Pitfalls in ictal EEG interpretationCritical care and intracranial recordings
ABSTRACT
EEG is the cornerstone examination for seizure diagnosis, especially nonconvulsive seizures in thecritically ill, but is still subject to many errors that can lead to a wrong diagnosis and unnecessary orinadequate 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 obtainedin 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):S26–S42
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 particularlytrue for continuous EEG (CEEG) monitoring in the intensive care unit (ICU), where artifacts aremore abundant and diverse and can at times be very misleading. The EEG background in critically illand comatose patients differs greatly from the background in alert individuals, and many patternsfrequently encountered in these patients are difficult to classify into ictal and nonictal categories.Technological advances, such as improved quantitative EEG (QEEG) techniques, networking, andinvasive intracortical EEG (ICE) monitoring have improved the performance and feasibility ofCEEG 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 ICUEEGs 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 extracerebralsignals can interfere with the cerebral activity, and obtaining a study not contaminated by artifact is a challengingand 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 totechnical issues than shorter ones. The ICU environment also significantly differs from the EEG lab or the epilepsymonitoring unit because of the presence of numerous electrical signal generators that can produce peculiar artifactsthat 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 notoriousseizure-mimicker (figures 3–5 and table 1).3,4
Some EEGwaveform 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 ofthe technologists, nurses, or others may be of great help in case of doubt. We strongly encourage frequent entry ofcomments 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 thearticle.
(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 voltageperiodic slow waves (blunt PLEDs) are present on the left (underlined). (B) After the administration of vecuronium, the right-sided “spikes” are no longerpresent. They were attributable to muscle artifact associated with twitching movements on the right side of the face. The movements were associated withthe 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 thiscase), 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#15Hz may affect the morphology of artifacts to the point ofdisguising them in waves that appear like abnormal cere-bral activity, including epileptiform discharges and seiz-ures (see figure 6).
THE OPERATED AND INJURED BRAIN ANDSKULL 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 fasterfrequencies (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 focaldistortion, 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 theopposite hemisphere.
However, the alteration of cortical anatomy afterbrain injury or surgery affects the spatial distribution ofelectric dipoles. Spikes and sharp waves may present with
aberrant morphology or polarity, or with very restrictedfields over a skull defect. The reader must be aware ofthis situation, either by reviewing the patient history orby recognizing other EEG features, to make a properinterpretation. Technologists should also record skulldefects carefully.
NONEPILEPTIC MOTOR MANIFESTATIONS CEEGstudies 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 thatare not epileptic. Up to 10% of presumedmotor seizuresin the ICU for which CEEG is requested are notseizures.5 These movements include myoclonus, aster-ixis, tremor, shivering, semipurposeful movements, pos-turing due to pain or herniation, and deep tendon reflexclonus (which can mimic stimulus-induced seizures).6
During these nonepileptic spells, the absence of ictalactivity 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
The EEG shows a bilateral sharply contoured rhythmic delta activity more prominent anteriorly with some degree of evolution in frequency, morphology, anddistribution, 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 benoted that the absence of ictal activity on scalp EEG doesnot rule out seizures because many focal seizures, includ-ing the majority of simple partial seizures in patients withepilepsy, do not have a clear scalp EEG correlate; thismay occur more often in the critically ill (see below).Video recording is very helpful in providing additionalinformation about the semiology of the spell. Bedsideexamination can also help at times. If the motor activityreliably ceases after repositioning the involved limb, itis most likely not a seizure. However, if the activity isinduced by stimulation, including repositioning thepatient, 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 alimb) rather than by a broad array of stimuli are mostlikely not seizures, although exceptions occur, such asparietal lobe reflex seizures.
THE (MIS)DIAGNOSISOFNONCONVULSIVESTATUSEPILEPTICUS IN COMATOSE PATIENTS The EEGbackground in comatose and critically ill patients differswidely from common EEG backgrounds seen in alertindividuals. With the increasing use of CEEG, it has
become clear that it is often difficult, and occasionallyimpossible, to distinguish ictal, interictal, and nonictalpatterns in encephalopathic patients. The interpre-tation of these periodic and rhythmic patterns is still asubject 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 Hzcan be seen in metabolic encephalopathy and postanoxiccoma, as well as during or after the course of nonconvul-sive seizures and nonconvulsive status epilepticus(NCSE), even if they do not appear “epileptiform.” Itis virtually impossible to reliably discriminate betweenencephalopathy and status epilepticus (SE)-associatedGPDs in a given individual although some group differ-ences exist: GPDs associated with seizures and SE tendto be sharper (higher amplitude and shorter duration)and appear on an interdischarge background of loweramplitude than GPDs associated with encephalopathy.7
However, there is too much overlap for this to be reliedon 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 oftenthought to be specific; they are not specific and can beseen during or after seizure and SE. To add to theconfusion, the morphology and frequency of periodicdischarges usually vary in the same patient, appearingepileptiform at one time and not at other times.
Whether periodic lateralized epileptiform dischargesrepresent an ictal or interictal phenomenon is probablyvariable. Rarely, they are clearly ictal and associated, forinstance, with contralateral synchronous periodic focalmotor activity. In most cases, however, they are devoidof any clinical manifestation and assumed to be“nonictal”—either interictal, or on an interictal-ictalcontinuum.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 bereceiving antiepileptic medication, especially if CEEG isnot being performed and closely monitored.
Another frequent misconception is that if an EEGpattern is induced or accentuated by stimulation it isnot ictal. It is now well recognized that alerting stimuliin comatose patients can repeatedly elicit periodic, rhyth-mic, or ictal discharges (globally referred to under theacronym SIRPIDs: Stimulus-Induced Rhythmic, Peri-odic, or Ictal Discharges; see figure 8),10 typically withno clinical correlate, but sometimes with focal motorseizures (see figure 9 and video).11
Overall, it is crucial to recognize that such patternsbelong to the same continuum of activities that may beictal at times and nonictal at others, including in the samepatient, fluctuating between the 2 or remaining
Table 1 Potential sources of artifactwhen recordingEEG in the intensive careunit
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
TheEEG in this92-year-oldmanwithmental status changesand renal failure shows rhythmic artifact (boxes), predominantly involving theanterior head regions (electro-des 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 eyemove-ment artifact. The patient was being dialyzed utilizing slow continuous ultrafiltration that resulted in this artifact. (Reproduced from Brenner and Hirsch,20 withpermission.)
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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 certaintyand to avoid dogmatic EEG interpretations that falselysuggest more EEG specificity than exists. EEG reportsin the critically ill often need to stress this uncertaintyand lack of specificity.
EEG criteria for the diagnosis of NCSE have beenproposed (table 3),12,13 although their validity has neverbeen prospectively investigated. When confronted witha pattern belonging to “the ictal-interictal continuum,”there are several pragmatic approaches. A common prac-tice used to distinguish ictal from nonictal EEG patternsis to determine whether they can be abolished by a trialof short-acting antiepileptic drug (AED), usually benzo-diazepines (table 4 and figure 12). However, most peri-odic discharges, including triphasic waves in metabolicencephalopathy, 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 notconcomitant to the EEG changes but when it occurs, itis usually within 24 hours after the trial.15 It is importantto note that the absence of clinical improvement doesnot rule out NCSE; unfortunately, most of these trialsare equivocal in the end. Trying nonsedating IV AEDs(valproate, fosphenytoin, levetiracetam, or lacosamide)may give the best chance of successfully terminating aseizure and showing clinical improvement.
Another possibility when confronted with equivocalEEG patterns is to investigate the metabolic/physiologicimpact of these discharges. Perfusion imaging withSPECT, CT, or MRI and functional imaging withFDG-PET, MR spectroscopy, or BOLD fMRI canreveal areas of hyperperfusion, hypermetabolism, lactateproduction, glutamate increase, etc., that would suggestthat the pattern is more likely to represent ictal activity,or, more importantly, that it may be causing metabolicstress and possibly secondary neuronal damage.16
More invasive monitoring with intracerebral micro-dialysis can provide additional evidence regardingwhether or not an EEG pattern is associated withneuronal stress/injury: increased lactate/pyruvateratio, 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 butalso after seizures and SE.18,19 We sometimes use serialserum NSE to determine the potential harm caused by aprolonged 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, 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.
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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 settingof 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 decreasesmuscle artifact, which is in the faster frequency range. With the 15-Hz filter, muscle artifact can be mistaken for cerebral beta activity or even epileptiformdischarges. Filters do not distinguish between artifact or cerebral activity, and inappropriate use of filters can often lead to misinterpretation. (Reproducedfrom 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 andslower over the right side, particularly in the frontal temporal area. The patient had a right-sided craniotomy. This is a breachrhythm (enhanced fast activity because of a skull defect, most marked at C4) as well as underlying dysfunction as manifest bythe 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 thatwas consistently elicited by stimulation. (A) The EEG initially shows diffuse background slowing, most prominent in the lefthemisphere; someone approaches the bedside at second 12 (arrow); this is followed by the onset of sharply contouredrhythmic 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, 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 patientwas stimulatedwith nostril tickle (arrow). This elicited the onset of bilateral alpha andbeta activity, which then evolvedin amplitude, frequency, and morphology into unequivocal electrographic seizure (B–D) Clinically, there were clonic movements ofthe left fingers (first arrow in C) and the patient’s eyes opened wide and deviated upward (second arrow in C) (see video on theNeurology® 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 alwaysbisynchronous, often polyspikes, superimposed on a background of rhythmic delta. This was interpreted as ictal at thispoint. (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 continuumand 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 continuumbecause 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) andnonictal-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 state or appearance of previously absent normal EEG patterns (such as posterior-dominant “alpha” 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 indefinitively.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 maywarrant more aggressive treatment. However, this needsto be investigated in controlled trials.
When confronted with equivocal EEG patterns, it isprobably reasonable to start treatment with an AED, butit is best to avoid prolonged anesthetic doses of sedativemedications. In these instances, IV fosphenytoin,valproate, levetiracetam, or lacosamide are good options.In addition, it is also probably useful to optimize patientcondition such as fever, and avoid proseizure drugs andmetabolic imbalances, including alkalosis; withdrawalfrom ethanol, barbiturates, or benzodiazepines needs tobe avoided as well. If all of this fails and there is someconfidence that the EEG pattern is contributing to thepatient’s altered mental status or is causing neuronalinjury, a 24-hour trial of suppression with midazolamor propofol is reasonable. However, prolonged aggressivetreatment should probably be avoided with equivocalEEG patterns, because the definite risks of prolongedintubation and sedation will often outweigh the possiblebenefit of seizure cessation; obviously, this needs to beassessed on a case-by-case basis, and there is plenty ofroom for clinical judgment given the lack of definitiveevidence.
QUANTITATIVE EEG QEEG is increasingly used tomonitor and trend CEEG data. QEEG analysis hasproven to be useful for detection of nonconvulsiveseizures and delayed cerebral ischemia. It can alsodetect other acute brain events, including raised intra-cranial pressure, rebleeding, hypoxemia, etc.20
Algorithms that transform and compress the raw EEGsignal in time-amplitude graphs (amplitude-integratedEEG or AEEG) or time-frequency spectra (fast-Fouriertransformation) allow the graphic display of long periodsof recordings (from several hours to days) on a singlecomputer screen, for faster reviewing and appreciationof long-term trends. QEEG can measure asymmetries,amplitudes, rhythmicity, power at specific frequencies,and can be run on individual channels or many channelscombined. Although this has immense potential, arti-facts captured during EEG recording are incorporatedin the analysis and can generate graphic patterns thatmimic seizures or ischemia (figure 13A). These QEEGdisplays should never be interpreted without review ofthe underlying raw EEG tracing, preferably by a board-certified electroencephalographer. In particular, we haveseen repeated examples both clinically and in the litera-ture of AEEG overinterpretation; it is virtually impossibleto tell increased amplitude due to artifact from a similarincrease in amplitude due to seizure without review ofthe raw EEG (figure 13, B and C). Furthermore, it canbe almost impossible to distinguish seizure from arti-fact even with review of the raw EEG when there areonly a couple channels of raw EEG recorded, as isstandard with these bedside devices. Thus, althoughAEEG can be very useful for assessment of back-ground EEG and for screening for possible seizures,it has only a moderate sensitivity and specificityfor seizures.21,22 Traditional complete EEG should beobtained whenever abnormalities are suggested on theAEEG.
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
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 previouslyabsent normal EEG patterns (e.g., posterior-dominant ‘‘alpha’’ rhythm). If EEG improves but patient does not, the result is equivocal.
a A 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 andEEG 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 outseizure, including during CEEG in the ICU. The use ofICE in severe acute brain injury, obtained via bedsideplacement of a mini-depth electrode through a burhole,23 has demonstrated the existence of small-scaleintracortical seizures with no or poor correlation atthe 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 orsecondary neuronal injury remains unclear.
In addition to recording unrecognized seizureactivity, ICE is less prone to electrode artifacts andoffers a higher signal:noise ratio than scalp EEG.This is useful for computerized detection of ische-mia or other secondary events, including with alarmswith rare false positives.23 However, the extracranialpart of the recording setup (wires, connections, am-plifiers, etc.) is still susceptible to interference withartifact-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.Multiple nonconvulsive seizureswere recorded (labeled), maximal on the left as evident on theAEEG (higher amplitudes on left) and the relative asymmetry index,going sharply downward (more power on left) with each seizure. The standard spectrogramand the asymmetry spectrogramboth demonstrate involvement of allfrequencies, 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) inwhich 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 2asymmetry panels do not show the typical seizure pattern with these artifactual increases in amplitude. This example shows the benefit of using multiple QEEGmeasures 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 ICEwith mini-depth electrode located in the right frontal cortex. The bottom 6 channels are from the mini-depth (ICE), andthe remainder are from standard scalp EEG. ICE shows rhythmic 3-Hz spike-and-wave complexes maximal at D3-D4 withdecrease in frequency and evolution in amplitude andmorphology. This is the offset of one of her typical seizures. There wasno 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 INTRACRANIALEEG Misinterpretation can arise from inadequate dis-playing of the EEG, particularly when faster frequenciesare involved. It is well known that during analog-to-dig-ital conversion of the EEG signal, a sampling rate of atleast twice the highest frequency component (referredto 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 frequentlyappreciated that the same rule also applies when thedigitized 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 atypical 21-inch monitor with 12803 1024 resolution,only 2.5 seconds should be displayed on the screen at atime. Similar issues can occur with vertical resolution,and too many channels displayed at once should beavoided. Computer-aided analysis of intracranial EEGwill become essential as broader band EEG (from DCto several hundredHz or more) is usedmore frequently,especially if clinical utility of high-frequency oscillationsis confirmed.25
CONCLUSION Every EEG should be interpreted withcare and caution to avoid pitfalls (table 5). This is espe-cially true for studies recorded in the ICU where artifactsare numerous and many EEG patterns may reflect dif-ferent processes, including ictal, interictal, andmetabolic,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 the seizure onset viewedwith a time base of 30mm/s. The earliest sustained ictal activity appears to be in the LMT (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 theearliest 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 the same signal viewed at a resolution of 190 pixels persecond. (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 overinterpretationand unnecessarily aggressive treatment. Newer methodsof EEG analysis are useful and improve the yield of EEGmonitoring but they are themselves subject to artifactand misinterpretation. Proper training is a crucial aspectof minimizing as many of the errors as possible.
AUTHOR CONTRIBUTIONSN. 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.
DISCLOSUREN. 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 ifsuccessfully treated
Corollary error: If they don’t 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 not“ictal” (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)
Neurology 80 (Suppl 1) January 1, 2013 S41
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DOI 10.1212/WNL.0b013e31827974f8 2013;80;S26Neurology
Nicolas Gaspard and Lawrence J. HirschPitfalls in ictal EEG interpretation : Critical care and intracranial recordings
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