Epilepsy Research (2015) 109, 197—202

journal homepage: www.elsevier.com/locate/epilepsyres

Seizure semiology identifies patients with

bilateral temporal lobe epilepsy
Anna Mira Loesch, Berend Feddersen, F. Irsel Tezer 1,
Elisabeth Hartl, Jan Rémi, Christian Vollmar, Soheyl Noachtar ∗

Epilepsy Center, Dept. of Neurology, University of Munich, Marchioninistr. 15, 81377 Munich, Germany

Received 21 May 2014; received in revised form 14 October 2014; accepted 11 November 2014
Available online 22 November 2014

KEYWORDS Summary
Temporal lobe Objective: Laterality in temporal lobe epilepsy is usually defined by EEG and imaging results. We
epilepsy; investigated whether the analysis of seizure semiology including lateralizing seizure phenomena
Bitemporal; identifies bilateral independent temporal lobe seizure onset.
Semiology; Methods: We investigated the seizure semiology in 17 patients in whom invasive EEG-video-
Lateralizing seizure monitoring documented bilateral temporal seizure onset. The results were compared to 20 left
phenomena; and 20 right consecutive temporal lobe epilepsy (TLE) patients who were seizure free after
Epilepsy surgery anterior temporal lobe resection. The seizure semiology was analyzed using the semiological
seizure classification with particular emphasis on the sequence of seizure phenomena over time
and lateralizing seizure phenomena. Statistical analysis included chi-square test or Fisher’s
exact test.
Results: Bitemporal lobe epilepsy patients had more frequently different seizure semiology
(100% vs. 40%; p < 0.001) and significantly more often lateralizing seizure phenomena pointing
to bilateral seizure onset compared to patients with unilateral TLE (67% vs. 11%; p < 0.001). The
sensitivity of identical vs. different seizure semiology for the identification of bilateral TLE was
high (100%) with a specificity of 60%. Lateralizing seizure phenomena had a low sensitivity (59%)
but a high specificity (89%). The combination of lateralizing seizure phenomena and different
seizure semiology showed a high specificity (94%) but a low sensitivity (59%).
Significance: The analysis of seizure semiology including lateralizing seizure phenomena adds
important clinical information to identify patients with bilateral TLE.
© 2014 Elsevier B.V. All rights reserved.

∗ Corresponding author. Tel.: +49 89 7095 3691; fax: +49 89 7095 6691.
E-mail addresses: annamira.loesch@med.uni-muenchen.de (A.M. Loesch), berend.feddersen@med.uni-muenchen.de (B. Feddersen),
irseltezer@yahoo.com.tr (F. Irsel Tezer), elisabeth.hartl@med.uni-muenchen.de (E. Hartl), jan.remi@med.uni-muenchen.de (J. Rémi),
christian.vollmar@med.uni-muenchen.de (C. Vollmar), soheyl.noachtar@med.uni-muenchen.de, noa@med.uni-muenchen.de (S. Noachtar).
1 Current address: Institute of Neurological Sciences and Psychiatry, Hacettepe University, School of Medicine, Ankara, Turkey.

http://dx.doi.org/10.1016/j.eplepsyres.2014.11.002
0920-1211/© 2014 Elsevier B.V. All rights reserved.
198
Introduction
Anterior temporal lobectomy is an established treatment
option for patients with medically refractory temporal lobe
epilepsy (TLE) and superior to medical treatment alone
(Wiebe et al., 2001). The prerequisite of resective tempo-
ral lobe epilepsy surgery is the exact lateralization of the
epileptogenic zone since patients with bilateral TLE will not
benefit from anterior temporal lobectomy (Noachtar and
Rémi, 2009).
The evaluation of TLE patients considered for anterior
lobectomy includes EEG-video monitoring, neuroimaging
and neuropsychological tests (Noachtar and Borggraefe,
2009). The decision on unilateral versus bilateral temporal
lobe seizure onset is usually based on results of EEG and
imaging. However, invasive EEG investigation with subdu-
ral or depth electrodes may still identify unilateral seizure
onset in selected TLE patients, in whom non-invasive evalu-
ation showed bilateral interictal and ictal results (So et al.,
1989). The improvement of MRI technology and the introduc-
tion of PET and ictal SPECT reduced the number of invasive
evaluations since bilateral abnormalities will likely exclude
the patients from further invasive evaluations and the asso-
ciated risks.
The initial seizure symptoms provide information on the
localization and lateralization of the seizure-onset zone
(Ebner et al., 1995; Henkel et al., 2002; Noachtar, 2001;
O’Dwyer et al., 2007; Wyllie et al., 1986). We investigated
whether the analysis of seizure semiology identifies patients
with independent bilateral temporal lobe seizure onset who
will not be candidates for resective epilepsy surgery.
Material and methods
We reviewed our EMU data base and included those 17
consecutive epilepsy patients who demonstrated bilateral
independent seizure onset in invasive evaluations (Table 1).
The first consecutive 40 patients of our database with left
or right TLE, who were seizure free after anterior temporal
lobe resection served as a control group. All patients had
medically refractory TLE and underwent a standardized non-
invasive presurgical evaluation (Noachtar and Borggraefe,
2009).
The lateralization of a given seizure was based on
the ictal invasive EEG seizure pattern. Continuous EEG-
video monitoring was first recorded with non-invasive and
sphenoidal electrodes (Vangard, Cleveland/Ohio; XLTEK,
London, Ontario/Canada). The additional invasive evalua-
tions included subdural or stereotactically implanted depth
electrodes in all 17 patients with bilateral temporal lobe
seizure onset.
The seizures videos were evaluated independently by two
experienced epileptologists (BF and IT) who were blinded to
the patient data. The seizure semiology was analyzed based
on the semiological seizure classification (Lüders et al.,
1998). Different seizure evolutions meant that the semio-
logy was different between seizures which arose from left
and right temporal lobes in a given patient. Patients who
only had auras were not included in this study since auras do
not show any objective and observable signs or symptoms.
A.M. Loesch et al.
An example of patient 4 illustrates the approach to define
identical or different seizure semiology:
(1) dialeptic seizure → left versive seizure → generalized
tonic clonic seizure,
(2) abdominal aura → complex motor seizure.
These two seizures were classified as different seizure
semiologies.
The sensitivity and specificity of the combination of
identical vs different seizure semiology, unilateral versus
bilateral lateralizing seizure phenomena were calculated for
unilateral and bilateral TLE.
2 analysis or Fisher’s exact test was used to evaluate
the significance of the relationship of seizure semiology and
lateralizing seizure phenomena in patients with bitemporal
and unilateral TLE. Significance was assumed at p < 0.05.
Results
A total of 407 seizures were evaluated in 17 patients with
bilateral TLE, 20 patients with right TLE and 20 patients
with left TLE. Different seizure semiology occurred in all 17
patients (100%) with independent bilateral temporal seizure
onset and in 16 of 40 patients (40%) with unilateral temporal
lobe seizure onset (p < 0.001).
Looking at the 53 patients in whom lateralizing seizure
phenomena were recorded, 10 of 17 patients with bilat-
eral TLE (67%) had lateralizing signs from both hemispheres
compared with four of 36 patients (11%) with unilateral TLE
(p < 0.001).
The specificity in identifying bilateral TLE was excellent
with the combination of different seizure semiology and
bilateral lateralizing seizure phenomena. This combination
was present in 10 of 17 patients with bitemporal seizure
onset and in two of 34 patients with unitemporal seizure
onset. The specificity of identifying bilateral TLE with these
semiological features was high (94%) but the sensitivity was
poor (59%).
In 13 patients of the 17 patients (76%) with invasively
proven bilateral TLE, MRI was either negative (n = 10) or
showed bilateral abnormalities (n = 3). All patients with uni-
lateral TLE showed a unilateral pathology in the MRI. The
sensitivity was 41% (specificity 0%). Seizure semiology in all
these 13 patients was different between left and right tem-
poral EEG seizure onset, whereas 24 of the 40 patients with
unilateral TLE showed an identical seizure semiology (sensi-
tivity and specificity 100%). All 6 patients with no pathology
or a bilateral pathology in the MRI who showed bilateral lat-
eralizing phenomena belonged to the group of the invasively
proven bilateral TLE. Just as all patients with an unilateral
pathology in the MRI combined with an identical semiology
were diagnosed as unilateral TLE (sensitivity and specificity
100%).
Discussion
This study shows that the analysis of seizure semiology
including lateralizing seizure phenomena identifies patients
with bitemporal independent seizure onset. This infor-
mation is important for patients considered for resective
Seizure semiology identifies patients with bilateral temporal lobe epilepsy 199

Table 1 Patient data and results of diagnostic evaluation in patients with invasively documented bilateral temporal seizure
onset.

Pat. Gender Age Age at MRI Interictal Ictal EEG Seizure semiology Lateralizing seizure
(#) (m/f) (yrs.) onset EEG phenomena
(yrs.)
1 f 13 2 nl Rt. Rt. temporal Abdominal Ipsilateral postictal
temporal aura → automotor nose rubbing
sz. → Lt. face clonic sz. Automatisms with
preserved
responsiveness
Contralateral hand
dystonia
Lt. temporal Lt. lateralized Automotor sz. → Rt. Ipsilateral postictal
face clonic sz. nose rubbing
2 m 28 6 Bilateral Rt. posterior Rt. temporal Subclinical Sutomatisms with
Mesial temporal Psychic preserved
temporal aura → automotor sz. responsiveness
sclerosis Lt. temporal Lt. temporal Abdominal Aphasia
aura → aphasic status
3 m 51 17 Rt. temporal Rt. frontal Rt. temporal Dialeptic sz. Lt. clonus
contusion Lt. clonic sz.
Lt. temporal Lt. Abdominal Ipsilateral postictal
Lt. fronto-temporal aura → automotor nose rubbing
lateralized sz. → Rt. arm tonic Rt. dystonia
sz. → generalized tonic
clonic sz.
4 m 40 3 Lt. Rt. Rt. temporal Dialeptic sz. → Lt. Lt. version
mesial temporal versive Lt. dystonia
temporal sz. → generalized tonic Ipsilateral postictal
sclerosis clonic sz. nose rubbing
Coughing
Lt. temporal Lt. temporal Abdominal Sign of 4 (Rt. arm
aura → complex motor extension)
sz.
Bilateral tonic sz.
5 m 43 31 nl Rt. Rt. temporal Acoustic aura → Lt. Lt. version
temporal versive sz. → bilateral Lt. clonus
clonic sz.
Lt. temporal Lt. temporal Rt. versive sz. → Rt. Rt. version
clonic sz. Rt. clonus
Acoustic aura → Rt.
clonic sz.
Acoustic
aura → automotor
sz. → Rt. clonic sz.
Rt. clonic sz.
6 m 17 9 nl Rt. Rt. temporal Aura → complex motor Lt. eye + Lt. face
temporal sz. → Lt. clonic clonus
sz. → generalized tonic Lt. version
clonic sz. Sign of 4 (Lt. arm
extension)
Rt. frontal Complex motor sz. —
Generalized tonic
clonic sz.
Lt. temporal Lt. temporal Complex motor Rt. version
Lt. frontal sz. → Rt. versive Rt. face clonus
sz. → generalized tonic Rt. dystonia
clonic sz. Sign of 4 (Rt. arm
extension)
200 A.M. Loesch et al.

Table 1 (Continued )

Pat. Gender Age Age at MRI Interictal Ictal EEG Seizure semiology Lateralizing seizure
(#) (m/f) (yrs.) onset EEG phenomena
(yrs.)
7 m 48 36 nl Rt. Rt. Complex motor Lt. version
temporal temporo-parietal sz. → Lt. versive
sz. → generalized tonic
clonic sz.
Lt. temporal Lt. temporal Abdominal/psychic Rt. version
Lt. frontal aura → automotor
sz. → Rt. versive
sz. → Rt. face tonic
sz. → generalized tonic
clonic sz.
8 m 23 18 nl Rt. Rt. temporal Lt. version → clonic sz. Lt. version
temporal Lt. face → generalized Sign of 4 (Lt. arm
tonic clonic sz. extension)
Lt.
version → generalized
tonic clonic sz.
Hypermotor sz. → Lt.
version → generalized
tonic clonic sz.
Lt. temporal Lt. temporal Rt. versive sz. → Rt. Rt. version
arm tonic sz. → Rt. Rt. arm clonus
arm clonic
sz. → generalized tonic
clonic sz.
Generalized tonic
clonic sz.
9 m 31 17 nl Rt. Rt. temporal Psychic Lt. automatisms
temporal aura → automotor Lt. version
sz. → Lt.
version → generalized
tonic clonic sz.
Lt. temporal Lt. temporal Psychic —
Lt. frontal aura → dialeptic sz.
10 f 27 26 Lt. Rt. Rt. temporal Acoustic Lt. version
mesial temporal aura → aphasic sz.
temporal Acoustic
sclerosis aura → aphasic
sz. → Lt. versive
sz. → generalized tonic
clonic sz.
Lt. temporal Lt. temporal Abdominal ictal aphasia
aura → aphasic sz.
Acoustic
aura → abdominal aura
Acoustic
aura → aphasic sz.
Subclinical sz.
11 f 52 38 nl Rt. Rt. temporal Subclinical sz. Rt. automatisms
temporal Automotor sz.
Rt. frontal
Lt. temporal Lt. temporal Automotor sz. —
12 m 51 28 bilateral Rt. Rt. temporal Abdominal —
mesial temporal aura → automotor. sz.
temporal Abdominal
sclerosis aura → dialeptic sz.
Seizure semiology identifies patients with bilateral temporal lobe epilepsy 201

Table 1 (Continued )

Pat. Gender Age Age at MRI Interictal Ictal EEG Seizure semiology Lateralizing seizure
(#) (m/f) (yrs.) onset EEG phenomena
(yrs.)

Lt. temporal Lt. temporal Sialeptic Rt. version

sz. → automotor Rt. arm tonic sz.
sz. → Rt. arm tonic Rt. arm clonus
sz. → Rt. arm clonic Rt. hand dystonia
sz. → Rt. versive
sz. → dystonia Rt.
hand → generalized
tonic clonic sz.
13 f 25 6 nl Rt. Rt. temporal Automotor Lt. version
temporal sz. → complex motor
sz. → Lt. versive
sz. → generalized tonic
clonic sz.
Lt. temporal Lt. temporal Automotor —
sz. → complex motor
sz.
14 f 29 9 Rt. mesial Rt. Rt. temporal Dialeptic sign of 4 (Lt. arm
temporal temporal sz. → generalized tonic extension)
sclerosis clonic sz. Ipsilateral postictal
Automotor nose rubbing
sz. → generalized tonic Rt. automatisms
clonic sz.
Lt. temporal Lt. temporal dialeptic Sign of 4 (Rt. arm
sz. → automotor extension)
sz. → generalized tonic Ipsilateral postictal
clonic sz. nose rubbing
Automotor sz. → Rt. Rt. version
versive
sz. → generalized tonic
clonic sz.
15 f 20 13 nl Rt. Rt. temporal Subclinical seizure —
temporal pattern
Lt. temporal Lt. temporal Subclinical status Postictal aphasia
Automotor sz.
16 f 38 25 nl Rt. Rt. temporal Automotor —
temporal sz. → generalized tonic
clonic sz.
Lt. temporal Lt. Generalized tonic —
fronto-temporal clonic sz.
17 f 42 24 nl Rt. Rt. temporal Aura → dialeptic sz. —
temporal Aura → automotor sz.
Lt. temporal Lt. temporal Subclinical seizure —
pattern
Abbrevations: # = number; m = male; f = female; yrs. = years; MRI = magnetic resonance imaging; EEG = electroencephalographie;
nl = normal; Lt. = left; Rt. = right; sz. = seizure

epilepsy surgery since bilateral TLE patients will not benefit
from unilateral temporal lobe resection. Most studies in TLE
support the concept that concordance of electroclinical data
with imaging and neuropsychological tests is predictive for
a good surgical outcome, whereas EEG indicators of bitem-
poral epileptogenicity such as bilateral temporal ictal EEG
seizure patterns and bilateral interictal epileptic discharges
on scalp EEG are associated with poor seizure outcome after
epilepsy surgery (Radhakrishnan et al., 1998; Schulz et al.,
2000). Consistency of EEG and imaging results is considered
important for the selection of patients TLE (Noachtar and
Rémi, 2009; Rémi et al., 2011).
The definition of bilateral TLE is usually based on invasive
evaluations in patients with previously bilateral non-invasive
interictal and ictal EEG abnormalities. However, invasive
studies may reveal unilateral seizure onset in some of these
patients who will eventually benefit from anterior tem-
poral lobectomy (So et al., 1989). Modern imaging with
202
MRI, PET and ictal SPECT and long experience with com-
parisons of invasive and non-invasive studies reduced the
need of invasive studies (Sperling et al., 1992). Based on the
improvement of MRI technology, invasive studies are rarely
performed in patients with unequivocal bilateral mesial
temporal sclerosis in view of the potential risks associ-
ated with invasive electrodes. Fluorodeoxyglucose positron
emission computed tomography (FDG-PET) and ictal single-
photon emission computed tomography (SPECT) may help to
lateralize the epileptogenic zone in MRI negative patients
(LoPinto-Khoury et al., 2012). However, if imaging studies
fail to demonstrate a resectable epileptogenic lesion, inva-
sive recordings are the only means to define the seizure
onset zone.
In the pioneering years of epilepsy surgery, patients
would be selected basically on seizure semiology and EEG
results (Bailey and Gibbs, 1951). The dramatic impact of
imaging on localization issues in epilepsy should not lead
to neglect clinical useful information. This is particular
important in patients, in whom imaging is negative since
semiological data may help to avoid invasive EEG evalua-
tions.
In conclusion, our results show that in addition to imaging
and EEG findings, seizure semiology contributes to the iden-
tification of bilateral TLE. The analysis of seizure semiology
may be particularly helpful in patients with non-lesional TLE
who were considered for invasive evaluations.
Conflict of interest statement
None of the authors has any conflict of interest to disclose.
We confirm that we have read the Journal’s position on
issues involved in ethical publication and affirm that this
report is consistent with those guidelines.
Acknowledgments
We wish to thank E. Sincini, R. Picinotti, E. Scherbaum,
R. Tschackert and O. Klein for technical assistance in the
EEG-video-monitoring unit.
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