The value of magnetoencephalography for seizure-onset zone localization in magnetic resonance imaging-negative partial epilepsy

Abstract

Surgical treatment of epilepsy is a challenge for patients with non-contributive brain magnetic resonance imaging. However, surgery is feasible if the seizure-onset zone is precisely delineated through intracranial electroencephalography recording. We recently described a method, volumetric imaging of epileptic spikes, to delineate the spiking volume of patients with focal epilepsy using magnetoencephalography. We postulated that the extent of the spiking volume delineated with volumetric imaging of epileptic spikes could predict the localizability of the seizure-onset zone by intracranial electroencephalography investigation and outcome of surgical treatment. Twenty-one patients with non-contributive magnetic resonance imaging findings were included. All patients underwent intracerebral electroencephalography investigation through stereotactically implanted depth electrodes (stereo-electroencephalography) and magnetoencephalography with delineation of the spiking volume using volumetric imaging of epileptic spikes. We evaluated the spatial congruence between the spiking volume determined by magnetoencephalography and the localization of the seizure-onset zone determined by stereo-electroencephalography. We also evaluated the outcome of stereo-electroencephalography and surgical treatment according to the extent of the spiking volume (focal, lateralized but non-focal or non-lateralized). For all patients, we found a spatial overlap between the seizure-onset zone and the spiking volume. For patients with a focal spiking volume, the seizure-onset zone defined by stereo-electroencephalography was clearly localized in all cases and most patients (6/7, 86%) had a good surgical outcome. Conversely, stereo-electroencephalography failed to delineate a seizure-onset zone in 57% of patients with a lateralized spiking volume, and in the two patients with bilateral spiking volume. Four of the 12 patients with non-focal spiking volumes were operated upon, none became seizure-free. As a whole, patients having focal magnetoencephalography results with volumetric imaging of epileptic spikes are good surgical candidates and the implantation strategy should incorporate volumetric imaging of epileptic spikes results. On the contrary, patients with non-focal magnetoencephalography results are less likely to have a localized seizure-onset zone and stereo electroencephalography is not advised unless clear localizing information is provided by other presurgical investigation methods.

Keywords: EEG; MEG; epilepsy surgery; epileptogenic zone; intracranial EEG; partial seizures.

Figure 1

MEG modelling of epileptic spikes and SEEG localization of the seizure-onset zone in a patient with a focal spiking volume (Patient 16). Top left: Example of one prototypical spike recorded with MEG for one single channel. Top right: Topographic map of the magnetic field recorded for all MEG channels at the main peak of the prototypical spike. Bottom left: The MEG spiking volume determined with VIES (red volume) is shown on representative MRI slices. On the same slices, the SEEG electrodes showing clear signal changes at seizure-onset are shown in blue. Bottom right: SEEG implantation scheme of Patient 16. The location of the penetrating points of intracranial electrodes is determined by co-registering the patient’s post-implantation MRI onto the cortical mesh extracted from the MRI. The MEG spiking volume projected onto the cortical surface is shown as a red area. SEEG electrodes showing clear signal change at seizure onset are shown in green and electrodes without ictal changes are shown in black. Notice that the spiking volume is spatially restricted and co-extensive with the seizure-onset zone determined with SEEG. The patient underwent surgery with a resection of the posterior part of the left temporal neocortex (superior and middle temporal gyrus) and is seizure free postoperatively after 22 months of follow-up.

Figure 2

MEG modelling of epileptic spikes and SEEG localization of the seizure-onset zone in a patient with a lateralized spiking volume (Patient 13). Top left: Example of one prototypical spike recorded with MEG for one single channel of Patient 13. Top right: Topographic map of the magnetic field recorded for all MEG channels at the main peak of the prototypical spike. Bottom left: The MEG spiking volume determined with VIES (red volume) is shown on representative MRI slices. On the same slices, the SEEG electrodes showing clear signal changes at seizure-onset are shown in blue, and electrodes without clear ictal activity are in white. Bottom right: SEEG implantation scheme of Patient 13. The location of the penetrating points of intracranial electrodes is determined by co-registering the patient’s post-implantation MRI onto the cortical mesh extracted from the MRI. The MEG spiking volume projected onto the cortical surface is shown as a red area. SEEG electrodes showing clear signal changes at seizure-onset are shown in green and electrodes without ictal changes are shown in black. Notice that the spiking volume is lateralized but not focal and only partly co-extensive with the seizure-onset zone determined with SEEG (several lobes are included in the MEG spiking volume). Surgery was contraindicated for Patient 13 as the seizure-onset zone was considered as non-localized based on SEEG.

Figure 3

MEG modelling of epileptic spikes and SEEG localization of the seizure-onset zone in a patient with a non-lateralized spiking volume. Top left: Example of one prototypical spike recorded with MEG for one single channel of Patient 7. Top right: Topographic map of the magnetic field recorded for all MEG channels at the main peak of the prototypical spike. Bottom left: The MEG spiking volume determined with VIES (red volume) is shown on representative MRI slices. On the same slices, the SEEG electrodes showing clear signal changes at seizure-onset are shown in blue, and electrodes without clear ictal activity are in white. Bottom right: SEEG implantation scheme of Patient 7. The location of the penetrating points of intracranial electrodes is determined by co-registering the patient’s post-implantation MRI onto the cortical mesh extracted from the MRI. The MEG spiking volume projected onto the cortical surface is shown as a red area. SEEG electrodes showing clear signal changes at seizure-onset are shown in green and electrodes without ictal changes are shown in black. Notice that the spiking volume is spatially very extensive and partly co-extensive with the seizure-onset zone determined with SEEG. The seizure-onset zone was considered as not perfectly delineated. However, because the epilepsy was very severe, the patient underwent surgical resection of left antero-mesial frontal cortex [frontal pole + anterior superior frontal gyrus (F1) + supplementary motor area and anterior cingulate gyrus] with an unsatisfactory surgical outcome (Engel III).