Intracranial electroencephalography seizure onset patterns and surgical outcomes in nonlesional extratemporal epilepsy.

OBJECT Patients with normal MR imaging (nonlesional) findings and medically refractory extratemporal epilepsy make up a disproportionate number of nonexcellent outcomes after epilepsy surgery. In this paper, the authors investigated the usefulness of intracranial electroencephalography (iEEG) in the identification of surgical candidates. METHODS Between 1992 and 2002, 51 consecutive patients with normal MR imaging findings and extratemporal epilepsy underwent intracranial electrode monitoring. The implantation of intracranial electrodes was determined by seizure semiology, interictal and ictal scalp EEG, SPECT, and in some patients PET studies. The demographics of patients at the time of surgery, lobar localization of electrode implantation, duration of follow-up, and Engel outcome score were abstracted from the Mayo Rochester Epilepsy Surgery Database. A blinded independent review of the iEEG records was conducted for this study. RESULTS Thirty-one (61%) of the 51 patients who underwent iEEG ultimately underwent resection for their epilepsy. For 28 (90.3%) of the 31 patients who had epilepsy surgery, adequate information regarding follow-up (> 1 year), seizure frequency, and iEEG recordings was available. Twenty-six (92.9%) of 28 patients had frontal lobe resections, and 2 had parietal lobe resections. The most common iEEG pattern at seizure onset in the surgically treated group was a focal high-frequency discharge (in 15 [53.6%] of 28 patients). Ten (35.7%) of the 28 surgically treated patients were seizure free. Fourteen (50%) had Engel Class I outcomes, and overall, 17 (60.7%) had significant improvement (Engel Class I and IIAB with > or =80% seizure reduction). Focal high-frequency oscillation at seizure onset was associated with Engel Class I surgical outcome (12 [85.7%] of 14 patients, p = 0.02), and it was uncommon in the nonexcellent outcome group (3 [21.4%] of 14 patients). CONCLUSIONS A focal high-frequency oscillation (> 20 Hz) at seizure onset on iEEG may identify patients with nonlesional extratemporal epilepsy who are likely to have an Engel Class I outcome after epilepsy surgery. The prospect of excellent outcome in nonlesional extratemporal lobe epilepsy prior to intracranial monitoring is poor (14 [27.5%] of 51 patients). However, iEEG can further stratify patients and help identify those with a greater likelihood of Engel Class I outcome after surgery.

[1]  J. Fermaglich Electric Fields of the Brain: The Neurophysics of EEG , 1982 .

[2]  G. Buzsáki Two-stage model of memory trace formation: A role for “noisy” brain states , 1989, Neuroscience.

[3]  R Llinás,et al.  Intrinsic electrical properties of nerve cells and their role in network oscillation. , 1990, Cold Spring Harbor symposia on quantitative biology.

[4]  P. V. Ness Surgical outcome for neocortical (extrahippocampal) focal epilepsy , 1991 .

[5]  P J Allen,et al.  Very high-frequency rhythmic activity during SEEG suppression in frontal lobe epilepsy. , 1991, Electroencephalography and clinical neurophysiology.

[6]  L F Quesney,et al.  Presurgical EEG investigation in frontal lobe epilepsy. , 1992, Epilepsy research. Supplement.

[7]  R. Fisher,et al.  High-frequency EEG activity at the start of seizures. , 1992, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

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

[9]  John W. Miller,et al.  Epilepsy surgery. , 1993, Neurologic clinics.

[10]  J. Hogg Magnetic resonance imaging. , 1994, Journal of the Royal Naval Medical Service.

[11]  G. Cascino,et al.  Commentary: How Has Neuroimaging Improved Patient Care? , 1994, Epilepsia.

[12]  G. Alarcón,et al.  Power spectrum and intracranial EEG patterns at seizure onset in partial epilepsy. , 1995, Electroencephalography and clinical neurophysiology.

[13]  C R Jack,et al.  Magnetic resonance imaging. Neuroimaging and anatomy. , 1995, Neuroimaging clinics of North America.

[14]  G Buzsáki,et al.  The hippocampo-neocortical dialogue. , 1996, Cerebral cortex.

[15]  C. Jack,et al.  Subtraction ictal SPECT co‐registered to MRI improves clinical usefulness of SPECT in localizing the surgical seizure focus , 1998, Neurology.

[16]  F W Sharbrough,et al.  Characterization and Comparison of Local Onset and Remote Propagated Electrographic Seizures Recorded with Intracranial Electrodes , 1998, Epilepsia.

[17]  B H Brinkmann,et al.  Subtraction ictal SPET co‐registered to MRI in partial epilepsy: Description and technical validation of the method with phantom and patient studies , 1998, Nuclear medicine communications.

[18]  G Buzsáki,et al.  Memory consolidation during sleep: a neurophysiological perspective. , 1998, Journal of sleep research.

[19]  G. Ojemann,et al.  Ictal Patterns of Neocortical Seizures Monitored with Intracranial Electrodes: Correlation with Surgical Outcome , 1999, Epilepsia.

[20]  Charles L. Wilson,et al.  Hippocampal and Entorhinal Cortex High‐Frequency Oscillations (100–500 Hz) in Human Epileptic Brain and in Kainic Acid‐Treated Rats with Chronic Seizures , 1999, Epilepsia.

[21]  Charles L. Wilson,et al.  High‐frequency oscillations in human brain , 1999, Hippocampus.

[22]  B H Brinkmann,et al.  Subtraction SPECT co-registered to MRI improves postictal SPECT localization of seizure foci , 1999, Neurology.

[23]  L F Quesney,et al.  Intracranial EEG investigation in neocortical epilepsy. , 2000, Advances in neurology.

[24]  G. Curio Ain't no rhythm fast enough: EEG bands beyond beta. , 2000, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[25]  G Curio,et al.  Linking 600-Hz “Spikelike” EEG/MEG Wavelets (“&sfgr;-Bursts”) to Cellular Substrates: Concepts and Caveats , 2000, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[26]  C. Jack,et al.  Factors Predictive of the Outcome of Frontal Lobe Epilepsy Surgery , 2000, Epilepsia.

[27]  B. Brinkmann,et al.  Subtraction peri-ictal SPECT is predictive of extratemporal epilepsy surgery outcome , 2000, Neurology.

[28]  W T Blume,et al.  Proposal for a New Classification of Outcome with Respect to Epileptic Seizures Following Epilepsy Surgery , 2001, Epilepsia.

[29]  Helen J. Cross,et al.  A Possible Role for Gap Junctions in Generation of Very Fast EEG Oscillations Preceding the Onset of, and Perhaps Initiating, Seizures , 2001, Epilepsia.

[30]  J. Zentner,et al.  Surgical treatment of epilepsies. , 2002, Acta neurochirurgica. Supplement.

[31]  Brian Litt,et al.  Evidence for self-organized criticality in human epileptic hippocampus , 2002, Neuroreport.

[32]  Terence J O'Brien,et al.  Focal Ictal β Discharge on Scalp EEG Predicts Excellent Outcome of Frontal Lobe Epilepsy Surgery , 2002, Epilepsia.

[33]  A. Siegel Frontal lobe epilepsy: diagnosis and surgical treatment , 2002 .

[34]  Jeffrey W Britton,et al.  Neurostimulation therapy for epilepsy: current modalities and future directions. , 2003, Mayo Clinic proceedings.

[35]  B. Brinkmann,et al.  Localization of the Epileptic Focus by Low-Resolution Electromagnetic Tomography in Patients with a Lesion Demonstrated by MRI , 2004, Brain Topography.

[36]  B. Litt,et al.  High-frequency oscillations and seizure generation in neocortical epilepsy. , 2004, Brain : a journal of neurology.

[37]  Charles M. Gray,et al.  Synchronous oscillations in neuronal systems: Mechanisms and functions , 1994, Journal of Computational Neuroscience.

[38]  F. Sharbrough,et al.  Subtraction SPECT Coregistered to MRI in Focal Malformations of Cortical Development: Localization of the Epileptogenic Zone in Epilepsy Surgery Candidates , 2004, Epilepsia.

[39]  Ayako Ochi,et al.  Focal cortical high-frequency oscillations trigger epileptic spasms: Confirmation by digital video subdural EEG , 2005, Clinical Neurophysiology.

[40]  J. Gotman,et al.  High-frequency oscillations during human focal seizures. , 2006, Brain : a journal of neurology.

[41]  Ayako Ochi,et al.  Topographic Movie of Ictal High‐Frequency Oscillations on the Brain Surface Using Subdural EEG in Neocortical Epilepsy , 2006, Epilepsia.

[42]  Ayako Ochi,et al.  Dynamic Changes of Ictal High‐Frequency Oscillations in Neocortical Epilepsy: Using Multiple Band Frequency Analysis , 2007, Epilepsia.

[43]  B. Litt,et al.  High-frequency oscillations in human temporal lobe: simultaneous microwire and clinical macroelectrode recordings. , 2008, Brain : a journal of neurology.