Epilepsy Research 131 (2017) 37–43

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

Panayiotopoulos Syndrome with a special emphasis of ictal

semiologic features
A. Destina Yalçın a,b , Hülya Ertaşoğlu Toydemir a,c,∗
a
Sişli Etfal Training and Research Hospital, Department of Neurology, Istanbul, Turkey1
b
Umraniye Training and Research Hospital, Department of Neurology, Istanbul, Turkey
c
Bakırköy Dr. Sadi Konuk Training and Research Hospital, Department of Neurology, Istanbul, Turkey

a r t i c l e i n f o a b s t r a c t

Article history: Purpose: The aim was to identify the demographic, electroencephalographic findings, clinical features,
Received 24 August 2016 especially ictal semiological symptoms of patients diagnosed with Panayiotopoulos Syndrome.
Received in revised form Method: The semiologic and EEG findings of 42 patients were reviewed. Statistical analysis was used to
27 December 2016
determine the frequencies of semiologic features and to define the symptom clusters.
Accepted 14 February 2017
Available online 16 February 2017
Results: The most common clinical features were nausea (54.8%), vomiting (50.0%), pallor (50.0%), devi-
ation of head and eyes (45.2%), generalized seizures (35.7%), ictal syncope (33.3%) and stomach ache
(26.2%). Visual manifestations which were observed in 38.9% of the patients were amaurosis, flashes of
Keywords:
Panayiotopoulos Syndrome colourful lights, flashes of brightful lights, visual hallucinations and blurring of vision. Autonomic status
Autonomic seizures epilepticus was observed in 21.4% of the patients. Cluster analysis of 13 most common symptoms showed
Occipital seizures a tendency toward 3 clusters. Pallor constituted a subgroup on its own whereas nausea, vomiting, devia-
tion of head and eyes tended to occur together in the second subgroup and the third subgroup included
semiologic features some of which were atypical for PS.
Conclusions: A broad spectrum of typical and atypical clinical features might be observed in patients with
PS. Some of the semiologic features of PS might have tendency to occur together. Overlapping of typical
autonomic features with some of the atypical features might suggest that PS, RE and ICOE-G were the
constituents of the same neurobiological spectrum. Our detailed data might contribute to the awareness
of a wide range of variabilites in the electroclinical features of PS.
© 2017 Elsevier B.V. All rights reserved.

1. Introduction Panayiotopoulos Syndrome (PS) is one of the benign child-

The recognition of epileptic syndromes with distinct aetiology,
clinical and EEG features, response to treatment and prognosis was
a milestone in epileptology. Related to this development the epilep-
tologists were aware of benign childhood epileptic syndromes with
excellent prognosis such as Rolandic Epilepsy (RE) which has been
well known since 1950s (Gibbs et al., 1954; Gibbs and Gibbs, 1960).
Many childhood epilepsies are idiopathic, age related and benign,
associated with normal neurodevelopmental status and eventual
total remission. Therefore a correct diagnosis is very important
patricularly in terms of avoiding of unneccesary treatment and their
side effects.
∗ Corresponding author.
E-mail address: hulyatoydemir@hotmail.com (H. Ertaşoğlu Toydemir).
1
Address where the work was done.
hood seizure susceptibility syndromes, which has drawn increasing
attention in the last two decades (Covanis and Panayiotopoulos,
2008; Değerliyurt et al., 2014; Dura-Trave et al., 2008; Michael
et al., 2010; Ohtsu et al., 2003; Panayiotopoulos, 1993, 2002;
Panayiotopoulos et al., 2008; Specchio et al., 2010). The syn-
drome usually affects normal children in early and mid-childhood
and is characterized by seizures, often prolonged with predomi-
nantly autonomic symptoms (Caraballo et al., 2007; Covanis, 2006;
Koutroumanidis, 2007; Michael et al., 2010; Panayiotopoulos,
2004). Interictal EEG shows in 80% of patients multifocal spikes
with occipital predominance often shifting from one region to
another in sequential EEG recordings of the same patient (Covanis
and Panayiotopoulos, 2008; Michael et al., 2010; Oguni et al.,
2001). Prognosis is excellent with one or few seizures during the
active period (Specchio et al., 2010). Continuous treatment with
antiepileptic drugs is not recommended.
This study focused on the demographic, electroencephalo-
graphic findings, clinical features and especially ictal semiological

http://dx.doi.org/10.1016/j.eplepsyres.2017.02.006
0920-1211/© 2017 Elsevier B.V. All rights reserved.
38 A.D. Yalçın, H. Ertaşoğlu Toydemir / Epilepsy Research 131 (2017) 37–43

Table 1 Table 2
Clinical characteristics of patients. Clinical features during the seizures.

Clinical Characteristics Years (Range/Mean) Clinical features Number of patients (%)

Age 15–33/22.6 ± 4.3 12 Nausea 23 (54.8)

Age at onset of epilepsy 1–12/7.3 ± 3.3 05 Vomiting 21 (50.0)
Number of patients (%) 07 Pallor 21 (50.0)
Sex (female/male) 22 (52.4)/20 (47.6) 10 Deviation of head and eyes 19 (45.2)
14 Generalized seizures 15 (35.7)
Number of seizures
03 Ictal syncope 14 (33.3)
1–3 21 (50.0)
11 Stomach ache 11 (26.2)
4–10 14 (33.3)
01 Amaurosis 8 (19.0)
>10 7 (16.7)
17 Flashes of colourful lights 7(16.7)
Autonomic status epilepticus 9 (21.4)
19 Staring 6(14.3)
13 Vertigo 6(14.3)
09 Headache 5 (11.9)
symptoms of patients diagnosed with Panayiotopoulos Syndrome 23 Diaphoresis 5 (11.9)
who were followed up prospectively by the epilepsy outpatient 02 Urinary/fecal incontinance 4(9.5)
28 Hemiconvulsion 3(7.1)
department of our hospital.
06 (Unilateral) hemifacial twitching 2 (4.8)
08 Mydriasis 2 (4.8)
2. Material and methods 16 Jaw locking 2 (4.8)
18 Flashes of brightful lights 2 (4.8)
25 Hypersalivation 2 (4.8)
An analysis of patients with PS between 1994 and 2014 was 27 Imbalance 2 (4.8)
performed. Demographic, semiologic and electroencephalographic 31 Pain in extremities 2 (4.8)
features of seizures were recorded. Information about the semio- 32 Diarrhea 2 (4.8)
logic features of the seizures were obtained from the patients and 33 Visual hallucinations 2 (4.8)
34 Breathlessness 2 (4.8)
parents who witnessed the seizures. 35 Palpitation 2 (4.8)
Besides detailed personal and family histories, all patients 04 Drowsiness 1 (2.4)
had neurological examinations, brain magnetic resonance imaging 15 Feeling of distress 1 (2.4)
(MRI) investigations and an electroencephalography (EEG). 20 Feeling of fear 1 (2.4)
21 Blurring of vision 1 (2.4)
PS has been described as ‘a benign age-related focal seizure dis-
22 Wandering around 1 (2.4)
order which is characterized by seizures, often prolonged, with 24 Contraction 1 (2.4)
predominantly autonomic symptoms, and by an EEG that shows 26 Inability to speak (speech arrest) 1 (2.4)
shifting and/or multiple foci, often with occipital predominance’ in 29 Nose bleeding 1 (2.4)
a consensus report (Ferrie et al., 2006). Patients who met the elec- 30 Cyanosis of lips 1 (2.4)
36 Dysarthria 1 (2.4)
troclinical criteria for PS according to this consensus view and who 37 Cardiac arrest 1 (2.4)
attended the regular follow-up in our epilepsy outpatient depart-
ment of Şişli Etfal Training and Research Hospital were included.
Inclusion criteria was determined as follows: subgroups: 1- following awakening, 2- during daytime (awake), 3-
both during nocturnal sleep and daytime and 4- during nocturnal
1 autonomic seizures whether associated with loss of conscious- sleep.
ness and secondary generalized convulsion or not, Statistical analysis was performed by SPSS 17.0 version. The
2 spike-wave complexes or sharp waves located in the posterior analysis included the parts listed below:
part of the hemispheres,
3 normal background activity, 1 The semiologic features of patients were listed using the data
4 normal neurological examination and mental development, derived from descriptive statistical analysis.
5 normal neuroimaging. 2 The frequences of semiologic features observed during the
seizure were noted.
Forty patients who fullfiled these inclusion criteria were the 3 Clusters of symptoms were analyzed using cluster analysis.
subject of the study. In addition, two other patients suffering from Cluster analysis was used to evaluate the symptoms appearing
a few seizures beginning with visual symptoms followed by sec- together more frequently and to find out whether there exists
ondary generalization and occuring during sleep were included in any subgroups in terms of semiologic findings in the series. This
the study because they fullfiled all criteria except first and had method was used previously in studies focusing on the semio-
excellent prognosis. Three patients who had moved to another city logic features of frontal and temporal lobe seizures (Barba et al.,
and could not attend to follow-up were not included in the study. 2007; Bonini et al., 2014; Kotagal et al., 1995; Toydemir et al.,
Informed consent was obtained from the parents of the children. 2015). However this method has not been used in the stud-
Patients with genetic or metabolic-structural epilepsy, abnor- ies including the patients with PS. As we aimed to emphasize
malities in neurological examination or abnormal background the semiologic features of patients with PS and obtained a list
activity on EEG were excluded from the study. Also patients with of 37 semiologic features, we performed a cluster analysis of
coincidental lesion on MRI, who were the subject of another study the semiologic features to find out which features tended to
of the authors, were not included in this study (Yalçın et al., 2009). appear together more frequently in our patients. Single link-
Age at seizure onset, detailed ictal semiologic features, existence age, complete linkage and average linkage methods were used
of autonomic status epilepticus, EEG and neuroimaging findings, to determine whether there existed any clusters or subclusters
circadian distribution and the number of seizures were evaluated. among the semiologic features and similar results were found
Visual manifestations, both positive and negative, were noted with all methods. Hence, the average linkage was used for clus-
peculiarly. ter analysis. Thirteen of the most frequent symptoms (detected
Ictal semiologic features of 42 patients diagnosed with PS were in at least 5 of the patients) were selected in order to maintain a
listed as 37 features. Timing of the seizures were grouped in four manageable number of symptoms for the analysis.
 A.D. Yalçın, H. Ertaşoğlu Toydemir / Epilepsy Research 131 (2017) 37–43
Fig. 1. The interictal EEG on awakening shows spike-wave complexes located in the posterior part of the right hemisphere.
Interpretation of cluster analysis
Connectivity based clustering (hierarchical clustering) shows
symptoms being more related to nearby symptoms than to the
symptoms farther away. The algorithms connect symptoms to form
clusters. A cluster can be described by the maximum distance
needed to connect parts of the cluster. Different clusters will form
at different distances and this can be represented by a dendrogram.
These dendrograms provide a hierarchy of clusters that merge with
each other at certain distances. In the dendrogram, the y-axis marks
the distance at which the clusters merge, while symptoms are
placed along x-axis. The y-axis represents the distance or dissimi-
larity between the clusters. The longer the horizontal line (on the
y-axis), the greater the difference.
3. Results
3.1. Clinical characteristics of patients
After an average 7.76-year-follow up period (min-max: 4–15
years), 42 patients diagnosed with PS were included in the study.
The clinical characteristics of patients are given in Table 1.
Neurological examination of all of the patients were normal.
Two patients had difficult labour in their past medical history. Our
patients did not have any comorbid diseases or genetic syndromes.
The school performance of all patients were above average.
None of our patients had a history of febrile convulsion (FC).
Seven percent of the patients had a family history of FC, 17% had
a family history of afebrile convulsion or epilepsy and one patient
had a family history of both FC and epilepsy.
We defined 37 types of clinical features some of which were
atypical for this syndrome. Clinical features are listed in Table 2.
The most common clinical features were nausea (54.8%), vomiting
39
(50.0%), pallor (50.0%), deviation of head and eyes (45.2%), gen-
eralized seizures (35.7%), ictal syncope (33.3%) and stomach ache
(26.2%).
Visual manifestations which were observed in 16 patients
(38.9%) were amaurosis, flashes of colourful lights, flashes of bright-
ful lights, visual hallucinations and blurring of vision. The most
common negative manifestation was amaurosis (19.0%) whereas
the most common positive manifestation was flashes of colourful
lights (16.7%). In the majority of the patients the visual symptoms
occured at the beginning of the seizures and were followed by
autonomic symptoms except two.
Autonomic seizures were seen in 83% of the patients. Autonomic
status epilepticus (ASE) was observed in 21.4% of the patients.
ASE had been observed as nausea, vomiting, pallor, stomach ache
and ictal syncope followed by loss of consciosness. Visual symp-
toms during autonomic status epilepticus were reported in 3 out
of 9 patients. All of them had experienced flashes of brightful or
colourful lights and amaurosis had been reported by two of them
following the positive visual manifestations.
Cardiac arrest occurred in one patient. He had 3 seizures totally.
First seizure occured after awaking when he was 12 years old. It
began with pallor, followed by deviation of head and eyes, urinary
incontinance and he was unresponsive for 30 min. He had his sec-
ond seizure 3 h after the first seizure in the hospital. Cardiac arrest
occurred after this generalized tonic clonic seizure. Third seizure
was seen a few months after the second again after awaking like
the first one. He complained about headache and stated visual hal-
lucination as ‘a woman who was spitting’, flashes of colourful lights
and amarosis. After the seizure, he continued sleeping. He had only
three seizures and he has been seizure free for 8 years. He has
still been receiving antiepileptic medication in low doses upon the
insistence of his parents.
40 A.D. Yalçın, H. Ertaşoğlu Toydemir / Epilepsy Research 131 (2017) 37–43
Fig. 2. EEG in the first stage of sleep shows spikes in the left frontotemporal region.
The timing of the seizures was following awakening (66.7%),
during daytime (awake) (14.3%), both during nocturnal sleep and
daytime (11.9%) and during nocturnal sleep (7.1%).
Eleven patients (26.2%) received antiepileptic drugs. The
antiepileptic drugs used in our series were oxcarbazepine (14.3%),
carbamazepine (9.5%) and valproate (2.4%).
3.2. Electrophysiological evaluation of the patients
The interictal scalp EEG of all patients showed spike-wave com-
plexes or sharp waves of high amplitude on the posterior part of
the hemisphere (Fig. 1). In all patients the background activity was
normal. These epileptiform discharges were recorded from right,
left or bilateral posterior part of the hemispher independently and
sometimes they occurred on different sides of the same patient.
Sleep EEG was performed in half of the patients. Spikes occuring on
extraoccipital regions were detected in 17 patients (40%), mainly in
sleep EEGs. They were located in centrotemporal, frontotemporal
and frontal regions (Fig. 2). Brief generalized discharges, compris-
ing slow waves intermixed with small spikes, were seen in three
patients again during sleep (Fig. 3).
3.3. Cluster analysis of semiologic features
The results of cluster analysis regarding 37 symptoms are shown
in Fig. 4. Cluster analysis of 13 most common symptoms showed a
tendency toward 3 clusters.
Cluster 1: pallor
Cluster 2: nausea, vomiting, deviation of head and eyes
Cluster 3: generalized seizures, ictal syncope, stomach ache,
amaurosis, flashes of colourful lights, staring, vertigo, headache,
hypersalivation
According to ANOVA, the level of significance was p < 0.01 for
ictal syncope (p = 0.007), deviation of head and eyes (p = 0.002),
hypersalivation (p = 0.005) and p < 0.05 for pallor (p = 0.012), nausea
(p = 0.015) and vertigo (p = 0.022).
4. Discussion
An average 7.76-year-follow up period (min-max: 4–15 years)
revealed that patients diagnosed with PS may present with a wide
range of semiologic features along with the typical autonomic
and behavioral features. The most common clinical features were
nausea, vomiting, pallor, deviation of head and eyes, generalized
seizures, ictal syncope and stomach ache. Cluster analysis, which
had not been used in previous studies regarding PS, showed a
tendency towards 3 subgroups of semiologic features. Pallor con-
stituted a subgroup on its own whereas nausea, vomiting, deviation
of head and eyes tended to occur together in the second subgroup
and the third subgroup included semiologic features some of which
were atypical for PS (generalized seizures, ictal syncope, stom-
ach ache, amaurosis, flashes of colourful lights, staring, vertigo,
headache and hypersalivation).
Most of the semiologic features of our patients were consistent
with the typical clinical features of PS. Pallor, nausea, vomiting were
the most common autonomic features whereas deviation of head
and eyes was the most common nonautonomic feature as in line
with the literature (Değerliyurt et al., 2014). However, atypical fea-
tures such as vertigo, imbalance, jaw locking, pain in extremities,
feeling of distress and dysarthria were also observed. Moreover,
 A.D. Yalçın, H. Ertaşoğlu Toydemir / Epilepsy Research 131 (2017) 37–43 41

Fig. 3. EEG in the first stage of sleep shows generalized spike-wave discharges.

Fig. 4. Cluster analysis of semiologic features.

visual manifestations, positive or negative, were variable including
visual hallucinations which implicated idiopathic childhood occipi-
tal epilepsy of Gastaut (ICOE-G). Rolandic symptoms such as speech
arrest and hypersalivation accompanied the typical and some of
the atypical features in our series. Both visual and rolandic symp-
toms which were the hallmarks of ICOE-G and RE overlapped with
the autonomic symptoms suggesting that these syndromes were
the constituents of the same neurobiological spectrum (Değerliyurt
et al., 2014; Koutroumanidis, 2007; Panayiotopoulos et al., 2008;
Taylor et al., 2008). Flashes of colourful lights, hypersalivation and
generalized seizures attracted attention among atypical symptoms
as they constituted a subgroup (Cluster 3) along with some typical
42 A.D. Yalçın, H. Ertaşoğlu Toydemir / Epilepsy Research 131 (2017) 37–43
symptoms. Atypical symptoms almost always accompanied auto-
nomic symptoms and occurred during sleep or after awakening.
Cluster analysis showed how typical and atypical symptoms tended
to appear together.
Visual manifestations which were observed in 38.9% of the
patients were amaurosis, flashes of colourful lights, flashes of
brightful lights, visual hallucinations and blurring of vision. The
frequency of visual symptoms was markedly higher than that of
previously reported. Two previous studies reported that visual
symptoms were observed in approximately 5% of their series.
Amaurosis was the most common negative manifestation (19.0%)
whereas the most common positive manifestation was flashes of
colourful lights (16.7%). These findings might suggest that visual
symptoms might be more common than expected and detailed
questioning of patients about visual manifestations might elicit the
frequency of visual symptoms.
Cluster analysis showed that ictal syncope might also be asso-
ciated with nonautonomic signs such as amaurosis, flashes of
colourful lights, staring, vertigo, headache during a seizure. Ictal
syncope might be considered as an epileptic ictal phenomenon if
accompanied by other autonomic features (Caraballo et al., 2007;
Oguni et al., 2001; Specchio et al., 2010). However the findings of
cluster analysis in our series suggest that ictal syncope might be an
epileptic event even if it is associated with nonautonomic features.
Most of our patients experienced their seizures during awaken-
ing (66.7%). Only 7.1% of the patients had seizures when they were
asleep. Caraballo et al. stated that nearly all patients had seizures
during sleep. Specchio et al. reported that seizures occurred dur-
ing sleep in 69.9% of the patients and during awakening in 12.9% of
them. In a previous report, it was proposed that 84% of the seizures
occurred soon after the child went to sleep or in the early hours
of the morning (Lada et al., 2003). Seizures in patients with PS are
sleep-related in general. According to the findings of our study and
most of the previous studies, it might be claimed that seizures were
precipitated with sleep and that seizures occurred mostly in the
early hours of sleep or soon after awakening.
None of our patients had the history of febrile convulsions in
their medical history. Seven percent of the patients had a family
history of FC. The rates of FC in patients and their families were not
as high as the rates reported in previous publications (Caraballo
et al., 2007; Cordelli et al., 2012; Değerliyurt et al., 2014; Dura-
Trave et al., 2008; Lada et al., 2003; Michael et al., 2010; Ohtsu
et al., 2003; Specchio et al., 2010).
One of our patients had ictal cardiorespiratory arrest which was
an extremely rare ictal finding, with only five cases being reported
previously (Dirani et al., 2015; Ferrie and Panayiotopoulos, 2002;
Grosso et al., 2007; Mujawar et al., 2011; Verrotti et al., 2005). As in
concordance with the previous cases, our patient experienced auto-
nomic status epilepticus (first seizure). However, cardiac arrest did
not occur following autonomic status epilepticus. It occurred fol-
lowing a generalized tonic clonic seizure (second seizure). Besides
autonomic status epilepticus, he had visual halucinations as ‘a
woman who was spitting’, amaurosis and flashes of colourful lights
(third seizure). He had only three seizures and has still been on
antiepileptic medication. This might suggest that patients who had
an episode of autonomic status epilepticus might be under risk of
developing such a potentially fatal seizure. Antiepileptic drug treat-
ment should be initiated or continued in order to minimize the risk
of experiencing such life-threatening events.
Autonomic status epilepticus was observed in 21.4% of our
patients (n = 9 patients) whereas it had been reported in one third
or half of the patients in most of the previous studies (Değerliyurt
et al., 2014; Koutroumanidis, 2007; Lada et al., 2003; Specchio et al.,
2010). Specchio et al. concluded that more than half of the seizures
were longer than 30 min and this did not affect remission or number
of seizures. The frequency of ASE in our series was lower than that
of previous series but 8 out of 9 patients had 1–3 seizures totally,
as in line with the report of Specchio et al.
Electroencephalography is the only diagnostic test to be abnor-
mal in PS. In about 90% of cases, the EEG shows multifocal, high
amplitude sharp and slow wave complexes. Posterior location pre-
dominates in most published reports but epileptiform activity may
occur in any area, frequently in the centrotemporal and frontal
regions (Yalçın and Demirtaş-Tatlıdede, 2012). The interictal EEG of
our patients revealed spike-wave complexes or sharp waves of high
amplitude located in the posterior part of the hemispheres. In the
majority of the patients the epileptiform discharges shifted from
one side to the other in different EEGs of the same patient. Extraoc-
cipital spikes were detected in 17 patients, mainly in sleep EEGs and
they were located in centrotemporal, frontotemporal and frontal
regions. Brief generalized discharges were seen in three patients
during sleep. The EEG findings of our patients were in concordance
with previous studies (Covanis and Panayiotopoulos, 2008; Michael
et al., 2010; Oguni et al., 2001). Sequence of the semiologic features
was variable and had no relationship with the localization of the
spikes.
Despite these atypical features, all patients had favorable out-
come and nearly half of our patients had 1–3 seizures during the
active period. Our patients except 4 of them had no seizure recur-
rence under treatment.
5. Conclusions
Panayiotopoulos Syndrome is a benign and common syndrome
with a broad spectrum of typical and atypical clinical features. Over-
lapping of typical autonomic features with some of the atypical
features which were the hallmarks of RE and ICOE-G might suggest
that PS, RE and ICOE-G were the constituents of the same neurobio-
logical spectrum. Some of the semiologic features of PS might have
tendency to occur together. Ictal features might frequently vary and
might not follow the same sequence in every seizure of the same
patient. We conclude that our detailed data might contribute to the
awareness of a wide range of variabilites in the clinical ictal features
of PS.
Disclosure
None of the authors has any conflict of interest to disclose.
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