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July 13, 2011
Letter to the Editor

Interictal scalp fast oscillations as a marker of the seizure onset zone

August 9, 2011 issue
77 (6) 524-531

Abstract

Objective:

This study aims to identify if oscillations at frequencies higher than the traditional EEG can be recorded on the scalp EEG of patients with focal epilepsy and to analyze the association of these oscillations with interictal discharges and the seizure onset zone (SOZ).

Methods:

The scalp EEG of 15 patients with focal epilepsy was studied. We analyzed the rates of gamma (40–80 Hz) and ripple (>80 Hz) oscillations, their co-occurrence with spikes, the number of channels with fast oscillations inside and outside the SOZ, and the specificity, sensitivity, and accuracy of gamma, ripples, and spikes to determine the SOZ.

Results:

Gamma and ripples frequently co-occurred with spikes (77.5% and 63% of cases). For all events, the proportion of channels with events was consistently higher inside than outside the SOZ: spikes (100% vs 70%), gamma (82% vs 33%), and ripples (48% vs 11%); p < 0.0001. The mean rates (events/min) were higher inside than outside the SOZ: spikes (2.64 ± 1.70 vs 0.69 ± 0.26, p = 0.02), gamma (0.77 ± 0.71 vs 0.20 ± 0.25, p = 0.02), and ripples (0.08 ± 0.12 vs 0.04 ± 0.09, p = 0.04). The sensitivity to identify the SOZ was spikes 100%, gamma 82%, and ripples 48%; the specificity was spikes 30%, gamma 68%, and ripples 89%; and the accuracy was spikes 43%, gamma 70%, and ripples 81%.

Conclusion:

The rates and the proportion of channels with gamma and ripple fast oscillations are higher inside the SOZ, indicating that they can be used as interictal scalp EEG markers for the SOZ. These fast oscillations are less sensitive but much more specific and accurate than spikes to delineate the SOZ.

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Supplementary Material

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Letters to the Editor
17 October 2011
Using Ripples from Scalp EEG to Localize the Seizure Onset Zone
Daniel M. Goldenholz, Resident physician
Masud Seyal, Lisa M. Bateman

Andrade et al. [1] propose a promising method for localizing the seizure onset zone (SOZ) in scalp EEG recordings. The methods are accessible for implementation in most EEG laboratories. Critically, when the SOZ is ill-defined on scalp recordings, ripples may help guide intracranial electrode placement; in the future they may sometimes circumvent the need for such electrodes. Because certain filter parameters can sometimes result in spurious high frequency oscillations [2], labs trying to reproduce these results will need the unstated filter settings used by the authors. The authors show examples of the ripples and artifacts prior to filtering, which suggest proper settings were chosen. Three of their patients were evaluated with scalp and intracranial recordings, showing agreement between the SOZ in each. Given that prior studies of ripples were performed with depth electrode recordings, it is unfortunate that those data were excluded from the present study. We look forward to reading more about that data, which would link prior studies to the present conclusions, in the near future. The next important steps are determining the relationship between scalp recorded ripples and surgical outcome, and perhaps to automating the method to increase inter-rater reliability. [3]

1. Andrade-Valenca LP, Dubeau F, Mari F, Zelmann R, Gotman J. Interictal scalp fast oscillations as a marker of the seizure onset zone. Neurology. 2011 Aug 9;77:524-31. Epub 2011 Jul 13.

2. Benar CG, Chauvie`re L, Bartolomei F, Wendling F. Pitfalls of high-pass filtering for detecting epileptic oscillations: a technical note on "false" ripples. Clin Neurophysiol 2010;121:301-310.

3 .Blanco JA, Stead M, Krieger A, Viventi J, Marsh WR, Lee KH, Worrell GA, Litt B. Unsupervised classification of high-frequency oscillations in human neocortical epilepsy and control patients. J Neurophysiol. 2010 Nov;104:2900-12. Epub 2010 Sep 1.

For full disclosures, contact editorial office at [email protected].
17 October 2011
Reply from the authors
Jean Gotman, Professor
Luciana Andrade-Valenca, Rina Zelmann, Francois Dubeau

Goldenholz et al. asked about our filter, which is a Finite Impulse Response filter of order 63. They also inquired about the relationship between scalp HFOs and those recorded in intracerebral electrodes. This is a complex problem for two reasons. Firstly, we do not have simultaneous scalp and intracerebral recordings. Secondly, intracerebral electrodes record from a small brain volume and it is unlikely that HFOs seen at one intracerebral contact could be visible on the scalp. As we discussed, [1] HFOs visible on the scalp may come from rare HFOs that occur synchronously over a relatively large area (3 or 4 cm2). We are currently analyzing simultaneous scalp and subdural recordings to further understand the relationship between intracerebral and scalp signals. Finally, Goldenholz et al. mention the need for automatic detection of scalp-recorded high frequencies. We refer them to our recently published method. [2] We hope that HFOs may become a marker of the epileptogenic zone [3] and a marker of developing epileptogenesis after an initial brain injury.

1. Andrade-Valenca LP, Dubeau F, Mari F, Zelmann R, Gotman J. Interictal scalp fast oscillations as a marker of the seizure onset zone. Neurology 2011;77:524-531.

2. von Ellenrieder N, Andrade-Valenca LP, Dubeau F, Gotman J. Automatic detection of fast oscillations (40-200 Hz) in scalp EEG recordings. Clin Neurophysiol, in press. http://dx.doi.org/10.1016/j.clinph.2011.07.050

3. Jacobs J, Zijlmans M, Zelmann R, et al. High-frequency electroencephalographic oscillations correlate with outcome of epilepsy surgery. Ann Neurol 2010;67:209-222.

For full disclosures, see original article.

Information & Authors

Information

Published In

Neurology®
Volume 77Number 6August 9, 2011
Pages: 524-531
PubMed: 21753167

Publication History

Received: September 17, 2010
Accepted: February 7, 2011
Published online: July 13, 2011
Published in print: August 9, 2011

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Disclosure

Dr. Andrade-Valenca received scholarship support from the Canadian Institutes of Health Research. Dr. Dubeau serves as an Associate Editor for Epileptic Disorders and received research support from the Canadian Institutes of Health Research. Dr. Mari received scholarship support from the Canadian Institutes of Health Research. R. Zelmann received scholarship support from the National Science and Engineering Research Council, Canada. Dr. Gotman has received funding for travel and research support from the Canadian Institutes of Health Research; serves on the editorial boards of Epilepsia and the Journal of Clinical Neurophysiology; and serves as a consultant for (and is former CEO of) Stellate and Lacerta Research, in both of which he is a major stockholder.

Authors

Affiliations & Disclosures

L.P. Andrade-Valenca, MD, PhD
From the Montreal Neurological Institute (L.P.A.-V., F.D., F.M., R.Z., J.G.), McGill University, Montreal, Canada; and Department of Neurology (L.P.A.-V.), University of Pernambuco-UPE, Recife, Pernambuco, Brazil.
F. Dubeau, MD
From the Montreal Neurological Institute (L.P.A.-V., F.D., F.M., R.Z., J.G.), McGill University, Montreal, Canada; and Department of Neurology (L.P.A.-V.), University of Pernambuco-UPE, Recife, Pernambuco, Brazil.
F. Mari, MD, PhD
From the Montreal Neurological Institute (L.P.A.-V., F.D., F.M., R.Z., J.G.), McGill University, Montreal, Canada; and Department of Neurology (L.P.A.-V.), University of Pernambuco-UPE, Recife, Pernambuco, Brazil.
R. Zelmann, MEng
From the Montreal Neurological Institute (L.P.A.-V., F.D., F.M., R.Z., J.G.), McGill University, Montreal, Canada; and Department of Neurology (L.P.A.-V.), University of Pernambuco-UPE, Recife, Pernambuco, Brazil.
J. Gotman, PhD
From the Montreal Neurological Institute (L.P.A.-V., F.D., F.M., R.Z., J.G.), McGill University, Montreal, Canada; and Department of Neurology (L.P.A.-V.), University of Pernambuco-UPE, Recife, Pernambuco, Brazil.

Notes

Address correspondence and reprint requests to Dr. Andrade-Valenca, 3801 University Street, Montreal Neurological Institute, McGill University, Montreal, Quebec, Canada H3A 2B4 [email protected]
Study funding: Supported by the Canadian Institutes of Health Research grants MOP-102710, MOP 10189.

Author Contributions

Dr. Andrade-Valença: drafting/revising the manuscript, study concept or design, analysis or interpretation of data, acquisition of data, statistical analysis. Dr. Dubeau: drafting/revising the manuscript, study concept or design, analysis or interpretation of data, study supervision. Dr. Mari: analysis or interpretation of data, acquisition of data. R. Zelmann: study concept or design, analysis or interpretation of data, signal processing of data. Dr. Gotman: drafting/revising the manuscript, study concept or design, analysis or interpretation of data, study supervision, obtaining funding.

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