life in patients with supratentorial glioblastomas and anaplastic astrocytomas. , 1987, Neurosurgery.

[54]  S. Ronner,et al.  Cortical mapping for defining the limits of tumor resection. , 1987, Neurosurgery.

[55]  D Le Bihan,et al.  Correspondence between functional magnetic resonance imaging somatotopy and individual brain anatomy of the central region: comparison with intraoperative stimulation in patients with brain tumors. , 2000, Journal of neurosurgery.

[56]  T. Allison,et al.  Functional magnetic resonance imaging of sensory and motor cortex: comparison with electrophysiological localization. , 1995, Journal of neurosurgery.

[57]  B Lütkenhöner,et al.  A Neuromagnetic Study of the Functional Organization of the Sensorimotor Cortex , 1994, The European journal of neuroscience.

[58]  J. Drake,et al.  Combined utility of functional MRI, cortical mapping, and frameless stereotaxy in the resection of lesions in eloquent areas of brain in children. , 1997, Pediatric neurosurgery.

[59]  T. Yoshimoto,et al.  Somatosensory, auditory, and visual evoked magnetic fields in patients with brain diseases. , 2000, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[60]  E. Benzel,et al.  Magnetic source imaging and brain surgery: presurgical and intraoperative planning in 26 patients. , 2000, Journal of neurosurgery.