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REVIEW

C URRENT
OPINION Recent advances in clinical electroencephalography
Birgit Frauscher a, Andrea O. Rossetti b and Sandor Beniczky c,d
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Purpose of review
Clinical electroencephalography (EEG) is a conservative medical field. This explains likely the significant
gap between clinical practice and new research developments. This narrative review discusses possible
causes of this discrepancy and how to circumvent them. More specifically, we summarize recent advances
in three applications of clinical EEG: source imaging (ESI), high-frequency oscillations (HFOs) and EEG in
critically ill patients.
Recent findings
Recently published studies on ESI provide further evidence for the accuracy and clinical utility of this
method in the multimodal presurgical evaluation of patients with drug-resistant focal epilepsy, and opened
new possibilities for further improvement of the accuracy. HFOs have received much attention as a novel
biomarker in epilepsy. However, recent studies questioned their clinical utility at the level of individual
patients. We discuss the impediments, show up possible solutions and highlight the perspectives of future
research in this field. EEG in the ICU has been one of the major driving forces in the development of
clinical EEG. We review the achievements and the limitations in this field.
Summary
This review will promote clinical implementation of recent advances in EEG, in the fields of ESI, HFOs and
EEG in the intensive care.
Keywords
electroencephalography, epilepsy, high-frequency oscillations, ICU, source imaging

INTRODUCTION although these can be effectively applied in EEG

Electroencephalogram (EEG) is one of the most
important diagnostic methods in patients with epi-
lepsy [1]. It confirms the diagnosis and it helps in
classification [1]. In 2024, we will celebrate 100 years
since the start of human EEG recordings. More than
58 000 peer-reviewed articles have been published
about clinical application of EEG in epilepsy, with
an increasing number of technical advances during
the last decades. Disappointingly, these advances
are rarely implemented in clinical centers, or imple-
mented with a long latency and in few places.
Arguably, clinical EEG is one of the most conserva-
tive medical fields: in most centers, EEGs are
recorded, visualized and interpreted almost the
same way as one generation ago.
The reluctance to embrace new technology in
clinical EEG is partly explained by the paucity of
compelling evidence for the validity of the
new methods. Studies describing new EEG tech-
nology are often of small sample-size, retrospec-
tive, and with a questionable gold standard.
Unfortunately, few articles on clinical EEG report
their findings along the STARD criteria (standards
for reporting diagnostic accuracy studies) [2],
studies too [3].
On the other hand, this reluctance has also been
present for aspects confirmed by numerous and
high-quality studies, meta-analyses and included
into international guidelines. Examples are the
extended EEG electrode array and EEG Source Imag-
ing (ESI) in presurgical evaluation. Although the
International Federation of Clinical Neurophysiol-
ogy (IFCN) recommended an extended EEG elec-
trode array, with 25 electrodes (including the
inferior temporal electrode chains) [4], many cen-
ters still use the classical 10–20 system of 19
a
Department of Neurology, Duke University Medical Center & Depart-
ment of Biomedical Engineering, Duke Pratt School of Engineering,
Durham, North Carolina, USA, bDepartment of Clinical Neuroscience,
Lausanne University Hospital (CHUV) and University of Lausanne,
Lausanne, Switzerland, cDepartment of Clinical Neurophysiology, Dan-
ish Epilepsy Centre, Dianalund and dAarhus University Hospital, Aarhus,
Denmark
Correspondence to Sandor Beniczky, Visby All
e 5, Dianalund 4293,
Denmark. E-mail: sbz@filadelfia.dk
Curr Opin Neurol 2024, 37:000–000
DOI:10.1097/WCO.0000000000001246

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Seizure disorders
KEY POINTS
 Recent advances in ESI include methods modelling
propagation, use of artificial intelligence and
automated analysis.
 A recent negative trial on the use of HFOs as epilepsy
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biomarker ignited new promising research avenues to
develop techniques to better record, detect and
analyse HFOs.
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 EEG use in the ICU has been considerably expanded;
recent efforts have been directed towards optimizing
recording length.
electrodes. In spite of two meta-analyses showing
the accuracy of ESI [5,6] and an IFCN guideline
recommending its use in presurgical evaluation
[7], only a minority of centers have integrated ESI
into their multimodal presurgical evaluation of
patients with drug-resistant focal epilepsy [8].
The International League Against Epilepsy
(ILAE) and the IFCN have joined forces to develop
clinical practice guidelines and international stand-
ards for the clinical application of EEG in epilepsy,
based on systematic literature search and grading
the published evidence. Recently, minimum stand-
ards for routine EEG and for long-term video-EEG
recordings have been published [9,10]. Hopefully,
this will contribute to updating the clinical practice
in many EEG laboratories.
This review article summarizes recent advances
in selected applications of clinical EEG: ESI, high-
frequency oscillations (HFOs) and EEG in critically
ill patients.
ELECTROENCEPHALOGRAM SOURCE
IMAGING
As mentioned already in the introduction, ESI has
been previously validated for clinical implementa-
tion in presurgical evaluation. Recently published
studies have provided further evidence for the accu-
racy and clinical utility of ESI, and opened new
possibilities for further improvement of the accu-
racy and a broader clinical implementation.
One of the challenges validating ESI is the lack of
a perfect gold standard for the localization, since all
approaches have advantages and disadvantages.
This was circumvented by analyzing the location
of single pulse electric stimulation [11,12].
Although this is an artificial signal (as opposed to
epileptiform discharges generated in the cortical
neurons), the location of the source (i.e., the corti-
cally placed electrode contacts) is certain, and these
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studies provide important information about the
accuracy and biophysical limitations of ESI. These
studies confirmed that electrical sources in the
brain, recorded with scalp electrodes, can be local-
ized with an error down to 1 cm.
A head-to-head comparison between electro-
magnetic source imaging and EEG-fMRI, evaluated
the accuracy of these methods to localize the irrita-
tive zone and seizure-onset zone (as defined by
&
SEEG) and to predict postsurgical outcome [13 ].
Seventeen patients were included. The authors con-
cluded that the irritative zone was better localized by
ESI, while the seizure-onset zone was better localized
by EEG-fMRI. However, source imaging was better
than EEG-fMRI to predict the postsurgical outcome
(80 vs. 54%).
A returning question about ESI has been the
reproducibility of the methods. Different inverse
solutions and software packages may lead to differ-
ent results [14]. Several aspects tailored to the indi-
vidual patient involve subjective decisions of the
expert performing the analysis. A recent study,
which included 25 consecutive patients analyzed
by six different experts, showed that when experts
used the same analysis pipeline and same software,
the inter-analyzer agreement was substantial [15].
These results support the need for standardization in
ESI methodology, applied in clinical practice.
Another way to standardize ESI is automating the
whole process or the most time-consuming parts of
it (semi-automated approach). A recently published
single-center, prospective study on semi-automated
ESI, which included 40 operated patients, found an
accuracy of 75%, which is similar to what has been
previously reported using the expert-based (manual)
&
methods [16 ].
Several new approaches gave promising results.
Signal-propagation induces additional uncertainty in
ESI. Recently, a method has been proposed to incor-
porate both local propagation via slower cortical
traveling waves and more distant, rapid propagation
&
via white matter conduction [17 ]. The retrospective
study included 38 patients who underwent intracra-
nial EEG recordings and diffusion-weighted imaging.
The authors concluded that the novel approach
accounting for the dual modes of propagation was
more accurate in predicting seizure outcomes than
the leading electrode location. Another, recently
published, novel method for localizing epileptiform
EEG discharges used Relative Source Power maps
&
[18 ]. In 33 patients with lesional, extratemporal
epilepsy, the authors found that the Relative Source
Power maps were more accurate and easier to inter-
pret than classical voltage maps. Another novel, data-
driven approach used an artificial intelligence-based
&&
source imaging framework [19 ]. The seminal article
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Recent advances in clinical electroencephalography Frauscher et al.
indicated that this may be more accurate than the
conventional ESI. The study included 20 patients and
compared the accuracy of source imaging with inva-
sive measurements and surgical outcome. These
novel methods, their accuracy and clinical utility
need to be confirmed in future, large, prospective
trials.
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HIGH-FREQUENCY OSCILLATIONS IN
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INTRACRANIAL
ELECTROENCEPHALOGRAM OF PATIENTS
WITH EPILEPSY
HFOs, defined as isolated events with at least four
consecutive oscillations exceeding 80 Hz (ripples
80–250 Hz, fast ripples >250 Hz), have been sug-
gested to have high clinical promise to improve
identification of the epileptogenic zone [20]. This
enthusiasm was based on several single-center and
uncontrolled studies, with more recent work ques-
tioning their usefulness at the individual level [21].
Identified gaps in knowledge potentially explaining
the lack of translation of HFOs into clinical patient
care have been absence of controlled and prospec-
tive studies to clarify more recent skepticism, lack of
studies performing head-to-head comparisons with
other new interictal epilepsy biomarkers, the chal-
lenge to disentangle physiological from pathologi-
cal HFOs required to optimize localization accuracy,
and absence of fully automated detection imple-
mented in commercial EEG software solutions.
Here, we will discuss recent research that addressed
these challenges.
In 2022, the first prospective randomized HFO
trial was published. Using a noninferiority design,
the authors randomized patients to either intraoper-
ative electrocorticography tailored epilepsy surgery
&&
guided by HFOs or by spikes [22 ]. The study results
were negative. HFOs were not noninferior to spikes,
that is, patients in the spike arm had higher rates of
seizure freedom (90%) than those of the HFO arm
(67%). However, the HFO arm had more patients
with diseases usually associated with poor outcome
compared to patients in the spike arm (adjusted risk
difference -7.9%), which might potentially explain
the negative results. When controlling for disease
associated with poor outcome, the goal of noninfer-
iority was reached for patients with extratemporal
but not temporal lobe epilepsy. This trial challenged
the clinical value of HFOs as an epilepsy biomarker,
&&
especially in temporal lobe epilepsy [22 ].
Multicenter head-to head comparisons with
other new interictal biomarkers performed equally
or better than HFOs with the advantage that they are
potentially easier to be implemented in clinical
& &
routine [23 ,24 ]. One recent study investigated
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the best of 135 spike features and showed that
epileptic spikes preceded by gamma activity
(30–100 Hz) outperformed both ripples as well as
the seizure-onset zone as current gold standard
&
[23 ]. Another study found that relative entropy
in the ripple band (80–250 Hz) performed equally
to normalized rates of high-frequency oscillations,
but in contrast to a patient-level normalization, it
&
was easy and fast to calculate [24 ].
The question remains if HFOs are indeed such a
promising biomarker as initially suggested. The
answer is not yet clear, as HFOs might potentially
still have their value but may require different anal-
ysis approaches. This is supported by recent work
showing that it is not rates but other features such
as time varying dynamics that best predict the epi-
leptogenic zone [25,26]. Similar to epileptic spikes
[27], HFOs remain more stable across time inside than
outside the epileptogenic zone. Moreover, it was
shown that HFOs combined with neuroimaging bio-
markers such as FDG-PET hypometabolism might
improve prediction accuracy of HFOs [28]. Also, dif-
ferent approaches attempted to disentangle physio-
logical from pathological HFOs with the ultimate aim
to increase the yield of HFOs and in particular ripples
as epilepsy biomarkers. One of these approaches
consists of normalizing HFO rates for interregional
&
differences [29 ]. The authors investigated 151
patients who underwent stereo-EEG and subsequent
resection, and normalized for interregional differen-
ces in HFO rates as possible via the MNI open iEEG
atlas [30]. Using normalized ripple rates, accuracy for
focus identification was 77.3% (27% sensitivity,
97.1% specificity, 80.6% positive predictive value,
78.2% negative predictive value) and 69.5% for out-
come prediction (58.6% sensitivity, 76.3% specific-
ity, 60.7% positive predictive value, 74.7% negative
predictive value). The improvement was particularly
marked for foci in cortex, where physiological ripples
are frequent. In these cases, the normalized ripple
rates outperformed fast ripple rate more than 1/min
and seizure onset zone for outcome prediction by 3.6
&
and 13.5%, respectively [29 ].
Another area of active research was that of how to
better record and detect epileptic HFOs, a nontrivial
task given challenges with artifacts, presence of phys-
iological HFOs, as well as the size of HFO generators.
Using flexible high-resolution cortical arrays with
large coverage allowed to capture microscale HFOs
in patients with epilepsy. Estimations for macro-elec-
trodes revealed that up to 60% of HFOs detected with
high-resolution cortical arrays would have been
missed using conventional electrodes used in clinical
&
care [31 ]. It remains to be seen if this will improve the
utility of HFOs to localize the epileptogenic zone in
clinical care. Apart from innovative approaches to
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Seizure disorders
optimize the recording of HFOs, various groups
focused on the development of more comprehensive
detection algorithms as well as the use of new record-
ing technologies using high-resolution cortical arrays
with large coverage. In contrast to traditional detec-
tors based on time frequency or signal amplitude
features alone [32], the latest HFO detector genera-
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tion is focusing on not only HFO detection but also
on de-noising true HFO detections from artifacts as
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well as real-time HFO detection, something that is
&
pertinent in intraoperative settings [33,34 ,35]. The
benefit of such systems was shown in a recent work
that demonstrated that a deep learning-based classi-
fication was able to distill pathological HFOs, regard-
less of the initial HFO detection methods; this is
promising, as it might aid to increase specificity of
HFOs for localization of the epileptogenic zone [36].
So far, no algorithm was benchmarked fully auto-
matically in different datasets. This however is key
when attempting to implement fully automatic HFO
detection algorithms in commercial software solu-
tions. One such endeavor is the ongoing HFO multi-
center study that will recruit more than 200 datasets
from nine centers with the aim to performing a
blinded central analysis to evaluate the detector’s
&
performance [37 ].
Even though significant progress has been made
in the field of HFO research, more evidence is awaited
to allow final clarification of the clinical usefulness of
HFOs. New ways of analysis as possible with modern
artificial intelligence-based approaches integrated in
commercial software solutions may open new paths
of the use of HFOs in clinical practice.
ELECTROENCEPHALOGRAM IN
CRITICALLY ILL PATIENTS
Much of the recent advances in clinical EEG have
been driven by its application in critically ill
patients. Consciousness-impaired patients in the
Table 1. Incidence of seizures or status epilepticus in patients with disorders of consciousness according to underlying causes
Ictal events (absolute percentage)
Lacking underlying neurological illness
Acute ischemic stroke
Intracerebral hemorrhage
Subarachnoid bleeding
Hypoxic-ischemic encephalopathy
Severe traumatic brain injury
Infectious encephalitis
Anti-NMDA-receptor encephalitis
Note that 90% of events are nonconvulsive. Data from [38].
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ICU are at risk of seizures or status epilepticus; their
incidence varies according to the underlying cause
(Table 1). The majority of these events are noncon-
vulsive, hence only detectable through EEG [38].
Conversely, three-fourth of patients having some
sort of abnormal movements in the ICU do not
actually seize [39]. Since most of ICU ictal events
are not clinically visible, and the majority of move-
ments are not ictal, the importance of systematically
coupling video recordings to the EEG appears
obvious.
Video-EEG is indicated in patients with unclear
consciousness impairment, to quantify the degree of
cerebral dysfunction, including prognostic evalua-
&
tion after cardiac arrest [40 ], to identify delayed
ischemia after subarachnoid hemorrhage [41], and
to follow-up patients undergoing anesthetic treat-
ment for status epilepticus [42]. Technical require-
ments in the ICU, while globally corresponding to
routine EEG (rEEG) recordings, have some specific-
ities. Impedances less than 5 kV are difficult to
obtain in an electrically charged environment,
therefore values up to 20 kV may be acceptable.
Also, use of computed tomography (CT) and MRI
compatible electrodes [43] should be encouraged, as
they considerably ease patients’ management, espe-
cially if undergoing continuous EEG (cEEG). Impor-
tantly, reactivity to stimuli should be routinely
tested, as it may be related to favorable outcome,
especially after cardiac arrest [44,45].
While a solid training of EEG interpretation
acquired in routine and long-term EEGs from
patients in various age groups is recommended,
standardized assessment of EEG features according
to the newest version of the American Clinical
Neurophysiology Society (ACNS) guidelines [46 ]
&&
is strongly encouraged; they allow generalizability
across readers and centers, representing a para-
mount step towards improvement of ICU patients’
care.
SE (relative proportion, referred to the left column)
5--10% 1/3
2--5% 1/2
15--25% 1/2
5--10% 1/2
20--30% 9/10
20--30% 1/2
30--40% 1/2
70--80% 3/4
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Recent advances in clinical electroencephalography Frauscher et al.
Recently, there have been several efforts to
develop the quantitative analysis of the ICU EEG
signal, for example to predict status epilepticus
recurrence based on graph theory [47], or reactivity
assessment using frequency spectra and entropy
[48,49], and deep learning [50], but as a whole these
approaches require specific technical competences
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and are still not generalizable outside the develop-
ing centers. Conversely, the use of commercially
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&
available quantitative EEG devices [51 ] reduces
interpretation times by at least two-third [52]; apart
from steadily improving spike and seizure detec-
tions [53], they encompass spectral analysis, rhyth-
micity spectrograms, amplitude-integrated EEG,
suppression ratio, alpha-delta ratio and other anal-
yses that may be customized by users. Nevertheless,
accuracy for detection of EEG features of interest
and artifacts requires availability of the raw trace,
and expertise in its interpretation.
Continuous EEG in the ICU is experiencing a
steadily rising popularity, driven by North America
[54]. Compared to routine (typically lasting 20–
30 min) EEG, it offers a significantly higher detec-
&
tion of ictal events [55 ], prognostic features related
to favorable outcome such as generalized rhythmic
delta or sleep spindles [56,57], and allows uninter-
rupted observation of patients at risk for delayed
ischemia, or undergoing anesthetic treatment for
status epilepticus. Continuous EEG should be sys-
tematically used in refractory status epilepticus
treatment and, as it improves treatment accuracy,
it has recently been associated with shorter duration
of anesthetics exposure [58]. In a randomized trial
on adult patients without already proven ictal
events, however, clinical outcome was not influ-
&
enced by EEG duration [55 ], probably since the
underlying biological background may prove more
relevant in terms of prognostication than identifi-
cation and treatment of repetitive epileptiform tran-
sients. This also applied to patients after cardiac
arrest [59]. Continuous EEG is related to higher costs
than routine EEG, requiring more recording
machines and personnel (particularly readers) for
a given setting. Therefore, depending on resource
availability and in an effort to optimize costs, it
seems reasonable to apply the recently validated
2HELPS2B score based on the ACNS nomenclature
for risk stratification of subsequent seizures/SE
& the IFCN. Clin Neurophysiol 2017; 128:2070–2077.
occurrence [60 ]. Furthermore, the validated TERSE
algorithm, considering consciousness level, seizure
occurrence, and detection of EEG features related to
seizures/status epilepticus risk (epileptiform dis-
charges, lateralized periodic discharges or rhythmic
delta, brief potentially-ictal rhythmic discharges)
may orient on the optimal EEG duration and help
reducing the recording time by two-third [61].
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CONCLUSION
Significant development in clinical EEG has been
reported recently. Novel, more accurate and user-
friendly ESI methods, automated and semi-auto-
mated analysis of HFOs and gamma activity preced-
ing epileptic spikes bear the potential of radically
changing the landscape of presurgical evaluation.
The increasing utilization of EEG in the ICU, along
with fine-tuning the indications, interpretation and
therapeutic consequences will help overcome the
extremely challenging conditions in critically
ill patients.
Acknowledgements
None.
Financial support and sponsorship
The authors did not receive funding for this work.
Conflicts of interest
B.F.’s research is supported by start-up funding of Duke
University and a project grant of the Canadian Institutes
of Health Research (PJT-175056). S.B. reports Research
grants from noncommercial entities (Independent
Research Fund Denmark; Innovation Fund Denmark;
European Union: Eurostars Programme/EUREKA; Euro-
pean Union: Horizon Europe Framework Programme
(HORIZON); Danish Agency for Higher Education and
Science: International Network Programme), speaker
honoraria (UCB, Eisai, Natus-Neuro) and serving as
scientific consultant (Epihunter, UNEEG). A.R. reports
no disclosures.
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