Invasive epilepsy surgery evaluation

Intracranial EEG (iEEG) recordings are widely used for the work up of pharmacoresistant epilepsy. Different iEEG recording techniques namely subdural grids, strips, depth electrodes and stereoencephalography (SEEG) are available with distinct limitations and advantages. Epilepsy centres mastering multiple techniques apply them in an individualised patient approach. These tools are used to map the seizure onset zone which is pivotal in approximating the epileptogenic zone, i.e. the zone which is indispensable for the generation of seizures and when resected will render the patient seizure free. Besides, the implanted electrodes can be used to define eloquent cortex through direct cortical stimulation. Different clinical scenarios exist which favour one iEEG recording technique over the other. Proximity of the presumed epileptogenic zone to eloquent cortex, for example, is a clinical scenario which may favour grid electrodes over SEEG. We here review the indication for iEEG for the work-up of patients suffering from pharmacoresistant epilepsy. In addition, we provide a description of the recording techniques focussing on the main techniques used: grid electrodes, depth electrodes and stereoencephalography. We then outline different clinical scenarios and the preferred technical approach for intracranial recordings in these scenarios. Finally, we highlight which advances have been made in the field of iEEG and which advances are in the pipeline waiting to be established for clinical use. This review provides the clinician with an update on the diagnostic use of intracranial EEG for epilepsy surgery and thus aids in understanding patient selection for this technique which may ultimately improve referral patterns.

[1]  J. H. Cross,et al.  Diagnostic test utilization in evaluation for resective epilepsy surgery in children , 2014, Epilepsia.

[2]  R. Flink,et al.  Intraoperative electrocorticography in epilepsy surgery: useful or not? , 2003, Seizure.

[3]  J. Delgado,et al.  Technique of intracranial electrode implacement for recording and stimulation and its possible therapeutic value in psychotic patients. , 1952, Confinia neurologica.

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

[5]  H. Altenburger,et al.  Elektrobiologische Vorgänge an der menschlichen Hirnrinde , 1935, Deutsche Zeitschrift für Nervenheilkunde.

[6]  Jean Gotman,et al.  Diagnostic utility of invasive EEG for epilepsy surgery: Indications, modalities, and techniques , 2016, Epilepsia.

[7]  G. Klem,et al.  The localizing value of ictal EEG in focal epilepsy , 2001, Neurology.

[8]  B. Swartz,et al.  Subdural recording and electrical stimulation for cortical mapping and induction of usual seizures. , 1994, Stereotactic and functional neurosurgery.

[9]  J. Talairach,et al.  Functional stereotaxic exploration of epilepsy. , 1962, Confinia neurologica.

[10]  H. Lüders,et al.  The epileptogenic zone: general principles. , 2006, Epileptic disorders : international epilepsy journal with videotape.

[11]  M. N. Shanmukha Swamy,et al.  Model-Based Seizure Detection for Intracranial EEG Recordings , 2012, IEEE Transactions on Biomedical Engineering.

[12]  J. H. Cross,et al.  Epilepsy surgery in children and adults , 2014, The Lancet Neurology.

[13]  R.N.Dej.,et al.  Epilepsy and the Functional Anatomy of the Human Brain , 1954, Neurology.

[14]  Jorge Gonzalez-Martinez,et al.  Long‐term seizure outcome after resective surgery in patients evaluated with intracranial electrodes , 2012, Epilepsia.

[15]  J. Ebersole,et al.  Intracranial EEG Substrates of Scalp EEG Interictal Spikes , 2005, Epilepsia.

[16]  G. Mathern,et al.  Definition of drug resistant epilepsy: Consensus proposal by the ad hoc Task Force of the ILAE Commission on Therapeutic Strategies , 2009, Epilepsia.

[17]  Felix Rosenow,et al.  The history of invasive EEG evaluation in epilepsy patients , 2016, Seizure.

[18]  C. Scott,et al.  Extraoperative Electrical Cortical Stimulation: Characteristics of Motor Responses and Correlation with Precentral Gyrus , 2011, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[19]  Christoph M. Michel,et al.  Epileptic source localization with high density EEG: how many electrodes are needed? , 2003, Clinical Neurophysiology.

[20]  H. Lüders,et al.  Presurgical evaluation of epilepsy. , 2001, Brain : a journal of neurology.

[21]  R P Lesser,et al.  The value of closely spaced scalp electrodes in the localization of epileptiform foci: a study of 26 patients with complex partial seizures. , 1986, Electroencephalography and clinical neurophysiology.

[22]  M. Duchowny,et al.  Medically resistant pediatric insular-opercular/perisylvian epilepsy. Part 2: outcome following resective surgery. , 2016, Journal of neurosurgery. Pediatrics.

[23]  J. Duncan,et al.  Applications of blood-oxygen-level-dependent functional magnetic resonance imaging and diffusion tensor imaging in epilepsy. , 2014, Neuroimaging clinics of North America.

[24]  Sebastien Ourselin,et al.  Utility of 3D multimodality imaging in the implantation of intracranial electrodes in epilepsy , 2015, Epilepsia.

[25]  Shalini Narayana,et al.  Is it time to replace the Wada test and put awake craniotomy to sleep? , 2014, Epilepsia.

[26]  Philippe Kahane,et al.  Definition and localization of the epileptogenic zone The Bancaud and Talairach view on the epileptogenic zone : a working hypothesis , 2006 .

[27]  Francesco Cardinale,et al.  Identification of reproducible ictal patterns based on quantified frequency analysis of intracranial EEG signals , 2011, Epilepsia.

[28]  Y. Li,et al.  Surgical treatment for epilepsy involving language cortices: A combined process of electrical cortical stimulation mapping and intra-operative continuous language assessment , 2013, Seizure.

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

[30]  Jorge Gonzalez-Martinez,et al.  Is SEEG safe? A systematic review and meta‐analysis of stereo‐electroencephalography–related complications , 2016, Epilepsia.

[31]  Pavel Krsek,et al.  Current use of imaging and electromagnetic source localization procedures in epilepsy surgery centers across Europe , 2016, Epilepsia.

[32]  P. House High-Frequency Electroencephalographic Oscillations Correlate With Outcome of Epilepsy Surgery , 2010 .

[33]  Fabrice Wendling,et al.  Local and remote epileptogenicity in focal cortical dysplasias and neurodevelopmental tumours. , 2009, Brain : a journal of neurology.

[34]  F. Bartolomei,et al.  Visual and semiautomated evaluation of epileptogenicity in focal cortical dysplasias — An intracranial EEG study , 2016, Epilepsy & Behavior.

[35]  J. Delgado,et al.  Permanent Implantation of Multilead Electrodes in the Brain * , 1952, The Yale journal of biology and medicine.

[36]  Sebastien Ourselin,et al.  Comparison of computer-assisted planning and manual planning for depth electrode implantations in epilepsy. , 2016, Journal of neurosurgery.

[37]  L Tassi,et al.  [Electroclinical manifestations elicited by intracerebral electric stimulation "shocks" in temporal lobe epilepsy]. , 1993, Neurophysiologie clinique = Clinical neurophysiology.

[38]  G Pfurtscheller,et al.  Frequency dependence of the transmission of the EEG from cortex to scalp. , 1975, Electroencephalography and clinical neurophysiology.

[39]  C. Scott,et al.  Clinical significance of nonhabitual seizures during intracranial EEG monitoring , 2014, Epilepsia.

[40]  Frederick Andermann,et al.  Intrinsic epileptogenicity of human dysplastic cortex as suggested by corticography and surgical results , 1995, Annals of neurology.

[41]  Brian Litt,et al.  A novel seizure detection algorithm informed by hidden Markov model event states , 2016, Journal of neural engineering.

[42]  J. Talairach,et al.  Lesion, "irritative" zone and epileptogenic focus. , 1966, Confinia neurologica.

[43]  J. Jacobs,et al.  High-frequency oscillations in epilepsy and surgical outcome. A meta-analysis , 2015, Front. Hum. Neurosci..

[44]  H. Berger,et al.  HANS BERGER ON THE ELECTROENCEPHALOGRAM OF MAN Supplement 28 : Electroencephalography and Clinical Neurophysiology , .

[45]  W. Feindel,et al.  The First Case of Invasive EEG Monitoring for the Surgical Treatment of Epilepsy: Historical Significance and Context , 2005, Epilepsia.

[46]  Fabrice Wendling,et al.  Localization of Epileptogenic Zone on Pre-surgical Intracranial EEG Recordings: Toward a Validation of Quantitative Signal Analysis Approaches , 2014, Brain Topography.

[47]  S. Palmer,et al.  The clinical effectiveness and cost-effectiveness of technologies used to visualise the seizure focus in people with refractory epilepsy being considered for surgery: a systematic review and decision-analytical model. , 2012, Health technology assessment.

[48]  Gary W. Mathern,et al.  Erratum: Definition of drug resistant epilepsy. Consensus proposal by the ad hoc task force of the ILAE commission on therapeutic strategies (Epilepsia (2010) 51 (1069-77)) , 2010 .

[49]  Beate Diehl,et al.  Comparison of bipolar versus monopolar extraoperative electrical cortical stimulation mapping in patients with focal epilepsy , 2014, Clinical Neurophysiology.

[50]  P. Chauvel,et al.  Epileptogenicity of brain structures in human temporal lobe epilepsy: a quantified study from intracerebral EEG. , 2008, Brain : a journal of neurology.

[51]  P Jayakar,et al.  Invasive EEG monitoring in children: when, where, and what? , 1999, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[52]  E. Eskandar,et al.  Decision analysis of intracranial monitoring in non-lesional epilepsy , 2016, Seizure.

[53]  Juan Bulacio,et al.  Technique, Results, and Complications Related to Robot-Assisted Stereoelectroencephalography. , 2016, Neurosurgery.

[54]  J. Gotman,et al.  High‐frequency electroencephalographic oscillations correlate with outcome of epilepsy surgery , 2010, Annals of neurology.

[55]  Heping Zhang,et al.  Localizing Value of Ictal–Interictal SPECT Analyzed by SPM (ISAS) , 2005, Epilepsia.

[56]  Philippe Kahane,et al.  Seizures induced by direct electrical cortical stimulation – Mechanisms and clinical considerations , 2016, Clinical Neurophysiology.

[57]  E. Beghi,et al.  Predictors of epilepsy surgery outcome: a meta-analysis , 2004, Epilepsy Research.

[58]  Bertil Rydenhag,et al.  Complications to invasive epilepsy surgery workup with subdural and depth electrodes: a prospective population-based observational study , 2013, Journal of Neurology, Neurosurgery & Psychiatry.

[59]  P. Kahane,et al.  Manifestations électrocliniques induites par la stimulation électrique intracérébrale par «chocs dans les épilepsies temporales , 1993, Neurophysiologie Clinique/Clinical Neurophysiology.

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

[61]  Andreas Schulze-Bonhage,et al.  Early Seizure Detection Algorithm Based on Intracranial EEG and Random Forest Classification , 2015, Int. J. Neural Syst..

[62]  Beate Diehl,et al.  SCALP EEG SOURCE ANALYSIS IN EXTRATEMPORAL LOBE SEIZURES: COMPARISON WITH INTRACRANIAL FINDINGS , 2010 .

[63]  Woltman Hw Symposium on intracerebral electrography; introduction. , 1953 .

[64]  H. W. Woltman Symposium on intracerebral electrography; introduction. , 1953, Proceedings of the staff meetings. Mayo Clinic.

[65]  Gabriele Arnulfo,et al.  Stereoelectroencephalography: surgical methodology, safety, and stereotactic application accuracy in 500 procedures. , 2013, Neurosurgery.

[66]  Ravindra Arya,et al.  Adverse events related to extraoperative invasive EEG monitoring with subdural grid electrodes: A systematic review and meta‐analysis , 2013, Epilepsia.