pitfalls in ictal eeg interpretation critical care and intracranial

7/21/2019 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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Nicolas Gaspard, MD,

PhD

Lawrence J. Hirsch, MD

Correspondence to

Dr. Hirsch:

[email protected]

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.

S26 2012 American Academy of Neurology

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


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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.)

Neurology 80 (Suppl 1) January 1, 2013 S27



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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.

S28 Neurology 80 (Suppl 1) January 1, 2013



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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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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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