Epilepsia, 50(Suppl. 7):13–17, 2009
doi: 10.1111/j.1528-1167.2009.02211.x
FIFTY YEARS OF LANDAU-KLEFFNER SYNDROME
Guidelines for EEG in encephalopathy related
to ESES/CSWS in children
Marjan Scheltens-de Boer
Department of Clinical Neurophysiology, Erasmus Medical Center, Rotterdam, The Netherlands
tion. The fluctuating clinical course and EEG findings complicate the diagnostic process and
evaluation of effect of therapy. Studies describing
quantitative aspects of the epileptiform abnormalities in EEG are overrepresented in literature,
whereas qualitative aspects are relatively undervalued. Guidelines for evaluation of the EEG in
these syndromes, which focus on both aspects, are
presented.
KEY WORDS: EEG, Epilepsy, Landau-Kleffner
syndrome, SWI, Cognitive decline.
SUMMARY
Electrical status epilepticus during slow sleep
(ESES) or continuous spikes and waves during slow
sleep (CSWS) is a phenomenon characterized by
strong activation of epileptiform activity in the
electroencephalogram (EEG) during sleep. The
literature contains several small series of patients
and many case reports. Large prospective studies
are lacking. Definitions of the syndromes and EEG
criteria and methods vary, as does their classifica-
Several encephalopathy syndromes in children exist, in
which the electroencephalogram (EEG) during sleep
mostly shows a strong activation of epileptiform activity.
Symptoms vary: deterioration of one or more cognitive
functions with or without motor, behavioral, and/or psychomotor decline. Mostly these children have or develop
epileptic seizures.
Tassinari et al. (1977) introduced the term electrical status epilepticus during slow sleep (ESES) for this EEG phenomenon, which was converted to status epilepticus
during sleep (SES) (Tassinari et al., 2000). In 1989 the
Commission on Classification and Terminology (CCT) of
the International League Against Epilepsy (ILAE) introduced the more descriptive term continuous spikes and
waves during slow sleep (CSWS). In this report I will
focus on the EEG aspects and present guidelines for evaluation of the EEG in patients with ESES/CSWS-related
syndromes.
described, but large prospective studies are lacking. In the
description of these patients, inconsistent criteria for the
EEG parameters and clinical syndromes and other diagnostic tests are used, which hamper objectivity, comparison, and generalization.
The EEG parameters, which are used in the literature
dealing with ESES/CSWS, roughly can be divided into
quantitative and qualitative parameters.
Quantitative parameters
The percentage of epileptiform activity during sleep
can be expressed as spike-wave index (SWI) (Tassinari
et al., 2000), originally described as the percentage of (diffuse) spikes and waves during slow-wave sleep. Various
criteria are used for ESES/CSWS: an SWI of at least 85%
(Tassinari et al., 2000), 50% (Beaumanoir, 1995;
Beaumanoir et al., 1995), 90% (Rossi et al., 1999), 60%
(Inutsuka et al., 2006), and 25% (Van Hirtum-Das et al.,
2006). Others merely mention a strong activation of
epileptiform activity during sleep (CCT of the ILAE,
1989). By some authors no significant drop in performance is thought to occur when the SWI is lower than 85%
(Beaumanoir, 1995; Beaumanoir et al., 1995; Guzzetta
et al., 2005). The fluctuating clinical course and EEG
findings complicate the diagnostic process and therapy
evaluation (Stroink et al., 1997; Tassinari et al., 2000).
The methods to determine the SWI vary: considering
the percentage of diffuse spikes-and-waves during the
whole-night non-REM (rapid eye movement) sleep
Review of the Literature
In the literature many small series and case reports of
patients with ESES/CSWS-related syndromes have been
Address correspondence to Marjan Scheltens-de Boer, MD, Department of Clinical Neurophysiology, room BA 400, Erasmus Medical
Centre’s Gravendijkwal 230, 3015 CE Rotterdam, The Netherlands.
E-mail: m.scheltens@erasmusmc.nl
Wiley Periodicals, Inc.
ª 2009 International League Against Epilepsy
13
14
M. Scheltens-de Boer
(Tassinari et al., 1977), percentage of spikes-and-waves
during at least 15 min slow wave sleep (Lewine et al.,
1999), percentage spikes-and-waves during the total duration of each cycle of slow wave sleep (Massa et al., 2000),
the percentage of seconds with ‡1 spike-wave complex
during the first 30 minutes non-REM sleep of the first and
last sleep cycles (Aeby et al., 2005), SWI of at least one
sleep–wake cycle (Saltik et al., 2005), SWI during the
whole-night, first non-REM cycle or nap EEG (Inutsuka
et al., 2006).
Although the importance of a high SWI during sleep is
agreed upon (Morrell et al., 1995; Roulet Perez, 1995;
Rossi et al., 1999; Eriksson et al., 2003; Smith &
Hoeppner, 2003; Holmes & Lenck-Santini, 2006), relatively little attention is paid to the SWI during the awake
stage. Some authors claim that epileptic activity itself
hampers cognitive function (Seri et al., 1998; Gordon,
2000; Pearl et al., 2001; Holmes & Lenck-Santini, 2006;
Praline et al., 2006; Tassinari & Rubboli, 2006).
Several authors developed grading scales to quantify
the amount of epileptiform activity during sleep: Mikati
et al. (2002) used a gradation of 0–4 [no spike-waves
(SW); 0–25% SW; 25–50% SW; 50–75% SW; 75–100%
SW, respectively]. Beaumanoir (1995) and Beaumanoir
et al. (1995) distinguished four categories: CSWS**
(>85%), CSWS* (50–80%), CSWS- (<50%) and CSWS0
(no epileptiform activity). Aeby et al. (2005) developed a
grading system of four items containing epileptiform and
nonepileptiform parameters.
The described ESES/CSWS-associated sleep stages
also vary. Patry et al. (1971) only consider slow wave
sleep as does the CCT of the ILAE (1989). Galanopoulou
et al. (2000) stress sleep stages 3 and 4, Rossi et al. (1999)
stages 1 and 2, and Genton et al. (1995) non-REM and
REM sleep.
A variation of the percentage epileptiform activity during the night is mentioned sporadically (Galanopoulou
et al., 2000; Tassinari et al., 2000), with predominance of
epileptiform activity during the first part of the night.
Only incidentally the amplitude of epileptiform activity
is considered (Veggiotti et al., 2001; Aeby et al., 2005).
Qualitative parameters
Morphology and frequency of epileptiform activity and
discharges are mentioned infrequently (Bureau, 1995;
Morikawa et al., 1995; Lewine et al., 1999; Tassinari
et al., 2000; Guzzetta et al., 2005; Popović Miocinović
et al., 2005, Saltik et al., 2005). The presence of dipoles is
mentioned by Morrell et al. (1995), Galanopoulou et al.
(2000), and Smith and Hoeppner (2003).
Distribution of epileptiform activity during sleep mostly
is described as secondary bilateral synchronized
(Kobayashi et al., 1994; Morrell et al., 1995; Galanopoulou et al., 2000; Tassinari et al., 2000; Aeby et al., 2005;
Guzzetta et al., 2005); other descriptions are less frequent:
Epilepsia, 50(Suppl. 7):13–17, 2009
doi: 10.1111/j.1528-1167.2009.02211.x
hemi-ESES (Hirsch et al., 1995; Galanopoulou et al.,
2000; Tassinari et al., 2000; Irwin et al., 2001; Veggiotti
et al., 2001; Aeby et al., 2005; Guzzetta et al., 2005;
Saltik et al., 2005); asymmetric ESES (Aeby et al., 2005;
Saltik et al., 2005); bitemporal ESES or BTESES in
Landau-Kleffner syndrome (Rossi et al., 1999); focal
ESES or FES (Genton et al., 1995; Tassinari et al., 2000;
Ballaban-Gil & Tuchman, 2000; Teixeira et al., 2007);
and multiple foci (Aeby et al., 2005; Saltik et al., 2005).
Epileptiform foci during the awake stage are generally
thought to be associated with symptomatology: For
instance, receptive aphasia is related to the localization of
spikes and waves in thetemporal region, whereas behavioral
disturbances and more global cognitive decline seem to be
correlated with a frontal localization of epileptiform activity
(Beaumanoir, 1995; Beaumanoir et al., 1995; Tassinari
et al., 2000). Saltik et al. (2005) use an elaborate description
of epileptiform activityaccording to localization.
The global picture of the epileptiform activity of the
EEG during sleep sometimes is described, that is, fragmented (Veggiotti et al., 2001), continuous (CCT of the
ILAE 1989), subcontinuous, and periodic.
Nonepileptiform abnormalities in the description of
ESES/CSWS-related EEGs are mentioned less frequently:
Background pattern (Rossi et al., 1999; Tassinari et al.,
2000; Yan Liu & Wong, 2000; Irwin et al., 2001; Aeby
et al., 2005), slow wave foci (Tassinari et al., 2000; Irwin
et al., 2001; Aeby et al., 2005; Popović Miocinović et al.,
2005; Saltik et al., 2005), (presence of) sleep stages and
sleep phenomena (Nobili et al., 2001; Guzzetta et al.,
2005; Saltik et al., 2005), and evolution of epileptic
activity during sleep (Tassinari et al., 2000). Inclusion of
these parameters probably yields a better correlation with
clinical symptoms (Aeby et al., 2005).
Sleep architecture
Sleep architecture is disturbed, which by itself might
have an adverse effect on cognitive function (Hirsch et al.,
1995; Mikati et al., 2002).
Certain sleep parameters such as delta waves and sleep
spindles might play a role in the activation of epileptic
activity in sleep (Yung et al., 2000; Nobili et al., 2001;
Guzzetta et al., 2005). Beaumanoir (1995), Beaumanoir
et al. (1995) found a decrease in sleep spindles in patients
with CSWS.
EEG methods
Several ways to register epileptiform EEG activity during wakefulness and/or sleep relating to ESES/CSWS are
reported: ambulatory 24-h EEG (Yan Liu & Wong, 2000),
polysomnography with or without video (Garca-PeÇas,
2005; Guzzetta et al., 2005; Popović Miocinović et al.,
2005; Inutsuka et al., 2006; Teixeira et al., 2007). Sleep
EEGs (whole night registration or nap EEGs) with
(Teixeira et al., 2007) or without sleep medication and
15
Guidelines for EEG in Encephalopathy Related to ESES/CSWS
with (Tachikawa et al., 2001; Eriksson et al., 2003), or
without video registration and conventional awake EEG
(Teixeira et al., 2007).
Clinical syndromes
Table 1 shows a summary of the ESES/CSWS-related
syndromes and their most important EEG aspects
(Gordon, 1997; Galanopoulou et al., 2000; Tassinari et al.,
2000; Nickels & Wirrell, 2008).
Generally autistic epileptiform regression (Tuchman &
Rapin, 1997), Lennox-Gastaut syndrome (Galanopoulou
et al., 2000; Tassinari et al., 2000), benign occipital epilepsy (Galanopoulou et al., 2000; Tassinari et al., 2000),
and myoclonic-astatic epilepsy or Doose’s syndrome
(Galanopoulou et al., 2000) are headed under differential
diagnosis.
It is debated whether the epileptiform activity during
ESES/CSWS in the absence of evident clinical seizures
has an epileptic significance (Kallen, 2001). Opinions
regarding the temporal relationship between the clinical
course and EEG findings vary from a strict one, a delayed
one, to no relationship at all (Paquier et al., 1992; Lagae
et al., 1998; Rossi et al., 1999; Galanopoulou et al., 2000;
Massa et al., 2000; Tassinari et al., 2000; Ducuing et al.,
2004).
Proposed New Guidelines
Based on the preceding the following new guidelines
may be formulated.
Strong activation (an SWI of at least 50%) of epileptiform activity during non-REM, and also sometimes
REM-sleep, should trigger the possibility of an ESES/
CSWS-related syndrome.
The distribution of epileptiform activity in the EEG during the awake stage and during sleep in patients with an
ESES/CSWS-related syndrome can be focal, multifocal,
unilateral, asymmetric bilateral, symmetric bilateral, diffuse, or more restricted. The ESES/CSWS pattern may be
(sub)continuous, fragmented, or periodic.
Not only epileptiform activity during sleep and the
awake stage but also background pattern, focal slow
activity, sleep characteristics of the EEG, and sleep
architecture probably play an important role in the determination of symptoms, their severity, and prognosis of
the ESES/CSWS-related syndromes and should be
described.
For scientific purposes, the SWI and discharges in a
preferentially ambulatory 24-h EEG if possible with video
registration should be described during the awake stage,
per sleep stage, and during the course of the night (stable,
decreasing, or increasing). For scientific purposes, extra
sensors can be added [electro-oculography (EOG), pulse
oximeter]; hypnogram can be made afterwards. In our
center I developed the following scale for the SWI: 0 (no
SW); 1 (0–20% SW); 2 (20–50% SW); 3 (50–85% SW); 4
(>85% SW) to facilitate comparison with literature. For a
more detailed description it seems better to use the terms
range, mean, and most encountered percentage epileptiform activity to differentiate a monotonous EEG pattern
from a more fragmented or periodic one. In addition, epileptic discharges have to be described separately with
accompanying clinical events if possible. This method
favors selection of the most representative parts of the
EEG in the future.
For clinical purposes, a nap EEG after sleep deprivation
without sleep medication combined with an EEG during
the awake stage probably will suffice. If there is a high
suspicion of CSWS, one could expand the registration to a
longer period, preferentially a 24-h EEG.
In long sleep registrations a selection of the first and last
sleep cycle or part of the EEG probably will suffice to reliably quantify the epileptiform activity. The criterion of at
least 50% epileptiform activity during non-REM and/or
REM sleep seems most adequate, especially if the clinical
picture fits a CSWS/ESES-related syndrome.
EEG follow-up: For clinical purposes, only on clinical
suspicion of relapse or when doubt exists regarding the
cause or clinical changes. For scientific purposes, frequent
(initially, for instance, biweekly, and later on quarterly),
Table 1. Clinical syndromes
Syndrome
CSWS/ESES syndrome
Landau-Kleffner
Atypical BECTS
Opercular syndrome
Features
Epileptic focus
Sleep stage with high SWI and %
Global cognitive decline, (atonic)
seizures, motor disturbances
Receptive/mixed aphasia,
verbal agnosia, infrequent seizures
Most nocturnal (partial) seizures
with cognitive and behavioral
disturbances
Resembling BECTS
Frontocentral/frontotemporal
Centrotemporal/Frontal
(Centro)temporal/ posterior temporal/
parietooccipital, (vertical dipole)
Centro(temporal),(horizontal dipole)
Non-REM >85% or
>50%, most diffuse
(Non-)REM Any %
BTESES/unilateral/diffuse
(Non-)REM <50 or >50%,
focal or diffuse
Centrotemporal (bilateral)
Non-REM (REM?) Any %
CSWS/ESES, continuous spikes-and-waves during slow sleep/electrical status epilepticus during slow sleep; BECTS, benign epilepsy with centrotemporal spikes; REM, rapid eye movement; BTESES, bitemporal ESES.
Epilepsia, 50(Suppl. 7):13–17, 2009
doi: 10.1111/j.1528-1167.2009.02211.x
16
M. Scheltens-de Boer
EEGs are recommended in order to correlate EEG parameters with the clinical course.
Large prospective multicenter studies with clear uniform clinical and EEG criteria, such as formulated in the
preceding text, have to be performed in the future for
determination of the optimal SWI to define the syndromes
and identification of possible other clinical important
parameters in the EEG.
Acknowledgments
Drs G.H. Visser and J.C. Perumpillichira and Prof W.F.M. Arts are
gratefully acknowledged for their help.
I confirm that I have read the Journal’s position on issues involved in
ethical publication and affirm that this report is consistent with those
guidelines.
Disclosure: I have no conflicts of interest to disclose.
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