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Pitfalls in ictal EEG interpretation

Critical care and intracranial recordings

Nicolas Gaspard, MD,


PhD
Lawrence J. Hirsch, MD

Correspondence to
Dr. Hirsch:
lawrence.hirsch@yale.edu

ABSTRACT

EEG is the cornerstone examination for seizure diagnosis, especially nonconvulsive seizures in the
critically ill, but is still subject to many errors that can lead to a wrong diagnosis and unnecessary or
inadequate treatment. Many of these pitfalls to EEG interpretation are avoidable. This article reviews common errors in EEG interpretation, focusing on ictal or potentially ictal recordings obtained
in critically ill patients. Issues discussed include artifacts, nonepileptic events, equivocal EEG patterns seen in comatose patients, and quantitative EEG artifacts. This review also covers some difficulties encountered with intracranial EEG recordings in patients undergoing epilepsy surgery,
including issues related to display resolution. Neurology 2013;80 (Suppl 1):S26S42
GLOSSARY
AED 5 antiepileptic drug; AEEG 5 amplitude-integrated EEG; CEEG 5 continuous EEG; GPD 5 generalized periodic
discharge; ICE 5 intracortical EEG; ICU 5 intensive care unit; NCSE 5 nonconvulsive status epilepticus; NSE 5 neuronspecific enolase; QEEG 5 quantitative EEG; SE 5 status epilepticus.

The diagnosis of seizures and epilepsy often depends on the correct interpretation of EEG studies.
Diagnosis almost completely relies on EEG for nonconvulsive seizures in the critically ill. Overinterpretation of an EEG is frequent and can lead to serious adverse consequences.1,2 This is particularly
true for continuous EEG (CEEG) monitoring in the intensive care unit (ICU), where artifacts are
more abundant and diverse and can at times be very misleading. The EEG background in critically ill
and comatose patients differs greatly from the background in alert individuals, and many patterns
frequently encountered in these patients are difficult to classify into ictal and nonictal categories.
Technological advances, such as improved quantitative EEG (QEEG) techniques, networking, and
invasive intracortical EEG (ICE) monitoring have improved the performance and feasibility of
CEEG but they are not by any means immune to artifacts and misinterpretation.
Herein, we address some of the most common pitfalls that should be avoided while reading ICU
EEGs and CEEGs, in order to avoid over- and underinterpretation and inappropriate treatment.
The ICU can be considered a hostile environment for EEG recording. Many sources of extracerebral
signals can interfere with the cerebral activity, and obtaining a study not contaminated by artifact is a challenging
and often impossible task. Some artifacts are common to all EEG recordings (EKG, eye movements, muscle activity, sweating, electrode instability, etc.) (figures 1 and 2 and table 1) but prolonged recordings are more prone to
technical issues than shorter ones. The ICU environment also significantly differs from the EEG lab or the epilepsy
monitoring unit because of the presence of numerous electrical signal generators that can produce peculiar artifacts
that require some experience to recognize. Examples include mechanical ventilation, ventricular assist devices,
oscillating beds, and dialysis and patient care, especially chest percussion by respiratory therapists, a notorious
seizure-mimicker (figures 35 and table 1).3,4
Some EEG waveform features, when present, should raise suspicion of the artifactual nature of a pattern (table 2),
although they are not absolute and can also be seen with cerebral activity. Simultaneous video recording and notes of
the technologists, nurses, or others may be of great help in case of doubt. We strongly encourage frequent entry of
comments into the EEG record at the bedside by any caregiver because this aids communication greatly.
When dealing with artifacts, it is tempting to make excess use of filters, especially the high-frequency (a.k.a.,
low-pass) filter to reduce muscle activity and the notch filter to hide 60-Hz electrical noise. However, setting
ARTIFACTS

Supplemental data at
www.neurology.org

From Yale University, School of Medicine, Neurology Department and Comprehensive Epilepsy Center, New Haven, CT.
Go to Neurology.org for full disclosures. Funding information and disclosures deemed relevant by the authors, if any, are provided at the end of the
article.
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Figure 1

Facial-twitching artifact mimicking periodic lateralized epileptiform discharges (PLEDs)

(A) The EEG in this 39-year-old woman shows periodic spike-wave-like or polyspike-wave-like potentials over the right hemisphere (boxes). Lower voltage
periodic slow waves (blunt PLEDs) are present on the left (underlined). (B) After the administration of vecuronium, the right-sided spikes are no longer
present. They were attributable to muscle artifact associated with twitching movements on the right side of the face. The movements were associated with
the low-voltage PLEDs present over the left hemisphere (now in boxes), maximal in the parasagittal region. Thus, the left PLEDs were real (and ictal in this
case), but the right PLEDs were artifact. (Reproduced from Brenner and Hirsch,20 with permission.)

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Figure 2

Chewing artifact mimicking seizures

The EEG shows a bilateral sharply contoured rhythmic delta activity more prominent anteriorly with some degree of evolution in frequency, morphology, and
distribution, thus qualifying for a seizure. The chewing movements of this awake patient while eating caused this activity.

the high-frequency (low-pass) filter at a frequency at #15


Hz may affect the morphology of artifacts to the point of
disguising them in waves that appear like abnormal cerebral activity, including epileptiform discharges and seizures (see figure 6).
THE OPERATED AND INJURED BRAIN AND
SKULL A skull defect, such as a bur hole or craniot-

omy, results in an increase in the voltage and the sharpness of cerebral activity and an accentuation of faster
frequencies (referred to as the breach rhythm or
breach effect). A small defect, such as after the insertion of an intraventricular catheter, can cause very focal
distortion, located over one electrode only (figure 7).
Care must be taken not to overinterpret sharply contoured waveforms within this breach rhythm as epileptiform discharges or a sign of dysfunction on the
opposite hemisphere.
However, the alteration of cortical anatomy after
brain injury or surgery affects the spatial distribution of
electric dipoles. Spikes and sharp waves may present with
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aberrant morphology or polarity, or with very restricted


fields over a skull defect. The reader must be aware of
this situation, either by reviewing the patient history or
by recognizing other EEG features, to make a proper
interpretation. Technologists should also record skull
defects carefully.
NONEPILEPTIC MOTOR MANIFESTATIONS CEEG
studies are often requested because of transient spontaneous motor spells that are ascribed to seizures. In fact,
there are many movements in critically ill patients that
are not epileptic. Up to 10% of presumed motor seizures
in the ICU for which CEEG is requested are not
seizures.5 These movements include myoclonus, asterixis, tremor, shivering, semipurposeful movements, posturing due to pain or herniation, and deep tendon reflex
clonus (which can mimic stimulus-induced seizures).6
During these nonepileptic spells, the absence of ictal
activity supports the diagnosis. Sometimes, however,
movement artifacts may obscure the EEG. In this case,
the diagnosis has to be made solely on clinical

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Table 1

Potential sources of artifact when recording EEG in the intensive care unit

Patient
Eyes and eyelids (eye movement, eyelid flutter, blinking, nystagmus, bobbing, etc.)
Orolingual movements (glossokinetic potential, chewing, etc.)
Muscle activity (myoclonus, micro-shivering, jaw clenching, tremor, etc.)
Cardiovascular activity (EKG, pulse artifact, etc.)
Respiration
Sweat
Patting/rocking (especially in infants)
Continuous EEG setup
Electrodes (instability, electrode pop, unequal impedances)
Wires
Jacks/jackboxes
Monitoring and life-support devices
60-Hz noise (or 50-Hz in some countries)
Mechanical ventilation (including water condensation in the ventilation tubing,
extracorporeal membrane oxygenation, rapid oscillation ventilators
IV drip
Hemofiltration, hemodialysis
Pacemaker
Implanted ventricular assist device
Oscillating bed
Staff
Chest percussion (for pulmonary care): most common mimic of seizures
Suctioning

interpretation, including video review. It should also be


noted that the absence of ictal activity on scalp EEG does
not rule out seizures because many focal seizures, including the majority of simple partial seizures in patients with
epilepsy, do not have a clear scalp EEG correlate; this
may occur more often in the critically ill (see below).
Video recording is very helpful in providing additional
information about the semiology of the spell. Bedside
examination can also help at times. If the motor activity
reliably ceases after repositioning the involved limb, it
is most likely not a seizure. However, if the activity is
induced by stimulation, including repositioning the
patient, it could still be a seizure. The type of stimulation
may sometimes point to the nature of the activity.
Reflex movements provoked only by a specific maneuver (deep tendon percussion, passive extension of a
limb) rather than by a broad array of stimuli are most
likely not seizures, although exceptions occur, such as
parietal lobe reflex seizures.
THE (MIS)DIAGNOSIS OF NONCONVULSIVE STATUS
EPILEPTICUS IN COMATOSE PATIENTS The EEG

background in comatose and critically ill patients differs


widely from common EEG backgrounds seen in alert
individuals. With the increasing use of CEEG, it has

become clear that it is often difficult, and occasionally


impossible, to distinguish ictal, interictal, and nonictal
patterns in encephalopathic patients. The interpretation of these periodic and rhythmic patterns is still a
subject of controversy and different viewpoints exist.
More clinical and animal studies are required to clarify their nature.
Generalized periodic discharges (GPDs) at 1 to 2 Hz
can be seen in metabolic encephalopathy and postanoxic
coma, as well as during or after the course of nonconvulsive seizures and nonconvulsive status epilepticus
(NCSE), even if they do not appear epileptiform. It
is virtually impossible to reliably discriminate between
encephalopathy and status epilepticus (SE)-associated
GPDs in a given individual although some group differences exist: GPDs associated with seizures and SE tend
to be sharper (higher amplitude and shorter duration)
and appear on an interdischarge background of lower
amplitude than GPDs associated with encephalopathy.7
However, there is too much overlap for this to be relied
on for a given individual.
Terms such as triphasic waves or the presence of an
anterior-posterior lag carry an etiologic connotation
(of toxic or metabolic encephalopathy) and are often
thought to be specific; they are not specific and can be
seen during or after seizure and SE. To add to the
confusion, the morphology and frequency of periodic
discharges usually vary in the same patient, appearing
epileptiform at one time and not at other times.
Whether periodic lateralized epileptiform discharges
represent an ictal or interictal phenomenon is probably
variable. Rarely, they are clearly ictal and associated, for
instance, with contralateral synchronous periodic focal
motor activity. In most cases, however, they are devoid
of any clinical manifestation and assumed to be
nonictaleither interictal, or on an interictal-ictal
continuum.8
Regardless, it should be remembered that up to 80%
of patients with periodic lateralized epileptiform discharges have seizures during the acute course of their illness8,9; thus, we believe all of these patients should be
receiving antiepileptic medication, especially if CEEG is
not being performed and closely monitored.
Another frequent misconception is that if an EEG
pattern is induced or accentuated by stimulation it is
not ictal. It is now well recognized that alerting stimuli
in comatose patients can repeatedly elicit periodic, rhythmic, or ictal discharges (globally referred to under the
acronym SIRPIDs: Stimulus-Induced Rhythmic, Periodic, or Ictal Discharges; see figure 8),10 typically with
no clinical correlate, but sometimes with focal motor
seizures (see figure 9 and video).11
Overall, it is crucial to recognize that such patterns
belong to the same continuum of activities that may be
ictal at times and nonictal at others, including in the same
patient, fluctuating between the 2 or remaining
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Figure 3

Mechanical ventilation artifact mimicking generalized periodic epileptiform discharges

This EEG shows generalized periodic polyspike-wave discharges (box). These discharges were synchronous to mechanical ventilation and were not cerebral;
they resolved when fluid was removed from the ventilator tubing.

Figure 4

Dialysis artifact

The EEG in this 92-year-old man with mental status changes and renal failure shows rhythmic artifact (boxes), predominantly involving the anterior head regions (electrodes Fp1 and Fp2), more marked on the right. The discharges are also present in the T4-T6 derivation, which provides evidence that this could not represent eye movement artifact. The patient was being dialyzed utilizing slow continuous ultrafiltration that resulted in this artifact. (Reproduced from Brenner and Hirsch,20 with
permission.)
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Figure 5

Chest percussion artifact mimicking a seizure

These 2 contiguous EEG pages show a rhythmic sharply contoured delta activity in the left temporoparietal region (box). There is evolution in amplitude,
morphology, and location. A physical therapist was performing chest percussion with the patient on their left side, explaining the potentially physiologic field.
Use of video allows rapid detection of this pattern, which could be misinterpreted as seizure otherwise.

equivocal, lying on what has been coined the ictalinterictal continuum (figures 10 and 11).
It is thus important to recognize this lack of certainty
and to avoid dogmatic EEG interpretations that falsely
suggest more EEG specificity than exists. EEG reports
in the critically ill often need to stress this uncertainty
and lack of specificity.
EEG criteria for the diagnosis of NCSE have been
proposed (table 3),12,13 although their validity has never
been prospectively investigated. When confronted with
a pattern belonging to the ictal-interictal continuum,
there are several pragmatic approaches. A common practice used to distinguish ictal from nonictal EEG patterns
is to determine whether they can be abolished by a trial
of short-acting antiepileptic drug (AED), usually benzodiazepines (table 4 and figure 12). However, most periodic discharges, including triphasic waves in metabolic
encephalopathy, can attenuate or disappear after benzodiazepine injection.14 The trial is thus helpful only

Table 2

Features that may suggest artifacts rather than cerebral activity

Distribution of the activity over multiple electrodes without a physiologic electrical field
Atypical multiple phase reversals
Activity localized to a single electrode
Highly stereotyped or very monomorphic pattern
Periodic pattern with perfect regularity
Evidence from the video recording pointing at the source of the artifact
(chewing, toothbrushing, patting, chest percussion, etc.)

when modification in the EEG is accompanied by clinical improvement. This improvement is often not
concomitant to the EEG changes but when it occurs, it
is usually within 24 hours after the trial.15 It is important
to note that the absence of clinical improvement does
not rule out NCSE; unfortunately, most of these trials
are equivocal in the end. Trying nonsedating IV AEDs
(valproate, fosphenytoin, levetiracetam, or lacosamide)
may give the best chance of successfully terminating a
seizure and showing clinical improvement.
Another possibility when confronted with equivocal
EEG patterns is to investigate the metabolic/physiologic
impact of these discharges. Perfusion imaging with
SPECT, CT, or MRI and functional imaging with
FDG-PET, MR spectroscopy, or BOLD fMRI can
reveal areas of hyperperfusion, hypermetabolism, lactate
production, glutamate increase, etc., that would suggest
that the pattern is more likely to represent ictal activity,
or, more importantly, that it may be causing metabolic
stress and possibly secondary neuronal damage.16
More invasive monitoring with intracerebral microdialysis can provide additional evidence regarding
whether or not an EEG pattern is associated with
neuronal stress/injury: increased lactate/pyruvate
ratio, glutamate, and glycerol are all suggestive of seizurerelated neuronal injury. Neuron-specific enolase (NSE)
levels in blood and CSF also reflect the extent of neuronal injury, for instance after traumatic brain injury,17 but
also after seizures and SE.18,19 We sometimes use serial
serum NSE to determine the potential harm caused by a
prolonged but equivocal pattern; a transient increase in
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Figure 6

Filtered muscle mimicking brain activity

(A) Faster frequency activity is present on the left (boxes) in this 79-year-old man. The high-frequency filter (HFF; a.k.a., low-pass filter) is set at a low setting
of 15 Hz. (B) The HFF is now set at a more standard 70 Hz. The fast activity on the left is attributable to unilateral muscle artifact. The 15-Hz filter decreases
muscle artifact, which is in the faster frequency range. With the 15-Hz filter, muscle artifact can be mistaken for cerebral beta activity or even epileptiform
discharges. Filters do not distinguish between artifact or cerebral activity, and inappropriate use of filters can often lead to misinterpretation. (Reproduced
from Brenner and Hirsch,20 with permission.)

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Figure 7

Breach rhythm

The EEG shows high-voltage beta activity, particularly in the right central region (long box). Activity is also of higher voltage and
slower over the right side, particularly in the frontal temporal area. The patient had a right-sided craniotomy. This is a breach
rhythm (enhanced fast activity because of a skull defect, most marked at C4) as well as underlying dysfunction as manifest by
the focal slowing (2 smaller boxes). (Reproduced from Brenner and Hirsch,20 with permission.)

Figure 8

SIRPIDs, ictal-appearing without clinical correlate

Three consecutive EEG pages (20 seconds per page) displaying a focal ictal-appearing discharge in the left hemisphere that
was consistently elicited by stimulation. (A) The EEG initially shows diffuse background slowing, most prominent in the left
hemisphere; someone approaches the bedside at second 12 (arrow); this is followed by the onset of sharply contoured
rhythmic delta activity mixed with faster frequencies in the left hemisphere, already visible in the last 3 seconds of the page
(box). (B) and (C) There is evolution of the discharge over the next 30 seconds, with change in amplitude, frequency, and morphology (presence of intermixed spikes and faster frequencies). This pattern thus qualifies for a stimulus-induced ictal-appearing discharge. There was no clinical correlate.
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Figure 9

SIRPIDs, with clinical correlate: Stimulus-induced focal motor seizure

(A) The patient was stimulated with nostril tickle (arrow). This elicited the onset of bilateral alpha and beta activity, which then evolved
in amplitude, frequency, and morphology into unequivocal electrographic seizure (BD) Clinically, there were clonic movements of
the left fingers (first arrow in C) and the patients eyes opened wide and deviated upward (second arrow in C) (see video on the
Neurology Web site at www.neurology.org). (Reproduced from Hirsch,11 with permission from John Wiley & Sons.)

Figure 10

Gradual resolution of nonconvulsive status epilepticus (NCSE): The ictal-interictal continuum

(A) The EEG shows posterior-predominant, approximately 1.5-Hz periodic epileptiform discharges, mostly but not always
bisynchronous, often polyspikes, superimposed on a background of rhythmic delta. This was interpreted as ictal at this
point. (B) The EEG shows a similar pattern, but a bit slower, with brief breaks in the rhythmicity for half a second or so,
and with more restricted field and more evidence of a bilateral independent pattern. This is on the ictal-interictal continuum
and was interpreted as bilateral independent posterior-predominant periodic lateralized epileptiform discharges (BIPLEDs)plus, more prominent on the right. (C) BIPLEDs, slower than 1 Hz and probably not ictal at this point. (D) Twelve-hour spectrogram showing the gradual resolution of NCSE. This example also supports the concept of an ictal-interictal continuum
because this patient has gradual transition for ictal to interictal, with a necessarily arbitrary cutoff point if trying to dichotomize. (Reproduced from Brenner and Hirsch,20 with permission.)
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Figure 11

Fluctuations on the ictal-interictal continuum

Six EEG pages of the same patient over 2 consecutive days showing a fluctuation of EEG patterns between ictal (DF; probably A, and possibly C) and
nonictal-appearing (B; possibly C) patterns within an 18-hour period. There was no clinical correlate.

Table 3

Criteria for the diagnosis of nonconvulsive seizures and nonconvulsive status epilepticusa,b

Any pattern satisfying any of the primary criteria and lasting 10 s (for nonconvulsive seizures) or 30 min (for nonconvulsive status epilepticus)
Primary criteria
1. Repetitive generalized or focal spikes, sharp waves, spike-and-wave complexes at $3/s
2. Repetitive generalized or focal spikes, sharp waves, spike-and-wave or sharp-and-slow wave complexes at ,3/s and the secondary criterion
3. Sequential rhythmic, periodic, or quasi-periodic waves at $1/s and unequivocal evolution in frequency (gradually increasing or decreasing by at least
1/s, e.g., 2 to 3/s), morphology, or location (gradual spread into or out of a region involving at least 2 electrodes). Evolution in amplitude alone is not sufficient.
Secondary criterion
1. Significant improvement in clinical state or appearance of previously absent normal EEG patterns (such as posterior-dominant alpha rhythm) temporally coupled to
acute administration of a rapidly acting antiepileptic drug. Resolution of the epileptiform discharges leaving diffuse slowing without clinical improvement and
without appearance of previously absent normal EEG patterns would not satisfy the secondary criterion.
a
It is important to note that when these criteria are not fulfilled, nonconvulsive status epilepticus has not been excluded; it simply cannot be ruled in
definitively.
b
Adapted from Young et al.12 and Chong and Hirsch.13

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Table 4

Antiepileptic drug trial for the diagnosis of nonconvulsive status epilepticusa,b

Indication
Rhythmic or periodic focal or generalized epileptiform discharges on EEG with neurologic impairment
Contraindication
Patients who are heavily sedated/paralyzed
Monitoring
EEG, pulse oximetry, blood pressure, electrocardiography, respiratory rate with dedicated nurse
Antiepileptic drug trial
Sequential small doses of rapidly acting, short-duration benzodiazepine such as midazolam at 1 mg or nonsedating IV antiepileptic drug such as levetiracetam,
valproate, fosphenytoin, or lacosamide
Between doses, repeated clinical and EEG assessment
Trial is stopped after any of the following:
Persistent resolution of the EEG pattern (and examination repeated)
Definite clinical improvement
Respiratory depression, hypotension, or other adverse effect
A maximum dose is reached (such as 0.2 mg/kg midazolam, although higher may be needed if taking chronic benzodiazepines)
Test is considered positive if there is resolution of the potentially ictal EEG pattern and either an improvement in the clinical state or the appearance of previously
absent normal EEG patterns (e.g., posterior-dominant alpha rhythm). If EEG improves but patient does not, the result is equivocal.
a
b

A negative or equivocal result does not rule out NCSE.


Adapted from Foreman and Hirsch,26 with permission from Elsevier.

NSE after the occurrence of the pattern without an alternative explanation suggests secondary damage and may
warrant more aggressive treatment. However, this needs
to be investigated in controlled trials.
When confronted with equivocal EEG patterns, it is
probably reasonable to start treatment with an AED, but
it is best to avoid prolonged anesthetic doses of sedative
medications. In these instances, IV fosphenytoin,
valproate, levetiracetam, or lacosamide are good options.
In addition, it is also probably useful to optimize patient
condition such as fever, and avoid proseizure drugs and
metabolic imbalances, including alkalosis; withdrawal
from ethanol, barbiturates, or benzodiazepines needs to
be avoided as well. If all of this fails and there is some
confidence that the EEG pattern is contributing to the
patients altered mental status or is causing neuronal
injury, a 24-hour trial of suppression with midazolam
or propofol is reasonable. However, prolonged aggressive
treatment should probably be avoided with equivocal
EEG patterns, because the definite risks of prolonged
intubation and sedation will often outweigh the possible
benefit of seizure cessation; obviously, this needs to be
assessed on a case-by-case basis, and there is plenty of
room for clinical judgment given the lack of definitive
evidence.
QEEG is increasingly used to
monitor and trend CEEG data. QEEG analysis has
proven to be useful for detection of nonconvulsive
seizures and delayed cerebral ischemia. It can also
detect other acute brain events, including raised intracranial pressure, rebleeding, hypoxemia, etc.20
QUANTITATIVE EEG

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Algorithms that transform and compress the raw EEG


signal in time-amplitude graphs (amplitude-integrated
EEG or AEEG) or time-frequency spectra (fast-Fourier
transformation) allow the graphic display of long periods
of recordings (from several hours to days) on a single
computer screen, for faster reviewing and appreciation
of long-term trends. QEEG can measure asymmetries,
amplitudes, rhythmicity, power at specific frequencies,
and can be run on individual channels or many channels
combined. Although this has immense potential, artifacts captured during EEG recording are incorporated
in the analysis and can generate graphic patterns that
mimic seizures or ischemia (figure 13A). These QEEG
displays should never be interpreted without review of
the underlying raw EEG tracing, preferably by a boardcertified electroencephalographer. In particular, we have
seen repeated examples both clinically and in the literature of AEEG overinterpretation; it is virtually impossible
to tell increased amplitude due to artifact from a similar
increase in amplitude due to seizure without review of
the raw EEG (figure 13, B and C). Furthermore, it can
be almost impossible to distinguish seizure from artifact even with review of the raw EEG when there are
only a couple channels of raw EEG recorded, as is
standard with these bedside devices. Thus, although
AEEG can be very useful for assessment of background EEG and for screening for possible seizures,
it has only a moderate sensitivity and specificity
for seizures.21,22 Traditional complete EEG should be
obtained whenever abnormalities are suggested on the
AEEG.

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Figure 12

Benzodiazepine trial

(A) EEG from a 20-year-old man who was thought to be in possible nonconvulsive status epilepticus (NCSE) associated with continual, widespread epileptiform activity (boxes). The patient was able to answer many questions correctly, although he was frequently slow in his responses. (B) His clinical state and
EEG improved after the administration of lorazepam confirming the diagnosis of NCSE. (Reproduced from Brenner and Hirsch,20 with permission.)

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Figure 13

QEEG: Multiple seizures and identical-appearing false positives on amplitude-integrated EEG (AEEG)

(A) Three to four hours of quantitative EEG (QEEG) from a man in his 60s with a left-hemisphere brain tumor, presenting with worsening memory and language.
Multiple nonconvulsive seizures were recorded (labeled), maximal on the left as evident on the AEEG (higher amplitudes on left) and the relative asymmetry index,
going sharply downward (more power on left) with each seizure. The standard spectrogram and the asymmetry spectrogram both demonstrate involvement of all
frequencies, and the rhythmic run detector shows a burst of rhythmicity with most of them. Note the 2 episodes labeled not seizure (and with dashed lines) in
which the AEEG tracing jumps up in a manner almost identical to the prior and subsequent seizures. However, these are due to muscle artifact. Note that the 2
asymmetry panels do not show the typical seizure pattern with these artifactual increases in amplitude. This example shows the benefit of using multiple QEEG
measures simultaneously, and again stresses the importance of not relying on 1 measure alone without reviewing the raw EEG. (B) EEG at B blinking,
movement, and muscle artifact only. No seizure. (C) EEG at C, left-sided seizure. (Reproduced from Brenner and Hirsch,20 with permission.)

A negative EEG never rules out


seizure, including during CEEG in the ICU. The use of
ICE in severe acute brain injury, obtained via bedside
placement of a mini-depth electrode through a bur
hole,23 has demonstrated the existence of small-scale
intracortical seizures with no or poor correlation at
the scalp (figure 14). This is likely attributable to multifocal, asynchronous, mini-seizures that are not adequately synchronized to be seen on scalp EEG.
Whether or not these contribute to deeper coma or
secondary neuronal injury remains unclear.
INTRACORTICAL EEG

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In addition to recording unrecognized seizure


activity, ICE is less prone to electrode artifacts and
offers a higher signal:noise ratio than scalp EEG.
This is useful for computerized detection of ischemia or other secondary events, including with alarms
with rare false positives.23 However, the extracranial
part of the recording setup (wires, connections, amplifiers, etc.) is still susceptible to interference with
artifact-generating sources. This applies to intracranial recordings in patients with epilepsy as well
(figure 15).

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Figure 14

Seizures detected by intracortical EEG (ICE) without correlate on scalp EEG

A 74-year-old woman with subarachnoid hemorrhage grade III and receiving multimodality monitoring, including ICE
with mini-depth electrode located in the right frontal cortex. The bottom 6 channels are from the mini-depth (ICE), and
the remainder are from standard scalp EEG. ICE shows rhythmic 3-Hz spike-and-wave complexes maximal at D3-D4 with
decrease in frequency and evolution in amplitude and morphology. This is the offset of one of her typical seizures. There was
no correlate on the scalp EEG despite a high-quality recording. (Reproduced from Brenner and Hirsch,20 with permission.)

Figure 15

Toothbrushing artifact during intracranial EEG recording mimicking seizure

This EEG shows a nonevolving, rhythmic, 5-Hz activity. This was induced by the patient brushing his teeth, causing movement of jackbox. (Reproduced from Goodkin and Quigg,27 with permission from Wolters Kluwer Health.)
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Figure 16

Low display resolution affecting the representation of higher frequencies in intracranial EEG (ICEEG) recording

(A) ICEEG at the seizure onset viewed with a time base of 30 mm/s. The earliest sustained ictal activity appears to be in the LMT (left mesial temporal) channels 6 to
8. (B) ICEEG at the seizure onset at a time base of 60 mm/s. At this setting, the low-amplitude fast activity in the LP (left parietal) channels is clearly visible as the
earliest sustained ictal activity (box). (C) Power spectral analysis of 2 electrode channels, LP15 and LMT7, for the same 1-second epoch at the seizure onset (represented by the black bar in A and B). Powers in the 10- to 120-Hz frequency range are shown for each channel. Note the activity at 70 to 85 Hz in LP15. (D) Frequency aliasing of a 30-Hz signal at a screen resolution of 95 pixels per second horizontally. Compare with the same signal viewed at a resolution of 190 pixels per
second. (Reproduced from Schevon et al.,24 with permission from John Wiley & Sons.)

DISPLAY RESOLUTION FOR VIEWING INTRACRANIAL


EEG Misinterpretation can arise from inadequate dis-

playing of the EEG, particularly when faster frequencies


are involved. It is well known that during analog-to-digital conversion of the EEG signal, a sampling rate of at
least twice the highest frequency component (referred
to as the Nyquist frequency) has to be used to avoid frequency aliasing; a rate at least 5 times is recommended,
because this is about what is needed for reliable reproduction of complex waveforms. It is less frequently
appreciated that the same rule also applies when the
digitized EEG signal is displayed on a monitor screen.
Using a screen resolution too low is a form of downsampling and can lead to the obliteration of higher frequencies or aliasing (appearance of false frequencies),
with possible adverse consequences, such as the erroneous localization of the seizure-onset zone (figure 16).24
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Neurology 80 (Suppl 1)

If one hopes to visualize up to 100-Hz activity on a


typical 21-inch monitor with 1280 3 1024 resolution,
only 2.5 seconds should be displayed on the screen at a
time. Similar issues can occur with vertical resolution,
and too many channels displayed at once should be
avoided. Computer-aided analysis of intracranial EEG
will become essential as broader band EEG (from DC
to several hundred Hz or more) is used more frequently,
especially if clinical utility of high-frequency oscillations
is confirmed.25
Every EEG should be interpreted with
care and caution to avoid pitfalls (table 5). This is especially true for studies recorded in the ICU where artifacts
are numerous and many EEG patterns may reflect different processes, including ictal, interictal, and metabolic,
often combined simultaneously and varying over time.
CONCLUSION

January 1, 2013

2012 American Academy of Neurology. Unauthorized reproduction of this article is prohibited.

Table 5

Some common errors related to interpreting intensive care unit EEG

Misinterpreting artifact as seizures

4.

5.

Assuming there is a clear dichotomy between ictal and interictal EEG patterns in
encephalopathic patients (there is not)
Underdiagnosing nonconvulsive seizures/status epilepticus on EEG
Believing that because some patterns can be ictal at times implies that they are always,
often, or usually ictal

6.

Assuming a comatose patient in nonconvulsive status will wake up immediately if


successfully treated
Corollary error: If they dont improve clinically, concluding it was not nonconvulsive status
epilepticus (it still could be, just not proven)

7.

Related error: Concluding that if an EEG pattern resolves with an antiepileptic drug, that
proves it was nonconvulsive status (might have been, but need clinical improvement to prove it)
Also related error: When doing a diagnostic benzodiazepine treatment trial, using too high of a
dose (and putting the patient into deep sleep/coma)
Concluding that if a pattern is induced or exacerbated by alerting or stimulation, it is not
ictal (it still can be)

8.

9.

Interpreting quantitative EEG, especially amplitude-integrated EEG, without the raw EEG or
without an electroencephalographer
Assuming that a negative scalp EEG rules out seizure (it does not)
Calling clinical spells seizures when not

10.

Assuming intracranial EEG recordings have no artifact


Overuse of filters (especially the high-frequency and notch filters)

11.

There are ways of trying to clarify their significance,


including AED trials, but this is often inconclusive.
In case of doubt, one has to avoid overinterpretation
and unnecessarily aggressive treatment. Newer methods
of EEG analysis are useful and improve the yield of EEG
monitoring but they are themselves subject to artifact
and misinterpretation. Proper training is a crucial aspect
of minimizing as many of the errors as possible.

12.

13.

14.

AUTHOR CONTRIBUTIONS
N. Gaspard and L.J. Hirsch drafted the article. L.J. Hirsch critically revised the
manuscript for intellectual content. Both gave their final approval of the
article.

15.

16.
DISCLOSURE
N. Gaspard reports no disclosures relevant to the manuscript. L. Hirsch has
received research support for investigator-initiated studies from Eisai, Pfizer,
UCB-Pharma, Lundbeck, and Upsher-Smith and consultation fees for advising
from Lundbeck, Upsher-Smith, and GlaxoSmithKline. Go to Neurology.org
for full disclosures.

17.

18.

Received January 11, 2012. Accepted in final form May 1, 2012.


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