Comparison of Algorithms for Detection of High

Frequency Oscillations in Intracranial EEG

J. Balach1, P. Jezdik1, R. Cmejla1, P. Krsek2, P. Marusic3, P. Jiruska4

1
Faculty of Electrical Engineering, Czech Technical University in Prague, Prague, Czech Republic
2
Department of Pediatric Neurology and 3Department of Neurology, 2nd Faculty of Medicine, Charles University in Prague,
University Hospital Motol, Prague, Czech Republic
4
Department of Developmental Epileptology, Institute of Physiology, Academy of Sciences of Czech Republic, Prague, Czech
Republic

balacjir@fel.cvut.cz, jezdip1@fel.cvut.cz, cmejla@fel.cvut.cz, pavel.krsek@post.cz, Petr.Marusic@fnmotol.cz,

jiruskapremysl@gmail.com

Abstract— High frequency oscillations (HFOs) are novel
biomarkers of epileptogenic tissue. Visual identification of HFO
in long-term EEG recordings is time consuming due to low HFOs
rate, low signal-to-noise ratio and presence of biological and
technical artifacts. In this study, we have examined several
algorithms of HFOs detection to facilitate analysis of intracranial
recordings and increase their diagnostic yield. We have evaluated
three newly designed and three published HFOs detectors.
Detectors were applied on datasets containing HFOs labeled by
experienced readers and their performance evaluated. Results of
the detection and properties of the algorithms are reviewed and
discussed in respect to clinical practice and their possible
utilization during the diagnostic workup in patients with
epilepsy.
Keywords—EEG; high-frequency oscillations; automated
detection; algortithm comparision; epilepsy
I. INTRODUCTION
Epilepsy is the second most common neurological disease
affecting 0.5-1% of the population [1]. Approximately 30% of
patients develop pharmacoresistant form of the epilepsy.
Small proportion of patients can benefit from the surgical
treatment. The main aim of epilepsy surgery is to remove
areas of the brain involved in seizure genesis – epileptogenic
zone [2].
Prior to surgery, patients must undergo thorough and
complex presurgical examination to determine the areas of the
brain which are necessary to remove to achieve the seizure
freedom. In cases where the exact resection margins can’t be
determined by non-invasive techniques, patients are implanted
with intracerebral electrodes and intracranial EEG (iEEG) is
recorded. The iEEG is usually recorded from large number of
electrode contacts. Traditional biomarkers of epileptic tissue
are interictal epileptiform discharges (spikes, sharp waves,
polyspikes etc.). However, interictal epileptiform discharges
have low specificity to mark the epileptogenic zone.
High frequency oscillations (HFOs) represent novel and
promising biomarker of the epileptogenic tissue. HFOs are
present at the seizure onset, during seizures and during periods
between seizures. Previous studies have demonstrated that
spatial distribution of pathological HFOs overlaps with the
areas of the seizure onset. Several studies also demonstrated
that HFOs mark the epileptogenic zone and resection of the
areas generating HFOs was associated with better outcome of
the epilepsy surgery [3]. Typically, frequency of HFOs ranges
from 70 Hz up to 600 Hz, but regional differences in HFO
frequency exist. In macroelectrode recordings, amplitude of
HFOs can reach up to tens of µV. Currently, interictal HFOs
are used as the main source of information about the
spatiotemporal profile of HFOs [4, 5].
The incidence of HFOs events is usually very low. To
obtain sufficient number of HFOs requires recording of iEEG
for long periods of time. To visually analyze long-term
recordings from dozens or hundreds of channels is extremely
difficult, virtually impossible. Visual assessment is also very
prone to bias. Accurate automatic detection of HFOs
represents an unmet need in clinical neurophysiology.
Numerous algorithms for automated HFO detection and
evaluation were already developed. Each detector utilizes
different algorithm for HFOs detection. In this study we have
compared the performance of three published detectors [6-8]
published with three new detectors.
II. HFO DETECTORS
In this study we have implemented three published
detectors and developed three new HFOs detecting algorithm.
Published detectors were following: RMS [6], Line Length [7]
and Hilbert [8].
RMS algorithm detects signal energy changes and
represents one of the earliest and commonly used HFO
detectors. The algorithm computes the RMS value of the
filtered signal (100-500 Hz) in sliding window. Sections
where the RMS value passes five times standard deviation
level with duration of at least 6 ms are marked as a probable

978-1-4799-2921-4/14/$31.00 ©2014 IEEE

HFOs event. If the absolute value of the filtered signal has at where are signal samples and N is number of the samples in
least six peaks with amplitude higher than three standard the sliding window of the length one second.
deviations, the event is confirmed as HFO. For the purpose of
this study, this detector is referred as RMS Detector [4, 6]. The Bayesian evidence is computed from the signal
filtered by 6th order Chebyshev2 high pass filter with cutoff
Second published detector utilizes the short line lengths frequency 80 Hz. Envelope of the evidence is estimated by
parameterization (sum of the signal differences in short time spline interpolation of all local maxima. The envelope is taken
window) to identify the HFOs. Signal is band pass filtered as the threshold value. All segments where the evidence
(80-100 Hz) and its spectrum is equalized by first order crosses the threshold are marked as candidate HFOs events.
differential filter. Threshold value is set as 97.5 percentile of Segments with time separation less than 50 ms are merged,
the cumulative distribution function from three minutes long while segments with duration less than 40 ms are discarded. In
epochs. This detector will be referred as Line Length Detector segments containing candidate HFOs events, instantaneous
[7]. frequency is calculated using Hilbert-Huang transformation.
Each segment with the mean frequency over 70 Hz is
Next implemented detector uses Hilbert envelope
classified as HFOs event.
estimation from the filtered signal (180-400 Hz). Threshold
value is five times the standard deviation calculated from the
entire recording. Local maxima of the envelope are marked as III. METHODS AND DATA
an identified event if they cross the threshold. This detector
will be referred as Hilbert Detector [8]. A. Data Source
For detector testing, two long term intracranial recordings
The first detector designed by our research group
from two patients were used. Data were low-pass filtered with
calculates Hilbert envelope of the filtered signal (80-500 Hz).
cutoff frequency 300 Hz and sampled at 1 kHz. Only channels
The threshold level is dynamically adjusted by estimation of
with visible HFO were chosen for expert labeling. Details are
the amplitude distribution in segments with duration of 4
shown in Table 1.
seconds. The threshold value is weighted with a combination
of median and mean of this distribution. In the last step, the
neighboring HFOs events with gap less than 40 ms are merged B. Testing Dataset
and marked as one event. Events with duration less than 50 ms Two biomedical engineers (J.B. and T.H.) visually
were removed. The detector was named ISARG H. Detector preselected the candidate HFOs events for expert labeling.
[9]. Several criteria for identification of HFOs events were already
published [6, 8, 11, 12]. We used these criteria to preselect the
The second developed detector (ISARG B. Detector) is HFOs. The event had to have sinusoid waveform with at least
based on the segmentation by short time energy change. three periods visible in the raw data. Ripples were defined as
Energy of the band pass (60-300 Hz) filtered signal is an oscillation present within the 70-200 Hz band-passed
measured in 100 ms sliding window with 60% overlap. The signal. Fast ripples were defined as an oscillation present in
threshold for detection was set to 95th percentile of the energy high-passed (>200 Hz) signal. Amplitude of the events had to
calculated from 90 s long epochs surrounding the window. be at least twice higher than the background activity of the
Number of local extremes is counted in the selected segments. filtered signal. HFOs could occur independently or
If there are at least 8 local extremes with sufficient gradient superimposed on interictal epileptiform discharge.
and with the energy increase in the frequency band above 75
Hz, the segment is considered as HFOs event. In total, 593 events (242 from patient 1 and 351 from
patient 2) were selected. All selected segments were reviewed
The last detector (ISARG Bayes Detector) utilizes and labeled by two neurologists and two biomedical engineers.
Bayesian evidence principle [10]. Detection of HFOs in iEEG To facilitate the labelling procedure, we have developed
can be seen as a detection of signal in random noise. Bayesian simple HFOs labelling application.
evidence in our experiments assumes existence of the simplest
model consisting of the constant signal in a random Gaussian
noise. The evidence for this simplest model will be maximal if
only noise is present in the signal. Decrease of the evidence TABLE 1. CHANNELS DESCRIPTION
suggests the presence of HFOs (higher amplitudes of HFOs
are associated with lower value of Bayesian evidence). No. of
selected
The simple form of the logarithm of Bayesian evidence BE channels duration
channels
electrode note
(probability of the data given by the model) was found from (No. of
electrodes x
the closed form of Bayesian evidence after the marginalization contacts)
of nuisance parameters and using model consisting of constant slow
in noise [10]: patient
97 3 minutes 16(2x8) subdural strip wave
1
sleep
slow
patient
94 9 minutes 8(1x8) subdural strip wave
(1) 2
sleep
 Using this application, reviewers were provided with the
complex information about the signal. Raw data on different 40
time scale, filtered data and the time-frequency plot were Ground Possible
shown for each candidate event. The candidate event could be 35 Gold Standard
Ground Trust
classified as “HFOs”, “Maybe HFOs”, “Not HFOs”. This
30
classification was numerically scored (1, 0.5, 0) for later
statistical evaluation.

HFO quantity [-]

25
Three sets of labeled events with different level of the
inter-reader agreement were generated. 20

 First (the most strict) set was called “Ground 15

Trust” (GT). Only events with agreement „is
HFO“ between all readers were accepted HFO: 10

(2)
0
60 70 80 90 100 110 120 130
HFO frequency [Hz]

where xi are evaluations of one event and N is number
of evaluators.
 Second (less strict) set represents agreement
between half of the readers. It is called „Gold
Standard“
(3)
 The last set (Ground Possible) contains HFO
events which were labeled as an HFO at least by
one expert or as a candidate HFOs by at least two
readers.
Fig. 1. Testing set HFOs frequency histogram
detection, when detected HFOs event does not have
corresponding event labeled by human reader; false negative
(FN) - missed detection when HFOs event was labeled by
reader but missed by the detector.
HFO detectors were applied on both datasets. Results were
compared with the labeled events. Statistical parameters were
determined for each detector and for each set. Sensitivity and
Positive Predictive Value measures were used to describe the
detector’s performance. Sensitivity represents percentage of
detected HFOs events
(5)

(4) Positive Predictive Value (PPV) represents percentage of

correct detections.
(6)
C. Statistic Evaluation of Detectors Performance
The detectors performance was evaluated using the
following parameters: true positive (TP) - correct detection of
HFOs labeled by reader; false positive (FP) - incorrect

TABLE 2. RESULTS OF DETECTOR PERFORMANCE

Number of Sensitivity [%] Positive Predictive Value [%]

detection Ground Trust Gold Standard Ground Possible Ground Trust Gold Standard Ground Possible

RMS Detector 229 55.00 44.66 33.85 24.02 49.34 57.64

Line Length Detector 7371 91.00 92.49 87.44 1.23 3.17 4.63

Hilbert Detector 7432 79.00 80.24 72.56 1.06 2.73 3.81

ISARG H. Detector 1053 93.00 91.70 87.69 8.83 22.03 32.48

ISARG B. Detector 305 52.00 50.59 39.29 17.05 41.97 50.16

ISARG Bayes Detector 3476 92.00 93.28 85.90 2.65 6.79 9.64

IV. RESULTS
100 signal segments corresponding to HFO event in
Ground Trust set, 253 segments in Gold Standard set and 390
segments in Ground Possible set were taken from all labeled
593 segments. All HFO events in sets have maximal energy on
frequencies from 60 Hz to 130 Hz. The Fig. 1 shows the
histogram of frequency bins of maximal energy in particular
HFO event in the set. Two dominant peaks are at 65 Hz and
90 Hz. This distribution falls in to ripples range.
Individual algorithms demonstrated different performance
Table 2. Line Length and Hilbert detectors had the highest
number of detections n=7371 and n=7432 respectively. The
lowest number of the detection was achieved by RMS and
ISARG B. detectors (n=229 and n=305). According to the
results, the detectors can be divided into two groups. One
group is characterized by high sensitivity. These algorithms
detect nearly all the labeled HFOs events, but suffer from the
high false positive detection rate. Second group of detectors
have high positive prediction value but lower sensitivity.
ISARG H. detector demonstrated the best performance from
all evaluated detectors. This detector has satisfactory PPV
with relatively high sensitivity.
V. DISCUSSION
In this study we have examined the performance of six
HFOs detectors. Line Length and Hilbert detector are
characterized by high sensitivity. Presence of high false
positive rate makes these detectors less practical for the
purpose of automatic detections. To decrease the number of
false positive detections would require implementation of
additional post-processing steps which would discard these
detections. Improvement their performance may also require
better understanding of false positive detections. False
detections may represent several types of artifacts, which have
spectral profile similar to pathological HFOs: filtration
artifacts of spikes or fast transients, main’s frequency
contaminations and its harmonics, muscles activity, etc.
However, false positive detection may also contain true HFOs
not labeled by readers. Algorithms with high Positive
Predictive Value (RMS or ISARG B) provide more reliable.
However, these detectors may miss large number of HFOs
which may relevant for the presurgical examination. Optimal
approach to HFOs detection must be determined in future. Our
study demonstrated benefits of each algorithm. Selection of
the appropriate detector may depend on the aims of the study.
The datasets used in this study enabled evaluation of the HFOs
mainly from the ripple frequency band. In future study we will
examine the performance of the detectors on wide band
signals. Using similar approach, we will evaluate whether the
detection of ripples and fast ripples will demonstrate similar or
different performance.
ACKNOWLEDGMENT
Supported by grants from the Ministry of Health of the
Czech Republic (IGA NT/14489-3, NT/13357), Neuron Fund
for Support of Science (Czech Republic, 2012/10) and Czech
Science Foundation (Czech Republic, P303/14-02634S) and
SGS 13/138/OHK3/2T/13
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