Simultaneous scalp EEG improves seizure lateralization during unilateral intracranial EEG evaluation in temporal lobe epilepsy

PURPOSE To determine if simultaneous bilateral scalp EEG (scEEG) can accurately detect a contralateral seizure onset in patients with unilateral intracranial EEG (IEEG) implantation. METHODS We evaluated 39 seizures from 9 patients with bitemporal epilepsy who underwent simultaneous scEEG and IEEG (SSIEEG). To simulate conditions of unilateral IEEG implantation with a missed contralateral seizure onset, we analyzed the IEEG recording contralateral to the seizure onset (CL- IEEG), in conjunction with simultaneous scEEG. The following criteria were evaluated between scEEG and CL- IEEG (1) latency: the time to onset of EEG seizure (2) location: concordance of ictal onset zones and (3) pattern: congruence of EEG morphology and frequency. RESULTS SSIEEG correctly lateralized 36/39 (92.3%) seizures compared to 13/39 (33.3%) seizures using CL- IEEG alone (OR = 24.0, p < 0.01), 33 (84.6%) seizures using scEEG alone (OR = 2.2, p = 0.29) and 26 (66.9%) seizures using time of clinical onset alone (OR = 6.0, p = 0.01). For the three criteria evaluated, (1) 22/39 (56.4%) seizures had an earlier onset on the scEEG, compared to CL- IEEG; (2) lack of congruence of location of seizure onset was noted in 33/39 (84.6%) of the seizures; and (3) 22/39 (56.4%) seizures did not have a congruent ictal pattern. CONCLUSIONS The chronological, topographic and morphologic features of SSIEEG can accurately detect the hemisphere of seizure onset in most cases with unilateral IEEG implantation. SSIEEG is significantly better than, IEEG, scEEG or clinical onset alone in this scenario. We propose that SSIEEG should be considered in all cases of intractable focal epilepsy undergoing unilateral IEEG evaluation.

[1]  Y. Schiller,et al.  Chronic Intracranial EEG Monitoring for Localizing the Epileptogenic Zone: An Electroclinical Correlation , 1998, Epilepsia.

[2]  F. H. Lopes da Silva,et al.  Comparison of Combined Versus Subdural or Intracerebral Electrodes Alone in Presurgical Focus Localization , 1998, Epilepsia.

[3]  E. Halgren,et al.  Side Matters: Diffusion Tensor Imaging Tractography in Left and Right Temporal Lobe Epilepsy , 2009, American Journal of Neuroradiology.

[4]  Jorge Gonzalez-Martinez,et al.  Stereoelectroencephalography in the “difficult to localize” refractory focal epilepsy: Early experience from a North American epilepsy center , 2013, Epilepsia.

[5]  L F Quesney,et al.  False lateralization by surface EEG of seizure onset in patients with temporal lobe epilepsy and gross focal cerebral lesions , 1987, Annals of neurology.

[6]  Don M. Tucker,et al.  Corrigendum: Dense Array EEG Source Estimation in Neocortical Epilepsy , 2013, Front. Neurol..

[7]  G W Somes,et al.  Long-term ictal monitoring with subdural strip electrodes: prognostic factors for selecting temporal lobectomy candidates. , 1992, Journal of neurosurgery.

[8]  Don M. Tucker,et al.  Comparison of dense array EEG with simultaneous intracranial EEG for Interictal spike detection and localization , 2012, Epilepsy Research.

[9]  C. N. Guy,et al.  Intracerebral propagation of interictal activity in partial epilepsy: implications for source localisation. , 1994, Journal of neurology, neurosurgery, and psychiatry.

[10]  Georgia Ramantani,et al.  Catching the Invisible: Mesial Temporal Source Contribution to Simultaneous EEG and SEEG Recordings , 2014, Brain Topography.

[11]  F. Sharbrough,et al.  Depth Electrode Studies in Temporal Lobe Epilepsy: Relation to Quantitative Magnetic Resonance Imaging and Operative Outcome , 1995, Epilepsia.

[12]  T L Babb,et al.  Interhemispheric Propagation Time of Human Hippocampal Seizures , 1986, Epilepsia.

[13]  H. Lüders,et al.  Ictal scalp EEG in temporal lobe epilepsy with unitemporal versus bitemporal interictal epileptiform discharges , 1995, Neurology.

[14]  Intracranial electrographic analysis of preictal spiking and ictal onset in uni- and bitemporal epilepsy. , 2015, Epileptic disorders : international epilepsy journal with videotape.

[15]  T. Morioka,et al.  Localization of epileptogenic zone in temporal lobe epilepsy by ictal scalp EEG , 2002, Seizure.

[16]  J Gotman,et al.  Relations Between EEG Seizure Morphology, Interhemispheric Spread, and Mesial Temporal Atrophy in Bitemporal Epilepsy , 1997, Epilepsia.

[17]  J. Engel,et al.  Functional connectivity of hippocampal networks in temporal lobe epilepsy , 2014, Epilepsia.

[18]  A. Schulze-Bonhage,et al.  Simultaneous subdural and scalp EEG correlates of frontal lobe epileptic sources , 2014, Epilepsia.

[19]  Gregory A Worrell,et al.  Lateralization of mesial temporal lobe epilepsy with chronic ambulatory electrocorticography , 2015, Epilepsia.

[20]  Chun Kee Chung,et al.  Extent of neocortical resection and surgical outcome of epilepsy: Intracranial EEG analysis , 2010, Epilepsia.

[21]  T. Babb,et al.  A Comparison of EEG Seizure Patterns Recorded with Surface and Depth Electrodes in Patients with Temporal Lobe Epilepsy , 1976, Epilepsia.

[22]  R. Richardson,et al.  Features of Simultaneous Scalp and Intracranial EEG That Predict Localization of Ictal Onset Zone , 2018, Clinical EEG and neuroscience.

[23]  John S. Ebersole,et al.  Localizing value of scalp EEG spikes: A simultaneous scalp and intracranial study , 2007, Clinical Neurophysiology.

[24]  J. Ebersole,et al.  Intracranial EEG Substrates of Scalp Ictal Patterns from Temporal Lobe Foci , 1997, Epilepsia.

[25]  Georgia Ramantani,et al.  Correlation of invasive EEG and scalp EEG , 2016, Seizure.

[26]  F Andermann,et al.  Periventricular and subcortical nodular heterotopia. A study of 33 patients. , 1995, Brain : a journal of neurology.

[27]  C D Binnie,et al.  Utility of stereoelectroencephalography in preoperative assessment of temporal lobe epilepsy. , 1994, Journal of neurology, neurosurgery, and psychiatry.

[28]  C. A. Marsan,et al.  Patterns of cortical discharges and their relation to routine scalp electroencephalography. , 1958, Electroencephalography and clinical neurophysiology.

[29]  J. Gotman,et al.  Intracranial electroencephalographic seizure-onset patterns: effect of underlying pathology. , 2014, Brain : a journal of neurology.

[30]  E Wyllie,et al.  Successful surgery for epilepsy due to early brain lesions despite generalized EEG findings , 2007, Neurology.

[31]  M R Sperling,et al.  Comparison of depth and subdural electrodes in recording temporal lobe seizures , 1989, Neurology.

[32]  Yasushi Miyagi,et al.  Correlation between scalp-recorded electroencephalographic and electrocorticographic activities during ictal period , 2007, Seizure.

[33]  M. Duchowny,et al.  The diagnostic utility of intracranial EEG monitoring for epilepsy surgery in children , 2015, Epilepsia.

[34]  P. Afra,et al.  False lateralization of seizure onset by scalp EEG in neocortical temporal lobe epilepsy , 2011, Seizure.

[35]  P. Crandall,et al.  Surface and Deep EEG Correlates of Surgical Outcome in Temporal Lobe Epilepsy , 1981, Epilepsia.

[36]  I. Fried,et al.  Unilateral Hippocampal Sclerosis with Contralateral Temporal Scalp Ictal Onset , 2004, Epilepsia.

[37]  Jean Gotman,et al.  Association between scalp and intracerebral electroencephalographic seizure‐onset patterns: A study in different lesional pathological substrates , 2018, Epilepsia.