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PAPER
Which electroencephalography (EEG) for epilepsy?
The relative usefulness of different EEG protocols in
patients with possible epilepsy
J P Leach, L J Stephen, C Salveta, M J Brodie
...............................................................................................................................
J Neurol Neurosurg Psychiatry 2006;77:1040–1042. doi: 10.1136/jnnp.2005.084871
See end of article for
authors’ affiliations
.......................
Correspondence to:
J P Leach, Epilepsy Unit,
Western Infirmary,
Glasgow G11 6NT, UK;
johnpaul.leach@sgh.scot.
nhs.uk
Background and aim: Electroencephalography (EEG) is an essential investigative tool for use in young
people with epilepsy. This study assesses the effects of different EEG protocols on the yield of EEG
abnormalities in young people with possible new epilepsy.
Methods: 85 patients presenting to the unit underwent three EEGs with differing protocols: routine EEG (r-
EEG), sleep-deprived EEG (SD-EEG), EEG carried out during drug-induced sleep (DI-EEG). The yield of
EEG abnormalities was compared using each EEG protocol.
Results: 98 patients were recruited to the study. Of the 85 patients who completed the study, 33 (39%)
showed no discernible abnormality on any of their EEG recordings. 36 patients (43%) showed generalised
spike and wave during at least one EEG recording, whereas 15 (18%) had a focal discharge evident at
some stage. SD-EEG had a sensitivity of 92% among these patients, whereas the sensitivity of DI-EEG and
r-EEG was 58% and 44%, respectively. The difference between the yield from SD-EEG was significantly
higher than that from other protocols (p
,
0.001). Among the 15 patients showing focal discharges, SD-
EEG provoked abnormalities in 11 (73%). r-EEG and DI-EEG each produced abnormalities in 40% and
27%, respectively. 7 patients (47%) had changes seen only after sleep deprivation. In 2 (13%), the only
abnormalities were seen on r-EEG. In only 1 patient with focal discharges (7%) was the focal change noted
solely after drug-induced sleep. These differences did not reach significance.
Conclusion: EEG has an important role in the classification of epilepsies. SD-EEG is an easy and
inexpensive way of increasing the yield of EEG abnormalities. Using this as the preferred protocol may
help reduce the numbers of EEGs carried out in young patients presenting with epilepsy.
Received
25 November 2005
Revised version received
12 June 2006
Accepted 21 June 2006
Published Online First
26 June 2006
.......................
tive tool for use in young people with epilepsy.
1–5
The
clinical onset of the idiopathic generalised epilepsies
(IGEs) is most common in adolescence and early adulthood,
and this is when EEG is most valuable.
5
Differentiation of
IGE from partial epilepsy should be done as early as possible,
because of the important implications it will have on
treatment choice,
6
planned duration of treatment
6
and
prognosis.
7
Despite its utility, EEG is not always easily
available in many parts of the UK. Clinical targeting is
desirable to allow efficient use of this resource.
8
The effect of sleep deprivation on EEG has long been
recognised.
239
For reasons that are unclear, the incidence of
epileptiform abnormalities on EEG is increased by sleep
deprivation. Some authors feel that this effect leads to an
enhanced yield of epileptiform abnormalities even when
compared with routine EEG (r-EEG) that includes a period of
sleep,
3
although one study did not support the special effect
of sleep deprivation.
4
Although the role of the EEG in early epilepsy is widely
recognised in this age group, there are few data on the
relative sensitivity of EEG protocols in detecting epileptiform
changes. One study
9
looked at the incidence and frequency of
epileptiform abnormalities after EEG with drug-induced
sleep (DI-EEG) and EEG after sleep deprivation (SD-EEG).
This cohort consisted largely of patients already on treatment
for localisation-related epilepsies.
Carpay et al
10
repeated SD-EEG in a cohort of younger
people with normal r-EEG and found that 34% of them
showed various epileptiform abnormalities. The age range
and selection criteria limit the applicability of these data. An
earlier study
11
had a previously normal r-EEG, some of whom were
receiving drugs for epilepsy. Despite this, 47 patients
exhibited some clearly ictal activity, but this selection
precluded direct comparison of elicited epileptiform changes
in different protocols.
In young adults with newly diagnosed epilepsies, the role
of provocative testing (either SD-EEG or DI-EEG) remains
unclear, as the relative yield of generalised discharges in each
protocol has yet to be properly compared. In young adults
with newly diagnosed epilepsy, which EEG protocol is best?
Should SD-EEG be the preferred protocol? Is DI-EEG as
sensitive or specific as SD-EEG in detecting abnormalities?
METHODS
Patients ,35 years of age with possible new epilepsy were
recruited to the study after receiving informed written
consent from them to undergo three EEGs before starting
treatment. All patients had experienced at least two general-
ised tonic–clonic seizures. This study was approved by the
West Glasgow medical ethics committee. Each patient was
assigned to undergo EEGs in random order, one of each of
the three protocols: without specific patient preparation (r-
EEG), after sleep deprivation (SD-EEG) or after receiving oral
temazepam (DI-EEG). Initial EEG was carried out approxi-
mately 4 weeks after the presenting event, whereas subse-
quent EEG recordings were separated by at least 7 days. The
particulars of the different protocols are as follows:
had carried out SD-EEG in 114 patients who
Abbreviations: DI-EEG, EEG during drug-induced sleep; EEG,
electroencephalography; IGE, idiopathic generalised epilepsy; r-EEG,
routine EEG; SD-EEG, EEG after sleep deprivation
www.jnnp.com
E
lectroencephalography (EEG) is an essential investiga-
EEG protocols in patients with epilepsy
1041
Table 1 Characteristics of each recording grouped by protocol
DI-EEG (n = 94)
r–EEG (n = 99)
SD-EEG (n = 92)
Median duration (min)
41
21.8
40.5
Range
18-60
15-42
10-57
IQR
37–44.5
19.5–23
36–44
Fast activity
42%
25%
22%
Deepest sleep stage attained (%)
Awake
11
53
5
Stage 1
22
21
13
Stage 2
61
25
60
Stage 3
6
0
14
Stage 4
1
0
8
DI-EEG, EEG during drug-induced sleep; EEG, electroencephalography; IQR, interquartile range; r-EEG, routine
EEG; SD-EEG, EEG after sleep deprivation.
N
r-EEG consisted of a normal recording, including approxi-
mately 3 min of hyperventilation and intermittent photic
stimulation at various frequencies.
N
SD-EEG consisted of a recording with the same activation
methods, carried out after a period of outpatient sleep
deprivation. Patients were asked to refrain from sleeping
the evening before the test and to fast from 22:00 h
onwards.
N
DI-EEG was recorded 30 min after ingestion of 10 mg oral
temazepam. Where possible, the same activation proce-
dures were undertaken.
beginning treatment; 13 patients failed to complete the
study, undergoing fewer than three EEGs before starting
treatment. Most patients were lost to follow-up, and none
were recorded as having withdrawn consent after seizure
induction.
Characteristics of recordings in each protocol
The stage of sleep attained in each group is shown in table 1.
As expected, more patients attained deeper stages of sleep
after sleep deprivation and to a lesser extent after receiving
temazepam. The duration of recording in each protocol is
shown in table 1. Of the 85 patients who completed the
study, 33 (39%) showed no epileptiform abnormality on any
of their EEG recordings (table 2). In all, 36 patients (43%)
showed generalised spike and wave during at least one EEG
recording, whereas 15 (18%) had a focal discharge evident at
some stage. One patient had generalised slow waves seen on
both SD-EEG and DI-EEG.
Fast-wave changes are an incidental finding more pre-
valent after use of certain drugs including benzodiazepines.
As expected, these were more common in the DI-EEG group.
Each recording was stopped when a patient had completed
hyperventilation, exposure to photic stimulation and sponta-
neously awoken from a period of sleep (if applicable). EEGs
were stored in digital form on CD-ROM. All EEGs were
reported by a consultant in neurology and clinical neurophy-
siology (JPL), who was blinded both to the clinical details
and to the protocol used in each individual recording. EEGs
were reported as being normal or abnormal, with abnorm-
alities defined as the presence of epileptiform abnormalities
in a focal or generalised distribution.
Statistical analysis
Statistical analysis was carried out, where appropriate, on a
PC using V.13.3 of Minitab for Windows. Three-way
comparisons were carried out using x
2
test to assess the
Sensitivity of each recording protocol
In all, 36 patients showed generalised spike and wave
discharges. SD-EEG had a sensitivity of 92% among these
patients, whereas sensitivity of DI-EEG and r-EEG was 58%
and 44%, respectively. Significant difference was observed
between SD-EEG and DI-EEG (p,0.001) and between SD-
EEG and r-EEG (p,0.001) but not on comparing DI-EEG
with r-EEG (p = 0.09).
In one patient, abnormalities were evident on r-EEG but
not on other protocols. In another patient, the only general-
ised discharges seen were during the DI-EEG. In contrast, 10
patients (28%) had their sole changes occurring after a period
of sleep deprivation. The incidence of ‘‘sole abnormalities’’
was significantly higher (p = 0.001) in SD-EEGs than in both
other groups.
Among the 15 patients showing focal discharges, SD-EEG
provoked abnormalities in 73%. r-EEG and DI-EEG each
produced abnormalities in 40% and 27%, respectively. In all, 7
patients (47%) had changes seen only after sleep deprivation.
In 2 patients (13%) the only abnormalities were seen on r-
EEG. In 1 patient (7%), the sole focal change noted was after
drug-induced sleep.
significance.
RESULTS
Demographics
In all, 98 patients were recruited to the study. The median age
of study recruits was 17.9 (interquartile range 15.7–
22.1) years. Eighty five patients completed the study before
Table 2 Electroencephalogram abnormalities with each
protocol among 85 patients completing the study
n (%)
Sensitivity
Paroxysmal spike and wave
36 (43%)
Yield SD-EEG
33
0.92
Yield DI-EEG
21
0.58
Yield r-EEG
16
0.44
Focal
15 (18%)
Yield SD-EEG
11
0.73
Yield DI-EEG
4
0.27
Yield r-EEG
6
0.40
3 normal EEGs
33 (39%)
Risk of clinical seizure occurrence during each
recording method
Two patients had a generalised seizure during at least one of
their recordings. One patient had a generalised tonic–clonic
seizure during SD-EEG, whereas another had a generalised
tonic–clonic seizure during both r-EEG and SD-EEG. No
generalised seizures occurred during DI-EEG. No generalised
Generalised slow waves
1 (1%)
Yield SD-EEG
1
100.00
Yield DI-EEG
1
100.00
Yield r-EEG
0
0.00
DI-EEG, EEG during drug-induced sleep, EEG, electroencephalogram;
r-EEG, routine EEG; SD-EEG, EEG after sleep deprivation.
www.jnnp.com
1042
Leach, Stephen, Salveta, et al
seizures were reported to have occurred after the patients left
the EEG department.
In contrast, using SD-EEG as the preferred protocol would
lead to 100 SD-EEGs being carried out (with around 39
yielding generalised spike and wave). The sensitivity of SD-
EEG would render repeat EEG unnecessary in all but those
cases with remaining strong clinical suspicion of IGE.
Therefore, we can assume that preferred use of r-EEG may
be expected to lead to 81 more EEGs being carried out per 100
EEG referrals than when SD-EEG is preferred. Put another
way, use of SD-EEG as preferred protocol could reduce the
number of EEGs required in young people with new-onset
epilepsy by 45%.
DISCUSSION
The role of EEG in the classification of epilepsies is an
important one; by directing resources, the diagnostic yield
and the confidence in a ‘‘negative’’ result are enhanced, and
the treatment and prognostication of seizure disorders is
thereby improved. This comparison of the yield of each
protocol allows us to ascertain the best way to use resources
by reducing the number of repeat EEGs needed for
classification. In particular, we believe that this study could
help clarify the relative sensitivities of SD-EEG, r-EEG and
DI-EEG.
The age of participants recruited to the study was
important, as EEG is recommended in classification of
epilepsy only in patients with onset before 35 years of age.
1
In this group of young patients, the yield of abnormalities
was as high as expected from other series.
12
This was,
however, less important than the relative yield from each of
the three EEG protocols.
This study suggests that SD-EEG is more likely to elicit
generalised or focal discharges than either of the other two
methods used here. Given the data, lack of generalised spike
and wave on SD-EEG may be enough reassurance that
repeating the EEG will not add more information. DI-EEG
was not as effective as SD-EEG in eliciting either focal or
generalised abnormalities. In fact, pre-dosing with temaze-
pam seems to reduce the incidence of focal discharges,
although this difference did not reach significance. Previous
studies failed to show any difference between drug-induced
sleep and sleep deprivation,
9
but their cohort was already on
treatment for refractory partial epilepsy. Additionally, the
substance used to induce sleep was a barbiturate, which may
have less acute antiepileptic effects than benzodiazepines.
Given its documented hypnotic effects without evidence of
anticonvulsant effects, melatonin (as is used in some
paediatric units to induce sleep for EEG) may be a useful
future comparator.
One explanation for increased yield of epileptiform
abnormalities after sleep deprivation may be a mere result
of repetition of the EEG rather than the inherent usefulness
of SD-EEG. In this study, however, the recordings were
carried out in random order, which would exclude an effect
of order of EEGs and an effect of temporal proximity to the
time of last seizure. The higher incidence of sole abnormal-
ities in the SD-EEG group confirms this as a more sensitive
activation. Although the duration of recording was slightly
longer in SD-EEG (10–60 min) than in the r-EEG (15–
42 min) group, any effect of recording length would be
expected in both SD-EEG and DI-EEG groups; this increase
in duration would not be enough to explain a higher yield of
abnormalities seen only in the SD-EEG group.
The resource implications of the initial use of sleep
deprivation may be considerable: of 100 young patients with
possible new epilepsy, use of r-EEG in the first instance (as is
standard in most units) may be expected to yield 19 patients
showing generalised spike and wave abnormalities. If an
assiduous search for generalised spike and wave is to be
carried out, the remaining 81 would undergo SD-EEG (with
around 21 yielding generalised spike and wave), giving a total
of 181 EEGs performed to fully screen 100 young patients
with possible IGE.
CONCLUSIONS
Outpatient sleep deprivation is an easy and cost-effective way
of enhancing generalised discharges during EEG recording.
There may be some negative aspects of carrying out SD-EEG;
recording times may be slightly longer and there may be a
slightly increased (in this study, non-significant) risk of sleep
deprivation precipitating generalised seizures. Patients
should be made aware of this before giving consent for the
recording. It may be prudent to ensure that anyone with a
history of sleep-deprived seizures undergoes routine EEG as a
first option.
The resource implications of SD-EEG as a preferred
protocol for EEG are considerable and favourable; even
allowing for the increased recording time, and the theoretical
increase in risk of causing generalised seizure activity, there
are benefits to be gained from adopting this protocol.
.....................
J P Leach, L J Stephen, C Salveta, M J Brodie, Epilepsy Unit, Western
Infirmary, Glasgow, UK
Competing interests: None.
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