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INVITED REVIEW

Normal Variants Are Commonly Overread as Interictal Epileptiform


Abnormalities
Joon Y. Kang* and Gregory L. Krauss*
*
Department of Neurology/Epilepsy Division, Johns Hopkins University School of Medicine, Baltimore, Maryland, U.S.A.

Summary: Electroencephalographers may misclassify benign syncope, for example, often have microvascular disease and EEG
variant EEG patterns as epileptiform discharges, resulting in wicket rhythms in drowsinessda careful review of the clinical
delays in the diagnosis and appropriate treatment of other history and the paroxysmal EEG pattern usually help distinguish
paroxysmal disorders, such as psychogenic nonepileptic seizures, normal variant patterns from interictal sharp waves and spikes
anxiety/panic disorders, and near syncope. These benign variant and avoid misdiagnosing epilepsy.
patterns include wicket spikes, small sharp spikes, and rhythmic Key Words: Benign or normal variant EEG patterns, Wickets
mid-temporal theta of drowsiness. Cautious interpretations of rhythms/spikes, Small sharp spikes, Rhythmic mid-temporal
semi-rhythmic sharp transients, usually gradually rising from the theta of drowsiness, Interictal epileptiform discharges, Epilepsy
EEG background in drowsiness, can help avoid misdiagnosing misdiagnosis.
patients as having seizures. Viewing the EEG as confirmatory for
a clear clinical diagnosis is also helpfuldelderly patients with (J Clin Neurophysiol 2019;36: 257–263)

prolonged video EEGs from an epilepsy monitoring unit and


reported that wicket spikes occurred most commonly in the left
INTRODUCTION temporal region (69%), possibly in association with cerebral
One of the most challenging aspects of interpreting EEGs is microvascular disease. Auditory stimulation and arousal can
distinguishing between pathologic activity and similar appearing attenuate wicket patterns, while drowsiness or light sleep and
normal physiologic findings called “normal” or “benign var- rapid eye movement sleep can activate wicket spikes.10,11
iants.” When benign variants appear in small fragments with Wicket spikes are commonly misinterpreted as IEDs be-
sharp morphology, the normal patterns can easily be misinter- cause of their unilateral distribution, temporal location, and
preted as epileptiform discharges. Benign variantsdwhich are spike-like appearance when occurring as single discharges. A
especially susceptible to overinterpretationdinclude the follow- number of features can be used to distinguish wicket spikes from
ing: wicket spikes/rhythms, benign epileptiform transients of temporal IEDs. Unlike IEDs, wicket spikes do not disturb the
sleep (small sharp spikes), and rhythmic mid-temporal theta background activity and do not have an after-going slow
bursts of drowsiness. Overinterpretation of these patterns often
wave.3,12 Single wicket spikes may be difficult to differentiate
results in misdiagnosisdwith subsequent inappropriate and
from IEDs. Wicket spikes are single fragments of wicket rhythms,
costly treatment.1–4
and an important clue is that most recordings with wicket spikes
The main purpose of this article was to provide an overview
have longer duration wicket rhythms present elsewhere in the
of several normal variants that are often mistaken as interictal
recording with a similar arcuate morphology. While light sleep/
epileptiform discharges (IEDs) and to provide basic points on
drowsiness activates both epileptiform discharges and wickets,
how to differentiate physiologic patterns from pathologic
rapid eye movement sleep suppresses IEDs and activates wicket
findings.
spikes.13,14
Wickets are seen infrequently on routine EEG recordings,
Wicket Spikes and Wicket Rhythms with a reported incidence range of 0.03% to 2.9% in several large
Wicket rhythms are medium to high voltage (60–210 mV), case series.15 The rarity of this pattern is most likely the reason
theta to alpha range (6–11 Hz), monophasic wave bursts that why wicket spikes are most often mistaken for IEDs; most EEG
usually evolve from the background as arcuate-shaped, brief readers do not gain enough experience identifying wickets during
(0.5–1 second) rhythmic discharges (Fig. 1).5,6 Wicket rhythms formal training.16 White strictly defined that wickets may be rare,
occur most commonly in drowsiness, are usually maximal over unspecified temporal “wicket-like” temporal sharp transients are
the temporal regions, and can occur unilaterally or bilaterally very common, and the main cause of overinterpretation.3
with shifting asymmetry, although one side can be more dom- Fluctuations of background activity in the temporal region with
inant than the other.7,8 Wicket spikes occur as single fragments of anterior or mid-temporal phase reversals may be mistaken for
wicket rhythms (Fig. 2). Azzam et al.9 recently reviewed 133 sharp waves.3 The presence of phase reversal does not make
a discharge epileptiform or even abnormal. Phase reversal is a
The authors have no funding or conflicts of interest to disclose.
Address correspondence and reprint requests to Joon Y. Kang, MD, 600 N Wolfe
relative measure of maximum surface polarity (usually negative)
Street Meyer 2-147, Baltimore, MD 21287, U.S.A.; e-mail: Jkang50@jhmi. used for localization and can be seen with normal physiologic
edu. patterns and artifact.
Copyright Ó 2019 by the American Clinical Neurophysiology Society
ISSN: 0736-0258/19/3604-0257 Wickets are most commonly seen in adults older than 30
DOI 10.1097/WNP.0000000000000613 years and are used to be believed to be more frequent in patients

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J. Y. Kang and G. L. Krauss Normal Variants Are Commonly Overread as Interictal

FIG. 1. Wicket rhythm observed in an 83-year-old man with a history of small multiple small strokes. There is a wicket rhythm present over
the right temporal area, occurring during drowsiness. Wicket rhythms are 6 to 11 Hz normal variants occurring over temporal regions mostly
in drowsiness.

with cerebrovascular disease, dizziness/vertigo, headaches, and is therefore essential that electroencephalographers carefully
migraines,7,9,12,17,18 but this is doubtful. Wickets typically first distinguish SSS from IEDs. Compared with IEDs, SSS have
are seen in mid to late adulthood, while epileptic IEDs often has a simple morphologic appearance with little variation in duration
an earlier age of onset (Fig. 3).19,20 However, wickets have no and amplitude when occurring within the same recording. SSS
association with epilepsy; in one study, wickets were four times tend to appear as single, sporadic transients and, when repeated,
more likely to be present in patients without a history of seizures are often separated by more than 10 seconds. Interictal epilep-
than in those with a history of seizures.5 tiform discharges often occur in repetitive clusters and may be
associated with accompanying focal slowing with disruption of
background rhythms. Unlike anterior temporal sharp waves, SSS
Small Sharp Spikes may have a broader distribution within the temporal lobe. While
Small sharp spikes (SSS), named by Gibbs and Gibbs in IEDs during wakefulness may be seen occasionally, SSS never
1952, are synonymous with benign epileptiform transients of appear during wakefulness and appear mainly in drowsiness. The
sleep21 and with benign sporadic sleep spikes. SSS are small appearance of stereotyped, isolated, small-amplitude spikes that
amplitude (,50 mV), brief (,50 ms), electronegative spikes in do not disrupt the background and appear only in drowsiness
the broad temporal region that appear almost exclusively during strongly suggest that the transient is SSS.
drowsiness or light non-rapid eye movement sleep (Fig. 4). SSS The clinical significance of SSS used to be controversial.
may occasionally be accompanied by an after-going slow wave; SSS were originally thought to be a pattern associated with
this slow wave usually has a smaller amplitude relative to the clinical seizures22–24 and as indicators of moderate epileptoge-
spike.16 When multiple SSS are present in a patient’s record, the nicity.25 This view has been disputed by several larger studies
overall lateralization should be symmetric. SSS are usually seen that found that SSS occur as frequently26 or more frequently in
in adults (2.9% between 30 and 40 years of age) and are almost patients without seizures as in patients with epileptic seizures.21
never seen in children younger than 10 years.22 SSS may be best Sleep deprivation has been shown to increase the frequency of
seen with nasopharyngeal electrodes, but these are no longer benign epileptiform transients of sleep in normal patients without
commonly used. epilepsy, which reinforces the thought that SSS are state-dependent,
SSS are one of the most common benign variants, appearing nonpathologic variants.27 However, a recent study with hippocam-
in up to 24% of scalp EEG recordings that include sleep.15,21,23 It pal implanted electrode investigations demonstrated that in some

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Normal Variants Are Commonly Overread as Interictal J. Y. Kang and G. L. Krauss

FIG. 2. Wicket spikes and wicket rhythms observed in a 63-year-old man with a history of HIV, a seizure, hypertension, and cerebrovascular
disease. A, There are several medium-voltage sharp wicket patterns recorded over the right temporal region with phase reversals at T4 and
F8-T4 leads. Isolated wicket spikes such as these appear similar to focal sharp waves. B, As seen later in the recording, most wicket spikes
also occur in brief runs of wickets with an arcuate appearance located over the temporal areas. Identifying these longer wicket discharges
can help identify the wicket spikes.

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J. Y. Kang and G. L. Krauss Normal Variants Are Commonly Overread as Interictal

similarities with epileptiform discharges that may be seen


during temporal lobe seizures (psychomotor seizures).12,29 This
normal variant consists of paroxysmal, medium- to high-
voltage (50–200 mV), theta (4–7 Hz) rhythmic bursts that are
maximal over the mid-temporal region.12,16,30 The square-
shaped 6-Hz waves may appear notched by a small, overriding,
10 to 12 Hz rounded component or flat-topped waves (Fig. 5).
There is little variability in morphology and frequency during
the bursts, but the amplitude may rise and fall at the onset and
end of the burst.16 Bursts may occur unilaterally or bilaterally in
an independent and synchronous fashion. If the bursts occur
unilaterally, there may be a left-sided predominance.31 Rhyth-
mic mid-temporal theta of drowsiness are best seen during early
drowsiness and disappear during deeper stages of sleep. Burst
duration is typically about 5 to 8 seconds, but can be as short as
FIG. 3. Distribution of age at onset of clinical episodes (n ¼ 25 for 1 second or last longer than 1 minute.12,16 Rhythmic mid-
each group). Adapted from Ref. 19. temporal theta of drowsiness appear in about 10% of recordings
in healthy, awake adults who are older than 60 years6 and in
patients (15 of 27), scalp SSS were time-locked to hippocampal about 1% of recordings in younger populations.30 Children
epileptiform discharges and to high-frequency oscillations.28 have higher amplitudes than adolescents.
Thus, it is possible that in some patients with mesial temporal Rhythmic mid-temporal theta of drowsiness may be con-
lobe epilepsy, SSS may be an early indicator of hippocampal fused (or overlap) with wicket rhythms in that both rhythms
pathologic condition. appear maximally in the temporal regions during light drowsi-
ness; however, RMTDs are slower in frequency and have longer
Rhythmic Mid-temporal Theta of Drowsiness duration (greater than 1 second) than wicket rhythms. The
Rhythmic mid-temporal theta of drowsiness (RMTDs), or waveforms of RMTDs may also appear notched rather than
the psychomotor variant, are so called because they share sharp because of the overriding, faster frequency.

FIG. 4. Small sharp spikes (benign epileptiform transients of sleep) observed in a 31-year-old man with a single tonic–clonic seizure. Small sharp
spikes in the recording are maximal first over the right temporal area (T4) and then the left temporal area (T3). These brief, low-amplitude spike
and slow wave discharges are ,50 ms duration and 50 mV amplitude, occur in early sleep in adults, and are not associated with epilepsy.

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Normal Variants Are Commonly Overread as Interictal J. Y. Kang and G. L. Krauss

FIG. 5. Rhythmic mid-temporal theta of drowsiness (RMTD). A 37-year-old man has thrashing movements during sleep. A run of RMTD
occurs over the left temporal region, maximal over the mid-anterior temporal region. Also called “psychomotor variant,” RMTD occur in
drowsiness and may spread from side-to-side as waxing and waning rhythmic discharges.

Rhythmic mid-temporal theta of drowsiness are generally on scalp EEG and occurs over several milliseconds (spikes 20–70
considered benign variants, largely because of lack of associated ms, sharp waves 70–200 ms). On scalp EEG, the approximate
clinical change. Hughes and Cayaffa29 reported that 8 of 11 source of the spikes/sharp waves can be inferred from the
subjects with RMTD had diminished latency in response, raising physiologic field reflected in nearby electrodes (corresponding
concerns about RMTDs’ ictal potential. A later study by Hughes voltage gradients are usually congruent with the amplitude of the
et al.,32 however, confirmed that RMTDs are the least epilepto- IED). Interictal epileptiform discharges may also be accompanied
genic of temporal discharges. Subsequent case studies have by focal slowing in the same region, which may be caused by an
consistently shown that prolonged, continuous runs (lasting up to underlying deep-seated interictal spike,38 but the focal slowing is
several hours) of RMTDs do not seem to impair function when
not specific for epilepsy.
the patient is tested.33,34 Rhythmic mid-temporal theta of
To help further differentiate benign variants from IEDs, one
drowsiness have been thought to be associated with psycholog-
can also examine the background patterns relative to the
ical symptoms32,35 and in one case, with an underlying temporal
transient. Benign variants such as wickets, SSS, and RMTDs
lesion.31 Magnetoencephalography studies of RMTDs in non-
epileptic and epileptic patients localized a maximum source for do not cause a paroxysmal disruption in the background, but
RMTD activity in the fissural cortex of the posterior inferior instead typically emerge from and fade into the background,
temporal region.36 without any slowing or disruption of the underlying physiologic
rhythms. Variants also have a simple morphologic appearance.
General Indicators of Benign Variants When sharp transients such as wickets occur in isolation, it is
One of the best ways to differentiate a benign variant from useful to examine the rest of the recording carefully to see
an IED is to first thoroughly understand the criteria for IED.37 whether similar, longer bursts of the pattern exist. The presence
The IEDs represent summated hypersynchronous neuronal firing of prolonged fragments within the same recording helps identify
with a paroxysmal depolarization shift with after-going hyper- normal benign variants and is a reassuring sign. Benign patterns
polarization, corresponding to a paroxysmal surface-negative also tend to have broader topography than focal IEDs; they can
spike/sharp activity with an after-going slow wave that can be appear in a broad region (i.e., the temporal lobe) and may shift in
clearly distinguished (and has a different frequency) from the lateralization within the same record. Last, the state of the patient
background activity. The IEDs often have a spiky/sharp mor- can help guide the interpretation. Most benign variants, such as
phology (often with steep upslope and more gradual downslope) SSS and wicket spikes, are activated by drowsiness and light

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J. Y. Kang and G. L. Krauss Normal Variants Are Commonly Overread as Interictal

FIG. 6. Rhythmic temporal activity in drowsiness. The recording is from a 24-year-old patient with probable syncope. A brief period of
drowsiness (stage I sleep) with relatively flat EEG is followed by brief arousal with a 10-Hz rhythmic pattern present for 3 seconds over the
left temporal area. This is followed again by brief drowsiness. Normal background patterns intermixed with drowsiness may be misidentified
as epileptiform discharges because of the focality, phase reversal, and rhythmicity of the discharges.

sleep. SSS, however, are never seen during wakefulness and outpatient EEG. Careful history-taking and analysis of clinical
rapid eye movement suppresses wicket spikes. events is critical to properly diagnosing epilepsy; the role of the
Sharply contoured simple fluctuation of background activity EEG should be supportive.37 When nonspecific transients occur
can be misinterpreted as epileptiform discharges, especially if there only once during an EEG finding, it may not be possible to
are anterior or mid-temporal phase reversals3 (Fig. 6). These determine whether a transient is an IED or a benign variant.
background patterns may be ascribed to extension of the alpha When this occurs, the finding should be described within the
activity into the temporal region, which during drowsiness may report with a comment that a suspicious transient was observed16
become isolated or fragmented, and combine with other frequen- and the study should be repeated if possible. It has been reported
cies (theta and beta) to create spike-like waveforms.39 Incomplete that repeating studies can increase the yield of detecting IEDs if
alpha attenuation may also resemble rhythmic temporal sharp the first EEG demonstrates nonspecific findings.42 If the above
activity. As with other benign physiologic patterns, these fluctua- methods do not apply, we recommend thatdwhen deciding the
tions do not disrupt the background rhythms and should not be significance of an isolated findingdelectroencephalographers
considered abnormal based on phase reversals. resort to the basic tenet of EEG interpretation: It is best not to
“overcall” a finding as being abnormal, and to err on the side of
“undercalling” labelling the finding as a normal variant, and to
place the possible finding in the context of the clinical history.
CONCLUSION/RECOMMENDATIONS
An estimated 20% to 30% of patients who are referred to
tertiary epilepsy centers are eventually diagnosed with non-
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Normal Variants Are Commonly Overread as Interictal J. Y. Kang and G. L. Krauss

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