Patients with multiple sclerosis (MS) suffer
from the repetitive yawning and sleep problems.
Yawning is observed in MS and other central
nervous system disorders and yawning and
swallowing may be controlled by the network of
the brain stem. Therefore, it is important to
investigate the MS patients with various
clinical and radiological locations in order to
understand the role of brainstem on the yawning
mechanisms. One hour polygraphic recording would
be crucial method for this purpose, because it
is easy to observe spontaneous yawning (SY) and
spontaneous swallowing (SS) together with their
electrophysiologic counterparts. Previous
studies reported that contagious yawn and
swallow are temporally related and frequency of
swallows was increased within 10s of post yawn
period in normal adult subjects.
The authors have re-investigated this
phenomenon by studying the SY and SS in
polygraphic recording in normal subjects and
patients with MS. Then they hypothesized that SY
is expected to be increased in MS patients.
49 patients with MS and 19 control subjects
were recruited in this study. The authors used a
twelve-channel electroencephalography (EEG)
device. Five channels were for electromyography
(EMG) recording. They also used one channel for
laryngeal sensor for vertical movements of the
larynx during swallowing. Cardiac rhythm,
respiration and sympathetic skin responses were
synchronously recorded during swallowing. They
evaluated rate of total SY, swallows inside the
yawning, before and after 10s of the yawning and
yawning unrelated with swallowing.
Patients with MS yawned more frequently than
healthy controls (p = 0,044). It was obvious
that the yawning unrelated with spontaneous
swallow was also significantly increased
compared to normal controls (p = 0,047), whereas
swallowing inside the yawn or before and after
10s of yawning were not significantly different
in both groups. Among 49 MS patients, 16 (32.6%)
had brainstem involvement. Yawning was observed
in only 6 (37.5%) of them.
Yawning is significantly increased in MS
patients compared to normal controls by using
the polygraphic method. There is no direct
relation of the brainstem and the origin of
yawning in MS patients according to clinical
picture and MRI findings. However safe swallows
during yawning could suggest that there is still
need to some brain stem mechanism and/or
oropharyngeal reflexes. Difficulties must be
emphasized to detect anatomic localization in MS
because of relapsing pattern of disease.
Résumé
Les patients atteints de sclérose en
plaques (SEP) souffrent de bâillements
répétitifs et de somnolence. Le
bâillement est observé au cours de
la SEP et d'autres maladies du système
nerveux central sans doute parce que le
bâillement et la déglutition sont
contrôlés par les réseaux
neuronaux du tronc cérébral.
Il est donc intéressant
d'étudier les patients atteints de SEP en
prenant en compte cliniquement et
radiologiquement les différentes
localisations lésionnelles afin de
comprendre plus précisément le
rôle du tronc cérébral dans
les mécanismes du bâillement.
Un enregistrement polygraphique d'une heure
est une méthode intéressante dans
ce but, car il est facile d'observer des
bâillement spontanés (SY) et la
déglutition spontanée (SS) et
leurs équivalents
électrophysiologiques. Des
études antérieures ont
rapporté que le bâillement
contagieux et la déglutition sont
liés temporellement. La fréquence
des déglutitions est augmentée
dans les10s qui suivent un bâillement chez
les sujets adultes normaux.
Les auteurs ont réexaminé ce
phénomène en étudiant le SY
et le SS en enregistrement polygraphique chez
des sujets normaux et chez des patients atteints
de SEP. Ensuite, ils ont émis
l'hypothèse que SY devrait être
augmenté chez les patients atteints de
SEP.
49 patients atteints de SEP et 19 sujets
témoins ont été
recrutés pour cette étude. Les
auteurs ont utilisé un dispositif
d'électroencéphalographie (EEG)
à douze canaux. Cinq canaux
étaient destinés à
l'enregistrement électromyographique
(EMG). Ils ont également utilisé
un canal pour un capteur laryngé
enregistrant les mouvements verticaux du larynx
pendant la déglutition. Le rythme
cardiaque, la respiration et les réponses
cutanées sympathiques ont
été enregistrées de
façon synchrone pendant la
déglutition. Ils ont évalué
le nombre de bâillements spontanés
et les déglutitions en lien avec un
bâillement, avant et après 10s du
bâillement et les bâillements sans
lien avec la déglutition.
Les patients atteints de SEP bâillent
plus fréquemment que les témoins
en bonne santé (p = 0,044). Il est apparu
que les bâillements sans lien avec la
déglutition spontanée sont
significativement plus fréquents par
rapport aux contrôles normaux (p = 0,047),
alors que la déglutition en lien avec le
bâillement n'est pas significativement
différente dans les deux groupes. Parmi
49 patients atteints de SEP, 16 (32,6%) avaient
une atteinte du tronc cérébral. Le
bâillement a été
observé chez seulement 6 (37,5%) d'entre
eux.
Le bâillement est significativement
augmenté chez les patients atteints de
SEP par rapport aux témoins normaux en
utilisant la méthode polygraphique. Il
n'y a pas de relation directe entre le tronc
cérébral et le
déclenchement du bâillement chez
les patients atteints de sclérose en
plaques d'après la clinique et les
résultats de l'IRM.
Cependant, les déglutitions
après le bâillement
suggèrent qu'il existe encore une
activité fonctionnelle du tronc
cérébral et / ou des
réflexes oropharyngés. Il faut
néanmoins souligner les
difficultés qui existent à la
localiser anatomiquement les lésions de
SEP, en raison de l'évolution par
poussées de la maladie.
1. Introduction
Spontaneous yawning (SY) is an involuntary
and stereotyped behavior common to human being
(Barbizet, 1958; Ertekin et al., 2015;
Walusinski and Deputte, 2004). It is more likely
to take place during wake-sleep and sleep-wake
transitions (Provine et al., 1987). It can be
easily recorded together with the spontaneous
swallowing (SS) in the polygraphic study in
lying position in one hour of the rest (Ertekin,
2014; Ertekin et al., 2013) or in all night
sleep (Uludag, Tiftikcioglu and Ertekin,
2016).
Patients with multiple sclerosis (MS) suffer
from the repetitive yawning and sleep problems
(Gallup et al., 2010; Sandyk, 1998; Thompson,
2014). Yawning is common in young female
patients who are fully ambulatory with a
relapsing-remitting course of disease (Sandyk,
1998). Yawning is observed in MS and other
central nervous system disorders such as
hypothalamus and cerebral cortical disorders and
yawning and swallowing may be controlled by the
network of the brainstem (Cattaneo et al., 2006;
Postert et al., 1996; Thompson et al., 2016;
Walusinski, 2009; Zilli, Giganti and Uga, 2008).
There are some evidence that the brainstem is
the origin of the spontaneous yawning
behavior:
1. Excessive yawning behavior is associated
with the ischemic lesion in the brainstem
(Cattaneo et al., 2006; Singer et al.,
2007)
2. Distorted yawning movements and complete
volitional paralysis of the bulbar muscles are
seen in Locked- in Syndrome (Bauer, Gerstenbrand
and Hengl, 1980; Krasnianski et al., 2003).
3. Yawning movements persist in anencephalic
infants (Daquin, Micallef and Blin, 2001).
4. Excessive yawning behavior is also
observed in patient with motor neuron disease
(Williams, 2000).
Postert et al. (1996) described excessive
yawning as a symptom of the brainstem
localization of MS. On the contrary diverse
opinions were also reported (Gallup, 2014;
Krestel et al., 2015; Platek, 2010; Thompson,
2014).
Yawning may be related with the Central
Pattern Generator (CPG) of the brainstem where
the swallowing and respiration are controlled
(Jean, 2001). If we look at yawning from the
view of swallowing and respiration; there is a
progressive slow opening of the mouth while the
dilatation of pharynx, larynx, thorax and
lowering of diaphragm muscle could be shown by
the radiological methods (Barbizet, 1958). The
increase of saliva flow was reported during
yawning (Inomata et al., 2005). Furthermore SS
occurs frequently in the period of SY (duration
about 4&endash;10 s) in normal subjects,
patients with brainstem infarction and
Parkinson's disease (Ertekin et al., 2015).
Therefore it is important to investigate MS
patients with various clinical and radiological
locations in order to understand the role of
brainstem on yawning mechanisms. Yawning was
evaluated by electrophysiological methods
previously (Thompson et al., 2014a, 2014b;
Thompson, 2013; Thompson and Bishop, 2012).
However in these studies, association of SY and
SS were not assessed and no muscle except
masseter was recorded. One hour polygraphic
recording would be crucial method for this
purpose, because it is easy to observe SY and SS
together with their electrophysiologic
counterparts (Ertekin, 2014; Ertekin et al.,
2013, 2015; Uludag et al., 2016).
It is well known that yawning is classified
into two types as spontaneous and contagious.
Both are similar in their motor action and their
triggering mechanism, although their
evolutionary nature and social meaning are
different (Baenninger, 1997; Provine and
Hamernik, 1986). It was reported that contagious
yawn and swallow are temporally related and
frequency of swallows was increased within 10 s
of post yawn period in normal adult subjects
(Abe et al., 2015). They concluded that swallows
after contagious yawning were increased. We have
re-investigated this phenomenon by studying the
SY and SS in polygraphic recording in normal
subjects and patients with MS. We investigated
the SY and its association with SS within 10 s
before and after yawning. We expected if this
phenomenon is present, it may indicate a
physiological linkage between brainstem
swallowing and yawning, if not, there is no
intimate relationship between the brainstem and
yawning.
Then we hypothesized that SY is expected to
increase in MS patients. However the origin of
yawning cannot strictly located to the brainstem
uniquely, when clinical and radiological
findings of the patients are compared.
Difficulties must be emphasized to detect
anatomic localization in MS because of relapsing
pattern of disease. SS can be recorded inside of
the yawning and increased rate of SS just before
and after SY would demonstrate the relationship
in between brainstem and yawning.
4. Discussion
Yawning was significantly increased in MS
patients. When we analyzed subgroups of yawning,
there is no increase rate of the SS just before
and after the SY within 10 s. Secondly, there
was no direct relations for the brainstem and
the origin of yawning in MS patients according
to clinical picture and MRI findings.
The mean sleeping time for normal controls
and the patients with MS was not statistically
different from each other during the
approximately 60-min recordings. This was
important because number of SS during sleep was
known to be reduced in comparing to awake state
(Afkari, 2007; Ertekin et al., 2013; Sato and
Nakashima, 2006; Uludag et al., 2016).
Yawning was significantly increased in MS
patients compared to normal controls. This was
well known finding and previously reported
(Baker, 2002; Gallup et al., 2010; Postert et
al., 1996; Sandyk, 1998; Thompson, 2014). It is
interesting that patients with MS suffer from
thermoregulatory dysfunction, repetitive yawning
and sleep problems (Gallup et al., 2010).
Yawning is proposed that could be controlled
by the network of brainstem (Cattaneo et al.,
2006; Postert et al., 1996; Walusinski, 2009;
Zilli et al., 2008). However, 14 of MS patients'
who were yawned MRI and clinical findings could
not demonstrate the involvement of the
brainstem. Only 6 of them had brainstem
involvement. Our findings on MS patients without
brainstem involvement were compatible to other
previous studies which did not suggest yawning
was under the control of the brainstem (Gallup,
2014; Krestel et al., 2015; Platek, 2010;
Thompson, 2014).
There are few theories that were developed
for yawning and its origin, among these, the
most recent and popular one is the cortical
theory of Thompson (2014). Indeed the yawning,
known to be associated with elevated cortisol
levels; may also occur in association with
fatigue; and this may explain why people with MS
yawn when they are observed to be frequently
fatigued (Thompson and Richer, 2015; Thompson,
2017, 2014). Similarly plasma ACTH levels at
night and just prior to awaking from sleep is
also associated in humans with yawning and
stretching behavior. Recurrent episodes of
uncontrollable yawning and body stretching also
occur in a subset of patients with MS during
electromagnetic cranial stimulation. This kind
of treatment was also found favorable to
therapeutic response to magnetic stimulation
(Sandyk, 1998). Our patients had never search
any treatment for their yawning and stretching
clinical responses. Although we could not
observe any clinical improvement but this should
also be investigated in further studies.
Another physiological fact is the SS which
was recorded inside of the SY, but this was not
found statistically significant. However, it was
reported that contagious yawn and swallow are
temporally related and frequency of swallow was
increased within 10 s of post yawn period in
normal adult subjects (Abe et al., 2015). In SY,
we could not found such a relationship that the
yawning after 10 s is able to increase rate of
swallows. Thus our finding may not be compatible
with finding of Abe (2014).
SY and SS can often be seen together but not
always associated with one another. Since the
duration of yawning is about 4&endash;10 s
(Askenasy, 1989; Ertekin et al., 2015;
Walusinski, 2009), SS could overlap with a
yawning randomly and there is a mechanism for
the safe swallow during yawning. Because SY
associated with swallows seen to be safe for our
patients and normal controls. We did not observe
any clinical signs of aspiration such as
coughing just after yawning, neither could we
observed any graphical changes suggesting the
laryngeal penetration. However this observation
could not be contrary for the final relationship
between yawning and brainstem where the origin
of yawning could be different but the safe
swallowing during yawning could be explained by
some brainstem mechanism or/and related
oropharyngeal reflexes. This point of view
should be elucidated in further studies.
In Conclusion:
1. Yawning is significantly increased in MS
patients compared to normal controls by using
the polygraphic method.
2. The SY and the SS are sometimes
associated and overlapped in both normal
controls and MS patients without any aspiration
into the airway.
3. There is no increased rate of SS just
below and after the SY within 10 s
4. There is no direct relation of the
brainstem and the origin of yawning in MS
patients according to clinical picture and MRI
findings. However safe swallows during yawning
could suggest that there is still need to some
brainstem mechanism and/or oropharyngeal
reflexes.
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(2015). Occurrences of Yawn and Swallow are
Temporally Related. Dysphagia, 30(1),
57&endash;66.
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Afkari, S. (2007). Measuring frequency of
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