Pitfalls in Ictal EEG Interpretation Critical Care and Intracranial
Transcript of Pitfalls in Ictal EEG Interpretation Critical Care and Intracranial
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DOI 10.1212/WNL.0b013e31827974f82013;80;S26Neurology
Nicolas Gaspard and Lawrence J. Hirschrecordings
Pitfalls in ictal EEG interpretation : Critical care and intracranial
January 14, 2013This information is current as of
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rights reserved. Print ISSN: 0028-3878. Online ISSN: 1526-632X.Allsince 1951, it is now a weekly with 48 issues per year. Copyright 2013 by AAN Enterprises, Inc.
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Nicolas Gaspard, MD,
PhD
Lawrence J. Hirsch, MD
Correspondence to
Dr. Hirsch:
Supplemental data atwww.neurology.org
Pitfalls in ictal EEG interpretationCritical care and intracranial recordings
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 re-
views 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 pat-
terns seen in comatose patients, and quantitative EEG artifacts. This review also covers some dif-
ficulties 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 periodicdischarge; ICE 5 intracortical EEG; ICU 5 intensive care unit; NCSE 5 nonconvulsive status epilepticus; NSE 5 neuron-specific 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. Overinter-
pretation 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.
ARTIFACTS 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 activ-
ity, 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
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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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 cere-
bral activity, including epileptiform discharges and seiz-
ures (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 sharp-
ness 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 inser-
tion of an intraventricular catheter, can cause very focal
distortion, located over one electrode only (figure 7).
Care must be taken not to overinterpret sharply con-
toured waveforms within this breach rhythm as epilep-
tiform 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
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 spontane-
ous 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, aster-
ixis, tremor, shivering, semipurposeful movements, pos-
turing 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
Figure 2 Chewing artifact mimicking seizures
TheEEG shows a bilateral sharply contouredrhythmicdelta activity more prominent anteriorly with some degreeof evolution in frequency, morphology, and
distribution, thus qualifying for a seizure. The chewing movements of this awake patient while eating caused this activity.
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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, includ-
ing 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 stimulationmay sometimes point to the nature of the activity.
Reflex movements provoked only by a specific maneu-
ver (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 interpre-
tation of these periodic and rhythmic patterns is still a
subject of controversy and different viewpoints exist.
More clinical and animal studies are required to clar-
ify 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 nonconvul-
sive seizures and nonconvulsive status epilepticus
(NCSE), even if they do not appearepileptiform. It
is virtually impossible to reliably discriminate between
encephalopathy and status epilepticus (SE)-associated
GPDs in a given individual although some group differ-
ences 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 focalmotor 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 dis-
charges have seizures during the acute course of their ill-
ness8,9; 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, rhyth-
mic, or ictal discharges (globally referred to under the
acronym SIRPIDs: Stimulus-Induced Rhythmic, Peri-
odic, 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
Table 1 Potentialsourcesof artifactwhen recordingEEG in theintensive 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
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Figure 3 Mechanical ventilation artifact mimicking generalized periodic epileptiform discharges
This EEG shows generalized periodic polyspike-wavedischarges (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 EEGin this92-year-old manwithmental status changes andrenal failure showsrhythmicartifact(boxes),predominantlyinvolving the anteriorheadregions (electro-
des Fp1 andFp2), more markedon the right. The discharges are also present in the T4-T6 derivation, which provides evidence that this could not representeyemove-
ment 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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equivocal, lying on what has been coined the ictal-
interictal 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 beenproposed (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 prac-
tice 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 benzo-
diazepines (table 4 and figure 12). However, most peri-
odic discharges, including triphasic waves in metabolic
encephalopathy, can attenuate or disappear after ben-
zodiazepine injection.14 The trial is thus helpful only
when modification in the EEG is accompanied by clin-
ical 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 micro-
dialysis 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 seizure-
related neuronal injury. Neuron-specific enolase (NSE)
levels in blood and CSF also reflect the extent of neuro-
nal 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
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.)
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, andlocation. A physical therapist was performing chest percussion with thepatient on their left side, explaining thepotentially physiologic field.Use of video allows rapid detection of this pattern, which could be misinterpreted as seizure otherwise.
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Figure 6 Filtered muscle mimicking brain activity
(A) Fasterfrequency activityis present on the left (boxes) in this 79-year-old man. Thehigh-frequencyfilter (HFF; a.k.a., low-pass filter) is setat a lowsetting
of 15 Hz.(B) TheHFF is nowset at a more standard 70 Hz.The fast activity on theleft is attributableto unilateral muscleartifact. The15-Hzfilter 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 EEGpages(20 seconds perpage)displaying a focal ictal-appearing dischargein theleft 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 fasterfrequencies in theleft hemisphere, already visible in thelast 3 seconds of thepage
(box).(B) and(C) There is evolution of thedischarge over thenext 30 seconds, with changein amplitude, frequency, andmor-
phology (presence of intermixed spikes and faster frequencies). This pattern thus qualifies for a stimulus-induced ictal-ap-
pearing 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 stimulatedwith nostril tickle(arrow).This elicitedtheonsetof bilateralalphaand beta activity,whichthen 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 spec-
trogram 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 dichot-
omize. (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 (D F; 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 least1/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 stateor appearance of previously absent normal EEG patterns (suchas posterior-dominantalpha rhythm) temporally coupled toacute administration of a rapidly acting antiepileptic drug. Resolution of the epileptiform discharges leaving diffuse slowing without clinical improvement andwithout 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.bAdapted from Young et al.12 and Chong and Hirsch.13
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NSE after the occurrence of the pattern without an alter-
native 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 prolongedintubation 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.
QUANTITATIVE EEG 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 intra-
cranial pressure, rebleeding, hypoxemia, etc.20
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, arti-
facts 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 board-
certified electroencephalographer. In particular, we have
seen repeated examples both clinically and in the litera-
ture of AEEGoverinterpretation; it is virtually impossible
to tell increased amplitude due to artifact from a similar
increase in amplitude due to seizure without review ofthe raw EEG (figure 13, B and C). Furthermore, it can
be almost impossible to distinguish seizure from arti-
fact 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 back-
ground 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.
Table 4 Antiepileptic drug trial for the diagnosis of nonconvulsive status epilepticus a,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 thepotentially ictal EEGpattern and eitheran improvement in theclinicalstate or theappearance of previouslyabsent normal EEG patterns (e.g., posterior-dominant alpha rhythm). If EEG improves but patient does not, the result is equivocal.
aA negative or equivocal result does not rule out NCSE.bAdapted from Foreman and Hirsch,26 with permission from Elsevier.
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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 epilep-
tiform 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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INTRACORTICAL EEG 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 mul-
tifocal, asynchronous, mini-seizures that are not ade-
quately synchronized to be seen on scalp EEG.
Whether or not these contribute to deeper coma or
secondary neuronal injury remains unclear.
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 ische-
mia or other secondary events, including with alarms
with rare false positives.23 However, the extracranial
part of the recording setup (wires, connections, am-
plifiers, etc.) is still susceptible to interference with
artifact-generating sources. This applies to intracra-
nial recordings in patients with epilepsy as well
(figure 15).
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.
Multiplenonconvulsiveseizures were recorded (labeled),maximal on the left as evident on theAEEG (higheramplitudes on left) andthe relative asymmetryindex,
going sharplydownward (more power on left) witheachseizure. Thestandard spectrogram andthe asymmetryspectrogram bothdemonstrate 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 theAEEG tracingjumps up in a manner almost identical to theprior and subsequent seizures. However, these are dueto muscle artifact. Note that the 2
asymmetry panels do not showthe 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.)
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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 frequencyand evolutionin amplitudeand morphology. This is theoffset of oneof hertypical seizures.Therewas
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 move-
ment of jackbox. (Reproduced from Goodkin and Quigg,27 with permission from Wolters Kluwer Health.)
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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-dig-
ital 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 fre-
quency aliasing; a rate at least 5 times is recommended,
because this is about what is needed for reliable repro-
duction 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 down-
sampling and can lead to the obliteration of higher fre-
quencies or aliasing (appearance of false frequencies),
with possible adverse consequences, such as the errone-
ous localization of the seizure-onset zone (figure 16).24
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
CONCLUSION Every EEG should be interpreted with
care and caution to avoid pitfalls (table 5). This is espe-
cially true for studies recorded in the ICU where artifacts
are numerous and many EEG patterns may reflect dif-
ferent processes, including ictal, interictal, and metabolic,
often combined simultaneously and varying over time.
Figure 16 Low display resolution affecting the representation of higher frequencies in intracranial EEG (ICEEG) recording
(A)ICEEG at theseizure onset viewed with a time base of 30 mm/s.The earliest sustained ictalactivity appears to be in theLMT (left mesial temporal) channels 6 to8. (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 (rep-
resented 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) Fre-
quency aliasing of a 30-Hz signal at a screen resolution of 95 pixels per second horizontally. Compare with thesame signal viewed at a resolution of 190 pixels per
second. (Reproduced from Schevon et al.,24 with permission from John Wiley & Sons.)
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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.
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.
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.
Received January 11, 2012. Accepted in final form May 1, 2012.
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Table 5 Some common errors related to interpreting intensive care unit EEG
Misinterpreting artifact as seizures
Assuming there is a clear dichotomy between ictal and interictal EEG patterns inencephalopathic 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
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 statusepilepticus (it still could be, just not proven)
Related error: Concluding that if an EEG pattern resolves with an antiepileptic drug, thatproves 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 adose (and putting the patient into deep sleep/coma)
Concluding that if a pattern is induced or exacerbated by alerting or stimulation, it is notictal (it still can be)
Interpreting quantitative EEG, especially amplitude-integrated EEG, without the raw EEG orwithout an electroencephalographer
Assuming that a negative scalp EEG rules out seizure (it does not)
Calling clinical spells seizures when not
Assuming intracranial EEG recordings have no artifact
Overuse of filters (especially the high-frequency and notch filters)
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conventional and two amplitude-integrated EEG classi-
fication systems. J Pediatr 2008;153:369374.
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troencephalography in acute brain injury. Ann Neurol
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management. Neurol Clin 2012;30:1141.
27. GoodkinHP, Quigg M. Toothbrushing EEG artifact recorded
from chronically implanted subdural electrodes. Neurology
2010;75:1850.
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DOI 10.1212/WNL.0b013e31827974f82013;80;S26Neurology
Nicolas Gaspard and Lawrence J. HirschPitfalls in ictal EEG interpretation : Critical care and intracranial recordings
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