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A, Hess Ch. Clinical significance of yawning
in disorders of consciousness and vigilance.
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Introduction
- Yawning is a frequent behaviour occurring in
most vertebrate species [1, 2] from
foetal stages [3] to old age
[4]. In mammals, it consists of an
involuntary sequence of about 5 to 10 seconds
duration with wide mouth opening, deep
inspiration, brief apnoea, and slow expiration.
Similar jaw movement sequences have also been
observed in reptiles, birds, amphibians, and
fish species, but it is controversial to which
degree such yawn-like behaviour is homologous to
human yawning [5, 6].
-
- The role of normal yawning remains currently
unknown, although numerous hypotheses have been
put forward throughout the centuries
[7]. It is also not known whether the
early morning yawns associated with stretching
of limb and neck muscles (stretch yawns) are a
separate entity or rather a stronger variant of
isolated yawns. From an evolutionary
perspective, one would expect that such a
ubiquitous and frequent behaviour provides an
advantage for survival. Yet, no consistent
physiological effects of yawning could be
demonstrated so far. In particular, the
wide-spread notion that yawning might oxygenate
the blood or increase vigilance could not be
confirmed experimentally [8, 9]. The
only specific effect of yawning that could be
demonstrated so far was its contagiousness in
humans and some &endash; but not all &endash;
animal species [10 - 13]. Yawning by
contagion is associated with activations in
neural networks responsible for empathy and
social skills [14 - 17]. Hence, there
seems to be a link between yawning and social
functions [18]. Although yawns are
usually accompanied by a pleasant feeling of
satisfaction, they can occur excessively in
which case they can lead to discomfort and
medical consultations [19]. Furthermore,
acute bursts of excessive yawning, also labelled
"chasm", should be recognized as early but
unspecific warning sign for imminent disorders
of consciousness and clinical worsening.
-
- Anatomy
- A good understanding of the anatomical basis
of yawning would be necessary to fully
appreciate the pathomechanisms of excessive
yawning. Unfortunately, research has been
essentially limited to investigations of
pharmacological triggers of yawns, and lesion
studies are scarce. Figure 1 gives an overview
of the main currently known pathways. It is
unclear whether there exists a centre for yawn
execution. However, given the implication of
oropharnyngeal muscles, it is assumed to be
located in ponto-bulbar parts of the brain stem.
This centre seems to receive afferents from
several deep brain structures, in particular
from the paraventricular nucleus of the
hypothalamus. Numerous neurotransmitters,
neuropeptides, and hormones have been found to
modulate yawning. Neuroendocrine substances as
diverse as, among others, dopamine,
acetylcholine, glutamate, serotonin, nitric
oxide, adrenocorticotropic hormone (ACTH)
related peptides, oxytocin, and steroid hormones
facilitate yawning wheras opioid peptides exert
an inhibitory effect. Some of these mediators
(e.g., dopamine, glutamate, oxytocin) interact
in the paraventricular nucleus of the
hypothalamus and induce yawning via
oxytoninergic projections to the hippocampus,
the pons, and the medulla oblongata. Other
pathways seem to be effective for serotonin,
acetylcholine, and ACTH related peptides
[20].
-
- Behavioural observations of contagious yawns
and recent lesion analyses further suggest that
cortical structures also contribute to yawn
control, in particular the insula [21],
but the corresponding pathways are unclear.
-
 - Chronic excessive yawning and
sleepiness
- There is convergent evidence from different
areas of research that sleepiness triggers
yawning. Behavioural studies consistently
reported that yawns occur most frequently before
and after sleep, i.e., during periods with lower
levels of alertness [22, 23]. The
circadian distribution of yawns follows the
individual sleep-wake rhythm [24, 25,
4], and the individual subjective feeling of
drowsiness correlates with increased yawning
rates [4]. Furthermore, yawns are
accompanied by electroencephalographic (EEG)
signs of drowsiness. In particular, power
density of delta waves over the vertex, which is
considered to be a marker of sleep pressure
[26], is greater before yawns than
before control movements without yawning
[9]. Accordingly, excessive daytime
sleepiness is the most frequent cause of
excessive yawning [19]. In this case,
excessive yawning is usually present chronically
over weeks to months. It can be due to lack of
sleep or secondary to other sleep pathologies
such as sleep apnoea syndrome. Frequent yawning
can therefore be one of the symptoms of
excessive daytime sleepiness but is often
overlooked. Similarly, patients can be
instructed to recognize yawns as sign of
sleepiness, in particular when driving.
-
- Acute bouts of yawning and disorders of
consciousness
- Excessive yawning can also appear acutely,
often in form of bouts or salvoes. In
particular, it can be frequently observed in
patients presenting current or imminent
disorders of consciousness and then opens a
large differential diagnosis. Syncopes and
malaises with a sudden overstimulation of the
parasympathetic system can be preceded by bouts
of yawning [27], sometimes even before
the appearance of nausea and pallor.
-
- The occurrence of yawning during medical
interventions may therefore not be due to
sleepiness or boredom of the patient, but should
prompt the medical attendant to put the patient
in a supine position. Similarly, excessive
yawning can be one of the first manifestations
of hypoglycaemia in diabetic patients
[19]. Yawning is associated with hunger
in healthy animals [6], and may
therefore be a physiological manifestation of
hypoglycaemia. The frequency of yawning tends to
increase in patients with brain lesions, in
particular stroke. Lesions in the internal
capsule [28], the brain stem
[29], as well as in the insula and the
caudate nucleus [21] seem to be
particularly associated with increased yawning.
The mechanisms of this increase are unknown. One
reason may be that patients with severe
hemiparesis after stroke can experience
automatic, involuntary movements of their
paralysed arm during yawns. Since this is
usually the only occasion when they see their
affected arm moving, they are particularly keen
to yawn. The movement consists of involuntary
rising of the arm and has been named
"parakinesia brachialis oscitans" [28].
It is associated with severe motor deficits and
disappears in case of clinical improvement. The
mechanisms are incompletely understood.
Walusinski et al. [28] suggested that it
may be mediated by spino-cerebellar pathways
which become autonomous due to damage of
corticospinal, cortico-nuclear and and
cortico-cerebellar tracts.
-
- Although the overall yawning frequency can
be increased in patients with brain lesions, the
appearance of acute, repetitive bouts of yawning
is suspicious of additional intracranial
hypertension. Although rare, its occurrence in
patients with recent trauma or stroke should
lead to the consideration of brain imaging. In
patients with reduced levels of consciousness,
the sudden appearance of yawning may be a sign
of herniation. Of particular interest to
epileptologists is yawning associated with
seizures. Post-ictal yawns are relatively common
and were described in 4% of patients with
temporal lobe epilepsy in a systematic
retrospective analysis. Interestingly, it
occurred only in patients with right temporal
seizure origin [30]. Post-ictal yawning
therefore seems to have a lateralizing value to
the nondominant hemisphere. In contrast, yawning
during actual seizures is very rare and only a
few cases have been described [31].
These patients had partial seizures of temporal
origin, but yawning during 3/sec spike-wave
episodes was also described in young patients
with probable idiopathic generalized epilepsy
[32]. An epileptic trigger of yawning is
particularly probable if it occurs in a
stereotyped way during seizures.
-
- Yawning is one of the most common and
consistent prodromal symptoms before migraine
attacks and seems to occur more frequently
before attacks with aura [33 - 35]. It
can also occur after the headache period
together with tiredness, depressed mood, and
concentration difficulties [36]. Rarely,
yawning can be painful by itself in patients who
do not suffer from headaches. In this case, pain
seems to be due to affections of
craniopharyngeal muscles or nerves
[37].
-
- The mechanisms by which these diverse
conditions increase yawning have not been
investigated. However, pathological yawns seem
to be triggered either by local compression or
irritation of the putative yawning centers (in
particular the hypothalamus), or by one of the
many neuroendocrine substances which have been
shown to facilitate yawns in animal models.
-
- Other causes for excessive yawning Excessive
yawning is not always accompanied by disorders
of consciousness or excessive sleepiness. For
instance, compression of the hypothalamus or the
pituitary gland are rare causes of yawn salvoes.
They can lead to particularly frequent and
disabling yawns [38, 19].
-
- Another important cause for excessive
yawning is the intake of neurological and
psychiatric medication. Serotoninergic and
tricyclic antidepressants are most frequently
involved [39 - 42, 19]. In this case, it
is important to recognize it as iatrogenic side
effect and not to misinterpret it as signs of
sleepiness or asthenia of the patients.
-
- Other rare conditions which have been
associated with excessive yawning include
progressive supranuclear palsy [43] and
amyotrophic lateral sclerosis [44]. The
mechanisms of this association are unknown.
Conclusions
-
- Frequent yawning can be a normal
manifestation of, among others, sleepiness,
boredom, hunger, and social interactions
[7], as well as associated with a large
variety of medical conditions. It is therefore
unspecific. Yet, in acute pathological
conditions, it usually appears early before the
appearance of disorders of consciousness or
clinical worsening. Its recognition can give the
clinician a head start for preparing therapeutic
and supportive measures.
-
- The management of excessive yawning consists
in finding and treating the underlying cause.
Table 1 gives an overview of the large
differential diagnosis. Medication associated
with yawning and excessive caffeine consumption
should be adapted first. Hereby, it is important
to avoid abrupt stopping of opiates or caffeine,
as this can lead to excessive yawning.
Insufficient sleep or sleep pathologies should
be actively searched. Finally, a careful history
taking and clinical examination may reveal
further abnormalities which guide the treatment,
e.g., if they reveal functional disorders,
headaches, or neurological deficits. Finally,
specialized exams may be considered in selective
cases to look for epileptic activity, pituitary
pathologies, or brain lesions. Treatment
consists in the elimination of the cause. There
is no established pharmacological therapy to
reduce yawning frequency, but based on a case
report, propranolol can be tried
[45].
-
- Finally, it is noteworthy that yawning can
also be reduced or suppressed by medical
conditions, in particular Parkinson's disease
[46] and neuroleptic drugs
[47].
-
 -
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