The main aim of this retrospective study was
to investigate the incidence and lateralizing
value of peri-ictal yawning in patients with
temporal lobe epilepsy (TLE) who underwent
successful surgery for epilepsy (Engel class I
outcome at the 2-year follow-up visit). We
reviewed a total of 97 patients (59 men and 38
women). Fifty-three patients had TLE arising
from the nondominant temporal lobe, and 44 had
TLE arising from the dominant temporal lobe. In
total, we reviewed 380 seizures. Of those, 202
seizures arose from the nondominant temporal
lobe and 178 from the dominant one. Peri-ictal
yawning was observed in 4 of 97 patients (4.1%)
and in 7 of 380 seizures (1.8%), in the
postictal period in all cases. Peri-ictal
yawning occurred only in patients with
right-sided, nondominant TLE. It may have a
lateralizing value.
1. Introduction
Yawning is a phylogenetically old,
stereotyped phenomenon that occurs in humans and
many animals. It is characterized by a standard
cascade of movements including wide opening of
the mouth and retraction of the tongue. This
movement pattern is often repetitive. Yawning is
associated with generalized stretching of the
muscles of the respiratory tract (diaphragm,
intercostal), face, and neck [1,21.
Pathological or excessive yawning has been
described in various medical conditions [31.
The occurrence of yawning associated with
epilepsy or epileptic seizures has been
repeatedly described, mostly in case reports.
Yawning has been noted in individuals with both
generalized and focal epilepsies [4-81.
However, there has not been a systematic review
of yawning as a part of peri-ictal semiology in
focal epilepsies.
The main aim of this retrospective study was
to investigate the incidence and lateralizing
value of peri-ictal yawning (PY) in a selected
population of patients with temporal lobe
epilepsy (TLE) who had undergone successful
surgery for epilepsy.
2. Methods
We reviewed 97 patients (59 men and 38
women) with intractable TLE, ranging from 14 to
58 years of age (mean ±SD=36.6±9.2),
with an average duration of epilepsy of 17.2
± 10.9 years. All patients underwent a
successful epilepsy surgery procedure and were
classified as Engel class I at the 2-year
follow-up visit. Histopathological examination
revealed hippocampal sclerosis (HS) in 60
patients and other lesions in 34 patients; 4
patients had no lesions. Histopathological
investigations revealed benign brain tumors in
12 patients, dysembryonic neuroepithelial tumors
in 8, vascular malformations in 7, both focal
cortical dysplasia and gliosis in 2, and
posttraumatic changes in 1 patient.
Fifty-three patients had TLE arising from
the nondominant temporal lobe and 44 had TLE
arising from the dominant temporal lobe. We
reviewed 380 seizures (234 seizures in patients
with HS and 146 seizures in patients with other
lesions). Of those, 202 seizures arose from the
nondominant temporal lobe and 178 from the
dominant lobe.
Ictal semiology was assessed from the first
clear-cut clinical ictal symptom to 3 minutes
after the seizure ended. The end of a seizure
was evaluated on an individual basis due to
clinical semiology and electroencephalographic
seizure offset.
All of the patients underwent the
standardized presurgical investigation,
including magnetic resonance imaging (MRI),
interictal and! or ictal HMPAO single-photon
emission tomography, fluorodeoxyglucose positron
emission tomography (FDG-PET),
neuropsychological assessment, and evaluation of
interictal and ictal scalp recordings. Of the 97
patients, 28 patients (78 of 380 seizures) were
recorded with invasive EEGs using either depth
or subdural electrodes. A Wada test was
performed individually to assess memory
lateralization.
3. Results
Postictal yawning was observed in 4 of 97
patients (4.1%) and 7 of 380 seizures (1.8%). In
the 4 patients in whom PY was observed, a total
of 11 seizures were recorded, of which 7
featured yawning (64%). All of these patients
had been evaluated with noninvasive video/EEG
(scalp and sphenoidal) monitoring; none of them
underwent invasive monitoring. In all of the
seizures, the yawning was postictal; the yawning
was repetitive (at least two times) in all but
one seizure.
In two seizures, PY occurred in the first
minute after the end of the seizure; in three
seizures, between the first and second minutes;
and in two seizures, between the second and
third minutes.
Postictal yawning was not forceful in any
seizure. Postictal testing showed that three
patients (five seizures) were not aware of the
yawning. The last patient was not asked.
3.1. Cases with PY
Case 1 was a 19-year-old right-handed woman
who underwent surgery for epilepsy in 1999. An
anteromedial temporal lobe resection on the
right side was performed; histopathological
investigation revealed HS. The ictal semiology
of her habitual seizures comprised epigastric
aura followed by complex partial seizure with
limb automatisms, oroalimentary automatisms,
left-sided hemidystonia, and postictal nose
wiping with the right upper limb. PY was noted
in two of two recorded seizures.
Case 2 was a 17-year-old right-handed man
with suspected low-grade glioma in the right
temporal lobe. He underwent a tailored
lesionectomy in 2006; histopathological
investigation revealed ganglioglioma (see Fig.
2). His seizures started with a nonspecified
aura (strange feeling"), followed by complex
partial seizure with automatisms, ictal speech,
right-sided goose bumps, and occasionally
secondary generalization. We observed postictal
yawning in one of four seizures.
Case 3 was a 45-year-old right-handed woman
with a cavernoma in the right temporal lobe who
underwent surgery for epilepsy in 1999;
histopathological investigation proved, in
correlation with MRI findings, a cavernous
angioma. The seizure semiology comprised psychic
aura (anxiety), oroalimentary and repetitive
limb automatisms, and vocalization. We noticed
PY in one of two seizures.
Case 4 was a 27-year-old right-handed man
who underwent surgery for epilepsy caused by a
dysembryonic neuroepithelial tumor in the
temporal pole on the right side in 1999;
histopathological investigation findings
correlated with MRI. The seizure semiology
included motionless staring without previous
aura, nontonic head turning to the right, and
slight oroalimentary automatisms. PY occurred in
all three seizures recorded in this
patient.
All four patients underwent the Wada test,
confirming left-sided speech dominance.
4. Discussion
To our knowledge, this is the first study to
systematically analyze the frequency of PY in
patients with TLE. We chose a pure series of
patients with TLE who underwent successful
epilepsy surgery and were classified as Engel
class I at the 2-year follow-up visit. We
observed PY in 4 patients (4.1%), in 11 seizures
(1.8%). In all cases, the yawning was postictal.
All patients with PY had right-sided,
nondominant TLE, which was confirmed with the
Wada test.
Although not systematically studied with any
particular type of epilepsy, yawning associated
with epileptic seizures has been previously
described in case reports of both focal and
generalized epilepsies. Penfield and jasper
[4J mentioned peri-ictal yawning in two
patients. The first had TLE caused by a tumor in
the left temporal lobe, and the second had focal
seizures with autonomic and sensory symptoms
associated with yawning. No other information
was provided. Goldie and Green [5J described
young patients who probably had idiopathic
generalized epilepsy, and in whom yawning was
associated with generalized 3-Hz spike-wave
episodes. Donat and Wright [6]
identified 11 children with atypical variants of
infantile spasms. In one of these patients, who
had an unspecified brain malformation, they
noted atypical spasms associated with yawning.
Muchnik et al. [7J described two patients
with TLE in whom the yawning occurred in
association with epileptic seizures. The first
patient was a 95-year-old man for whom yawning
was followed by a complex partial seizure during
a state of drowsiness. An EEG of this patient
revealed bilateral independent temporal sharp
waves. A CT scan of the patient showed diffuse
cortical atrophy; no lesion was seen within the
temporal lobe. The second patient was a
17-year-old woman with complex partial seizures
and secondary generalized seizures followed by
yawning in the postictal period. The interictal
EEG of this patient also showed bitemporal
epileptic findings. Brain MRI was negative, but
the patient had had insulin-dependent diabetes
mellitus since the age of 14. The authors
stressed that her seizures did not occur in any
temporal relationship with hypoglycemia. Most
recently, Yankovsky et al. [8] reported
a 48-year-old woman with multiple seizure types,
including simple sensorimotor partial seizures
of the left upper limb, complex partial seizures
with dystonic posturing of the left upper limb,
non-forceful deviation of the head to the left
side associated with unresponsiveness, sudden
falls, and secondarily generalized tonic-clonic
seizures. In the postictal period of several
simple and complex partial seizures, the patient
had repetitive and forceful yawning. Interictal
EEG revealed interictal epileptic activity over
the wide centro-parieto-temporal regions on the
right side (speech/nondominant side). The MRI
results were normal, and two previous epilepsy
surgery procedures did not lead to
improvement.
Yawning is a common behavioral act in a wide
variety of vertebrate species, but its functions
are not well understood. Despite the widely held
beliefs that it serves as a signal of boredom,
that it results from a lack of oxygen, and that
it is a socially contagious act, we lack a
comprehensive, satisfactory explanation of its
mechanisms [9J. Yawning is usually
associated with transitions between wakefulness
and sleep or with satiety. This complex motor
behavior requires the coordination of the motor
nuclei of the brainstem (V, VII, IX, X, XI, XII
cranial nerves) and of the spinal cord. Yawning
is controlled by the hypothalamic
paraventricular nucleus (PVN). This hypothalamic
structure is the site of coordination between
the central and peripheral autonomic systems.
The PVN plays an important role in other
functions, such as metabolic balance, blood
pressure, heart rate, and erection [3J.
Electrical lesioning of parvocellular neurons in
the PVN inhibits yawning [3J. A group of
oxytocin neurons situated in the PVN zone
project to the hippocampus, the brainstem, and
the spinal cord. Stimulation of these neurons
with dopamine or its agonists histamine and
oxytocin triggers yawning, whereas GABA and
opioids have an inhibitory effect [10,111.
Focal epileptic seizures are often associated
with heart rate changes, which are probably
triggered by the influence of the hypothalamus
during epileptic seizures [12,131. Although
largely hypothetical, hypothalamic impairment is
the most probable explanation for yawning in the
peri-ictal period.
Direct activation of the brainstem
structures involved in yawning may be another
explanation of PY. Yet another possible
explanation is impairment of the brainstem
structures involved in alertness. In this case,
yawning should be associated with the change in
alertness or drowsiness. None of our patients
associated their yawning with changed alertness,
although this association was described by both
patients in one case report [71.
Postictal yawning may be one of the rare
vegetative ictal signs in patients with TLE that
lateralizes the ictal onset to the temporal lobe
of the speech/nondominant hemisphere. Although
there are some controversies in the literature,
other vegetative signs that have some
lateralizing value in TLE are peri-ictal water
drinking [14], vomiting [15,16],
spitting [17,18], and peri-ictal urinary
urge [191.
Our study is the first to systematically
analyze postictal yawning in patients with
temporal lobe epilepsy. Further studies are
needed to confirm the possible lateralizing
value of postictal yawning.
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