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Epileptic high-frequency oscillations: detection and classification

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Abstract

High-frequency oscillations (HFOs) in intracranial electroencephalograms of patients with epilepsy are regarded as promising biomarkers of epileptogenic zones. Their detection and classification can be achieved by visual assessment or automated approaches, although manual processing of large recordings can be laborious. As a result, an automated analysis scheme is indispensable to enable the clinical use of HFOs. In this paper, we present a two-stage strategy to detect and classify HFOs, which starts with a threshold-based approach to detect plausible HFO events followed by an event classification to discriminate different oscillations. Unlike existing approaches, the detection process in the proposed schemes starts by calculating various multi-channel features that allow interrelations among electrodes to be exploited for detection. On this basis, the detection thresholds are set epoch-by-epoch, relying on a two-component Gaussian mixture model to avoid threshold overestimation. The events deemed to be plausible HFOs are then subjected to classification. By simultaneously examining the raw data and time-frequency maps of these events, they are ultimately sorted into the following categories: HFOs, spikes, and spikes with HFOs, so that the oscillations solely caused by filtering sharp transients can be discriminated. Experimental results using simulated data and intracranial recordings from three epileptic patients demonstrate that our proposed schemes achieve promising sensitivity and precision, especially when the noise level is high.

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References

  • Amiri, M., Lina, J.-M., Pizzo, F., & Gotman, J. (2016). High frequency oscillations and spikes: Separating real HFOs from false oscillations. Clinical Neurophysiology, 127, 187–196.

    Article  Google Scholar 

  • Bénar, C.-G., Chauvière, L., Bartolomei, F., & Wendling, F. (2010). Pitfalls of high-pass filtering for detecting epileptic oscillations: A technical note on false ripples. Clinical Neurophysiology, 121, 301–310.

    Article  Google Scholar 

  • Burnos, S., Hilfiker, P., Sürücü, O., Scholkmann, F., Krayenbühl, N., Grunwald, T., et al. (2014). Human intracranial high frequency oscillations (HFOs) detected by automatic time–frequency analysis. PLoS ONE, 9, 94381.

    Article  Google Scholar 

  • Chaibi, S., Lajnef, T., Sakka, Z., Samet, M., & Kachouri, A. (2013b). A comparaison of methods for detection of high frequency oscillations (HFOs) in human intacerberal EEG recordings. American Journal of Signal Processing, 3, 25–34.

    Google Scholar 

  • Chaibi, S., Lajnef, T., Sakka, Z., Samet, M., & Kachouri, A. (2014). A reliable approach to distinguish between transient with and without HFOs using TQWT and MCA. Journal of Neuroscience Methods, 232, 36–46.

    Article  Google Scholar 

  • Chaibi, S., Sakka, Z., Lajnef, T., Samet, M., & Kachouri, A. (2013a). Automated detection and classification of high frequency oscillations (HFOs) in human intracereberal EEG. Biomedical Signal Processing and Control, 8, 927–934.

    Article  Google Scholar 

  • Chou, C.-W., Chen, C., Kwan, S.-Y., & Wu, S.-C. (2016). Multi-channel algorithms for epileptic high-frequency oscillation detection. In Proceedings of IEEE EMBC.

  • Crépon, B., Navarro, V., Hasboun, D., Clemenceau, S., Martinerie, J., Baulac, M., et al. (2010). Mapping interictal oscillations greater than 200 Hz recorded with intracranial macroelectrodes in human epilepsy. Brain, 133, 33–45.

    Article  Google Scholar 

  • Dümpelmann, M., Jacobs, J., Kerber, K., & Schulze-Bonhage, A. (2012). Automatic 80–250 Hz ripple high frequency oscillation detection in invasive subdural grid and strip recordings in epilepsy by a radial basis function neural network. Clinical Neurophysiology, 123, 1721–1731.

    Article  Google Scholar 

  • Eadie, M. J. (2012). Shortcomings in the current treatment of epilepsy. Expert Review of Neurotherapeutics, 12, 1419–1427.

    Article  Google Scholar 

  • Fedele, T., Burnos, S., Boran, E., Krayenbühl, N., Hilfiker, P., Grunwald, T., et al. (2017). Resection of high frequency oscillations predicts seizure outcome in the individual patient. Scientific Reports, 7, 13836.

    Article  Google Scholar 

  • Gardner, A. B., Worrell, G. A., Marsh, E., Dlugos, D., & Litt, B. (2007). Human and automated detection of high-frequency oscillations in clinical intracranial EEG recordings. Clinical Neurophysiology, 118, 1134–1143.

    Article  Google Scholar 

  • Gliske, S. V., Irwin, Z. T., Chestek, C., & Stacey, W. C. (2016b). Effect of sampling rate and filter settings on high frequency oscillation detections. Clinical Neurophysiology, 127, 3042–3050.

    Article  Google Scholar 

  • Gliske, S. V., Irwin, Z. T., Davis, K. A., Sahaya, K., Chestek, C., & Stacey, W. C. (2016a). Universal automated high frequency oscillation detector for real-time, long term EEG. Clinical Neurophysiology, 127, 1057–1066.

    Article  Google Scholar 

  • Jacobs, J., LeVan, P., Chander, R., Hall, J., Dubeau, F., & Gotman, J. (2008). Interictal high-frequency oscillations (80–500 Hz) are an indicator of seizure onset areas independent of spikes in the human epileptic brain. Epilepsia, 49, 1893–1907.

    Article  Google Scholar 

  • Jacobs, J., Staba, R., Asano, E., Otsubo, H., Wu, J., Zijlmans, M., et al. (2012). High-frequency oscillations (HFOs) in clinical epilepsy. Progress in Neurobiology, 98, 302–315.

    Article  Google Scholar 

  • Jacobs, J., Zijlmans, M., Zelmann, R., Chatillon, C. É., Hall, J., Olivier, A., et al. (2010). High-frequency electroencephalographic oscillations correlate with outcome of epilepsy surgery. Annals of Neurology, 67, 209–220.

    Article  Google Scholar 

  • Jirsch, J., Urrestarazu, E., LeVan, P., Olivier, A., Dubeau, F., & Gotman, J. (2006). High-frequency oscillations during human focal seizures. Brain, 129, 1593–1608.

    Article  Google Scholar 

  • Jmail, N., Gavaret, M., Bartolomei, F., & Bénar, C.-G. (2017). Despiking SEEG signals reveals dynamics of gamma band preictal activity. Physiological Measurement, 38, 42.

    Article  Google Scholar 

  • Jmail, N., Gavaret, M., Wendling, F., Kachouri, A., Hamadi, G., Badier, J.-M., et al. (2011). A comparison of methods for separation of transient and oscillatory signals in EEG. Journal of Neuroscience Methods, 199, 273–289.

    Article  Google Scholar 

  • Kerber, K., Dümpelmann, M., Schelter, B., Le Van, P., Korinthenberg, R., Schulze-Bonhage, A., et al. (2014). Differentiation of specific ripple patterns helps to identify epileptogenic areas for surgical procedures. Clinical Neurophysiology, 125, 1339–1345.

    Article  Google Scholar 

  • Lilly, J. M., & Olhede, S. C. (2009). Higher-order properties of analytic wavelets. IEEE Transactions on Signal Processing, 57, 146–160.

    Article  MathSciNet  Google Scholar 

  • Liu, S., Sha, Z., Sencer, A., Aydoseli, A., Bebek, N., Abosch, A., et al. (2016). Exploring the time–frequency content of high frequency oscillations for automated identification of seizure onset zone in epilepsy. Journal of Neural Engineering, 13, 026026.

    Article  Google Scholar 

  • McLachlan, G., & Krishnan, T. (2008). The EM algorithm and extensions (2nd ed.). New York: Wiley.

    Book  Google Scholar 

  • Mukhopadhyay, S., & Ray, G. (1998). A new interpretation of nonlinear energy operator and its efficacy in spike detection. IEEE Transactions on Biomedical Engineering, 45, 180–187.

    Article  Google Scholar 

  • Navarrete, M., Pyrzowski, J., Corlier, J., Valderrama, M., & Le Van Quyen, M. (2017). Automated detection of high-frequency oscillations in electrophysiological signals: Methodological advances. Journal of Physiology-Paris, 110(4), 316–326.

    Article  Google Scholar 

  • Otsu, N. (1979). A threshold selection method from gray-level histograms. IEEE Transactions on Systems, Man, and Cybernetics, 9, 62–66.

    Article  Google Scholar 

  • Pail, M., Halámek, J., Daniel, P., Kuba, R., Tyrlíková, I., Chrastina, J., et al. (2013). Intracerebrally recorded high frequency oscillations: Simple visual assessment versus automated detection. Clinical Neurophysiology, 124, 1935–1942.

    Article  Google Scholar 

  • Roehri, N., Lina, J.-M., Mosher, J. C., Bartolomei, F., & Bénar, C.-G. (2016). Time–frequency strategies for increasing high-frequency oscillation detectability in intracerebral EEG. IEEE Transactions on Biomedical Engineering, 63, 2595–2606.

    Article  Google Scholar 

  • Roehri, N., Pizzo, F., Bartolomei, F., Wendling, F., & Bénar, C.-G. (2017). What are the assets and weaknesses of HFO detectors? A benchmark framework based on realistic simulations. PLoS ONE, 12, 0174702.

    Article  Google Scholar 

  • Rosner, B. (1995). Fundamentals of biostatistics (4th ed.). London: Duxbury Press.

    Google Scholar 

  • Sokolova, M., & Lapalme, G. (2009). A systematic analysis of performance measures for classification tasks. Information Processing & Management, 45, 427–437.

    Article  Google Scholar 

  • Staba, R. J., Wilson, C. L., Bragin, A., Fried, I., & Engel, J. (2002). Quantitative analysis of high-frequency oscillations (80–500 Hz) recorded in human epileptic hippocampus and entorhinal cortex. Journal of Neurophysiology, 88, 1743–1752.

    Article  Google Scholar 

  • von Ellenrieder, N., Dubeau, F., Gotman, J., & Frauscher, B. (2017). Physiological and pathological high-frequency oscillations have distinct sleep-homeostatic properties. NeuroImage: Clinical, 14, 566–573.

    Article  Google Scholar 

  • Wang, S., Wang, I. Z., Bulacio, J. C., Mosher, J. C., Gonzalez-Martinez, J., Alexopoulos, A. V., et al. (2013). Ripple classification helps to localize the seizure-onset zone in neocortical epilepsy. Epilepsia, 54, 370–376.

    Article  Google Scholar 

  • Worrell, G. A., Jerbi, K., Kobayashi, K., Lina, J.-M., Zelmann, R., & Le Van Quyen, M. (2012). Recording and analysis techniques for high-frequency oscillations. Progress in Neurobiology, 98, 265–278.

    Article  Google Scholar 

  • Wu, J., Sankar, R., Lerner, J., Matsumoto, J., Vinters, H., & Mathern, G. (2010). Removing interictal fast ripples on electrocorticography linked with seizure freedom in children. Neurology, 75, 1686–1694.

    Article  Google Scholar 

  • Yao, D. (2000). Electric potential produced by a dipole in a homogeneous conducting sphere. IEEE Transactions on Biomedical Engineering, 47, 964–966.

    Article  Google Scholar 

  • Zelmann, R., Mari, F., Jacobs, J., Zijlmans, M., Dubeau, F., & Gotman, J. (2012). A comparison between detectors of high frequency oscillations. Clinical Neurophysiology, 123, 106–116.

    Article  Google Scholar 

  • Zijlmans, M., Jacobs, J., Kahn, Y. U., Zelmann, R., Dubeau, F., & Gotman, J. (2011). Ictal and interictal high frequency oscillations in patients with focal epilepsy. Clinical Neurophysiology, 122, 664–671.

    Article  Google Scholar 

  • Zijlmans, M., Jacobs, J., Zelmann, R., Dubeau, F., & Gotman, J. (2009). High-frequency oscillations mirror disease activity in patients with epilepsy. Neurology, 72, 979–986.

    Article  Google Scholar 

Download references

Acknowledgements

The authors would like to acknowledge the financial support of the Ministry of Science and Technology of Taiwan, R.O.C. for the projects under Contract Nos. MOST 104-2221-E-007-145 and MOST 105-2221-E-007-090.

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Correspondence to Shun-Chi Wu or Chien Chen.

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Wu, SC., Chou, CW., Chen, C. et al. Epileptic high-frequency oscillations: detection and classification. Multidim Syst Sign Process 31, 965–988 (2020). https://doi.org/10.1007/s11045-019-00693-0

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