Normal ''suspicious'' EEG

William O. Tatum Neurology 2013;80;S4 DOI 10.1212/WNL.0b013e31827974df This information is current as of January 14, 2013

The online version of this article, along with updated information and services, is located on the World Wide Web at: http://www.neurology.org/content/80/1_Supplement_1/S4.full.html

Neurology is the official journal of the American Academy of Neurology. Published continuously since 1951, it is now a weekly with 48 issues per year. Copyright 2013 by AAN Enterprises, Inc. All rights reserved. Print ISSN: 0028-3878. Online ISSN: 1526-632X.

Normal suspicious EEG

William O. Tatum, DO, FAAN

ABSTRACT

Correspondence to Dr. Tatum: tatum.william@mayo.edu

The EEG is a unique measure of electrical brain function and is widely used in patients with seizures. Many normal variants and variations of normal EEG have a predilection for the temporal lobe and mimic epileptiform discharges. The high prevalence of temporal lobe epilepsy and the propensity for normal variants to occupy the temporal lobe may result in an undesired bias, leading to misidentification of normal waveforms. Learning the common pitfalls, such as the variations of normal EEG, benign variants, and common artifacts, are essential lessons in EEG. Continuing education and acquiring experience in EEG interpretation are the basic tools to ensure patient safety. Above all, judging the results of the EEG interpretation in light of the patients clinical symptoms is a prerequisite to ensure proper management. Neurology 2013;80 (Suppl 1):S4S11
GLOSSARY
ED 5 epileptiform discharge; SREDA 5 subclinical rhythmic EEG discharges in adults.

The immediate result incurred by a misinterpreted EEG demonstrating epileptiform discharges (EDs) potentially includes lost driving privileges, impaired quality of life, the potential for compromised employment and social situations, and adverse effects from antiepileptic drug exposure. To accurately interpret an abnormal EEG, one must first have the ability to identify normal patterns. Just as a normal EEG does not exclude a clinical diagnosis of epilepsy (i.e., frontal lobe epilepsy), an abnormal EEG finding may not be related to the provisional diagnosis or presenting symptoms (i.e., dizziness). Unfortunately, an EEG may also be designated as abnormal based on misinterpretation. Particular suspicious waveforms may result in EEG misinterpretation. This review highlights normal EEG that is potentially subject to misinterpretation. In 29% to 55% of patients with epilepsy, the initial EEG will show EDs. Approximately 15% of these patients have repeatedly negative studies or normal-appearing EEG. This demonstrates the limitations of routine scalp EEG for detecting diagnostic abnormalities.1 Even when clear pathologic EDs with a specific profile are encountered, a spectrum of waveforms exists that range from normal to abnormal (figure 1). Indeed, patients with EDs that do not have epilepsy are encountered at rates ranging from 0.2% to 3.5%.2 Children are far more likely to have asymptomatic EDs compared with adults. Focal or generalized EDs have been reported in 3.5% of children without epilepsy; the vast majority of these EEG findings disappeared by early adolescence without developing seizures or epilepsy.3 Although EDs are rarely seen in patients who do not experience seizures, these waveforms that appear epileptiform may be seen in chronic nonepileptic states (i.e., cerebral palsy) or are the result of an acute neurologic injury in patients without clinical seizures.1
According to a longstanding global coalition of societies, which foster advances in EEG, the International Federation of Societies of Electroencephalography and Clinical Neurophysiology,4 EDs exist as transient potentials that are clearly distinguishable from background activity, have a pointed peak, and are described as a spike or a sharp wave. Spikes typically have a duration of 20 to 70 milliseconds, whereas a sharp wave with a negative surface component typically has a duration of 70 to 200 milliseconds. These criteria alone
EPILEPTIFORM DISCHARGES
From the Department of Neurology, Mayo College of Medicine, Mayo Clinic, Jacksonville, FL. Go to Neurology.org for full disclosures. Funding information and disclosures deemed relevant by the author, if any, are provided at the end of the article. S4 2012 American Academy of Neurology

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Figure 1

Abnormal interictal EEG

Abnormal interictal EEG in several adult patients with localization-related epilepsy demonstrating (A) a burst of repetitive T3 spike-and-slow waves (arrow), with a broad hemispheric field of spread (red arrow); (B) a burst of suspicious abnormal left temporal sharp waves (red arrow) and normal right rhythmic midtemporal theta bursts in drowsiness (black arrow); (C) a burst of bioccipital sharp and slow waves in a patient with right temporal-occipital epilepsy (note the variability in sharp wave amplitude and morphology); and (D) a positive sharp wave in a patient after left temporal lobe surgery.

are not adequate enough to distinguish EDs from other waveform types and many EEG readers are not familiar enough with the parameters that distinguish an abnormal sharp waveform from a normal variant, even though these guidelines exist (table).5 Using these criteria, . the majority of these sharp waveforms or spike configurations may be explained away or ignored; those

withstanding . usually prove to be highly correlated with clinical/pathologic actualities.5 The suggestion made 40 years ago to remain conservative when interpreting is still relevant today and is reinforced by the number of patients proven to have been misdiagnosed (based on follow-up video-EEG monitoring) on the basis of misinterpretation of routine EEGs.6,7 The rate

Table

Adapted from Maulsbys guidelines5 for assessing spikes and sharp waves

1. Every spiky-looking wave is an artifact unless there are one or more good reasons for suspecting otherwise. 2. Spikes and sharp waves of cerebral origin always occupy a definable electrical field on the scalp and should always be seen in 2 or more nearby electrode sites. 3. Clinically significant spikes and sharp waves are almost always surface negative in polarity initially, or at least the sharpest or highest voltage component of the wave is usually surface negative. 4. Most spike or sharp wave discharges of clinical import are followed by a slow wave or series of slow deflections. If it does not have a slow after-wave, be more suspicious of artifact or of a sudden alteration in voltage of physiologic background rhythms. 5. Ignore sharp or spiky events that can be logically explained by simple alterations in voltage of the existing background rhythms or by superimposition of several components in the background activity of the record. 6. There are several types of physiologic spikes or sharp waves, particularly during sleep; these should be thoroughly familiar to the interpreter and can be discriminated from abnormalities by knowledge of the patients age, state of consciousness, location on the scalp, and form or pattern of the wave in question.

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of such misdiagnoses is even higher for nonspecialists.8 Incorrect designation of EDs contributes to the clinical issue of misdiagnosis.1,3,57 There are guidelines available for conducting EEG studies,9 but those available for defining and identifying EDs do not exist for EEG interpretation. To date, studies on interrater reliability of EEG interpretation are scarce or focus on non-ED topics; furthermore, there is even considerable interreader variability among experts.10 Computer-based spike detectors aid in recognizing suspicious transients but the rate of overidentification is higher than the rate for human interpreters.11 Standardizing the parameters for clear electronegative spikes and sharp waves (involving distinct changes in frequency and amplitude), coupled with concomitant focal slowing, an after-going slow wave, and occupying a believable cerebral field in the absence of an alternative explanation such as an artifact or normal variant, may help improve our rate of correctly identifying EDs that are associated with seizures.
PITFALLS OF PATTERN RECOGNITION

Pattern recognition is inherently prone to pitfalls when rules of polarity and convention are ignored. The function of a bipolar montage is to compare 2 active electrode sites, whereas a reference montage compares an active and common electrode site. Phase reversals identify the sites of maximal electronegativity (or electropositivity). Therefore, the occurrence of a phase reversal may signify a normal finding (figure 2) and is not necessarily synonymous with an abnormality in the EEG (figure 1A). It is important to note that a "phase reversal" alone does not signify an abnormal EEG although it is frequently interpreted that way. It is well known that phase reversals are present

in almost every normal sleep record (figure 2A). The electrical convention relies on the electrophysiologic difference between both electrodes in the pair. When the voltage of the first electrode is more electronegative than the second electrode, the deflection of the waveform is in an upward direction (figure 2A). Similarly, if the voltage of the second electrode is more negative than the first electrode, then the deflection of the waveform is in a downward direction.12 Normal and abnormal phase reversals may exist as electronegative events. Infrequently, phase reversals that are electropositive may occur with abnormal spikes and sharp waves (figure 1D).13 Additionally, the superimposition of normal waveforms (or artifact) may appear to be abnormal but instead reflect a combination of innocuous potentials with different frequencies (figure 3). Any routine frequency (i.e., alpha, beta, theta, and delta) or waveform (i.e., mu and lambda) in the normal waking EEG may manifest activity that mimics EDs. Within the limited repertoire of recorded frequencies, durations, and amplitudes, some waveforms may be normal in one setting (i.e., alpha during wakefulness), but abnormal in others (alpha coma). Scenarios in which confusion exists between normal and abnormal waveforms (misidentified EDs on a prior EEG) occurred in 41 of 127 patients (32%) with psychogenic nonepileptic attacks who were incorrectly treated for epilepsy because of overinterpretation of normal fluctuations in alpha rhythm (figure 4).14 In an outpatient epilepsy clinic setting, incorrect abnormal EEG designations frequently correlated with multiple unexplained symptoms.15 During sleep, V waves and positive occipital sharp transients of sleep may be incorrectly identified as sharp waves

Figure 2

Adult EEG

Adult EEG demonstrating (A) normal vertex sharp waves in a transverse bipolar montage. Note the downward and upward deflections that comprise a phase reversal (boxes). The arrow denotes the site of maximal electronegativity seen in channels Fz and Cz. (B) Breach rhythm after a right frontotemporal craniotomy with a series of phase reversals in the right midtemporal region that are spiky (box) and reflect a breach rhythm and not abnormal epileptiform discharges. S6 Neurology 80 (Suppl 1) January 1, 2013

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Figure 3

A normal burst of theta in the EEG of an adult during drowsiness

The findings were reported as suspicious for atypical spike-and-wave patterns that were due to normal superimposition of background frequencies and artifact. Note the prominent intermixed beta activity and electrode artifact at F7 and F3 that combine to make the appearance spikier.

(figure 2A). This is particularly important during drowsiness and light sleep in youth, because many vertex waves and positive occipital sharp transients of sleep may appear spiky, mimicking EDs. Drowsiness tends to produce normal paroxysmal features that look like generalized EDs (figure 5).16 Additionally, sharp transients are identified in .90% of normal drowsy patients, which can also result in misidentification of EDs.17 Typically, identification of normal physiologic V waves is not difficult if montages other than a longitudinal bipolar are used, but the spatial distribution may catch the readers eye and lead to overidentification of EDs (figure 2A). Breach rhythms that emerge after craniotomy may appear spikier because of superimposed beta activity, but are a normal expected finding for such conditions (figure 2B). Normal variants such as wicket spikes (figure 6) have been previously detailed,12,14,15,18 although there are robust examples of wicket spikes that

mimic EDs. These nonevolving rhythmic bursts represent a normal finding that is unrelated to seizure manifestations. Benign epileptiform transients of sleep and rhythmic midtemporal theta bursts of drowsiness may also appear similar to an ED (figure 7). Positive bursts, measured at 14 and 6 Hz and often low-amplitude 6-Hz (phantom) spike-and-wave patterns, although indeed epileptiform, reflect benign waveform variants of uncertain significance.12 Wicket waves are among the most frequently misread pattern of uncertain significance with 25 of 46 (54%) interpreted as EDs, often on the basis of single discharges.18 Single potentials or brief trains of sharply contoured waveforms recorded over the temporal regions during drowsiness are usually symmetric in their rate of rise and fall. These waveforms are identical in frequency to their fellow waveforms and do not have an after-going slow wave, nor are they associated with other abnormal
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Figure 4

Normal alpha in an adult EEG with a phase reversal at the T6 electrode derivation that was identified as suspicious for an epileptiform discharge (arrows)

features such as complex EDs or focal slowing in the same region of their occurrence. The occurrence of such waveforms underscores the need for conservative interpretation. Dramatic subclinical rhythmic EEG discharges in adults (SREDA) resemble an electrographic seizure, although it bears no relationship to epilepsy and is rare, occurring in less than 0.05%.12 Most interpreters will never encounter a SREDA, so misinterpretation of a SREDA as seizure activity is unanticipated. Focal epilepsy is the most common human adult epilepsy with two-thirds of cases originating in the temporal lobe.19 Temporal waveforms in the EEG are also the most common potentials misinterpreted as EDs.20 Therefore, even without prior knowledge of the reason the EEG is performed, the interpreter may be subconsciously suspicious because of the prevalence of temporal lobe epilepsy.12,14,15,18 When the reason for referral is a spell or seizure, there might be an inherent bias to identify EDs in the EEG that help support the diagnosis of epilepsy biasing the reader to foster overinterpretation. Coupled with a lack of training
SUSPICIOUS MINDS
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and inexperience, the correct electroclinical diagnosis that is averted by a misinterpreted EEG may defy correction of the mistreatment of epilepsy and remain an undisclosed problem unless video-EEG is performed.14 The problems of fluctuation in the accuracy of EEG interpretation may vary from person to person and even in the same person over time.21 When controversial or epileptiform waveforms are encountered based on the appearance of the waveform alone, a conservative approach is always warranted (figure 8). True EDs may be encountered during EEG interpretation, although this should not be equated with an automatic clinical association with epilepsy and the finding interpreted within the clinical context of the symptoms.22 For diagnostic purposes when identifying EDs, I use the 2 minute rule: if 2 minutes after review of the EEG, a discharge is unable to be clearly categorized as an ED, a conservative interpretation should apply, and the waveform interpreted as nonepileptiform. Results that use words such as borderline to represent the impression of the EEG features are noncommittal and suggest that the interpreter is unable to distinguish normal from abnormal.

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Figure 5

Normal EEG in an 18-year-old showing a hypnagogic (drowsy) burst (oval) of paroxysmal theta and delta frequencies that appears sharply contoured

This reflects normal electrocerebral activity during sleep transition. Note the change in the EEG immediately after the burst to reflect the change in state. The MARK applied by the technologist signifies a suspicious burst.

Figure 6

Wicket spikes appearing in repetitive bursts during the awake state in a 57-year-old (circles)

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Figure 7

Rhythmic midtemporal theta bursts of drowsiness in the EEG of a young adult

Note the sharply contoured waveform that mimics the appearance of bilateral bursts of repetitive temporal sharp waves (boxes).

Figure 8

Adult EEG demonstrating lambda waves during scanning eye movements (black arrows)

Although the pattern may appear morphologically as a sharp wave, the location, positive polarity, and the relationship to scanning eye movements (reading) are distinctive. Note the disappearance of the lambda waves after eye closure (red arrows) with return of the normal alpha rhythm that further identifies this feature as a normal finding. S10 Neurology 80 (Suppl 1) January 1, 2013

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Reporting reliability is reinforced if a confident description of ED distribution, morphology, frequency, duration, and field is encountered. If the report is confusing to the clinician, then experience and reliability may be questionable, especially when the report is at odds with the clinical state of the patient. In the age of digital EEG, including an image of the abnormal waveforms would help to provide the clinician a chance to validate suspicious findings that might carry serious and long-term clinical ramifications. Designating an EEG as normal when the waveform is abnormal will probably not lead to harmful treatment. However, an incorrectly identified abnormal EEG based on the presence of EDs may lead to a misdiagnosis and mistreatment as epilepsy. Some neurologists have no formal training in EEG, no board certification in clinical neurophysiology, no affiliation with EEG education, nor routinely interpret EEGs, yet provide care to patients with seizures.23 Guidelines for interpreting abnormal waveforms are needed to prevent misinterpreted EEGs from imparting long-term diagnostic and treatment delays that may be masked for years before recognition of the underlying problem.24 Therefore, it is incumbent upon all physicians interpreting EEGs to remain conservative in their interpretation.
CONCLUDING STATEMENTS AUTHOR CONTRIBUTIONS
W.O. Tatum: drafting/revising the manuscript, contribution of vital reagents/tools/patients, study supervision.

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The author thanks Dr. Barbara Westmoreland for her helpful review and suggestions and Mrs. Kelly Viola for her editorial assistance with the manuscript.

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DISCLOSURE
The author reports no disclosures relevant to the manuscript. Go to Neurology. org for full disclosures.

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Received November 16, 2011. Accepted in final form September 25, 2012. REFERENCES 1. Pillai J, Sperling MR. Interictal EEG and the diagnosis of epilepsy. Epilepsia 2006;47(suppl 1):1422. 2. Zivin L, Ajmone Marsan C. Incidence and prognostic significance of epileptiform activity in the EEG of non-epileptic subjects. Brain 1968;91:751778. 3. Cavazutti GB, Cappella L, Nalin A. Longitudinal study of epileptiform EEG patterns in normal children. Epilepsia 1980;21:4355. 4. IFSECN. A glossary of terms commonly used by clinical electroencephalographers. Electroencephalogr Clin Neurophysiol 1974;37:538548. 5. Maulsby RL. Some guidelines for assessment of spikes and sharp waves in EEG tracings. Am J EEG Technol 1971;11:316.

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Normal ''suspicious'' EEG William O. Tatum Neurology 2013;80;S4 DOI 10.1212/WNL.0b013e31827974df This information is current as of January 14, 2013
Updated Information & Services References including high resolution figures, can be found at: http://www.neurology.org/content/80/1_Supplement_1/S4.full. html This article cites 23 articles, 6 of which can be accessed free at: http://www.neurology.org/content/80/1_Supplement_1/S4.full. html#ref-list-1 This article, along with others on similar topics, appears in the following collection(s): All Epilepsy/Seizures http://www.neurology.org/cgi/collection/all_epilepsy_seizures EEG http://www.neurology.org/cgi/collection/eeg_ Information about reproducing this article in parts (figures, tables) or in its entirety can be found online at: http://www.neurology.org/misc/about.xhtml#permissions Information about ordering reprints can be found online: http://www.neurology.org/misc/addir.xhtml#reprintsus

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