Prediction of seizure outcome improved by fast ripples detected in low-noise intraoperative corticogram

OBJECTIVE Fast ripples (FR, 250-500Hz) in the intraoperative corticogram have recently been proposed as specific predictors of surgical outcome in epilepsy patients. However, online FR detection is restricted by their low signal-to-noise ratio. Here we propose the integration of low-noise EEG with unsupervised FR detection. METHODS Pre- and post-resection ECoG (N=9 patients) was simultaneously recorded by a commercial device (CD) and by a custom-made low-noise amplifier (LNA). FR were analyzed by an automated detector previously validated on visual markings in a different dataset. RESULTS Across all recordings, in the FR band the background noise was lower in LNA than in CD (p<0.001). FR rates were higher in LNA than CD recordings (0.9±1.4 vs 0.4±0.9, p<0.001). Comparison between FR rates in post-resection ECoG and surgery outcome resulted in positive predictive value PPV=100% in CD and LNA, and negative predictive value NPV=38% in CD and NPV=50% for LNA. Prediction accuracy was 44% for CD and 67% for LNA. CONCLUSIONS Prediction of seizure outcome was improved by the optimal integration of low-noise EEG and unsupervised FR detection. SIGNIFICANCE Accurate, automated and fast FR rating is essential for consideration of FR in the intraoperative setting.

[1]  Walter J. Freeman,et al.  Origin, structure, and role of background EEG activity. Part 3. Neural frame classification , 2005, Clinical Neurophysiology.

[2]  J. Gotman,et al.  High-frequency oscillations (HFOs) in clinical epilepsy , 2012, Progress in Neurobiology.

[3]  Jerome Engel,et al.  High-frequency oscillations in epileptic brain , 2010, Current opinion in neurology.

[4]  G Curio,et al.  Extension of non-invasive EEG into the kHz range for evoked thalamocortical activity by means of very low noise amplifiers , 2011, Physiological measurement.

[5]  Y. Netzer,et al.  The design of low-noise amplifiers , 1981, Proceedings of the IEEE.

[6]  Lalu Mansinha,et al.  Localization of the complex spectrum: the S transform , 1996, IEEE Trans. Signal Process..

[7]  J. Sarnthein,et al.  Human Intracranial High Frequency Oscillations (HFOs) Detected by Automatic Time-Frequency Analysis , 2014, PloS one.

[8]  L. Trahms,et al.  The influence of amplifier, interface and biological noise on signal quality in high-resolution EEG recordings , 2006, Physiological measurement.

[9]  Gabriel Curio,et al.  Non-invasive single-trial EEG detection of evoked human neocortical population spikes , 2015, NeuroImage.

[10]  Andreas Schulze-Bonhage,et al.  Reoperation for refractory epilepsy in childhood: a second chance for selected patients. , 2013, Neurosurgery.

[11]  L. Xiong,et al.  Different Propofol–Remifentanil or Sevoflurane–Remifentanil Bispectral Index Levels for Electrocorticographic Spike Identification during Epilepsy Surgery , 2013, Anesthesiology.

[12]  J. Jefferys,et al.  High‐frequency oscillations as a new biomarker in epilepsy , 2012, Annals of neurology.

[13]  R. Zelmann,et al.  High frequency oscillations in intra-operative electrocorticography before and after epilepsy surgery , 2014, Clinical Neurophysiology.

[14]  Gilles Plourde,et al.  Attenuation of High-Frequency (50–200 Hz) Thalamocortical Electroencephalographic Rhythms by Isoflurane in Rats Is More Pronounced for the Thalamus Than for the Cortex , 2016, Anesthesia and analgesia.

[15]  G. Curio,et al.  Ultra-low-noise EEG/MEG systems enable bimodal non-invasive detection of spike-like human somatosensory evoked responses at 1 kHz , 2015, Physiological measurement.

[16]  Viraj M Shah,et al.  Anesthesia considerations in epilepsy surgery. , 2016, International journal of surgery.

[17]  A. D. Watts,et al.  The effect of sevoflurane and isoflurane anesthesia on interictal spike activity among patients with refractory epilepsy. , 1999, Anesthesia and analgesia.

[18]  Tommaso Fedele,et al.  Automatic detection of high frequency oscillations during epilepsy surgery predicts seizure outcome , 2016, Clinical Neurophysiology.

[19]  C. Bénar,et al.  Pitfalls of high-pass filtering for detecting epileptic oscillations: A technical note on “false” ripples , 2010, Clinical Neurophysiology.

[20]  Maeike Zijlmans,et al.  Epileptic high‐frequency oscillations in intraoperative electrocorticography: The effect of propofol , 2012, Epilepsia.

[21]  D. Louis Collins,et al.  High‐frequency oscillations, extent of surgical resection, and surgical outcome in drug‐resistant focal epilepsy , 2013, Epilepsia.

[22]  G. Curio,et al.  Recording human cortical population spikes non-invasively – An EEG tutorial , 2015, Journal of Neuroscience Methods.

[23]  Naoki Akamatsu,et al.  Effects of General Anesthesia on High-Frequency Oscillations in Somatosensory Evoked Potentials , 2006, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[24]  Maeike Zijlmans,et al.  Residual fast ripples in the intraoperative corticogram predict epilepsy surgery outcome , 2015, Neurology.

[25]  G. Mathern,et al.  Removing interictal fast ripples on electrocorticography linked with seizure freedom in children , 2010, Neurology.

[26]  Ayako Ochi,et al.  Focal resection of fast ripples on extraoperative intracranial EEG improves seizure outcome in pediatric epilepsy , 2011, Epilepsia.

[27]  Jean Gotman,et al.  The morphology of high frequency oscillations (HFO) does not improve delineating the epileptogenic zone , 2016, Clinical Neurophysiology.

[28]  Andreas Schulze-Bonhage,et al.  Epilepsy surgery for glioneuronal tumors in childhood: avoid loss of time. , 2014, Neurosurgery.

[29]  T. Fedele.  High-frequency electroencephalography (hf-EEG): non-invasive detection of spike-related brain activity , 2014 .

[30]  Gabriel Curio,et al.  Non-invasive single-trial detection of variable population spike responses in human somatosensory evoked potentials , 2016, Clinical Neurophysiology.

[31]  I. Constant,et al.  Sevoflurane and epileptiform EEG changes , 2005, Paediatric anaesthesia.

[32]  G. Buzsáki,et al.  Neuronal Oscillations in Cortical Networks , 2004, Science.

[33]  Andreas Schulze-Bonhage,et al.  Seizure and cognitive outcomes of epilepsy surgery in infancy and early childhood. , 2013, European journal of paediatric neurology : EJPN : official journal of the European Paediatric Neurology Society.

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

[35]  M. Burghoff,et al.  Towards non-invasive multi-unit spike recordings: Mapping 1kHz EEG signals over human somatosensory cortex , 2011, Clinical Neurophysiology.