Pitfalls in Scalp High-Frequency Oscillation Detection From Long-Term EEG Monitoring

Abstract

Aims: Intracranially recorded high-frequency oscillations (>80 Hz) are considered a candidate epilepsy biomarker. Recent studies claimed their detectability on the scalp surface. We aimed to investigate the applicability of high-frequency oscillation analysis to routine surface EEG obtained at an epilepsy monitoring unit. Methods: We retrospectively analyzed surface EEGs of 18 patients with focal epilepsy and six controls, recorded during sleep under maximal medication withdrawal. As a proof of principle, the occurrence of motor task-related events during wakefulness was analyzed in a subsample of six patients with seizure- or syncope-related motor symptoms. Ripples (80-250 Hz) and fast ripples (>250 Hz) were identified by semi-automatic detection. Using semi-parametric statistics, differences in spontaneous and task-related occurrence rates were examined within subjects and between diagnostic groups considering the factors diagnosis, brain region, ripple type, and task condition. Results: We detected high-frequency oscillations in 17 out of 18 patients and in four out of six controls. Results did not show statistically significant differences in the mean rates of event occurrences, neither regarding the laterality of the epileptic focus, nor with respect to active and inactive task conditions, or the moving hand laterality. Significant differences in general spontaneous incidence [WTS(1) = 9.594; p = 0.005] that indicated higher rates of fast ripples compared to ripples, notably in patients with epilepsy compared to the control group, may be explained by variations in data quality. Conclusion: The current analysis methods are prone to biases. A common agreement on a standard operating procedure is needed to ensure reliable and economic detection of high-frequency oscillations.

Keywords: HFO detection; electroencephalography; epilepsy; high-frequency oscillations; long-term EEG; video-EEG monitoring.

Figure 1

Regions of interest (ROI) electrode maps for the analysis of HFO occurrence during sleep (ROI Sleep) and motor task performance (ROI Task).

Figure 2

Spontaneous HFO incidence in patients with epilepsy and controls: HFO mean (95% CI) rates per minute recorded during sleep over ROI Sleep.

Figure 3

Spontaneous HFO incidence and the epileptic focus laterality: HFO mean (95% CI) rates per minute recorded during sleep over ROI Sleep hemispheres.

Figure 4

Task-related HFO occurrence in patients with motor symptoms: Trigger normalized HFO mean (95% CI) rates over ROI Task hemispheres ipsilateral and contralateral to the moving hand during typing trials and intertrial resting.

Figure 5

Examples of detected EoI. (A) A “false” ripple due to a filtered artifact detected over T11–P11 in patient P53. (B) Background noise mimicking high-frequency activity in the filtered EEG signal of patient P21. (C) A ripple embedded in noise on channels Fp1–F3 of patient P23. Given are signals filtered between 80 and 500 Hz (left), the raw signal (right), and their respective time–frequency plots.